Adaptive learning of host preference in a herbivorous arthropod (original) (raw)
Related papers
Intraspecific variation in induction of feeding preference and performance in a herbivorous mite
Experimental and Applied Acarology, 2000
Induction of food preference has often been observed in herbivorous insects. The term is used to indicate preference of individuals for the host plant they have already experienced over one they have not experienced. A typical set-up is one where individuals first feed on host X or Y, and are then offered a choice between host X and Y. This set-up -and hence the body of empirical data -has been criticised for lack of a control treatment to untangle the effects of the separate hosts. In this study, we use a design with a third, unrelated host as control to investigate induction of preference in the herbivorous arthropod, Tetranychus urticae. We provide evidence of induced preference, as well as induced performance, and show that there is considerable variation in these two traits among strains. We suggest induced resistance to toxic secondary plant chemicals as one potential explanation for induced performance. This in itself suggests associative learning as the most likely candidate learning mechanism for induction of preference in this species. Phenotypically plastic effects underlying induced performance may be a general aspect of induction of preference in herbivorous arthropods, which warrants closer attention to these phenomena.
Adaptive learning in arthropods: spider mites learn to distinguish food quality
Experimental and Applied Acarology, 2000
Manyy herbivorous arthropods have been shown to possess learning capabilities,, yet fitness effects of learning are largely unknown. In this paper, wee test whether two-spotted spider mites (Tetranychus urticae) learn to distinguishh food quality in choice tests, and whether this results in fitness benefits.. Food consisted of cucumber plants with one of three degrees of feedingg damage: undamaged (no mites), mildly damaged (infested by a mitee strain adapted to tomato) and heavily damaged (infested by a mite strainn adapted to cucumber). Mites were subjected to one choice test in a greenhousee and three sequential choice tests on leaf disks. Thereafter, individuall mite performance was measured as oviposition rate over four days.. In the course of the three small-scale choice tests, preference shiftedd towards less damaged food. The performance tests showed that learningg was adaptive: mites learned to prefer the food type that yielded the higherr oviposition rate. Interestingly, innate preferences in the greenhousee tests were close to those shown after learning in the small-scale tests.. Given that both strains of mites had not experienced cucumber for severall years, we hypothesise that the preference in the greenhouse was duee to avoidance of mite odours rather than odours of damaged plants. Throughh its effect on foraging behavior, adaptive learning may promote thee evolution of host plant specialisation in herbivorous arthropods.
Predatory mites learn to discriminate between plant volatiles induced by prey and nonprey herbivores
Animal Behaviour, 2005
Many carnivorous arthropods can use chemical information from plants to locate their herbivorous prey. The composition of blends of herbivore-induced plant volatiles can vary with plant and herbivore species and thus carnivores are confronted with variable information about the presence of their prey. Such environmental variation is expected to favour learning. We investigated the learning ability of the predatory mite Phytoseiulus persimilis, a specialized natural enemy of polyphagous spider mites. We reared mites on different plant species, and subsequently tested their preference for volatiles from lima bean plants infested with either the prey herbivore Tetranychus urticae or the nonprey caterpillar Spodoptera exigua in a Y-tube olfactometer. Predators reared on lima bean preferred the volatiles induced by T. urticae, whereas predators reared on cucumber did not. We also investigated the foraging behaviour of mites after a nonrewarding experience during the adult phase (i.e. food deprivation in the presence of S. exiguainduced volatiles from lima bean) or after a rewarding experience (i.e. feeding in the presence of T. urticaeinduced volatiles). The rewarding experience had a much larger impact on the foraging responses. Predatory mites with multiple experiences (i.e. a nonrewarding experience followed by a rewarding experience) had the strongest preference for T. urticae-induced versus S. exigua-induced volatiles. We conclude that these learning abilities enable the predatory mites to forage in an environment where their prey can feed on a different plant species than the one on which the predator developed, and where nonprey caterpillars are also present.
Entomologia Experimentalis et Applicata, 2007
The relationship between oviposition preference and larval performance is a central topic in insectplant biology. In this study, we investigate whether the oligophagous flea beetle, Altica fragariae Nakane (Coleoptera: Chrysomelidae), exhibits a positive preference-performance relationship, and whether oviposition preference develops over time. We tested the beetles using four sympatric plant species: Duchesnea indica (Andrews) Focke (the normal host plant), Agrimonia pilosa Ledeb. (a secondary host plant), and Potentilla chinensis Ser. and Sanguisorba officinalis L. (host plants of two related Altica species) (all Rosaceae). In no-choice experiments, both oviposition rate and offspring fitness parameters (eclosion rate, development time, and body mass) were highest on D. indica . Oviposition rate was much lower on P. chinensis than on A. pilosa , whereas offspring fitness parameters did not differ significantly between these two host plants. Offspring fitness were lowest for S. officinalis , and adult females refused to oviposit on this acceptable non-host in a no-choice situation. Repeated two-choice experiments showed that the proportion of oviposition on one of the novel host plants decreased significantly over time when the alternative host plant was D. indica . In repeated two-choice experiments using A. pilosa and P. chinensis , females mainly fed on A. pilosa but distributed their eggs equally over the two host plants, in accordance with the lack of difference in offspring fitness on those hosts. Together, these results showed that A. fragariae females develop a positive preference-performance relationship over time. We suggest that A. fragariae achieves this through adaptive learning of oviposition preference: not only does the female learn to discriminate among the host plants when there is a fitness difference for her offspring, but the female also fails to discriminate when there is no fitness difference.
Biological Control, 2019
Generalist predators potentially have access to a wide array of prey, but it is little studied how experience with specific prey affects preference for this prey. In particular, it is unknown how experience with pest prey affects predator foraging decisions in cases where the pest is nutritious but protected by a repelling, potentially deadly defence. We investigated preference of the soil predatory mite Gaeolaelaps aculeifer Canestrini for the risky pest springtail Protaphorura fimata Gisin relative to the safe non-pest springtail Folsomia candida Willem. Egg production under foraging on live or dead individuals of either prey showed that the two species had equal nutritional quality for G. aculeifer, but indicated that live F. candida were more difficult to catch than live P. fimata. Importantly, some G. aculeifer were killed by P. fimata defence secretions, demonstrating that live P. fimata are risky prey. Preference for P. fimata was generally high when mites were given a choice between a live individual of either prey, but this preference was reduced following exposure to live individuals of P. fimata. Furthermore, fewer G. aculeifer killed a prey and time until kill was longer after experience with live P. fimata. These findings indicate that live P. fimata induced a partial aversion on G. aculeifer during exposure. Our study shows that generalist predators can reduce their preference for risky prey following exposure. This indicates that generalist predators used in biological control against risky prey are most efficient against this prey if not exposed to it prior to release.
Royal Society Open Science, 2018
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.
Oecologia, 2019
Foraging animals face the difficult task to find resources in complex environments that contain conflicting information. The presence of a non-suitable resource that provides attractive cues can be expected to confuse foraging animals and to reduce their foraging efficiency. We used the parasitoid Cotesia glomerata to study the effect of non-host-infested plants and associative learning on parasitoid foraging efficiency. Inexperienced C. glomerata did not prefer volatiles emitted from host (Pieris brassicae)-infested plants over volatiles from non-host (Mamestra brassicae)-infested plants and parasitoids that had to pass non-host-infested plants needed eight times longer to reach the host-infested plant compared to parasitoids that had to pass undamaged plants. Contrary to our expectations, oviposition experience on a host-infested leaf decreased foraging efficiency due to more frequent visits of non-host-infested plants. Oviposition experience did not only increase the responsiveness of C. glomerata to the host-infested plants, but also the attraction towards herbivore-induced plant volatiles in general. Experience with non-host-infested leaves on the contrary resulted in a reduced attraction towards non-host-infested plants, but did not increase foraging efficiency. Our study shows that HIPVs emitted by non-host-infested plants can confuse foraging parasitoids and reduce their foraging efficiency when non-host-infested plants are abundant. Our results further suggest that the effect of experience on foraging efficiency in the presence of non-host-infested plants depends on the similarity between the rewarding and the non-rewarding cue as well as on the completeness of information that parasitoids have acquired about the rewarding and non-rewarding cues.
Entomologia Experimentalis et Applicata, 2011
Black vine weevils, Otiorhynchus sulcatus (Fabricius) (Coleoptera: Curculionidae), are globally-distributed polyphagous pests of many horticultural crops. We investigated how adult weevils were affected by host switching and, in particular, how host plant species nutritional and defensive chemistry affected subsequent host plant species selection and oviposition. Adults were fed one of three host plant species, blackcurrant [Ribes nigrum L. (Grossulariaceae)], raspberry [Rubus idaeus L. (Rosaceae)], or strawberry [Fragaria x ananassa Duchesne (Rosaceae)], throughout their pre-reproductive periods and then subjected to behavioral choice assays with these plants. Foliar chemistry differed significantly among the three host plant species. Compared to raspberry and strawberry foliage, blackcurrant foliage was 13% lower in nitrogen, 3% higher in carbon, and 28% higher in phenolic compounds. Initial host plant species had a significant effect on weevil mortality, with more weevils dying when previously fed blackcurrant (12%) than strawberry (3%) or raspberry (0%) regardless of subsequent host. Initial host plant species also affected oviposition, with weevils laying only ca. two eggs per week when previously fed blackcurrant, compared to those on raspberry or strawberry (ca. 11 and 15 eggs per week, respectively). When given a choice, weevils discriminated among host plant species and tended to oviposit on plants on which they had previously fed, even when the plant was nutritionally inferior for egg production and adult survival. In contrast, feeding behavior was only affected by the current host plant species. Feeding and oviposition were related to leaf chemistry only in blackcurrant, as leaf consumption was negatively correlated with foliar carbon and zinc concentrations, and positively correlated with foliar phosphorus and potassium concentrations.
Experimental & applied acarology, 2000
When the chemical cues co-occurring with prey vary in time and space, foraging predators profit from an ability to repeatedly associate chemical cues with the presence of their prey. We demonstrate the ability of a predatory arthropod (the plant-inhabiting mite, Phytoseiulus persimilis) to learn the association of a positive stimulus (herbivorous prey, Tetranychus urticae) or a negative stimulus (hunger) with a chemical cue (herbivore-induced plant volatiles or green leaf volatiles). It has been suggested that the rate at which the integration of information becomes manifest as a change in behaviour, differs between categories of natural enemies (parasitoids versus insect predators: specialist versus generalist predators). We argue that these differences do not necessarily reflect differential learning ability, but rather relate to the ecologically relevant time scale at which the biotic environment changes.
Associative learning of host presence in non-host environments influences parasitoid foraging
Ecological Entomology
1. Parasitoids are known to utilise learning of herbivore-induced plant volatiles (HIPVs) when foraging for their herbivorous host. In natural situations these hosts share food plants with other, non-suitable herbivores (non-hosts). Simultaneous infestation of plants by hosts and non-hosts has been found to result in induction of HIPVs that differ from host-infested plants. Each non-host herbivore may have different effects on HIPVs when sharing the food plant with hosts, and thus parasitoids may learn that plants with a specific non-host herbivore also contain the host. 2. This study investigated the adaptive nature of learning by a foraging parasitoid that had acquired oviposition experience on a plant infested with both hosts and different non-hosts in the laboratory and in semi-field experiments. 3. In two-choice preference tests, the parasitoid Cotesia glomerata shifted its preference towards HIPVs of a plant-host-non-host complex previously associated with an oviposition experience. It could, indeed, learn that the presence of its host is associated with HIPVs induced by simultaneous feeding of its host Pieris brassicae and either the non-host caterpillar Mamestra brassicae or the non-host aphid Myzus persicae. However, the learned preference found in the laboratory did not translate into parasitisation preferences for hosts accompanying non-host caterpillars or aphids in a semi-field situation. 4. This paper discusses the importance of learning in parasitoid foraging, and debates why observed learned preferences for HIPVs in the laboratory may cancel out under some field experimental conditions.