Dicyphus predatory bugs pre-established on tomato plants reduce Nesiodiocoris tenuis population growth
Description
Abstract Generalist predators are increasingly used in biological pest control for greenhouse crops, as they control multiple pests and persist in crops even when prey is scarce. However, some of these predators may cause plant damage due to their omnivorous feeding behaviour. In many European regions, the omnivorous predator Nesidiocoris tenuis (Reuter) (Hemiptera: Miridae) is considered to be a serious tomato pest, regardless of the biological control services it offers, and Integrated Pest Management (IPM) strategies are based instead on Macrolophus pygmaeus (Rambur). However, as N. tenuis may competitively displace M. pygmaeus and cause severe damage, growers often resort to pesticide use, disrupting their biological control practice. In this study, we evaluated the competitive interactions of three mirid predators, Dicyphus errans Wolff, Dicyphus bolivari Lindberg and Dicyphus cerastii Wagner, with N. tenuis. The results showed that pre-establishment of heterospecific mirid species can successfully suppress N. tenuis in the greenhouse; population growth was reduced by more than 90% compared to plants without competing predators. Further laboratory trials revealed reciprocal intraguild predation between these species in the absence of extraguild prey. Dicyphus adults predated on N. tenuis nymphs, while this was not found for M. pygmaeus. In olfactometer bioassays, N. tenuis females preferred plants previously exposed to heterospecifics but not conspecifics, suggesting that this mirid does not avoid competition. These results suggest that the three Dicyphus species could be interesting candidates for preventive releases in tomato crops due to their ability to effectively suppress N. tenuis population growth.
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Statistical analyses Generalized linear mixed models (GLMM) were fitted for the greenhouse experiment using the glmmTMB function (Brooks et al. 2017). First, the effect of the pre-established Dicyphus predators on the population build-up of N. tenuis was tested. A GLMM was fitted with N. tenuis as the response variable, and the identity of the Dicyphus predator (including no predator) as the fixed effect. To test the effect N. tenuis had on the population build-up of the Dicyphus predator, a GLMM was fitted with Dicyphus adults as the response variable. The fixed effects were the identity of the Dicyphus predator (D. errans, D. bolivari and D. cerastii), the presence/absence of N. tenuis, and their interaction. In both models, block and time were included as random effects, to account for temporal pseudo-replication of measures. Error distributions for both models were tested visually with diagnostic plots (Hartig 2021) and by evaluating the dispersion parameter of the model (Gelman and Hill 2006). Negative binomial distribution was chosen as the best fitting, based on AICc criteria (Burnham and Anderson 2004). The data of the IGP laboratory experiments were analysed through means of Generalized Linear Model (GLM) with binomial error structure. The factorial analysis in the situation where N. tenuis nymphs were offered to the 5 different adult predators (N. tenuis as the intraguild prey) included two factors, the extraguild prey (Ephestia eggs; present or absent), and the predator’s identity. In the reverse situation, where N. tenuis adults were offered nymphs of the 5 different mirid species (N. tenuis as the intraguild predator), the model included three factors, the absence or presence of the intraguild predator and extraguild prey, as well as the nymph’s (prey) species identity with five different levels. As natural mortality during the experiments was different for mirid nymphs acting as intraguild prey and due to significant interaction between intraguild predator and prey, separate models were fitted for each intraguild prey. To account for over- or under-dispersion in the GLMs when detected, the quasibinomial error distribution was used (McCullagh and Nelder 1989). When main effects were found significant, treatment means were compared through Tukey’s HSD tests. In the olfactometer experiments, responses of N. tenuis females to different pairs of odors were analyzed by Pearson's Chi-square Test for Independence. All statistical analyses were performed using the statistical software R 4.0.2 (R Core Team 2021).