Familiar Prey Research Articles

Rearing Neoseiulus cucumeris and Amblyseius swirskii (Mesostigmata: Phytoseiidae) on non-target species reduces their predation efficacy on target species

Abstract In Florida, strawberries are prone to infestation by Tetranychus urticae Koch (twospotted spider mite; Trombidiformes: Tetranychidae) and Scirtothrips dorsalis Hood (chilli thrips; Thysanoptera: Thripidae). Management of these pests using conventional insecticides is becoming difficult, thereby forcing many growers to adopt the use of commercially available biological control agents including Neoseiulus cucumeris Oudemans and Amblyseius swirskii Athias-Henriot (both Mesostigmata: Phytoseiidae). These predators are mass reared on prey different from T. urticae, and their prey switching capacity is unknown. Therefore, the objective of this study was to compare the predation capacity of A. swirskii and N. cucumeris feeding on familiar and unfamiliar prey. Thus, using T. urticae as a non-familiar prey model organism, a no choice test was conducted where A. swirskii and N. cucumeris were each provided with Acarus spp. (commonly used as prey for commercial rearing of predatory mites) as familiar prey and eggs, deutonymphs, and adult females of T. urticae as unfamiliar prey. Prey consumption was recorded at 12, 24, 36 and 48 h. Our results show that both A. swirskii and N. cucumeris exhibited higher prey consumption when prey was familiar (Acarus spp.) compared to unfamiliar prey. Additionally, both predators showed higher consumption of eggs compared to T. urticae nymphs and adults. In 12 h, both predators had consumed 50 % of eggs, however, 36–48 h were required for 50 % of the T. urticae adults and nymphs to be consumed. Therefore, strawberry growers utilizing these predatory mites ought to refrain from the use of insecticides known to be detrimental to predatory mites for a period of at least 48 h to allow the predators to adjust to the new prey and environment.

Categorizing experience-based foraging plasticity in mites: age dependency, primacy effects and memory persistence.

Behavioural plasticity can be categorized into activational (also termed contextual) and developmental plasticity. Activational plasticity allows immediate contextual behavioural changes, whereas developmental plasticity is characterized by time-lagged changes based on memory of previous experiences (learning). Behavioural plasticity tends to decline with age but whether this holds true for both plasticity categories and the effects of first-in-life experiences is poorly understood. We tackled this issue by assessing the foraging plasticity of plant-inhabiting predatory mites, Amblyseius swirskii, on thrips and spider mites following age-dependent prey experience, i.e. after hatching or after reaching maturity. Juvenile and young adult predator females were alternately presented thrips and spider mites, for establishing 1st and 2nd prey-in-life experiences, and tested, as gravid females, for their foraging plasticity when offered both prey species. Prey experience by juvenile predators resulted in clear learning effects, which were evident in likelier and earlier attacks on familiar prey, and higher proportional inclusion of familiar prey in total diet. First prey-in-life experience by juvenile but not adult predators resulted in primacy effects regarding attack latency. Prey experience by adult predators resulted mainly in prey-unspecific physiological changes, with easy-to-grasp spider mites providing higher net energy gains than difficult-to-grasp thrips. Prey experience by juvenile, but not adult, predators was adaptive, which was evident in a negative correlation between attack latencies and egg production. Overall, our study provides key evidence that similar experiences by juvenile and adult predators, including first-in-life experiences, may be associated with different types of behavioural plasticity, i.e. developmental and activational plasticity.

Aversive Learning in the Praying Mantis (Tenodera aridifolia), a Sit and Wait Predator

Animals learn to associate sensory cues with the palatability of food in order to avoid bitterness in food (a common sign of toxicity). Associations are important for active foraging predators to avoid unpalatable prey and to invest energy in searching for palatable prey only. However, it has been suggested that sit-and-wait predators might rely on the opportunity that palatable prey approach them by chance: the most efficient strategy could be to catch every available prey and then decide whether to ingest them or not. In the present study, we investigated avoidance learning in a sit-and-wait predator, the praying mantis (Tenodera aridifolia). To examine the effects of conspicuousness and novelty of prey on avoidance learning, we used three different prey species: mealworms (novel prey), honeybees (novel prey with conspicuous signals) and crickets (familiar prey). We sequentially presented the prey species in pairs and made one of them artificially bitter. In the absence of bitterness, the mantises consumed bees and crickets more frequently than mealworms. When the prey were made bitter, the mantises still continued to attack bitter crickets as expected. However, they reduced their attacks on bitter mealworms more than on bitter bees. This contrasts with the fact that conspicuous signals (e.g. coloration in bees) facilitate avoidance learning in active foraging predators. Surprisingly, we found that the bitter bees were totally rejected after an attack whereas bitter mealworms were partially eaten (~35%). Our results highlight the fact that the mantises might maintain a selection pressure on bees, and perhaps on aposematic species in general.

Differences in neophobia between cane toads from introduced and native populations

For species moving into new environments, locating and using unfamiliar resources is crucial for survival. The cane toad (Rhinella marina) has been successful in many countries worldwide, persisting in both urban and rural landscapes. Given that animals exploiting urban habitats are confronted with novel feeding opportunities, individuals in those areas are expected to exhibit reduced neophobic tendencies compared with individuals in rural populations. Additionally, individuals persisting in introduced populations are expected to be less neophobic than individuals in native populations, taking advantage of novelty as their range expands. To investigate such predictions, we examined the response to novel prey and a novel object in native toads in Panama and introduced populations (urban and rural) in Florida. Toads were tested in an arena with novel or familiar prey and later with a novel object next to familiar prey. We found differences in response to novelty between cane toads in different ranges but not in different habitats. Most introduced individuals from both urban and rural habitats consumed novel prey with no difference in latency to eat between prey types. Few native toads, however, consumed any prey during trials, spending most of their time moving about the arena. When familiar prey was presented near a novel object, more than half of the introduced toads ate, but no native individuals ate. This study emphasizes the importance of behavior as a mechanism used by invasive species to exploit novel resources and successfully colonize new environments.

Dietary wariness influences the response of foraging birds to competitors

Foraging animals must choose between familiar prey and novel prey of uncertain profitability and potential toxicity. Owing to a healthy aversion to potentially dangerous prey, foragers show an initial transient wariness of novel food (neophobia). In addition, some individuals display a much longer period of avoidance before incorporating the novel food into their diet (termed dietary conservatism). There are two stable foraging strategies found within forager populations: (1) adventurous consumers (AC) which rapidly accept novel foods and (2) foragers showing dietary conservatism (DC). The expression of these two strategies may also vary with environmental conditions. We measured the effect of competition on the plasticity of foraging strategies when domestic chicks, Gallus gallus domesticus, foraged for familiar and novel coloured crumbs with or without competitor chicks. In addition we investigated the effect of prey detectability on the response of foragers to a competitor, by making the familiar food cryptic or conspicuous. AC birds responded to competition by accepting the novel prey more quickly than when foraging alone, regardless of how hard familiar food was to find. In contrast, DC birds failed to reduce their wariness in response to competition when the competitor's food choice was obscured. The foraging strategies of the birds were thus found to be plastic in their expression, but this plasticity differed between inherently AC and DC individuals. The implications of these results are discussed in relation to the foraging strategies of wild and domestic birds.

The role of learning by a predator, Rivulus hartii, in the rare‐morph survival advantage in guppies

Negative frequency-dependent selection (NFDS), where rare types are favoured by selection, can maintain diversity. However, the ecological processes that mediate NFDS are often not known. Male guppies (Poecilia reticulata) exhibit extreme diversity of colour patterning and, in a previous field experiment, rare morphs had a survival advantage. Here, we test the hypothesis that predators impose NFDS because they are efficient at capturing familiar prey morphs, but are less efficient at capturing unfamiliar morphs. Over a series of trials, we presented Rivulus hartii, a natural predator of guppies, with male guppies with the same colour patterning (A trials); then, for a second series of trials, we presented the rivulus with guppies with a new colour pattern (B trials). The success of rivulus at capturing guppies on the first attack increased over successive A trials. First attack success decreased significantly for the early B trials, and then increased during successive B trials, eventually reaching the same level as in the best A trials. This experiment demonstrates that learning, perhaps through long-term search image formation, plays a role in predation success on familiar vs. unfamiliar prey morphs. These results support the hypothesis that predator learning contributes to the maintenance of the extreme male guppy polymorphism seen in nature.

Visual and Chemical Prey Cues as Complementary Predator Attractants in a Tropical Stream Fish Assemblage

To date, little attention has been devoted to possible complementary effects of multiple forms of public information similar information on the foraging behaviour of predators. In order to examine how predators may incorporate multiple information sources, we conducted a series of predator attraction trials in the Lower Aripo River, Trinidad. Four combinations of visual (present or absent) and chemical cues (present or absent) from each of two prey species were presented. The occurrences of three locally abundant predatory species present within a 1 m radius of cue introduction sites were recorded. The relative attractiveness of cue type to each predator was directly related to their primary foraging modes, with visual ambush predators demonstrating an attraction to visual cues, benthivores to chemical cues, and active social foragers demonstrating complementary responses to paired cues. Predator species-pair counts were greatest in response to cues from the more abundant prey species, indicating that individuals may adopt riskier foraging strategies when presented with more familiar prey cues. These differences in predator attraction patterns demonstrate complementary effects of multiple sensory cues on the short-term habitat use and foraging behaviour of predators under fully natural conditions.

Kin recognition by juvenile predatory mites: prior association or phenotype matching?

Kin recognition, the biased treatment of conspecific individuals based on genetic relatedness, is a widespread phenomenon in animals. The most common mechanisms mediating kin recognition are prior association (familiarity) and phenotype matching. Recognition based on prior association allows identifying familiar individuals. Recognition based on phenotype matching is an extension of prior-association-based recognition and allows identifying familiar and unfamiliar individuals due to a shared phenotypic trait. I investigated which of the two mechanisms is used by cannibalistic juvenile predatory mites, Phytoseiulus persimilis. Protonymphs that were associated with either siblings or non-kin discriminated familiar and unfamiliar larvae and preferentially cannibalized the latter irrespective of genetic relatedness. In contrast, despite previous association with either siblings or non-kin, protonymphs did not discriminate unfamiliar sibling and unfamiliar non-kin larvae. Association in the larval stage therefore mediated kin recognition based on familiarity, but not phenotype matching in cannibalistic P. persimilis protonymphs. Furthermore, in the presence of a familiar prey individual, sibling cannibalism occurred significantly sooner than non-kin cannibalism. This quick sibling cannibalism may have been the consequence of preferential association of siblings and/or may indicate the occurrence of an alternative cannibal phenotype. I discuss the adaptive significance of prior-association-based recognition for P. persimilis juveniles and emphasize the ability of P. persimilis to use multiple recognition mechanisms in dependence of the ontogeny and the ecological context.

Complementary and lateralized forms of processing in Bufo marinus for novel and familiar prey

Amphibian vision is one of the most comprehensively studied of all vertebrate sensory systems. However, the processes of object recognition and memory in anuran amphibians have resisted satisfactory explanation. Our research shows that insight to the issue of visual discrimination and recognition in toads may be gained by investigation of the specialized and complementary functions carried out by the left and right brain hemispheres. We report that specialized processes associated with the left eye (right hemisphere) of the Bufo marinus toad carry out decisions to view and strike at complex prey stimuli recognized as ‘novel.’ This was demonstrated in the toads’ preferences when provided a choice between identical novel insect models presented simultaneously into the left and right lateral, monocular visual fields. In a second experiment, videotaped trials of toad groups competing in an open field for live crickets were analysed for lateralized prey-catching behaviour. Concomitant with a preference for directing agonistic strikes at conspecifics within the left visual hemifield, toads were found to posses a significant preference for directing predatory responses at the familiar prey viewed in the right visual hemifield. The preference for directing prey-catching responses at freely moving crickets in the right visual hemifield supports the earlier findings drawn from automated and familiar model insect prey. We present a hypothesis explaining differences in hemispheric processing in toads responding to ‘novel’ and ‘familiar’ prey types, utilizing a range of long-term memories found to be lateralized in other vertebrates.

PERSPECTIVE: THE EVOLUTION OF WARNING COLORATION IS NOT PARADOXICAL

Animals that are brightly colored have intrigued scientists since the time of Darwin, because it seems surprising that prey should have evolved to be clearly visible to predators. Often this self-advertisement is explained by the prey being unprofitable in some way, with the conspicuous warning coloration helping to protect the prey because it signals to potential predators that the prey is unprofitable. However, such signals only work in this way once predators have learned to associate the conspicuous color with the unprofitability of the prey. The evolution of warning coloration is still widely considered to be a paradox, because it has traditionally been assumed that the very first brightly colored individuals would be at an immediate selective disadvantage because of their greater conspicuousness to predators that are naive to the meaning of the signal. As a result, it has been difficult to understand how a novel conspicuous color morph could ever avoid extinction for long enough for predators to become educated about the signal. Thus, the traditional view that the evolution of warning coloration is difficult to explain rests entirely on assumptions about the foraging behavior of predators. However, we review recent evidence from a range of studies of predator foraging decisions, which refute these established assumptions. These studies show that: (1) Many predators are so conservative in their food preferences that even very conspicuous novel prey morphs are not necessarily at a selective disadvantage. (2) The survival and spread of novel color morphs can be simulated in field and aviary experiments using real predators (birds) foraging on successive generations of artificial prey populations. This work demonstrates that the foraging preferences of predators can regularly (though not always) result in the increase to fixation of a novel morph appearing in a population of familiar-colored prey. Such fixation events occur even if both novel and familiar prey are fully palatable and despite the novel food being much more conspicuous than the familiar prey. These studies therefore provide strong empirical evidence that conspicuous coloration can evolve readily, and repeatedly, as a result of the conservative foraging decisions of predators.

PERSPECTIVE: THE EVOLUTION OF WARNING COLORATION IS NOT PARADOXICAL

Animals that are brightly colored have intrigued scientists since the time of Darwin, because it seems surprising that prey should have evolved to be clearly visible to predators. Often this self-advertisement is explained by the prey being unprofitable in some way, with the conspicuous warning coloration helping to protect the prey because it signals to potential predators that the prey is unprofitable. However, such signals only work in this way once predators have learned to associate the conspicuous color with the unprofitability of the prey. The evolution of warning coloration is still widely considered to be a paradox, because it has traditionally been assumed that the very first brightly colored individuals would be at an immediate selective disadvantage because of their greater conspicuousness to predators that are naive to the meaning of the signal. As a result, it has been difficult to understand how a novel conspicuous color morph could ever avoid extinction for long enough for predators to become educated about the signal. Thus, the traditional view that the evolution of warning coloration is difficult to explain rests entirely on assumptions about the foraging behavior of predators. However, we review recent evidence from a range of studies of predator foraging decisions, which refute these established assumptions. These studies show that: (1) Many predators are so conservative in their food preferences that even very conspicuous novel prey morphs are not necessarily at a selective disadvantage. (2) The survival and spread of novel color morphs can be simulated in field and aviary experiments using real predators (birds) foraging on successive generations of artificial prey populations. This work demonstrates that the foraging preferences of predators can regularly (though not always) result in the increase to fixation of a novel morph appearing in a population of familiar-colored prey. Such fixation events occur even if both novel and familiar prey are fully palatable and despite the novel food being much more conspicuous than the familiar prey. These studies therefore provide strong empirical evidence that conspicuous coloration can evolve readily, and repeatedly, as a result of the conservative foraging decisions of predators.

Predatory Efficiency of Crayfish: Comparison Between Indigenous and Non-Indigenous Species

The invasive crayfish Procambarus clarkii is highly dispersed within lentic waters in northern and central Italy. It is a polytrophic predator, exerting a strong influence on animal communities, including amphibians, fish, gastropods, and insect larvae. The indigenous species Austropotamobius italicus, inhabiting lotic waters, behaves as a generalist – but not opportunistic – species. The object of this study was to compare the predatory pressure exercised by the two species on potential prey, i.e., anuran tadpoles, urodelan larvae, fish fry, larvae of insects, and gastropods. Three main conclusions were drawn: (1) both species are skilled predators, adopting a sit-and-wait strategy, (2) the two crayfish seemed to form a `search image' of familiar prey, as the result of either visual or chemical perceptual changes, and (3) at least in the laboratory, P. clarkii readily switched to naive prey for it (tadpoles of Rana italica and larvae of Limnephilidae), unlike the less opportunistic A. italicus. These results furnish suggestions on the trophic preferences of the two crayfish species and provide a partial understanding of the effects that the invasive species have on the community dynamics.

The allometry of cannibalism in piscivorous fishes

Cannibalism is a widespread phenomenon that can have strong population and community effects. In this study, I compare the prey size – predator size relationships of diets with and without cannibalized prey for four piscivorous species and five populations that are commonly cannibalistic and where large databases exist. I then examine the resultant trophic niche breadths (range of relative prey size consumed) to quantify whether inclusion of cannibalized prey in the diet slows down the decline in trophic niche breadth that many large predators exhibit as they grow. When comparing diets including cannibalized prey with those without, consistent differences were found among all predator species. In all cases, the slope of the upper bound of the predator size – prey size scatters was larger for cannibal predators compared with noncannibals, suggesting selectivity for larger cannibal prey, which may be driven by higher rates of size-dependent capture success with familiar prey. The slopes of the upper bounds of the cannibal relative prey size vs. predator size scatter also tended to be larger than the upper-bound slopes for diets without conspecific prey. Finally, for all species, mean trophic breadth of diets including cannibalized prey were larger than those not including cannibal prey, suggesting that relatively large prey sizes may always be available for cannibals.

Stimulus control of predatory behavior by the Iberian wall lizard (Podarcis hispanica, Sauria, Lacertidae): effects of familiarity with prey.

The authors examine the relative roles of vision and chemoreception and the influence of previous experience with prey on the predatory behavior of Iberian wall lizards (Podarcis hispanica). Experiment 1 compared the responses to visual, chemical, and a combination of visual and chemical cues of a familiar prey by 2 groups of lizards that had been kept in captivity for either 3 months or 21 days. Experiment 2 assessed the responses of lizards kept in the laboratory for more than 3 months to a novel prey species. The results reveal that feeding on a prey species affects the lizards' responses to chemical stimuli from that prey. The response to chemical cues of a novel prey requires a 1st-feeding experience with that prey. Lizards that have been fed the same prey species for several months cease responding to the chemical stimuli of that particular prey.

Feeding behaviour of greenback flounder larvae, Rhombosolea tapirina (Günther) with differing exposure histories to live prey

This study examined the feeding performance of cultured larvae of the greenback flounder Rhombosolea tapirina, using the live feed organisms, Brachionus plicatilis and Artemia sp., to determine the primary sensory modality involved in feeding, and the effect of previous exposure to prey on subsequent prey selection. The proportion of larvae that fed on rotifers in the light (400–700 nm daylight fluorescent tubes — light intensity of 5–6 μmol s −1 m −2), increased significantly from 66% to 96% from day 12 to day 27 post-hatching, respectively. In comparison, the proportion of larvae that fed on rotifers in total darkness, never exceeded 5% during the same period. This indicates that greenback flounder larvae are primarily dependent upon vision to feed. Prior feeding experience of greenback flounder larvae with either rotifers only (R-treatment) or a mixed diet of Artemia and rotifers (A&R-treatment) significantly affected subsequent prey selection when larvae were offered a mixed diet of Artemia and rotifers. It did not, however, affect the temporal onset of selection of the novel prey species ( Artemia) by R-treatment larvae. Therefore, the differences in prey selection by larvae, with or without prior exposure to Artemia prey, were not due to the inability of larvae to handle and ingest a novel prey species, but they reflect positive selection for familiar prey. The latter indicates a learned component in the feeding behaviour of fish larvae. This has implications for the timing of the introduction of new live prey species during intensive culture of marine fish larvae.

Enhancement of the response of rock crabs, Cancer irroratus, to prey odors following feeding experience

The rock crab, Cancer irroratus Say, uses chemically mediated learning in the search for food. Rock crabs are opportunistic benthic predators and scavengers. Observations indicate that although they eat a variety of items, they are more sensitive to, and prefer, odors of food items that they have been eating. We found that C. irroratus is more responsive to a familiar food source than to an unfamiliar one and can distinguish between the odors of two different prey after being fed one species for an extended time. Initial preferences for two mytilid bivalves, Mytilus edulis and Geukensia demissa, were determined in a Y-maze. Crabs were then fed only one of the mussel species for 28 days and retested, using sequential and simultaneous presentations, for their responses to familiar and unfamiliar prey odors. Crabs increased their responses to familiar prey odors, but not to unfamiliar odors. In foraging tests, crabs ate M. edulis more often regardless of the species to which they had been familiarized.

Effect of Diets Supplemented with Live Food on the Foraging Behavior of Cultured Fall Chinook Salmon

Abstract The use of diets supplemented with live food to increase the postrelease foraging ability of hatchery-reared fall chinook salmon Oncorhvnchus tshawytscha was investigated. Replicate groups of fry were reared in six 2.4-m-diameter circular tanks and fed one of two diets. Fish in three tanks received a commercially available pelletized diet; fish in the other three tanks were given the opportunity to forage on natural live prey (mysids, mosquito larvae, chironomid larvae, and daphnia) prior to their daily ration of pellets. Foraging by individual fish was observed in special 200-L tanks, and fish conditioned to live food fed on twice as many familiar prey (chironomids) and novel prey (mayfly larvae) as unconditioned fish fed on. This suggests that diets supplemented with live food can be used to increase the postrelease foraging effectiveness of hatchery-reared chinook salmon.

Wild Birds Prefer the Familiar Colour Pattern When Feeding on Similar Artificial Morphs

Apostatic (frequency-dependent) selection by visually hunting predators could be responsible for maintaining colour polymorphisms in prey species. We report here the results of six experiments on wild birds feeding on 'populations' of two similar green 'morphs' of an artificial prey which had a single dark green stripe or were plain. Birds foraging on lawns were fed on one type and then given a choice of equal numbers of the two; they were then fed on the second type and again given a choice. In four experiments each training period lasted one day; in the remaining two experiments, five days. The results showed that birds tended to prefer the familiar prey - even after the shorter training sessions. Although training effects are not a prerequisite for apostatic selection we conclude that the results provide evidence for behaviour that could lead to the maintenance of prey polymorphisms in which morphs are differentiated by the presence or absence of inconspicuous patterns. D. L. Raymond and J. A. Allen, Dept of Biology, Univ. of Southampton, Southampton S09 3TU, England.

Effects of poisoning on predatory and ingestive behavior toward artificial prey in rats (Rattus norvegicus).

Ingestion of novel prey by vertebrate predators that is followed by illness typically decreases the predators' eating the prey more readily than their pursuing or killing it. We used artificial prey-food items (rolling ball bearings that predicted food pellets) to model and extend this finding in laboratory rats. During daily experimental sessions presentations of a novel bearing-food combination were intermixed with presentations of a familiar bearing-food combination. The poisoned animals received lithium chloride injections after each session. Experiment 1a showed that: (a) Poisoning markedly decreased ingestion of the novel food without decreasing the frequency of contact (nose, seize, carry, or chew) with the novel bearing predicting that food. (b) However, poisoning did significantly decrease the average duration of contact with the novel bearing. (c) Poisoning did not decrease behavior toward the familiar food and bearing. Experiment 1b showed that after moderate exposure to pairings of the novel food and bearing, poisoning decreased behavior toward both novel and familiar food and bearings. The results indicate that important aspects of predation can be simulated and examined in the laboratory by using artificial prey-food items. These results also support the conclusions that predatory behavior and ingestion reflect separable modes of behavior and that the presence of novel prey interferes with the generalization of poisoning effects to familiar prey.

Food Conditioning and Prey Selection by Young Yellow Perch (Perca flavescens)

We tested how diet conditioning influences prey species selection by age-0 yellow perch (Perca flavescens) in laboratory experiments. We conditioned yellow perch to diets of different ratios of Daphnia pulex and Diaptomus sicilis and then offered them an experimental 1:1 test mixture of each prey. The influence of conditioning on prey selection was found not to be random, and prey were consumed neither in proportion to the 1:1 test mix nor to the ratio of prey in the conditioning diet. Young yellow perch switched to novel prey and did not specialize on the most frequently encountered prey in conditioning diets. However, when yellow perch were conditioned and tested on the 1:1 Diaptomus to Daphnia mix, these fish selected Diaptomus until they reached 35–40 mm total length when they switched to the larger bodied Daphnia. We hypothesize that young yellow perch may switch to novel prey because nutritional advantages associated with diet breadth may outweigh the advantage of feeding on familiar prey.