Ecology

Introduced through human activities, such as travels and transcontinental trade, and supported by climate change, several invasive species can settle in habitats where formerly they could not survive. The presence of allochthonous species can negatively affect native species reducing biodiversity, represent a threat to human health and, in the case of phytophagous insects, cause serious damage to the agroeconomic system29. Characterized by rapid spread and enormous impact, an invasion like that of D. suzukii has few precedents. This species is thus becoming a model of study in the biology of alien species and for the development of pest management techniques30.The protection of crops from D. suzukii invasion is mainly conducted by means of insecticides31 which, as known, are unselective, in many cases remain in the environment and, if persistent on fruit, are harmful to human and animal health32. In addition, their efficiency can be reduced by weather events such as rainfall, and their prolonged use may induce resistance phenomena in target insects. Moreover, the preference of D. suzukii for ripening fruit requires that any treatment be carried out close to the harvesting, which inevitably means that insecticide residues can remain on the marketed fruit33. Alternatively to synthetic chemicals, natural compounds that can act as repellents, toxicants by contact or ingestion, and overall deterrents, have been tested mainly against D. suzukii adults34. All these control procedures have positive aspects, such as low cost, sometimes good effectiveness, and ease of use for farmers, but, as mentioned, their massive use affects environment and organisms at various levels. Considering the limits of the chemical control, several studies have addressed the problem of D. suzukii management through the development and improvement of biological control methods. However, given the recent introduction of this insect in Europe and America specific projects in these areas are still limited. Until now, only the main entomopathogens commonly used in biological control, have been tested against D. suzukii35.Several serovars of Bt were tested at different concentrations on D. suzukii. Cossentine et al.27 described the results of the assays with 22 serotypes of Bt, and among them, only few are effective against the target dipteran. In particular, the serovars thuringiensis, kurstaki, thompsoni, pakistani, and bolivia show an effectiveness of more than 75% on first stage larvae. The mortality rates, however, are related to a dietary administration of at least 108 spores/mL, below this concentration the insecticidal activity is not relevant. Moreover, the efficacy on adult individuals is extremely low, only the serovar thuringiensis induces a mortality of about 44%. In the literature, data on the low effects of serovar israelensis on this fly are also reported36. The data obtained from our trials, carried out with the serovar kurstaki, agree with Cossentine et al.27, demonstrating that only high concentrations of the bacterium produce significant effects on larvae in a relatively short time (24–48 h).As regards the insecticidal activity of EPN, the literature includes several studies carried out in laboratory or field with applications on plants and soil. The data collected using different species of nematodes, such as S. carpocapsae (Sc), S. feltiae, S. kraussei, H. bacteriophora25,37,38,39 and the rare species Oscheius onirici40, are quite promising but, as observed for Bt, also for EPN high concentrations are required, and their effectiveness is very variable between laboratory and field studies. In accordance with previous results29, our current data indicate a good efficacy of Sc: treatments with an amount of 1.6 × 103 IJs (corresponding to 80 IJ/cm2) resulted in a larvae mortality above 98%, 48 h post-treatment.Since the reproduction of D. suzukii occurs by spawning in the mesocarp of the fruit, the technical limit of the application of bio-insecticides such as Bt or EPN cannot be disregarded. Larvae development is protected by the fruit pulp and this may be one of the causes of the low effectiveness of Bt in field applications. As known, to be effective, Bt must be ingested and should therefore reach the larva by penetrating inside the fruit; perhaps a timely spraying of the crops before oviposition could theoretically promote the penetration of microorganisms thanks to the drive of ovipositor. Based on these considerations, it is reasonable to assume that coupling Bt with EPN, which, being motile, can actively reach the targets, could significantly improve the effectiveness of D. suzukii control methods in the field.The simultaneous application of two control agents, with different modes of action, may result in additive or complementary effects. In particular, the tissue damage inflicted by Bt to the intestinal epithelium could facilitate the access of nematodes in the passage from the gut to the hemocoel (Fig. 9). When in the hemolymph, the nematode and its symbionts implement strategies of immunoevasion and immunodepression of host immune responses4,41,42, leading to a drastic and more rapid physiological alteration that results in the death of the target insect in a shorter time.Figure 9A possible model of the effects induced by the combined administration of B. thuringiensis (Bt) and S. carpocapsae (EPN) to D. suzukii larvae. The presence of B. thuringiensis, ingested during feeding by D. suzukii larvae, could facilitate and speed up the passage of S. carpocapsae from the intestine to the hemocoelic cavity. Bt toxins, produced as parasporal inclusions, are activated in the intestinal lumen of the larva. Active toxins interact with the membrane receptors of the intestinal epithelium and are responsible for the formation of pores that alter the physiology of the cells leading to their lysis. The resulting epithelial lesions could provide an easy access route for EPN to other body regions of the larvae.Full size imageAs previously reported, and supported by literature, it is desirable that studies on biological control of D. suzukii will be increased and possibly new strategies for the use of bio-insecticides will be tested. In this perspective, we started a project aimed at assessing whether the association of entomopathogenic organisms and microorganisms is a promising strategy, capable of making safer and faster measures to control the diffusion of insect pests. Besides this, a need to reduce Bt concentrations used in field application has arisen from recent observations on the possible insecticidal effect on non-target insect populations, caused by intensive use and consequent bioaccumulation of the bacterium in crop applications43. It is also known that high concentrations of Bt serovars which produce the cry1Ba1 and 1 beta-exotoxin toxins, are toxic not only to several dipterans but also to mammals44,45.Even when using EPN, limitations have been highlighted: such as with Bt, they are susceptible to runoff in case of rainfall, have a significant sensitivity to drying at high temperatures, and, depending on the species, are more or less effective in certain environmental conditions as well as susceptible to the presence of pesticides46,47.On the basis of these considerations and the relevant literature, and after excluding adverse effects on the nematode induced by the presence of Bt, we conducted the assays with combinations of Bt and Sc, administering them both simultaneously and time-shifted. According to our data, the mortality of D. suzukii larvae increases from  More

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