Xiao-Ling Tan

Aphid-induced plant volatiles affect the attractiveness of tomato plants to Bemisia tabaci and associated natural enemies

An in‐depth understanding of plant‐mediated interactions between herbivores and their natural enemies is essential in community ecology and co‐evolution, and for developing sustainable pest management strategies. The influence of Myzus persicae (Sulzer) (Hemiptera: Aphididae)‐induced tomato plant [Solanum lycopersicum L. (Solanaceae)] volatile compounds on the olfactory responses of Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae), three predator species [Coccinella septempunctata L., Propylea japonica (Mulstant) (both Coleoptera: Coccinellidae), and Orius sauteri (Poppius) (Hemiptera: Anthocoridae)], two whitefly parasitoid species [Encarsia formosa (Gahan) and Encarsia sophia (Girault & Dodd) (Hymenoptera: Aphelinidae)], and one aphid parasitoid species [Aphidius gifuensis Ashmead (Hymenoptera: Aphidiidae)] were examined in two‐choice tests using a four‐arm olfactometer. Tomato plants were experimentally manipulated for aphid density, duration of aphid feeding, and interval between aphid removal and the behavioral test. We also compared the systemic effects of aphid feeding on the olfactory behavior of whiteflies and natural enemies according to three relative leaf positions: the aphid‐infested leaf itself and two adjacent leaves (above and below). Bemisia tabaci were deterred by the odors of the leaves infested with aphids in all treatments. All six natural enemies were attracted to the leaves infested with aphids. Bemisia tabaci deterrence by volatiles was greater for leaves at the highest aphid density, and with increasing duration of exposure to aphid feeding. In contrast, the attraction to leaves was greater for the three parasitoids than for the three predators both with increasing aphid density and increasing duration of plant exposure to aphids. There was no significant influence of leaf position on preference of B. tabaci, the two species of lady beetles, and the aphid parasitoid. The two Encarsia species were attracted to the leaf above the aphid‐infested leaves, indicating that systemic volatiles were released by adjacent leaves. On the other hand, O. sauteri was only attracted by the aphid‐infested leaf itself. Our results showed that M. persicae‐infested host plants emitted volatiles that could inhibit the colonization by B. tabaci and also attract natural enemies of both aphids and whiteflies. The results of this study may need to be considered further for optimizing pest management methods.

Effect of temperature and photoperiod on the development, reproduction, and predation of the predatory ladybird Cheilomenes sexmaculata (Coleoptera: Coccinellidae).

ABSTRACT The polyphagous predatory ladybird Cheilomenes sexmaculata (F.) (Coleoptera: Coccinellidae) is distributed throughout southern China and has been investigated as a potential biological control agent against herbivorous insects in various agroecosystems. In the current study,weevaluated the preimaginal development, eclosion rate, reproduction, fertility, adult longevity, and prey consumption of C. sexmaculata under five temperature and five photoperiod regimens. The results showed that preadult developmental duration decreased significantly with increasing temperature and amount of daylight. Adult eclosion rate was highest at 35°C and under conditions of complete darkness. Higher temperatures shortened the duration of copulation and preoviposition, prolonged the duration of oviposition, and increased the level of fecundity. Hatchability was highest at 30°C . By contrast, the shortest copulation and oviposition duration and lowest level of fecundity and hatchability occurred with a completely dark photoperiod. Temperature and the gender of C. sexmaculata influenced adult longevity. In addition, there was a significant interaction effect of photoperiod and gender on adult longevity. Furthermore, prey consumption by fourth instar larvae and adult females both increased with increasing temperature and photoperiod. Our results reveal the high thermal and light sensitivities of C. sexmaculata, which highlight the importance of environment regulation in the mass rearing of this natural enemy for application as a biological control in agroecosystems in China.

Optimization and evaluation of microencapsulated artificial diet for mass rearing the predatory ladybird propylea japonica (Coleoptera: Coccinellidae)

Artificial diet optimization is a key aspect in mass rearing of natural enemies since it influences the quality and feeding effectiveness, and thus the success of the biological control program. Here, we introduced the microencapsulation method to package liquid artificial diet for feeding of the ladybird Propylea japonica. An orthogonal test of the quality of microencapsulated artificial diets (ADMs) was performed on key variables in production; Ca‐alginate concentration, chitosan concentration and weight ratio of wall material to inner diet. We compared the development and reproduction of P. japonica fed on the ADMs under different cold‐stored periods with those fed on fresh aphids and liquid artificial diets, in addition to a comparison of respiration, locomotion and predation. Our results indicated that chitosan concentration and ratio of shell to core significantly influence the quality of ADMs. The optimal recipe is 1.0% Ca‐alginate, 1.6% chitosan and shell : core = 1 : 2. Insects reared on fresh optimized ADMs were similar to those fed on fresh prey in all developmental and reproductive characteristics except for survival ratio and female fertility. ADMs appeared more beneficial than using a liquid artificial diet, although this may decrease with the prolonging of the cold‐storage period. P. japonica fed either on fresh ADMs or fresh prey showed improved respiration and predation abilities compared to where liquid artificial diet was used. Our study indicates advantages of microencapsulation in the production of artificial diet for predatory ladybird rearing. A microencapsulated diet can directly increase the efficiency and stability of mass rearing.

Mixed release of two parasitoids and a polyphagous ladybird as a potential strategy to control the tobacco whitefly Bemisia tabaci.

A mixed species release of parasitoids is used to suppress outbreaks of tobacco whitefly, Bemisia tabaci (Hemiptera: Aleyrodidae); however, this biocontrol may be inhibited by interspecific interactions. We investigated the effects of mixed releases of natural enemies of B. tabaci on predation rates, parasite performance and adult parasitoid emergence under greenhouse conditions. We tested the polyphagous predatory ladybird Harmonia axyridis (Coleoptera: Coccinellidae) and two whitefly-specific parasitoids, namely Encarsia formosa and Encarsia sophia (both, Hymenoptera: Aphelinidae). Harmonia axyridis exhibited the lowest rates of predation when released with each parasitoid than with both parasitoid species together and showed a significant preference for non-parasitized nymphs as prey. Both E. formosa and E. sophia parasitized more B. tabaci when released with the ladybird than when the wasps were released either alone or mixed with the other parasitoid. We also found that the presence of H. axyridis significantly reduced adult parasitoid emergence; the highest rate of adult emergence was obtained with parasitoids released alone. Our results indicate that different combinations of natural enemies can influence observed rates of predation, parasitism, and parasitoid emergence. Therefore, the combination of natural enemies to be used for a particular biological control program should depend on the specific objectives.

Direct and indirect impacts of infestation of tomato plant by Myzus persicae (Hemiptera: Aphididae) on Bemisia tabaci (Hemiptera: Aleyrodidae).

The impacts of infestation by the green peach aphid (Myzus persicae) on sweetpotato whitefly (Bemisia tabaci) settling on tomato were determined in seven separate experiments with whole plants and with detached leaves through manipulation of four factors: durations of aphid infestation, density of aphids, intervals between aphid removal after different durations of infestation and the time of whitefly release, and leaf positions on the plants. The results demonstrated that B. tabaci preferred to settle on the plant leaves that had not been infested by aphids when they had a choice. The plant leaves on which aphids were still present (direct effect) had fewer whiteflies than those previously infested by aphids (indirect effect). The whiteflies were able to settle on the plant which aphids had previously infested, and also could settle on leaves with aphids if no uninfested plants were available. Tests of direct factors revealed that duration of aphid infestation had a stronger effect on whitefly landing preference than aphid density; whitefly preference was the least when 20 aphids fed on the leaves for 72 h. Tests of indirect effects revealed that the major factor that affected whitefly preference for a host plant was the interval between the time of aphid removal after infestation and the time of whitefly release. The importance of the four factors that affected the induced plant defense against whiteflies can be arranged in the following order: time intervals between aphid removal and whitefly release > durations of aphid infestation > density of aphids > leaf positions on the plants. In conclusion, the density of aphid infestation and time for which they were feeding influenced the production of induced compounds by tomatoes, the whitefly responses to the plants, and reduced interspecific competition.

Does a multi-plant diet benefit a polyphagous herbivore? A case study with Bemisia tabaci

Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) is a highly polyphagous herbivore. This research was conducted to compare the development of B. tabaci reared in a multi‐plant treatment (polyculture) with those in single‐plant treatments (monocultures). Adult B. tabaci females fed on a mixture of tomato, cabbage, cotton, cucumber, and kidney bean survived longer and laid more eggs than those fed exclusively on one of these plant species. Egg numbers per plant laid in the polyculture treatment were positively correlated with those laid on the same plant species in the monoculture treatments, and egg numbers per plant laid on tomato, cotton, and cucumber in the polyculture were significantly higher than those laid on the same plants in the monocultures. Concentrations of total protein and trehalose in B. tabaci were not significantly different after 7 days of feeding in the respective treatments, but activities of superoxide dismutases (SOD) and alkaline phosphatase (AKP) of B. tabaci in polyculture were lower than those in monoculture. Conversely, activities of trehalase, sucrase, and amylase in B. tabaci kept in polyculture were higher than those of insects from the monoculture. In each of the monoculture treatments, there was a negative correlation between AKP in B. tabaci and oviposition, and also between AKP and amylase. SOD and sucrase activities in B. tabaci were positively correlated with polyphenol oxidase (PPO) and peroxidase (POD) activities in plants. In the plants damaged by whiteflies in the polyculture treatment, activities of SOD in cucumber, PPO in cotton and kidney bean, and POD in tomato and cucumber were lower than those in the monoculture treatments, whereas SOD in cabbage and catalase (CAT) in tomato in the polyculture treatment were higher than those in the monoculture treatments.

Acceptance and suitability of four plant substrates for rearing Orius sauteri (Hemiptera: Anthocoridae)

Orius sauteri (Poppius) is an important hemipterous predator that has been mass-reared for biological control of numerous pests in protected crop-production systems. To find a good oviposition substrate for mass-rearing this predator under insectary conditions [25°C, 65 ± 5% relative humidity, and a photoperiod of 16:8 (L:D) h], we compared kidney bean, soybean, broad bean sprouts and fresh leaves of kidney bean. We found that O. sauteri made more punctures and laid more eggs in kidney bean sprouts than in the other substrates examined. However, there were no significant differences among substrates in the proportion of punctures receiving eggs. Female O. sauteri laid the most eggs (as many as 68 eggs) in kidney bean sprouts and also had the shortest pre-oviposition period on this plant material. In addition, there were no significant differences in total oviposition durations or female longevity among the four plant substrates. The hatch rates of nymphs in the sprouts and leaves of kidney bean (>90%) were higher than those in soybean and broad bean sprouts. Thus, we found that the kidney bean sprout was the most suitable substrate for mass-rearing of O. sauteri.

Optimization an Optimal Artificial Diet for the Predatory Bug Orius sauteri (Hemiptera: Anthocoridae)

Background The flower bug Orius sauteri is an important polyphagous predator that is widely used for the biological control of mites and aphids. However, the optimal conditions for mass rearing of this insect are still unclear, thus limiting its application. Methodology In this study, we investigated the optimal ingredients of an artificial diet for raising O. sauteri using a microencapsulation technique. The ingredients included egg yolk (vitellus), whole-pupa homogenate of the Tussah silk moth (Antheraea paphia), honey, sucrose, rapeseed (Brassica napus) pollen and sinkaline. We tested 25 combinations of the above ingredients using an orthogonal experimental design. Using statistical analysis, we confirmed the main effect factors amongst the components, and selected five optimal combinations based on different biological and physiological characters. Principal Findings The results showed that, although different artificial diet formats significantly influenced the development and reproductive ability of O. sauteri, the complete development of O. sauteri to sexual maturity could only be achieved by optimizing the artificial diet according to specific biological characters. In general, pupae of A. paphia had more influence on O sauteri development than did artificial components. The results of a follow-up test of locomotory and respiratory capacity indicated that respiratory quotient, metabolic rate and average creeping speed were all influenced by different diets. Furthermore, the field evaluations of mating preference, predatory consumption and population dispersion also demonstrated the benefits that could be provided by optimal artificial diets. Conclusions A microencapsulated artificial diet overcame many of the difficulties highlighted by previous studies on the mass rearing of O. sauteri. Optimization of the microencapsulated artificial diet directly increased the biological and physiological characters investigated. Successive physiological tests and field investigations were used to evaluate the outcome of different artificial diet combinations on the quality of the reared O. sauteri.

Using Calendula officinalis as a floral resource to enhance aphid and thrips suppression by the flower bug Orius sauteri (Hemiptera: Anthocoridae)

BACKGROUND The flower bug Orius sauteri (Poppius) (Hemiptera: Anthocoridae) is widely used as a biocontrol agent against thrips and aphids infesting greenhouse vegetables in Asia. The survival and oviposition of such predators, as well as the biocontrol services they provide, may be enhanced by adding extra floral resources to the crops. In the present study we investigated the effects of the plant Calendula officinalis L., used as a floral resource, for promoting the control of Myzus persicae (Sulzer) and Frankliniella occidentalis (Pergande) by O. sauteri under laboratory and greenhouse conditions. RESULTS Results showed that the presence of C. officinalis enhanced aphid and thrips suppression via an increased O. sauteri population growth. The predator populations responded positively to the addition of C. officinalis in the system, and they also varied as a function of the temperatures tested under laboratory conditions. In a similar way, predator populations varied among seasons, with the highest densities recorded in May in the greenhouse. CONCLUSION C. officinalis can be used to increase available resources for natural enemies used in agricultural crops, notably in greenhouses. This study also provides evidence that increasing floral resources can enhance pest suppression provided by O. sauteri.

Innate positive chemotaxis to pollen from crops and banker plants in predaceous biological control agents: towards new field lures?

Predator-prey interactions form the core of biological control of arthropod pests. Which tools can be used to monitor and collect carnivorous arthropods in natural habitats and targeted crops? Eco-friendly and effective field lures are urgently needed. In this research, we carried out olfactometer experiments assess innate positive chemotaxis to pollen of seven crop and banker plant by two important predatory biological control agents: the coccinellid Propylea japonica (Thunberg) and the anthocorid Orius sauteri (Poppius). We compared the attractiveness of pollens from crops and banker plants to that of common prey homogenates (aphids and thrips, respectively). Attractiveness of the tested odor sources was checked via field trapping experiments conducted in organic apple orchards and by release-recapture assays in organic greenhouse tomato crops. Maize and canola pollen were attractive to both P. japonica and O. sauteri, in laboratory and field assays. P. japonica was highly attracted by balm mint pollen, whereas O. sauteri was attracted by alfalfa pollen. Our results encourage the use of pollen from crops and banker plants as low-cost and eco-friendly attractors to enhance the monitoring and attraction of arthropod predators in biological control programs.