Sister predatory mites collectively protect their eggs against predators.

Group-living animals sometimes cooperatively protect their offspring against predators. This behavior is observed in a wide range of taxa but, to the best of our knowledge, this is the first report of its occurrence in arthropods that are not eusocial. Adult female predatory mites Gynaeseius liturivorus protect their eggs against egg predators, the predatory mite species Neoseiulus californicus. In the field, several adult female G. liturivorus were often found on the same plant structures such as folded leaves. We tested whether these females might protect their eggs cooperatively, focusing on kinship between the females. When two adult female G. liturivorus were kept in the absence of egg predators, their reproduction was not affected by their kinship. The presence of egg predators reduced the number of G. liturivorus eggs. However, reproduction of two G. liturivorus sisters was higher than that of two non-sisters. Together, sisters guarded the oviposition site longer than non-sisters. We further tested if non-sisters increased egg guarding by having developed together from eggs to adults and found no such effect. Although it remains unclear how adult female G. liturivorus recognize conspecifics as kin or sisters, our results suggest that G. liturivorus sisters reduced predation on their offspring by cooperatively guarding their eggs.

Leaf trichome-mediated predator effects on the distribution of herbivorous mites within a kidney bean plant.

Some predators prefer to settle on leaf patches with microstructures (e.g., trichomes and domatia), leaving traces on the patches. Herbivorous arthropods, in turn, select leaf patches in response to these traces left by predators. It remains unclear whether traces of predators on leaf patches affect the distribution of herbivorous prey within plants through plant microstructure. Therefore, we examined the distribution of herbivorous mite (Tetranychus urticae) and predatory mite (Phytoseiulus persimilis) by investigating their oviposition pattern. We used a kidney bean plant (Phaseolus vulgaris) with two expanded primary leaves and the first trifoliate leaf, focusing on leaf trichomes as the microstructure. The density of trichomes was higher on the first trifoliate leaf than on the primary leaves and on the abaxial surface of the leaves than on the adaxial surface. Adult female P. persimilis laid more eggs on the first trifoliate leaf to the primary leaves. Although adult female T. urticae preferred to oviposit on the abaxial surface of primary leaves, previous exposure of plants to predators diminished this preference. The altered egg distribution would be a response to the traces of P. persimilis rather than eggs of P. persimilis. Our findings indicate that T. urticae reproduces on leaf patches with traces of predators without altering their oviposition preference. Given that the presence of predator traces is known to reduce the reproduction of T. urticae, it may have a substantial effect on the population of T. urticae in the next generations on kidney bean plants.

Role of kin recognition in oviposition preference and cannibalism by the predatory mite Gynaeseius liturivorus.

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.

Distribution and oviposition site selection by predatory mites in the presence of intraguild predators.

When intraguild prey and intraguild predators feed and reproduce in the same habitat and relatively immobile juveniles are the vulnerable stage, predation risk depends on oviposition site selection by the adult females. We studied how the availability of oviposition sites affected the distribution of two predatory mite species, Neoseiulus cucumeris (Oudemans) and Iphiseius degenerans (Berlese), over two patches that both contained food. The two plant-inhabiting species feed on pollen and thrips, prey on each other's juveniles, and prefer to oviposit on hairy parts of the leaf. When an artificial oviposition site was provided on one of two connected patches, both predator species strongly preferred this patch. Whereas the distributions of adults and eggs of N. cucumeris over the two patches were not affected by the presence of heterospecifics, the proportions of adults and eggs of I. degenerans on the patch with an oviposition site were reduced by the presence of N. cucumeris. A similar change in distribution was induced by cues of N. cucumeris on the oviposition site, without these mites being present. Hence, intraguild prey can weaken the strength of intraguild predation through patch selection, which in turn may promote coexistence of the two predator species.

Do aphid carcasses on the backs of larvae of green lacewing work as chemical mimicry against aphid-tending ants?

Ants attack and exclude natural enemies of aphids in ant-aphid mutualisms. However, larvae of the green lacewing, Mallada desjardinsi, prey on the cowpea aphid, Aphis craccivora, without exclusion by aphid-tending ants. Lacewing larvae are protected from ants by carrying aphid carcasses on their backs. Here, we tested whether cuticular hydrocarbons (CHCs) of aphid carcasses affected the aggressiveness of aphid-tending ants. Aphid carcasses were washed with n-hexane to remove lipids. Lacewing larvae with washed aphid carcasses were attacked by aphid-tending ants more frequently than those with untreated aphid carcasses. We measured the aggressiveness of aphid-tending ants to lacewing larvae that were either carrying a piece of cotton wool (a dummy aphid carcass) treated with CHCs from aphids or lacewing larvae, or carrying aphid carcasses. The rates of attack by ants on lacewing larvae carrying CHCs of aphids or aphid carcasses were lower than that of attack on lacewing larvae with conspecific CHCs. Chemical analysis by gas chromatography/mass spectrometry showed similarity of CHCs between aphids and aphid carcasses. These results suggest that aphid carcasses on the backs of lacewing larvae function via chemical camouflage to limit attacks by aphid-tending ants.

Do plants use airborne cues to recognize herbivores on their neighbours?

Plants show defensive responses after exposure to volatiles from neighbouring plants infested by herbivores. When a plant's neighbours host only species of herbivores that do not feed on the plant itself, the plant can conserve energy by maintaining a low defence level. An intriguing question is whether plants respond differently to volatiles from plants infested by herbivores that pose greater or lesser degrees of danger. We examined the secretion of extrafloral nectar (EFN) in lima bean plants exposed to volatiles from cabbage plants infested by common cutworm, two-spotted spider mites, or diamondback moth larvae. Although the first two herbivore species feed on lima bean plants, diamondback moth larvae do not. As a control, lima bean plants were exposed to volatiles from uninfested cabbage plants. Only when exposed to volatiles from cabbage plants infested by spider mites did lima bean plants significantly increase their EFN secretion compared with the control. Increased EFN secretion can function as an indirect defence by supplying the natural enemies of herbivores with an alternative food source. Of the three herbivore species, spider mites were the most likely to move from cabbage plants to lima bean plants and presumably posed the greatest threat. Although chemical analyses showed differences among treatments in volatiles produced by herbivore-infested cabbage plants, which compounds or blends triggered the increased secretion of EFN by lima bean plants remains unclear. Thus, our results show that plants may tune their defence levels according to herbivore risk level.

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.

Predator avoidance by phytophagous mites is affected by the presence of herbivores in a neighboring patch.

When predators invade a leaf patch inhabited by herbivores, the herbivores disperse to a neighboring predator-free leaf patch, thus escaping from the predators. However, the neighboring patch might already be used by con- or heterospecific herbivores. We used laboratory bioassays to examine whether perception of odor from con- or heterospecific competitors on a neighbored lima bean leaf patch influences dispersal behavior of the herbivorous mite Tetranychus urticae when attacked by predatory mites Phytoseiulus persimilis. The dispersal rates of T. urticae that perceived odors from leaf patches infested by conspecifics or cowpea aphids (Aphis craccivora) did not differ from the control (the dispersal rate of T. urticae that perceived odor from uninfested leaf patches). By contrast, the dispersal rate of T. urticae was reduced when they perceived odors from leaf patches that were currently or had previously been infested by larvae of the common cutworm (Spodoptera litura). Previous herbivory by S. litura larvae induced resistance in leaf patches to T. urticae as indicated by the reduced number of eggs laid by T. urticae. Our results are discussed with respect to the feeding behavior of the tested competitors of T. urticae and the impact of the plant and arthropod community on the dispersal behavior of these mites.

Predation-related odours reduce oviposition in a herbivorous mite.

When adult females of the herbivorous mite, Tetranychus urticae, were exposed to the predatory mite, Phytoseiulus persimilis, they laid fewer eggs than females that had not been exposed to P. persimilis when transferred onto a new leaf patch. However, when T. urticae females were exposed to either products of P. persimilis or artificially damaged conspecific eggs on a leaf patch, the number of T. urticae eggs on a new leaf patch did not differ significantly from the control. The reduced oviposition was neither due to the feeding activity on the leaf patch with P. persimilis nor to that on the new leaf patch. There was also no significant difference between the number of T. urticae eggs produced on a new leaf patch following exposure to the odours of a neighbouring leaf patch where there had previously been either P. persimilis or T. urticae adults. However, female T. urticae that had been exposed to odours from neighbouring leaf patches on which both T. urticae and P. persimilis had been placed produced significantly fewer eggs on a new leaf patch than those that had not been exposed to such odours. Neither odours from neighbouring intact leaf patches on which T. urticae eggs were preyed on by P. persimilis, nor odours from a neighbouring Parafilm patch on which T. urticae was preyed on by P. persimilis affected the oviposition of T. urticae. These data suggest that the presence of T. urticae, P. persimilis and a leaf patch are needed for the emission of odours to reduce oviposition in T. urticae.

Predatory interactions between prey affect patch selection by predators.

ABSTRACT: When predators can use several prey species as food sources, they are known to select prey according to foraging efficiency and food quality. However, interactions between the prey species may also affect prey choice, and this has received limited attention. The effect of one such interaction, intraguild predation between prey, on patch selection by predators was studied here. The predatory mite Neoseiulus californicus preys on young larvae of the western flower thrips Frankliniella occidentalis and on all stages of the two-spotted spider mite Tetranychus urticae. The two prey species co-occur on several plant species, on which they compete for resources, and western flower thrips feed on eggs of the spider mites. A further complicating factor is that the thrips can also feed on the eggs of the predator. We found that performance of the predatory mite was highest on patches with spider mites, intermediate on patches with spider mites plus thrips larvae and lowest on patches with thrips larvae alone. Patch selection and oviposition preference of predators matched performance: predators preferred patches with spider mites over patches with spider mites plus thrips. Patches with thrips only were not significantly more attractive than empty patches. We also investigated the cues involved in patch selection and found that the attractiveness of patches with spider mites was significantly reduced by the presence of cues associated with killed spider mite eggs. This explains the reduced attractiveness of patches with both prey. Our results point at the importance of predatory interactions among prey species for patch selection by predators. SIGNIFICANCE STATEMENT: Patch selection by predators is known to be affected by factors such as prey quality, the presence of competitors and predators, but little is known on the effects of interactions among prey species present on patch selection. In this paper, we show that patch selection by a predator is affected by such interactions, specifically by the feeding of one prey species on eggs of the other.

Predator-prey role reversals, juvenile experience and adult antipredator behaviour.

Although biologists routinely label animals as predators and prey, the ecological role of individuals is often far from clear. There are many examples of role reversals in predators and prey, where adult prey attack vulnerable young predators. This implies that juvenile prey that escape from predation and become adult can kill juvenile predators. We show that such an exposure of juvenile prey to adult predators results in behavioural changes later in life: after becoming adult, these prey killed juvenile predators at a faster rate than prey that had not been exposed. The attacks were specifically aimed at predators of the species to which they had been exposed. This suggests that prey recognize the species of predator to which they were exposed during their juvenile stage. Our results show that juvenile experience affects adult behaviour after a role reversal.

Predator avoidance in phytophagous mites: response to present danger depends on alternative host quality.

We studied whether volatiles released by putative host plants affect the antipredator response of an herbivorous mite, Tetranychus urticae, when the patch was invaded by Phytoseiulus persimilis. Tetranychus urticae laid a lower number of eggs on tomato leaves than on lima bean leaves, suggesting that lima bean is a preferred host food source for T. urticae. In addition, T. urticae preferred lima bean plant volatiles to tomato plant volatiles in a Y-tube olfactometer test. To investigate the antipredator response of T. urticae, we examined the migration of T. urticae from a lima bean leaf disc to a neighbouring leaf disc (either a tomato or lima bean leaf disc) when ten predators were introduced into the original lima bean disc. A Parafilm bridge allowed for migration between the leaf discs. No migrations occurred between leaf discs when there were no predators introduced to the original leaf disc. However, when predators were introduced migrations did occur. When the neighbouring leaf disc was upwind of the original disc, the migration rate of the mite from original lima bean leaf disc to a neighbouring tomato leaf disc was significantly lower than that to a neighbouring lima bean leaf disc. By contrast, when the neighbouring leaf disc was downwind of the original leaf disc, there was no difference in the migration rates between lima bean leaf discs and tomato leaf discs. The number of T. urticae killed by P. persimilis for each treatment was not different, and this clearly shows that the danger was the same in all treatments regardless of the decision made by T. urticae. From these results, we conclude that T. urticae change their antipredator response by evaluating the difference in host plant volatiles in the patch they inhabit.

Duration of priming of two indirect plant defenses.

When plants are infested by herbivores, they emit herbivore-induced plant volatiles (HIPVs) that attract carnivorous natural enemies of herbivores. Furthermore, there are increasing evidences that defenses of intact plants against herbivores are primed when exposed to HIPVs. We previously reported that lima bean leaf volatiles induced by the herbivorous mites Tetranychus urticae primed two T. urtiae-induced indirect defenses in neighboring conspecific plants: HIPV emission and extrafloral nectar (EFN) secretion. An intriguing unanswered question is whether the durations of these two defenses are the same. Here, we show that the durations of the two defenses were the same for up to two days after the initiation of T. urticae damage. The two induced primed defense would act as a battery of defense in exposed plants.

Herbivore-induced extrafloral nectar production in lima bean plants enhanced by previous exposure to volatiles from infested conspecifics.

In response to herbivory by spider mites (Tetranychus urticae), lima bean plants produced significantly greater quantities of extrafloral nectar (EFN) than intact conspecific plants. Moreover, EFN amounts of infested plants depended on exposure to odor of infested neighbor plants. Two d after spider mite infestation, a test plant produced more EFN when exposed prior to infestation to volatiles from infested neighbor plants than when exposed to volatiles from uninfested conspecific plants. However, this effect was only detectable 2 d after spider mite infestation and vanished 4 d after infestation. These results suggest that EFN production is enhanced during the earlier stages of damage by T. urticae in response to previous exposure to volatiles from infested neighbor plants.

Induced production of extrafloral nectar in intact lima bean plants in response to volatiles from spider mite-infested conspecific plants as a possible indirect defense against spider mites.

We found that intact lima bean plants increased the secretion of extrafloral nectar (EFN) after exposure to Tetranychus urticae-induced plant volatiles. Predatory mites, Phytoseiulus persimilis, dispersed more slowly from an exposed intact plant than from a control plant (plant exposed to volatiles from intact conspecific). The predators also dispersed more slowly from those plants that were provided with extra EFN than from untreated plants. We further show that EFN was a potential alternative food source for P. persimilis. From these results, we concluded that increased EFN was involved in the slow dispersal of P. persimilis from the plants exposed to herbivore-induced plant volatiles. Our data suggest that the increase of EFN in an HIPV-exposed intact plant could be an induced indirect defense against spider mites.

Exposure of lima bean leaves to volatiles from herbivore-induced conspecific plants results in emission of carnivore attractants: active or passive process?

There is increasing evidence that volatiles emitted by herbivore-damaged plants can cause responses in downwind undamaged neighboring plants, such as the attraction of carnivorous enemies of herbivores. One of the open questions is whether this involves an active (production of volatiles) or passive (adsorption of volatiles) response of the uninfested downwind plant. This issue is addressed in the present study. Uninfested lima bean leaves that were exposed to volatiles from conspecific leaves infested with the spider mite Tetranychus urticae, emitted very similar blends of volatiles to those emitted from infested leaves themselves. Treating leaves with a protein-synthesis inhibitor prior to infesting them with spider mites completely suppressed the production of herbivore-induced volatiles in the infested leaves. Conversely, inhibitor treatment to uninfested leaves prior to exposure to volatiles from infested leaves did not affect the emission of volatiles from the exposed, uninfested leaves. This evidence supports the hypothesis that response of the exposed downwind plant is passive. T. urticae-infested leaves that had been previously exposed to volatiles from infested leaves emitted more herbivore-induced volatiles than T. urticae-infested leaves previously exposed to volatiles from uninfested leaves. The former leaves were also more attractive to the predatory mite, Phytoseiulus persimilis, than the latter. This shows that previous exposure of plants to volatiles from herbivore-infested neighbors results in a stronger response of plants in terms of predator attraction when herbivores damage the plant. This supports the hypothesis that the downwind uninfested plant is actively involved. Both adsorption and production of volatiles can mediate the attraction of carnivorous mites to plants that have been exposed to volatiles from infested neighbors.