Potential of the predatory mite Phytoseius finitimus (Acari: Phytoseiidae) to feed and reproduce on greenhouse pests

Phytoseiid mites of the genus Phytoseius are natural enemies of tetranychid and eriophyid herbivorous mites mostly found on hairy plants where they feed on prey, as well as on pollen. Nevertheless, the nutritional ecology and the role of these predators in biological pest control are only rarely addressed. In the present study, we evaluated the potential of Phytoseius finitimus to feed and reproduce on three major greenhouse pests, the two-spotted spider mite, the greenhouse whitefly and the western flower thrips. Additionally, we estimated the effect of cattail pollen when provided to the predator alone or in mixed diets with prey. Contrary to thrips larvae, both spider mite larvae and whitefly crawlers sustained the development of P. finitimus. In addition, females consumed more spider mite eggs and larvae, as well as whitefly crawlers than thrips larvae, but laid eggs when feeding on all prey. When provided alone, cattail pollen sustained the development and reproduction of the predator. The addition of pollen in mixed diets with prey reduced prey consumption, though it increased the predator’s egg production. We discuss the implications of our findings for biological pest control.     

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.     

Host-plant species modifies the diet of an omnivore feeding on three trophic levels

The diet choice of omnivores feeding on two adjacent trophic levels (either plants and herbivores or herbivores and predators) has been studied extensively. However, omnivores usually feed on more than two trophic levels, and this diet choice and its consequences for population dynamics have hardly been studied. We report how host-plant quality affects the diet choice of western flower thrips feeding on three trophic levels: plants (cucumber or sweet pepper), eggs of spider mites and eggs of a predatory mite that attacks spider mites. Spider mites feed on the same host plants as thrips and produce a web that hampers predator mobility. To assess the indirect effects of spider mites on predation by thrips, the thrips were offered spider-mite eggs and predatory-mite eggs on cucumber or sweet pepper leaf discs that were either clean, damaged by spider mites but without spider-mite web, or damaged and webbed. We show that, overall, thrips consumed more eggs on sweet pepper, a plant of low quality, than on cucumber, a high quality host plant. On damaged and webbed leaf discs (mimicking the natural situation), thrips killed more predator eggs than spider-mite eggs on sweet pepper, but they killed equal numbers of eggs of each species on cucumber. This is because web hampered predation on spider-mite eggs by thrips on sweet pepper, but not on cucumber, whereas it did not affect predation on predatory-mite eggs. We used the data obtained to parameterize a model of the local dynamics of this system. The model predicts that total predation by the omnivore has little effects on population dynamics, whereas differential attack of predator eggs and spider-mite eggs by the omnivore has large effects on the dynamics of both mite species on the two host plants.     

Oviposition patterns in a predatory mite reduce the risk of egg predation caused by prey

Abstract 1. Predatory arthropods lay their eggs such that their offspring have sufficient prey at their disposal and run a low risk of being eaten by conspecific and heterospecific predators, but what happens if the prey attacks eggs of the predator? 2. The egg distribution and time allocation of adult female predatory mites Iphiseius degenerans as affected by predation of their eggs by prey, the western flower thrips Frankliniella occidentalis, were studied on sweet pepper plants. The predatory mites attack the first instar of thrips but all active stages of thrips are capable of killing the eggs of the predator; however the predatory mite is used for biological control of thrips. 3. The majority of predatory mite eggs was laid on the underside of leaves in hair tufts (domatia). During the experiment, females spent increasing amounts of time in flowers where they fed on pollen and thrips larvae. The risk of predation on predator eggs by thrips was lower on leaves than in flowers where the majority of thrips resides. Moreover, predation risk was higher outside leaf domatia than inside. 4. This suggests that predators avoid ovipositing in places with abundant prey to prevent their eggs from being eaten by thrips.     

Juvenile prey induce antipredator behaviour in adult predators

It is generally assumed that the choice of oviposition sites in arthropods is affected by the presence of food for the offspring on the one hand and by predation risk on the other hand. But where should females oviposit when the food itself poses a predation risk for their offspring? Here, we address this question by studying the oviposition behaviour of the predatory mite Amblyseius swirskii in reaction to the presence of its counterattacking prey, the western flower thrips Frankliniella occidentalis. We offered the mites a choice between two potential oviposition sites, one with and one without food. We used two types of food: thrips larvae, which are predators of eggs of predatory mite but are consumed by older predator stages, and pollen, a food source that poses no risk to the predators. With pollen as food, the predators preferred ovipositing on the site with food. This might facilitate the foraging for food by the immature offspring that will emerge from the eggs. With thrips as food, female predators preferred ovipositing on the site without thrips. Predators that oviposited more on the site with thrips larvae killed more thrips larvae than females that oviposited on the site without food, but this did not result in higher oviposition. This suggests that the females killed thrips to protect their offspring. Our results show that predators display complex anti-predator behaviour in response to the presence of counter-attacking prey.     

The benefits of clustering eggs: the role of egg predation and larval cannibalism in a predatory mite

Many arthropods produce clusters of eggs, but an unambiguous explanation for the evolution of egg clustering is still lacking. We test several hypotheses for the production of egg clusters by the predatory mite Iphiseius degenerans. This predator feeds on pollen, thrips larvae and nectar in flowers, but oviposits in clusters in tufts of leaf hairs (acarodomatia), where eggs run a lower risk of being killed by thrips, the prey of this predatory mite. The observed clustering is not caused by a shortage of oviposition sites; females preferably oviposit in a domatium containing eggs rather than in an empty domatium. To explain this preference, we first examined the effect of egg clusters on the risk of cannibalism. We found that eggs are invulnerable to cannibalism, whereas larvae emerging from single eggs or from clusters were equally vulnerable. Subsequently, we considered the killing of eggs resulting from counter-attacks by prey, i.e. the western flower thrips. We found no indication that a cluster of eggs protects eggs from predation by thrips. However, when eggs were clustered in a domatium rather than scattered over domatia, the proportion of eggs killed by thrips was lower. Hence, oviposition in clusters has no effect on its own and oviposition in domatia reduces predation risk by thrips, but oviposition in clusters in domatia leads to a synergistic effect on the survival of predator eggs. This synergism probably arises because eggs in clusters within tufts of leaf hairs are more difficult for thrips to reach. These experiments highlight a novel explanation of egg clustering, i.e. adaptation to counter-attacking prey. Moreover, they show that plant domatia protect predator eggs from predation.     

The effect of two prey species, Chrysomphalusaonidum and Corcyra cephalonica, on the qualityof the predatory thrips, Aleurodothripsfasciapennis, reared in the laboratory

Periodic and augmentative releases of natural enemies are often required to enhance biological control and integrated pest management programs. One requirement for these programs to be practical is that natural enemies can be easily and economically mass-reared. This study assessed the effects of dieton the quality of the F₃ and F₄laboratory-reared generations of the predatory thrips,Aleurodothrips fasciapennis. Diets were eggs and crawlers of the diaspidid scale Chrysomphalusaonidum and eggs of the pyralid moth Corcyracephalonica. It was found that both the F₃ and F₄ generations were not viable when reared on the eggs and crawlers of C. aonidum due to very low fecundity and, in the F₄ generation, increased larval mortality. In contrast, thrips reared on the eggs of C. cephalonica were viable in both generations but an increase in larval mortality from the F₃ to the F₄ generation did result in are duction in viability. These results are discussed in terms of genetic, environmental and behavioural factors that may have influenced the quality of the thrips. It is concluded that genetic factors(inbreeding suppression, genetic drift or selection),the behaviour of scale crawlers and the predatory behaviour of thrips were probably of little value in explaining the results. The most likely explanation was that the diet supplied to thrips was of in adequatenutritional quality. It was not possible to distinguish whether this was due to low intrinsic quality of the prey or an indirect effect of experimental conditions on prey quality. This revised version was published online in July 2006 with corrections to the Cover Date.     

Non-consumptive effects of predatory mites on thrips and its host plant

Recent reviews on trait-mediated interactions in food webs suggest that trait-mediated effects are as important in triggering top–down trophic cascades as are density-mediated effects. Trait-mediated interactions between predator and prey result from non-consumptive predator effects changing behavioural and/or life history traits of prey. However, in biological control the occurrence of trait-mediated interactions between predators, prey and plants has been largely ignored. Here, we show that non-consumptive predator effects on prey cascade down to the plant in an agro-ecological food chain. The study system consisted of the predatory mites P. persimilis and N. californicus , the herbivorous non-target prey western flower thrips F. occidentalis and the host plant bean. Irrespective of predator species and risk posed to prey, the presence of predator eggs led to increased ambulation, increased mortality and decreased oviposition of thrips. Furthermore, the presence of predator eggs reduced leaf damage caused by thrips. To our knowledge this is the first experimental evidence suggesting a positive trophic cascade triggered by non-consumptive predator effects on non-target prey in an augmentative biological control system.     

The Mirid Bug Dicyphus tamaninii as a Greenhouse Whitefly and Western Flower Thrips Predator on Cucumber

Dicyphus tamaninii Wagner is a polyphagous predator that also feeds on plants. Its effectiveness against several pests has been tested and good results have been obtained on tomato, but not on cucumber. This paper reports the results of three exclusion cage experiments. The first was carried out to evaluate the effectiveness of D. tamaninii for reducing greenhouse whitefly and western flower thrips populations on cucumber. The second experiment examined the safety of the mirid bug in terms of the potential for damaging cucumber fruits even at very low prey densities. Two predator (3 and 18 insects/plant) and variable prey release rates were used. The predator was able to reduce whitefly populations greatly, even at high initial pest infestation levels, especially at the higher release rate. Western flower thrips populations were maintained at very low densities a few weeks after the predator had been introduced into cages at the two release rates tested. The mirid bug was barely able to reproduce on cucumber in the absence of prey. Mirid feeding punctures on cucumber fruit or yield decrease due to the action of mirids were not observed. The potential of this mirid bug for inoculative and conservation biological control is discussed.     

Flower visitation and oviposition behavior of Frankliniella occidentalis (Tysan., Thripidae) on cucumber plants

Oviposition behaviour of western flower thrips, Frankliniella occidentalis (Pergande) on greenhouse cucumber, Cucumis satifus (L.) was investigated. Most eggs were laid in the leaves, along veins and under leaf hairs, with only a few on plant stems and flowers. Oviposition rate was higher during the day than during the night. During the day, more adult thrips were found in the flowers than during the night. The number of adult thrips per flower increased rapidly after sunrise with the highest densities occurring around noon and thereafter the number of thrips in flowers decreased during the afternoon. No differences were found in the number of larvae (first and second instars) in flowers during the same period. The number of adult thrips on male and female cucumber flowers was not different, indicating that pollen is not the only attraction in flowers for thrips.     

Predatory mites avoid ovipositing near counterattacking prey

Attacking prey is not without risk; predators may endure counterattackby the prey. Here, we study the oviposition behaviour of a predatory mite(Iphiseius degenerans) in relation to its prey, thewesternflower thrips (Frankliniella occidentalis). This thrips iscapable of killing the eggs of the predator. Thrips and predatory mites - apartfrom feeding on each other - can also feed and reproduce on a diet of pollen.Because thrips may aggregate at pollen patches, such patches may be risky foroviposition by the predatory mites. We found that, in absence of thrips,predatory mites lay their eggs close to pollen, but further away when thripsarepresent. Predatory mite eggs near pollen were killed more frequently by thripsthan when they were deposited further away. The oviposition behaviour of thepredatory mite was also studied in absence of thrips, but in presence of thealarm pheromone of thrips. This pheromone is normally secreted upon contactwithpredators or competitors. When applied close to the pollen, predatory mitesoviposited significantly further away from it. When the alarm pheromone wasapplied away from the food source, most eggs were found near the pollen. Theseresults indicate that female predatory mites show flexible ovipositionbehaviourin response to the presence of their counterattacking prey.     

Virus infection alters the predatory behavior of an omnivorous vector

The interactions between parasites and their hosts can cause profound changes in host behavior, including changes that can alter other trophic interactions. The western flower thrips Frankliniella occidentalis is an important omnivorous insect vector of Tomato spotted wilt virus (TSWV), which infects crops worldwide and also infects its thrips vector. Here, we show that tospovirus‐infected female thrips become more predaceous, illustrating how the functional role of omnivores may change in response to pathogen infection. Our findings support the hypothesis that increased predation among virus‐infected female thrips compensates for the detrimental effects of virus infection. Because predatory behavior is unlikely to increase virus transmission to plants, it is doubtful that this shift in feeding behavior is due to an adaptive parasite manipulation of vector behavior. In this study, increases in predatory behavior were observed in female thrips, but not in male thrips. This sexually dimorphic compensatory response indicates that male and female thrips utilize different feeding strategies to compensate for parasite infection, the expression of which is constrained by resource availability. Our findings demonstrate a novel, but potentially common pathway by which viruses can influence the structure of trophic interactions in food webs.     

Predation capacity of two predatory laelapid mites on soil-dwelling thrips stages

The life cycle of the Western Flower Thrips, Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae), one of the most important glasshouse pests, includes a soil passage composed of three instars that deserve more attention in terms of biocontrol strategies. It has been repeatedly reported that two polyphagous predatory mites, Stratiolaelaps miles (Berlese) and Hypoaspis (Geolaelaps) aculeifer (Canestrini) (Acari: Laelapidae), also prey on these thrips stages, in addition to several other soil inhabiting prey species. However, the potential thrips consumption rates have never been quantified for these predatory mites. Therefore, an arena experiment was carried out to investigate the potential predation rates of the two mites on second instar larvae, prepupae, and pupae of F. occidentalis. In addition, the fecundity on the thrips diet was assessed and compared to oviposition rate on a nematode prey. All thrips instars were accepted as prey by each mite species. Females of H. aculeifer preyed on 3.5 (± 0.5) thrips instars and laid 2.5 (± 0.87) eggs per day, whereas females of S. miles preyed on 1.64 (± 0.3) thrips and laid 0.8 (± 0.53) eggs. Males of both species killed 0.6 (± 0.3) thrips per day. The fitness of the two predatory mites on F. occidentalis as prey and their suitability as biocontrol agents are elucidated. Reasons for reduced thrips control in the soil environment, in contrast to the results obtained in arena assays are discussed.     

Effects of nutrients and predators on an old-field food chain: interactions of top-down and bottom-up processes

In theory, selection favours predators that select prey in order to maximise reproductive success. We studied the association between preference and performance of the generalist predator Orius laevigatus with respect to two prey species: spider mites ( Tetranychus urticae ) and western flower thrips ( Frankliniella occidentalis ). Under ample prey supply, the predators had higher maximum reproductive success (measured as intrinsic population growth rate r ) on thrips than on spider mites; hence thrips represent a higher prey quality to the bugs. This was at odds with the observed preference of the predatory bug for plants (patches) with high densities of spider mites to plants with moderate densities of thrips in release-recapture experiments. Thus, prey quality does not suffice to explain the preference of predators for plants with prey. The quality of a patch as an oviposition site (i.e. the number of eggs produced on a patch per bug per day) also did not match preference patterns. Hence, patch preference was not correlated to prey quality or oviposition rate on prey patches. However, patch productivity, i.e. the total number of offspring surviving until adulthood that can be produced by one female on a patch, was correlated with preference. This was further tested by offering the predators a choice between plants with high densities of spider mites and plants with high densities of thrips in an independent set of release-recapture experiments. These two types of prey patches were found equivalent in terms of patch productivity. Indeed, the predators showed no preference for either of the two types of patches, which is in agreement with our predictions. This suggests that the predatory bugs select patches based on patch productivity rather than on prey quality or oviposition rate on a patch.     

Biological control of aphids in the presence of thrips and their enemies

Generalist predators are often used in biological control programs, although they can be detrimental for pest control through interference with other natural enemies. Here, we assess the effects of generalist natural enemies on the control of two major pest species in sweet pepper: the green peach aphid Myzus persicae (Sulzer) and the western flower thrips Frankliniella occidentalis (Pergande). In greenhouses, two commonly used specialist natural enemies of aphids, the parasitoid Aphidius colemani Viereck and the predatory midge Aphidoletes aphidimyza (Rondani), were released together with either Neoseiulus cucumeris Oudemans, a predator of thrips and a hyperpredator of A. aphidimyza, or Orius majusculus (Reuter), a predator of thrips and aphids and intraguild predator of both specialist natural enemies. The combined use of O. majusculus, predatory midges and parasitoids clearly enhanced the suppression of aphids and consequently decreased the number of honeydew-contaminated fruits. Although intraguild predation by O. majusculus on predatory midges and parasitoids will have affected control of aphids negatively, this was apparently offset by the consumption of aphids by O. majusculus. In contrast, the hyperpredator N. cucumeris does not prey upon aphids, but seemed to release aphids from control by consuming eggs of the midge. Both N. cucumeris and O. majusculus did not affect rates of aphid parasitism by A. colemani. Thrips were also controlled effectively by O. majusculus. A laboratory experiment showed that adult predatory bugs feed on thrips as well as aphids and have no clear preference. Thus, the presence of thrips probably promoted the establishment of the predatory bugs and thereby the control of aphids. Our study shows that intraguild predation, which is potentially negative for biological control, may be more than compensated by positive effects of generalist predators, such as the control of multiple pests, and the establishment of natural enemies prior to pest invasions. Future work on biological control should focus on the impact of species interactions in communities of herbivorous arthropods and their enemies.     

Feeding and ovipositing on plants by an omnivorous insect predator

Omnivory (i.e., feeding at more than one trophic level) is common in many ecological communities. To date, most studies of omnivory have focused on systems that include omnivores that feed on several prey items, primarily in aquatic systems. Yet, many terrestrial insect predators feed not only on prey but also on plants. The difference between systems with plant-feeding omnivores and those with exclusively prey-feeding omnivores calls for special attention. The first step towards understanding the interactions between plant-feeding omnivores and their prey is to determine how omnivores respond to variations in plant properties. In this study, I investigated two major aspects of the interactions between the plant-feeding predatory bug Orius insidiosus and four host plants of its prey; the behavioral aspect, in which plants are selected for oviposition and the physiological aspect, in which plants differ in their suitability for the insect's growth, survival, and reproduction. No prey was offered to the omnivore during any of the experiments, but older nymphs and adults were fed prey eggs prior to their use in the experiments. Data show that O. insidiosus females almost completely rejected corn leaves for oviposition; nymph and adult survival was highest on bean; and female fecundity was higher on bean than tomato, pepper or corn foliage. the significance of the apparent ability of O. insidiosus to discriminate among plants and the observed correlation between oviposition preference and offspring performance in bean and in corn is discussed.     

西花蓟马在黄瓜和架豆上的空间分布型及理论抽样数

西花蓟马Frankliniella occidentalis（Pergande）已在北京部分蔬菜园区成功定居,对蔬菜生产造成危害。为了解该虫在蔬菜田的种群空间分布型,指导田间取样,本文应用几种聚集度指标的计算公式以及Taylor、Iwao的回归方程式,分析和测定了西花蓟马的种群空间分布格局。结果表明：在黄瓜和架豆上西花蓟马的空间分布型一致,均为聚集分布型;该虫的空间分布型不受种群密度的影响,并且也不随取样时间的变化而变化。种群数量动态研究显示西花蓟马成虫和若虫在黄瓜植株的中部叶片分布较多（从顶部向下数第4叶至第17叶片上成、若虫的分布数量多于其他叶片上的数量）,未展开的叶片、嫩叶和下部老叶危害较轻。用Iwao回归法中α、β参数计算出在允许误差范围内的理论抽样数。     

Host plant effects on the behaviour and performance of Amblyseius swirskii (Acari: Phytoseiidae)

Biological control in ornamental crops is challenging due to the wide diversity of crops and cultivars. In this study, we tested the hypothesis that trichome density on different host plants influences the behavior and performance of the predatory mite Amblyseius swirskii Athias-Henriot (Acari: Phytoseiidae). Behavioural observations of this predator in the presence or absence of prey (western flower thrips, Frankliniella occidentalis Pergande) (Thysanoptera: Thripidae) were done on leaf squares of ornamental plant species differing in trichome density (rose, chrysanthemum and gerbera) and compared to a smooth surface (plastic). Tomato leaves were used to observe the influence of glandular trichomes. The performance of A. swirskii was assessed by measuring predation and oviposition rate. Behaviour of A. swirskii was influenced by plant species. Up to a certain density of trichomes, trichome number had a negative effect on walking speed. It was highest on plastic, followed by rose. No differences were found among chrysanthemum, gerbera and tomato. Walking speed was slightly higher on disks without prey. Proportion of time spent walking was the same on leaf disks of all plant species, with and without prey. No effect of glandular trichomes on tomato leaves was seen. Most thrips were killed and consumed on gerbera, and least on rose. Predation rates on chrysanthemum and plastic were intermediate. In contrast, no differences in oviposition rate were found among plant species. The results of this study indicate that trichome density can explain some of the variability in efficacy of A. swirskii on different crops. Release rates of A. swirskii may need to be adjusted depending on the crop in which it is used.     

Ornamental pepper as banker plants for establishment of Amblyseius swirskii (Acari: Phytoseiidae) for biological control of multiple pests in greenhouse vegetable production

Silverleaf whitefly, Bemisia tabaci biotype B (Gennadius) (Hemiptera: Aleyrodidae), western flower thrips, Frankliniella occidentalis (Pergande), and chilli thrips, Scirtothrips dorsalis Hood (Thysanoptera: Thripidae), are key pests of vegetable crops in the US. The present study established ornamental peppers as banker plants supporting Amblyseius swirskii (Acari: Phytoseiidae) against the three pests. Specifically, this study (a) evaluated survival and population buildup of A. swirskii on three ornamental pepper varieties, Masquerade (MA), Red Missile (RM), and Explosive Ember (EE) in both laboratory and greenhouses and (b) determined the predation of A. swirskii reared on ornamental pepper plants to the targeted pests under greenhouse conditions. The results showed that the three pepper varieties were excellent banker plants and able to support at least ∼1000 of all stages of A. swirskii per plant in greenhouse conditions and allow them to complete their life cycle. A. swirskii dispersed or released from the banker plants to target plants, resulting in significant suppression of the three pests, i.e., after 14 d post-release, a significantly lower average of 2.75 B. tabaci and 13.4 all stages of thrips (chilli thrips and western flower thrips) were found per bean plant, respectively, compared to 379.5 B. tabaci and 235.4 all stages of thrips per plant in the control. Furthermore, our experiment observed that the sweet pepper seedlings closed to banker plants were healthy, whereas those without banker plants were heavily infested by chilli thrips; their growth seriously stunted or died. This is the first report of ornamental pepper as banker plants supporting A. swirskii against three notorious pests. This established banker plant system could be a new addition to the integrated pest management programs for sustainable control of these three pests in greenhouse vegetables.     

Diet-dependent effects of gut bacteria on their insect host: the symbiosis of Erwinia sp. and western flower thrips

Studies on bacteria in the gut of insect species are numerous, but their focus is hardly ever on the impact on host performance. We showed earlier that Erwinia bacteria occur in the gut of western flower thrips, most probably acquired during feeding. Here, we investigate whether thrips gain a net benefit or pay a net cost because of these gut bacteria. On a diet of cucumber leaves, the time to maturity is shorter and the oviposition rate is higher in thrips with bacteria than in thrips without (aposymbionts). When fed on cucumber leaves and pollen, aposymbionts develop faster and lay more eggs. So Erwinia bacteria benefit or parasitize their thrips hosts depending on the diet, which is in accordance with theoretical predictions for fitness of organisms engaged in symbiotic interactions. Possibly, the transmission of gut bacteria has not become strictly vertical because of this diet-dependent fitness variability.