Role of larval host plant experience and solanaceous plant volatile emissions in Tuta absoluta (Lepidoptera: Gelechiidae) host finding behavior

The tomato leafminer, Tuta absoluta (Lepidoptera: Gelechiidae), is considered to be a major pest that damages tomato (Solanum lycopersicum L; Solanaceae) crops in South American, European, and Mediterranean countries. This insect species is polyphagous (i.e., feeds on many types of food); hence, it could also develop on other cultivated host plants, principally solanaceous plants, such as potato (S. tuberosum L.; Solanaceae) and eggplant (S. melongena L.; Solanaceae). Therefore, we tested the hypothesis that host plant choice by adult T. absoluta is influenced by plant volatile organic compounds and larval host plant experience. One tomato cultivar (cv.) ‘Moneymaker’ and three potato cv. ‘Charlotte’ ‘Bintje,’ and ‘Nicola’ were tested. Using a flying tunnel, we observed that females reared on tomato preferred flying toward tomato and, to a lesser extent, potato cv. ‘Charlotte.’ These preferences might be explained by the high release of terpenes by these two plants. When conducting oviposition choice assays, we found no preference between tomato and potato in the number of eggs laid by females that had been previously reared on either host plant. This study indicates that the host finding behavior of T. absoluta is mediated by solanaceous volatiles, while oviposition behavior appears to depend on additional stimuli. These results provide baseline information for use in the development of new control strategies against T. absoluta using semiochemicals and plant breeding.     

Effects of water stress on plant volatile emission and insect oviposition preference in an agroecosystem

1. Drought has become more common and severe in many parts of the world due to climate change. The effect of water stress on insect oviposition preference that is key determinant for their fitness has received less attention.
2. Here, we examined how water stress may affect oviposition selection of Ostrinia furnacalis for maize plants in the greenhouse, and tested difference in volatile compounds emitted from treated maize, and electronantennogram and bioassay responses of O. furnacalis to the volatile profiles in maize plants.
3. Ostrinia furnacalis were more prone to lay eggs on the well-watered maize. Most plant volatile compounds differed significantly among the three water treatments, including increased emissions of β-caryophyllene, (E)-2-hexenal, and linalool, and decreased emission of (Z)-3-hexen-1-ol when subjected to increasing intensity of drought.
4. Varied volatile profiles of maize may drive oviposition decision of O. furnacalis, because O. furnacalis showed a clear oviposition preference for (Z)-3-hexen-1-ol, while not for β-caryophyllene, (E)-2-hexenal, and linalool, at the concentration of 1000 ppm.
5. This study advances understanding of drought effects on plant–insect interactions through volatile profiles. Our finding calls for attention to oviposition selection for insect pest management in agricultural settings, especially in regions under changing precipitation patterns.

     

How does a predator find its prey? Nesidiocoris tenuis is able to detect Tuta absoluta by HIPVs

The Zoophytophagous predator, Nesidiocoris tenuis (Reuter) (Hemiptera: Miridae) is one of the most important candidates for controlling Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) in tomato crops. This predator uses different signals including morphological plant traits, prey insects, and volatile substances produced by the infested plants and prey signals to find its suitable prey. These signals are different in each cultivar of a plant. We aimed to understand how N. tenuis finds its prey using volatiles from tomato plants damaged or infested with T. absoluta. The predator’s responses to various plant treatments on two cultivars of tomato plants were tested in a flight tunnel and a four-choice olfactometer. The volatile compounds released from the treatments were also collected and identified. The results of the olfactory experiments showed that the predators even in the absence of light chose the plants bearing their insect prey. This behavior was not the same in both cultivars, and N. tenuis had a tendency toward mechanically damaged of Early Urbana Y cultivar more than Cal JN3 cultivar. The differences in the amount of monoterpenes, sesquiterpenes, and eugenol between cultivars may play a role in the differential attraction of N. tenuis towards infested plants. The difference in the volatile compounds was evident in two cultivars, and this was consistent with our bioassay results. Therefore, the choice of appropriate cultivar and use of herbivore-infested plant volatiles are important for developing a control strategy against T. absoluta and attract its predators.     

Flight behavior and oviposition of <Emphasis Type="Italic">Tuta absoluta</Emphasis> on susceptible and resistant genotypes of <Emphasis Type="Italic">Solanum lycopersicum</Emphasis>

Plants produce volatile chemical compounds that can negatively affect the preference (antixenosis) or the performance (antibiosis) of herbivorous insects. It is thought that these volatile compounds are used as cues by herbivorous insects to determine the suitability of the plant for egg deposition and, hence, offspring performance. Here, we investigated whether volatiles produced by tomato plants play a role in modulating the flight and oviposition behavior of mated Tuta absoluta females. We found that the behavioral steps displayed by mated females did not differ when they flew toward resistant or susceptible tomato genotypes, but they reached the susceptible genotypes faster than the resistant ones. Moreover, females landed more often and laid more eggs on the most susceptible genotype, the Santa Clara variety. Because this variety is known to be of high quality for the development of T. absoluta larvae, the female’s decision to land and lay more eggs on this genotype seems to be mainly to maximize offspring performance. However, this is not so straightforward because the proportion of landings and eggs laid by T. absoluta on another susceptible genotype tested in this study was not significantly higher than on the resistant genotypes. Finally, although future studies are still needed, considering the antixenotic and antibiotic traits of the resistant genotypes studied here, they are likely to succeed if used in integrated pest management.     

Assessment of Tuta absoluta yield loss in Iranian tomato crops

The South American tomato pinworm, Tuta absoluta Meyrick (Lepidoptera: Gelechiidae), a devastating pest of tomato plants, originates from South America but it has been considered an invasive pest for Iran since 2010. To assess crop loss caused by this pest, a study was conducted in a 600 m² field under a randomised complete block design. The impact of different initial densities of T. absoluta, including control (without infestation), one, two, four, and eight T. absoluta eggs on each host plant in the first and second year was investigated with an additional treatment (16 pinworm eggs per host plant) used in the second year. Yield attributes including length and width of fruits, numbers of infested and intact fruits along with their weights were sampled and assessed on a weekly basis. In addition, the correlation between the number of galleries and these characteristics was also investigated. Crop loss data demonstrated that the effect of different infestation levels on fruit size and the weight of intact fruits was not significant over both years. However, the effect of treatment on the percentage and weight of infested fruits was shown to be significantly different in 2014 and 2015. Furthermore, there was a negative significant correlation between the number of galleries and weight of infested fruits in both years. Collectively, these results will be useful for enhancing pest management programs of T. absoluta in Iran.     

Intermittent exposure to traces of green leaf volatiles triggers the production of (Z)-3-hexen-1-yl acetate and (Z)-3-hexen-1-ol in exposed plants

Intermittent exposure during a period of 3 weeks of undamaged Arabidopsis plants to trace amounts of volatiles emitted by freshly damaged Arabidopsis plants resulted in an increase of subsequent artificial-damage-induced production of (Z)-3-hexen-1-yl acetate and (Z)-3-hexen-1-ol in the exposed Arabidopsis plants when compared with Arabidopsis plants exposed to undamaged Arabidopsis plant volatiles (control plants). We previously showed that (Z)-3-hexen-1-yl acetate attracts a parasitic wasp, Cotesia glomerata. Thus, the induced production of this volatile explained our previously reported finding that, when artificially damaged, the exposed plants were more attractive to C. glomerata than control plants.     

Volatiles induced by the larvae of the Asian corn borer (Ostrinia furnacalis) in maize plants affect behavior of conspecific larvae and female adults

Abstract  Effects of maize ( Zea mays L.) volatiles induced by larvae of the Asian corn borer, Ostrinia furnacalis (Guenée), on the orientation behaviors of Asian corn borer larvae and oviposition of the females were investigated. Nineteen volatile chemicals, with terpenes being the major components, were identified from maize plants attacked by third instar Asian corn borer larvae. Coupled gas chromatographic-electroantennographic detection (GC-EAD) analyses revealed some electroantennographic differences between female and male Asian corn borer antennae in response to larvae-induced maize volatiles; female responded to ( E )-2-hexenal, nonanal, ( Z )-3-hexen-1-ol and three unknown compounds while the male only responded to ( E )-2-hexenal, nonanal and one unknown compound. In laboratory orientation bioassays, Asian corn borer neonate larvae were attracted to extracts collected from Asian corn borer-damaged plants as well as to synthetic farnesene, but were repelled by ( Z )-3-hexen-1-ol. In laboratory oviposition bioassays, gravid females laid fewer eggs on plants damaged by larvae than on mechanically damaged plants or undamaged plants. Adult Asian corn borer females deposited fewer eggs on wax paper treated with ( E )-2-hexenal or ( Z )-3-hexen-1-ol than on wax paper treated with hexane (control). The results suggest that Asian corn borer can affect the behaviors of conspecific larvae and adults by changing host plant volatiles.     

The effect of methyl salicylate on the induction of direct and indirect plant defense mechanisms in poplar (Populus × euramericana ‘Nanlin 895’)

The objective of this study was to investigate the effect of different concentrations of methyl salicylate (MeSA) on direct defense and indirect defense in poplar cuttings (Populus × euramericana ‘Nanlin 895’). Four defense-related enzyme activities, such as superoxide dismutase (SOD, EC1.15.1.1), oxydoreductases peroxidase (POD, EC1.11.1.7), catalase (CAT, EC1.11.1.6), and polyphenol oxidase (PPO, EC 1.14.18.1), were measured. The results showed that the SOD activities were induced by 1.0 and 10.0 mM MeSA and the POD activities were induced by MeSA. The CAT activity was induced at low concentrations of MeSA but was inhibited by high concentrations, and the PPO activity was affected by 0.1, 1.0, and 10.0 mM MeSA. Furthermore, the volatiles were detected using gas chromatography–mass spectrometry and gas chromatography. Twenty-one volatile compounds were tentatively identified in the emissions from plant leaves. Of these volatile compounds, (Z)-3-hexen-1-ol and cis-3-hexenyl acetate emissions were the highest. (Z)-3-Nonen-1-ol, (E)-2-hexen-1-ol, 1-octanol, (E,Z)-3,6-nonadien-1-ol, β-ionone, and hexadecanamide were six compounds that were only produced after treatment by 10.0 mM MeSA. These results showed that direct and indirect defense mechanisms in poplars were induced by MeSA.     

The predatory mirid Dicyphus maroccanus as a new potential biological control agent in tomato crops

The first record of the omnivorous predator Dicyphus maroccanus Wagner (Hemiptera: Miridae) inhabiting tomato crops in the Valencia region (East Coast of Spain) was in 2009. Since then, D. maroccanus has often been found preying on the eggs of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) in this area. To evaluate this predator’s potential as a biological control agent, its life-history traits in the presence and absence of prey [(eggs of Ephestia kuehniella Zeller (Lepidoptera: Pyralidae)] on tomato plants were studied under laboratory conditions. Immature stages that preyed on eggs of E. kuehniella developed successfully. However, no nymph completed development on the plant without the addition of E. kuehniella eggs. To reach adulthood, male and female D. maroccanus nymphs consumed 267 and 312 E. kuehniella eggs, respectively. The net reproductive rate (R₀) was estimated to be 34.52 female eggs per female, the generation time (T) was 40.48 days, and the estimated intrinsic rate of increase (r_m) was 0.0868 females per female per day at 25 °C. In a second experiment, the capacity to detect plants infested or not infested with T. absoluta was studied using a Y-tube olfactometer. Female D. maroccanus were strongly attracted to the odor of T. absoluta-infested plants. In a third experiment, the capacity of D. maroccanus to control T. absoluta on tomato plants was investigated under extended laboratory conditions. Dicyphus maroccanus significantly reduced the number of T. absoluta-infested leaves in over 90 % of cases relative to control conditions. These results suggest that D. maroccanus could play a significant role in T. absoluta management. The potential of this zoophytophagous predator as a biocontrol agent on tomato crops is discussed.     

Is the Performance of a Specialist Herbivore Affected by Female Choices and the Adaptability of the Offspring?

The performance of herbivorous insects is related to the locations of defenses and nutrients found in the different plant organs on which they feed. In this context, the females of herbivorous insect species select certain parts of the plant where their offspring can develop well. In addition, their offspring can adapt to plant defenses. A system where these ecological relationships can be studied occurs in the specialist herbivore, Tuta absoluta, on tomato plants. In our experiments we evaluated: (i) the performance of the herbivore T. absoluta in relation to the tomato plant parts on which their offspring had fed, (ii) the spatial distribution of the insect stages on the plant canopy and (iii) the larval resistance to starvation and their walking speed at different instar stages. We found that the T. absoluta females preferred to lay their eggs in the tomato plant parts where their offspring had greater chances of success. We verified that the T. absoluta females laid their eggs on both sides of the leaves to better exploit resources. We also observed that the older larvae (3^rd and 4^th instars) moved to the most nutritious parts of the plant, thus increasing their performance. The T. absoluta females and offspring (larvae) were capable of identifying plant sites where their chances of better performance were higher. Additionally, their offspring (larvae) spread across the plant to better exploit the available plant nutrients. These behavioral strategies of T. absoluta facilitate improvement in their performance after acquiring better resources, which help reduce their mortality by preventing the stimulation of plant defense compounds and the action of natural enemies.     

Dispersion and Persistence of <Emphasis Type="Italic">Trichogrammatoidea bactrae</Emphasis> (Nagaraja) over <Emphasis Type="Italic">Tuta absoluta</Emphasis> (Meyrick), in Tomato Greenhouses

Inundative biological control depends on the ability of natural enemies to disperse and persist in the environment. The objective was to evaluate the dispersion and persistence of Trichogrammatoidea bactrae (Nagaraja) on Tuta absoluta (Meyrick) eggs. Inundative releases of this parasitoid were performed in experimental tomato greenhouses. For vertical dispersion, leaves of the upper and middle third of plants were artificially infested with T. absoluta eggs; for horizontal dispersion, plants at increasing distances from a release point were infested. These eggs were renewed at days 2 and 4 to evaluate persistence. The amount of parasitized patches was registered. Logistic regression analysis was used. The position of the eggs in the plant did not affect the DE (discovery efficiency: proportion of parasitized patches). Time since release negatively affected the DE, while distance affected it only when plants were higher. These results could be used to adjust the release methodology of T. bactrae.     

Between plant and diurnal variation in quantities and ratios of volatile compounds emitted by Vicia faba plants

Ratios of volatile phytochemicals potentially offer a means for insects to recognise their host-plant species. However, for this to occur ratios of volatiles would need to be sufficiently consistent between plants and over time to constitute a host-characteristic cue. In this context we collected headspace samples from Vicia faba plants to determine how consistent ratios of key volatile phytochemicals used in host location by one of its insect pests, the black bean aphid, Aphis fabae, were. These were (E)-2-hexenal, (Z)-3-hexen-1-ol, 1-hexanol, benzaldehyde, 6-methyl-5-hepten-2-one, octanal, (Z)-3-hexen-1-yl acetate, (R)-linalool, methyl salicylate, decanal, undecanal, (E)-caryophyllene, (E)-β-farnesene, (S)-germacrene D, and (E, E)-4,8,12-trimethyl-1,3,7,11-tridecatetraene, which had previously been found to be electrophysiologically and behaviourally active to A. fabae. Although the quantities of volatiles produced by V. faba showed large between plant and diurnal variation, correlations between quantities of compounds indicated that the ratios of certain pairs of volatiles were very consistent. This suggests that there is a host-characteristic cue available to A. fabae in the form of ratios of volatiles.     

Interrelated responses of tomato plants and the leaf miner Tuta absoluta to nitrogen supply

Plant–insect interactions are strongly modified by environmental factors. This study evaluates the influence of nitrogen fertilisation on the tomato (Solanum lycopersicum L.) cv. Santa clara and the leafminer (Tuta absoluta (Meyrick), Lepidoptera: Gelechiidae). Greenhouse‐grown tomato plants were fed hydroponically on a complete nutrient solution containing either a high nitrogen concentration (HN) sustaining maximum growth or a low nitrogen concentration (LN) limiting plant growth. Insect‐free plants were compared with plants attacked by T. absoluta. Seven and 14 days after artificial oviposition leading to efficacious hatching and larvae development, we measured total carbon, nitrogen and soluble protein as well as defence compounds (phenolics, glycoalkaloids, polyphenol oxidase activity) in the HN versus LN plants. Only in the HN treatment did T. absoluta infestation slightly impair leaf growth and induce polyphenol oxidase (PPO) activity in the foliage. Neither the concentration of phenolic compounds and proteins nor the distribution of nitrogen within the plant was affected by T. absoluta infestation. In contrast, LN nutrition impaired T. absoluta‐induced PPO activity. It decreased protein and total nitrogen concentration of plant organs and enhanced the accumulation of constitutive phenolics and tomatine. Moreover, LN nutrition impaired T. absoluta development by notably decreasing pupal weight and lengthening the development period from egg to adult. Adjusting the level of nitrogen nutrition may thus be a means of altering the life cycle of T. absoluta. This study provides a comprehensive dataset concerning interrelated responses of tomato plants and T. absoluta to nitrogen nutrition.     

Fusarium infection in maize: volatile induction of infected and neighboring uninfected plants has the potential to attract a pest cereal leaf beetle, Oulema melanopus

Fusarium infection of maize leaves and/or roots through the soil can stimulate the emission of volatile organic compounds (VOCs). It is also well known that VOC emission from maize plants can repel or attract pests. In our experiments, we studied VOC induction responses of Zea mays L. ssp. mays cv. ‘Prosna’ having Fusarium infection (mix of four species) in leaves or roots, then tested for VOC induction of uninfected neighboring plants, and finally examined wind-tunnel behavioral responses of the adult cereal leaf beetle, Oulema melanopus L. (Chrysomelidae: Coleoptera) behavior to four induced VOCs. In the first part of our experiment, we confirmed that several green leaf volatiles (GLVs; (Z)-3-hexenal, (E)-2-hexenal, (Z)-3-hexen-1-ol, (E)-2-hexen-1-ol, (Z)-3-hexen-1-yl acetate, 1-hexyl acetate), terpenes (β-pinene, β-myrcene, Z-ocimene, linalool, β-caryophyllene), and shikimic acid pathway derivatives (benzyl acetate, methyl salicylate, indole) were positively induced from maize plants infected by Fusarium spp. The quantities of induced VOCs were higher at 7 d than 3 d post-infection and greater when plants were infected with Fusarium on leaves rather than through soil. In the second part of our experiment, uninfected maize plants also showed significantly positive induction of several VOCs when neighboring an infected plant where the degree of induction was negatively related to the distance from the infected plant. In the third part of our experiment, a Y-tube bioassay was used to evaluate upwind orientation of adult cereal leaf beetles to four individual VOCs. Female and male O. melanopus were significantly attracted to the GLVs (Z)-3-hexenal and (Z)-3-hexenyl acetate, and the terpenes linalool and β-caryophyllene. Our results indicate that a pathogen can induce several VOCs in maize plants that also induce VOCs in neighboring uninfected plants, though VOC induction could increase the range at which an insect pest species is attracted to VOC inducing plants.     

Development,Reproduction, Survival,and Demographic Patterns of <Emphasis Type="Italic">Tuta absoluta</Emphasis> (Meyrick) (Lepidoptera: Gelechiidae) on Different Commercial Tomato Cultivars

The increase in the production of tomato, Solanum lycopersicon Mill. (Solanaceae), has favored the proliferation of pests, especially Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). In this study, the development, reproduction, survival, and demographic parameters of T. absoluta reared on six commercial tomato cultivars (Cherry, Cordilheira, Giuliana, Nemoneta, Paron, and Santa Clara) were evaluated. Tuta absoluta completed its development in all tomato cultivars. Development from newly hatched caterpillar to newly emerged adult varied between 24.8 and 28.2 days. Female fecundity ranged from 126.3 to 166.9 eggs, with fertility from 54.2 to 84.1%. Mortality during egg-adult development varied between 21.4 and 46.4% for insects reared on cultivars Cherry and Giuliana, respectively. The cultivars Cordilheira, Giuliana, and Santa Clara are promising options to tomato producers in order to decrease the attack and proliferation of T. absoluta. However, the development and population growth of T. absoluta is faster on the tomato cultivar Cherry.     

Functional response and egg distribution among hosts by Pseudapanteles dignus,a larval endoparasitoid of Tuta absoluta

The functional response of a biocontrol agent has been classically pointed out as a quantitative evaluation criterion to understand its killing capacity to an arthropod pest. In this paper, we revisited the functional response of the internal larval parasitoid Pseudapanteles dignus (Muesebeck) (Hymenoptera: Braconidae), a candidate for biocontrol of the South American tomato leafminer, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae), measured as the daily egg oviposition of single parasitoid females at increasing densities of T. absoluta larvae through dissection of hosts. The functional response curve of the number of parasitized hosts was fitted out taking into account the number of eggs laid and their distribution among hosts at each T. absoluta larval density. The data also allowed us to discuss the self-superparasitism strategy of this parasitoid as an adaptive trait. Pseudapanteles dignus showed a sigmoid shape functional response and a contagious distribution of eggs among hosts, favouring self-superparasitism and laying a similar number of eggs in each superparasitized host at each T. absoluta density. This research is firstly intended to ascertain about the oviposition behaviour of P. dignus and additionally to provide information on its reproduction to be applied in mass rearing procedures and augmentative releases against T. absoluta.     

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.     

Identification of plant chemicals attracting and repelling whiteflies

The harmful side effects of chemical pest control have focused increasing attention on the potential for environmentally friendly, sustainable and efficient methods to control the sweet potato whitefly, Bemisia tabaci (Gennadius). One control method employs a volatile repellent (push), and an alluring volatile trap (pull) to manipulate the distribution and control the whitefly. Here, a Y-tube olfactometer was used to investigate the orientation responses of the whitefly toward the volatile components of six plants: tomato, tobacco, cabbage, cotton, cucumber and celery. Gas chromatography coupled with mass spectrometry was used to identify and quantify extracts from the six plants. Six treatments were conducted to demonstrate the “push–pull” method’s effects on the host selection behaviors of B. tabaci in a greenhouse. Four of the plant extracts tested had exceedingly attractive effects on the adult insects, but not those from celery. B. tabaci exhibited a prominent attraction response to (E)-2-hexenal, 3-hexen-1-ol and mixtures of these compounds, with the response rates exceeding 80 % for all tested proportions. Limonene diluted 500 times had a 62 % greater deterrent effect on adults than was observed in its absence, and it repelled egg-laying by more than 80 % in the greenhouse experiment. These data show that (E)-2-hexenal, 3-hexen-1-ol and limonene can be expected to be used for the “push–pull” method to control B. tabaci.