Correction to: Cleome hassleriana plants fully support the development and reproduction of Nesidiocoris tenuis

BioControl - A correction to this paper has been published: https://doi.org/10.1007/s10526-021-10089-4     

Zoophytophagy in the plantbug Nesidiocoris tenuis

1 The zoophytophagy of Nesidiocoris tenuis (Reuter) (Heteroptera: Miridae) was characterized in relation to prey availability and environmental factors by: (i) monitoring its population dynamics in tomato greenhouses; (ii) analysis of the influence of N. tenuis and whitefly density, temperature and humidity on the intensity of N. tenuis plant feeding; and (iii) laboratory assays under controlled conditions to determine the intensity of plant feeding in relation to prey availability, temperature and humidity. 2 A negative relationship was found between plant feeding and predated whiteflies in tomato greenhouses. Plant feeding was directly related to N. tenuis density and temperature and inversely related to whitefly density. The significance of prey availability and temperature was corroborated in laboratory assays. The intensification of plant feeding at low prey density indicates switching from zoophagy to phytophagy as prey become scarce. 3 Nesidiocoris tenuis showed a typical predator dynamic in relation to variance in prey density. Populations increased after whitefly outbreaks and decreased after whitefly had been depleted. The rapid decrease of N. tenuis populations after whitefly decreased, however, suggests that plants are a poorer nutrient source than whitefly for this species.     

Effects of an alternative diet of Artemia cysts on the development and reproduction of Nesidiocoris tenuis (Hemiptera: Miridae)

The small green mirid Nesidiocoris tenuis Reuter (Hemiptera: Miridae) preys on pest insects such as whiteflies and serves as a biological control agent in many greenhouses. However, this mirid is limited in its application, because individuals tend to escape from agricultural fields and soon die due to a lack of available food sources. In addition, the food traditionally used to culture N. tenuis is expensive. Thus, identifying low-cost foods for N. tenuis would help to increase the species’ further utilization. Brine shrimp (Artemia spp., Anostraca: Artemiidae) cysts are potentially useful as a low-cost alternative diet to sustain populations of predatory natural enemies. We evaluated the developmental and reproductive performance of N. tenuis when reared on Artemia salina L. cysts supplied in dry or wet form. The dry cysts showed a similar performance to that of Mediterranean flour moth (Ephestia kuehniella Zeller, Lepidoptera: Pyralidae) eggs, which are often used as a nutritional diet for mass rearing of N. tenuis. Although the wet cysts contributed to growth, compared to other diets, they were inferior in nymphal development time and longevity. These results suggest that relatively inexpensive Artemia dry cysts can be used to successfully breed N. tenuis and sustain populations in crop fields.

     

Plantless rearing of the zoophytophagous bug Nesidiocoris tenuis

Nesidiocoris tenuis Reuter (Heteroptera: Miridae) is widely distributed in the Mediterranean area, where it is used as an augmentative biological control agent of several pests. This zoophytophagous predator maintains a close relationship with its host plants using them not only to feed on, but also as an oviposition substrate. In the present study, a plantless rearing system was developed and developmental and reproductive parameters of bugs that had no access to plant material were compared with their counterparts living on plants. Eggs deposited in an artificial substrate took longer to develop and had lower hatching rates than those laid in tomato leaves. However, the biological parameters of nymphs that had hatched from the artificial substrate did not differ from those of nymphs that had emerged from plants, suggesting that, besides water, no essential nutrients are absorbed from the oviposition substrate during embryogenesis. Our results regarding the role of plant feeding indicate that water acquisition is the critical function of phytophagy in N. tenuis. In addition, supplementary nutrients derived from plants had a positive effect on adult weight and significantly enhanced survival in the absence of prey. Plantless rearing for five generations led to a prolonged preoviposition period and lower egg hatching rates and adult weights, but other developmental and reproductive parameters were not adversely affected. Our experiments suggest that prolonged plantless rearing of N. tenuis is possible provided that the mirid has access to a nutritionally superior food like Ephestia kuehniella eggs.     

Nutritional variations at Nesidiocoris tenuis feeding sites and reciprocal interactions between the mirid and tomato plants

Nesidiocoris tenuis (Reuter) (Hemiptera: Miridae) uses a flush‐and‐lacerate feeding strategy producing necrotic rings (NR) at feeding sites in tomato plants. The aim was to investigate the variation in the concentrations of amino acids (aa) and sugars at feeding sites, and its effect on this mirid's life‐history traits and behaviour. The concentration of nutrients was measured in different parts of stems damaged by N. tenuis and mechanically using liquid chromatography. aa concentrations increased below NR; around and above NR, the concentrations of essential and non‐essential aa declined. The concentration of glucose was lower around NR and below. The change in the distribution of aa was similar in NR and mechanically damaged stems, whereas there were no differences in sugar contents. Development time and nymphal mortality were measured on fresh leaflets, leaflets with NR and leaflets plus Ephestia kuehniella Zeller (Lepidoptera: Pyralidae). Without prey, development took longer on NR than on fresh leaflets. Development was quicker and mortality lower on leaflets plus moth eggs. Finally, behavioural events were recorded in fifth‐instar nymphs of N. tenuis in: (i) double‐choice experiments (DCE) using leaflets with and without NR; (ii) DCE using leaflets exposed and non‐previously exposed to nymphs and (iii) fresh tomato leaflets plus Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) nymphs. In (i), feeding events lasted longer at NR sites; in (ii), the behaviour of the nymphs on previously exposed leaflets was not significantly different from fresh leaflets; and in (iii), most of the time was dedicated to prey feeding. The overall results indicate that N. tenuis do not take advantage of the inhibited translocation of nutrients in the phloem. The poorer performance of nymphs on leaflets from plants previously exposed to N. tenuis might be due to a general decrease in the concentration of nutrients or to the activation of plant defences.     

Tracking the movement of Nesidiocoris tenuis among banker plants and crops in a tomato greenhouse by DNA markers of host plants

The zoophytophagous predator, Nesidiocoris tenuis (Reuter) (Hemiptera: Miridae), is an important biological control agent. To maintain this insect, several non-crop host plants are used as banker plants in greenhouse crop systems. To optimize the efficiency of the predator-banker plant interaction, it is necessary to investigate how individual predators move between banker plants and crops. However, the movement is difficult to quantify under field conditions. Therefore, we investigated the movement of N. tenuis between tomato plants (Solanum lycopersicum L., Solanales: Solanaceae) and three banker plants (Cleome hassleriana Chod., Brassicales: Cleomaceae; Sesamum indicum L., Lamiales: Pedaliaceae; and Verbena × hybrida Voss, Lamiales: Verbenaceae) in a greenhouse by conducting PCR using plant-species-specific primers. Laboratory analysis results showed that our molecular method could detect N. tenuis activity within a relatively short time (≤ 24 h). In addition, N. tenuis predation on a pest species was unlikely to result in false detection of plant DNA in the pest (suggesting that N. tenuis had been on the plants). Multiple plant species were detected in adult insects collected from the greenhouse plants, indicating that N. tenuis frequently moved across the mentioned plant species. The movement patterns of N. tenuis between plant species varied substantially based on the plant species from which they were collected, which suggested each of the plant species had different functions for N. tenuis. Our findings revealed that planting multiple host plants would stabilize the N. tenuis population in biological control programs.

     

Geographic variation in thermal and photoperiodic effects on development of zoophytophagous plant bug Nesidiocoris tenuis

The zoophytophagous plant bug Nesidiocoris tenuis (Reuter) is increasingly used for biological control of various agricultural pests. Its native range includes Southern Europe, North Africa, Southern and South‐Eastern Asia, although only the Mediterranean strains have been studied experimentally. We investigated effects of temperature and photoperiod on nymphal survival and development, rate of female maturation and egg load in two strains of N. tenuis originating from temperate and subtropical regions of South‐Eastern Asia: the ‘Temperate strain’ (from Suwon, Republic of Korea, yearly average air temperature is 13.3°C) and the ‘Subtropical strain’ (from Miyazaki, Japan, yearly average air temperature is 18.2°C). Nymphs and adults were reared on tomato leaflets and fed with eggs of the grain moth Sitotroga cerealella under four temperatures (15, 20, 25 and 30°C) and three photoperiods (10, 12 and 14 h of light per day). In spite of long‐term (40–50 generations) rearing under constant laboratory conditions, the studied strains still show a correlation between thermotolerance indices and climate at origin. In particular, at the low temperature of 15°C, survival of nymphs of the Temperate strain was double that of the Subtropical strain, whereas at the higher tested temperatures, survival of the Subtropical strain was not significantly different or even was higher than that of the Temperate strain. The duration of nymphal development in the Temperate strain was significantly shorter than that in the Subtropical strain at 15–25°C, but not at 30°C. In both strains, nymphal survival, duration of nymphal development and rate of female maturation were not significantly dependent on photoperiod, and diapause was not observed under any conditions tested. We conclude that the Subtropical strain of N. tenuis is better adapted to high temperatures, whereas the Temperate strain is more promising for application in greenhouses at medium and low temperatures.     

Sugar as nutritional supplement for the zoophytophagous predator Nesidiocoris tenuis

Nesidiocoris tenuis (Reuter) (Hemiptera: Miridae) is a zoophytophagous predator widely used in integrated pest management programs in both greenhouse and open-field tomato crops. Mass rearing of N. tenuis is greatly dependent on Ephestia kuehniella Zeller (Lepidoptera: Pyralidae) eggs as food source. Moreover, the addition of this factitious prey after the inoculative releases of N. tenuis under field conditions is recommended to facilitate establishment of this mirid. However, E. kuehniella eggs are expensive and availability is limited. One possible strategy to reduce the amount of E. kuehniella eggs needed is the provision of sugar. In this work, the effect of sucrose as nutritional supplement on selected life-history traits of N. tenuis was studied. The addition of sucrose (0.5 M) ad libitum to a diet of E. kuehniella eggs significantly increased the progeny of N. tenuis and did not affect survival of nymphs nor developmental time. Moreover, addition of sucrose significantly reduced the number of E. kuehniella eggs consumed. These results may have practical implications of interest in mass rearing systems of N. tenuis and its management in fields and greenhouses as a part of biological control programs.     

烟盲蝽用芝麻饲养的效果及捕食能力评估

烟盲蝽Nesidiocoris tenuis是一种杂食性天敌昆虫。本研究通过比较芝麻饲养和补充烟粉虱Bemisia tabaci猎物饲养烟盲蝽的生物学特征,评估了用芝麻人工饲养烟盲蝽的饲养效果和该种群对自然猎物的捕食能力。结果显示,用芝麻饲养的烟盲蝽若虫发育历期较长,成虫后足胫节长度较小。然而,烟盲蝽的雌性比例、存活率、成虫生殖力以及对烟粉虱和烟蚜的捕食量没有显著差异。两个种群连续繁殖10代时,芝麻饲养的烟盲蝽种群的内禀增长率为0.2152,与补充猎物饲养的烟盲蝽种群的内禀增长率0.2398相近。以上结果表明,仅用芝麻提供营养可以进行烟盲蝽的人工饲养,并且这种方法为烟盲蝽的规模化饲养和基于芝麻种植的田间饲养模式的建立提供了参考依据。     

Response of the zoophytophagous predators Macrolophus pygmaeus and Nesidiocoris tenuis to volatiles of uninfested plants and to plants infested by prey or conspecifics

Knowledge about the orientation mechanisms used by two important predaceous mirids (Macrolophus pygmaeus Rambour and Nesidiocoris tenuis (Reuter)) in finding their prey (whitefly Bemisia tabaci (Gennadius) and the tomato borer Tuta absoluta (Meyrick)) is limited. In a Y-tube olfactometer, we tested the behavioral responses of naïve and experienced predators to uninfested plants, herbivore-induced plant volatiles (HIPVs) from plants infested with T. absoluta and/or B. tabaci, the sex pheromone of T. absoluta, and volatiles produced by plants injured by the predators. Nesidiocoris tenuis responds to volatiles produced by uninfested plants only after experience with the plant, whereas naïve and experienced M. pygmaeus show positive chemotaxis. Both predators are attracted to volatiles from prey-infested plants, and we provide the first evidence that experience affects this response in M. pygmaeus. Infestation of the same plant by both prey species elicited similar responses by the two predators as plants infested by either herbivore singly. Neither predator responded to sex pheromones of T. absoluta. Macrolophus pygmaeus avoided plants injured by conspecifics, while N. tenuis females were attracted by such plants. The implications of these results for augmentative biological control are discussed.     

Sampling of Nesidiocoris tenuis (Heteroptera: Miridae) in tomato crops

The number of N. tenuis on the upper, middle, and bottom leaves of tomato plants was correlated; nymphs were most abundant on middle and adults on upper leaves. The dispersion pattern of N. tenuis is aggregated and can be described using a negative binomial distribution. A binomial sampling method is proposed.     

烟盲蝽对不同虫态烟粉虱的捕食作用及捕食偏好性

杂食性昆虫烟盲蝽Nesidiocoris tenuis是烟粉虱Bemisia tabaci的重要天敌之一。为探索烟盲蝽对不同虫态烟粉虱的捕食作用及捕食偏好性,在室内进行了非选择性和选择性试验。结果表明,在非选择性试验中,烟盲蝽雌成虫、雄成虫以及5龄若虫可以捕食烟粉虱成虫和各龄若虫,但极少捕食卵。其中,烟盲蝽雌成虫、雄成虫及5龄若虫对烟粉虱1龄若虫的捕食量最大,分别为134.2头、101.3头和88.1头,其次是2~3龄若虫,捕食量分别为94.1头、64.2头和53.4头。而在选择性试验中烟盲蝽雄虫更偏好捕食烟粉虱的2~3龄若虫,其次是1龄若虫、4龄若虫和成虫。该结果对了解烟盲蝽控制烟粉虱的作用以及如何对烟盲蝽和其他天敌组合应用提供了参考信息。     

Sugars as complementary alternative food for the establishment of Nesidiocoris tenuis in greenhouse tomato

Nesidiocoris tenuis (Reuter) (Hemiptera: Miridae) is an omnivorous generalist predator which is augmentatively released and conserved for control of whiteflies (Hemiptera: Aleyrodidae) and Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) in tomato crops. Eggs of Ephestia kuehniella Zeller (Lepidoptera: Pyralidae) are often provided as factitious prey to improve the establishment of N. tenuis after its release. We first tested different amounts of E. kuehniella eggs per plant to optimize N. tenuis establishment and then investigated whether the amount of eggs that optimized N. tenuis establishment might be reduced by adding sugars (hydrocapsules filled with 0.5 m sucrose) under walk‐in cage and commercial greenhouse conditions. These experiments demonstrated that the addition of sugar to the diet of N. tenuis could half the amount of E. kuehniella eggs required to establish N. tenuis. Under greenhouse conditions, the progeny of N. tenuis per plant did not differ significantly between E. kuehniella alone or the half amount of E. kuehniella plus hydrocapsules. These results demonstrated that the sugar could partially substitute for E. kuehniella eggs improve establishment of N. tenuis and suggest that natural sugars such as nectar and honeydew might also beneficial.     

Efficacy of sulphur on Tuta absoluta and its side effects on the predator Nesidiocoris tenuis

The South American tomato pinworm, Tuta absoluta (Meyrick), is one of the major pests of tomato crop. Since its detection in the Mediterranean basin, it has been commonly controlled using chemical insecticides. However, inoculation and conservation of predatory mirids, integrated with sprays of selective insecticides, has been demonstrated to be a cost‐effective strategy for controlling this pest. In this work, we tested the efficacy of two sulphur formulations, dustable and wettable powder, for controlling T. absoluta on tomato under greenhouse and open‐field conditions. In addition, the side effects of both sulphur formulations on the predator, Nesidiocoris tenuis (Reuter), were evaluated under laboratory conditions. Dustable sulphur, applied weekly on tomato seedlings artificially infested with T. absoluta in greenhouse conditions, significantly reduced the infestation levels and was demonstrated to have a repellent effect on oviposition. Wettable sulphur was not effective for controlling T. absoluta populations in both greenhouse and open‐field experiments. In the side effect trials conducted with N. tenuis, only dustable sulphur resulted in being moderately harmful as a fresh residue and slightly harmful as a 7‐day‐old residue; no effects were recorded exposing the predator to 14‐day‐old sulphur residues. In contrast, wettable sulphur was classified as harmless to N. tenuis. Our results suggest that the use of sulphur, especially as dustable powder, could be considered as a tool in T. absoluta management strategies, although its side effects on N. tenuis should be taken into account. The implications of these results for the use of sulphur formulations in pest and disease management programmes in tomato crops are discussed.     

Suitability of the tomato borer Tuta absoluta as prey for Macrolophus pygmaeus and Nesidiocoris tenuis

The tomato borer, Tuta absoluta (Meyrick) (Lep.: Gelechiidae), is an important tomato pest native to South America, which appeared in eastern Spain at the end of 2006. Prey suitability of T. absoluta eggs and larval instars was examined under laboratory conditions to evaluate whether two indigenous predators, Macrolophus pygmaeus (Rambur) and Nesidiocoris tenuis Reuter (Hem.: Miridae), can adapt to this invasive pest. Both predators preyed actively on T. absoluta eggs and all larval stages, although they preferred first‐instar larvae. Our results demonstrate that both mirids can adapt to this invasive pest, contributing to their value as biological control agents in tomato crops.     

Morphological structure of the antennal sensilla of Nesidiocoris tenuis observed with a scanning electron microscope

烟盲蝽Nesidiocoris tenuis (Reuter)作为一种杂食性昆虫,是蔬菜害虫的重要捕食者.利用扫描电镜对烟盲蝽雌雄成虫的触角进行观察,结果表明:烟盲蝽触角由基节、柄节、梗节和鞭节组成.绝大部分触角感器位于触角的腹面和外侧面.触角感器共有9种,分别为毛形感器、刺形感器、锥形感器、钟形感器、腔锥形感器、具弯钩形感器、腔形感器、乳形感器和Bǒhm氏鬃毛.腔锥形感器仅见于雌性触角,其他8种感器在雌雄两性触角上的类型和分布没有明显的区别.     

烟盲蝽成虫触角感器的扫描电镜观察

烟盲蝽Nesidiocoris tenuis(Reuter)作为一种杂食性昆虫,是蔬菜害虫的重要捕食者。利用扫描电镜对烟盲蝽雌雄成虫的触角进行观察,结果表明:烟盲蝽触角由基节、柄节、梗节和鞭节组成。绝大部分触角感器位于触角的腹面和外侧面。触角感器共有9种,分别为毛形感器、刺形感器、锥形感器、钟形感器、腔锥形感器、具弯钩形感器、腔形感器、乳形感器和Bhm氏鬃毛。腔锥形感器仅见于雌性触角,其他8种感器在雌雄两性触角上的类型和分布没有明显的区别。     

Intraguild predation and sublethal interactions between two zoophytophagous mirids,Macrolophus pygmaeus and Nesidiocoris tenuis

The omnivorous predators Macrolophus pygmaeus and Nesidiocoris tenuis (Hemiptera: Miridae) are important biological control agents of pests on tomato crops. In this study, potential intraguild predation (IGP) interactions between the two species were investigated on tomato. We examined: (a) the within plant distribution of both species in the field, (b) the within plant distribution of each predatory species when co-occurred at high densities on tomato caged plants, (c) their behavioral interactions when enclosed in experimental arenas and (d) the development young and old nymphs of M. pygmaeus when enclosed together with N. tenuis adults. Results revealed that the two predators showed a different distribution pattern on the plants, with N. tenuis exploiting mostly the upper part, whereas M. pygmaeus were mostly observed on the 5th to the 7th leaf from the top. However, when the predators co-occurred, N. tenuis or M. pygmaeus individuals were recorded with increased numbers on the lower or the higher part of the plant, respectively. In the presence of N. tenuis adult young nymphs of M. pygmaeus completed their development to the adult stage, when alternative prey (lepidopteran eggs) was present on the plant, however failed to reach adulthood in the absence of alternative prey. A high percentage of the dead nymphs found with their body fluids totally sucked indicating predation by N. tenuis. However, large 4th instar nymphs of M. pygmaeus were much less vulnerable to N. tenuis than younger. The behavior of N. tenuis was affected by the presence of M. pygmaeus, but at a rate similar to that when two individuals of N. tenuis were enclosed together. Contacts between the predators were recorded in a similar frequency in mono- and heterospecific treatments, whereas aggressive behavior was not observed. This study shows that intraguild interactions between M. pygmaeus and N. tenuis occur but are not intensive. The potential implications of the outcomes for biological control are discussed.