Approaches to conserving natural enemy populations in greenhouse crops: current methods and future prospects

Biological pest control in greenhouse crops is usually based on periodical releases of mass-produced natural enemies, and this method has been successfully applied for decades. However, in some cases there are shortcomings in pest control efficacy, which often can be attributed to the poor establishment of natural enemies. Their establishment and population numbers can be enhanced by providing additional resources, such as alternative food, prey, hosts, oviposition sites or shelters. Furthermore, natural enemy efficacy can be enhanced by using volatiles, adapting the greenhouse climate, avoiding pesticide side-effects and minimizing disrupting food web complexities. The special case of high value crops in a protected greenhouse environment offers tremendous opportunities to design and manage the system in ways that increase crop resilience to pest infestations. While we have outlined opportunities and tools to develop such systems, this review also identifies knowledge gaps, where additional research is needed to optimize these tools

Predatory efficacy of Dicyphus errans on different prey

The Palaearctic predator Dicyphus errans (Hemiptera: Miridae) lives omnivorously on various host plants, preying on a wide range of small arthropods, including some new invasive alien species. These characteristics make it a promising biological control agent (BCA) in organic greenhouses. The capacity of a BCA to find, kill and consume prey plays a fundamental role in trophic interactions and population dynamics in a predator-prey system. The functional response of a predator, which describes how the individual rate of prey consumption changes in response to prey density, is a key component to assess its effectiveness in pest control and the stability of its own populations. Therefore, the functional response of D. errans on different prey was studied to improve our knowledge on the potential of this mirid, which is naturally widespread in European organic greenhouses. Laboratory experiments were carried out on three exotic pests: the poinsettia thrips Echinothrips americanus (Thysanoptera: Thripidae), the greenhouse whitefly Trialeurodes vaporariorum (Hemiptera: Aleyrodidae), and the tomato borer Tuta absoluta (Lepidoptera: Gelechiidae), to build functional response curves. Prey was offered at different densities to single females of D. errans for 24 h. The predation behaviour of D. errans on all the prey species was defined by Type II functional response curves. The female could daily prey about 62 adults of E. americanus, 114 pupae of T. vaporariorum, and 236 eggs of T. absoluta. The high voracity of this generalist predator on different prey confirmed its suitability as a BCA. For effective and stable pest control strategies, a prior to pest establishment of D. errans in organic greenhouses may prevent pest escaping in case of high infestation rates, even if the type II functional response reaches saturation at very high prey densities

Evaluation of mirid predatory bugs and release strategy for aphid control in sweet pepper

Zoophytophagous predators of the family Miridae (Heteroptera), which feed both on plant and prey, often maintain a close relationship with certain host plants. In this study, we aimed to select a suitable mirid predatory bug for aphid control in sweet pepper. Four species were compared: Macrolophus pygmaeus (Rambur), Dicyphus errans (Wolff), Dicyphus tamaninii Wagner and Deraeocoris pallens (Reuter). They were assessed on their establishment on sweet pepper plants with and without supplemental food (eggs of the flour moth Ephestia kuehniella Zeller and decapsulated cysts of the brine shrimp Artemia franciscana Kellogg) and on their effects on aphids with releases before and after aphid infestations. None of the predator species was able to control an established population of aphids on sweet pepper plants; however, the predators M. pygmaeus and D. tamaninii could successfully reduce aphid populations when released prior to an artificially introduced aphid infestation. The best results were achieved with M. pygmaeus in combination with a weekly application of supplemental food. Hence, our results demonstrate that the order and level of plant colonization by mirid predators and aphids determines how successful biological control is. Further studies are needed to evaluate the performance of mirid predatory bugs in sweet pepper crops in commercial greenhouses with multiple pests and natural enemies, in particular to understand how increased variation in food sources affects their feeding behaviour and preferences

Functional response of the mirid predators Dicyphus bolivari and Dicyphus errans and their efficacy as biological control agents of Tuta absoluta on tomato

Dicyphus bolivari Lindberg and Dicyphus errans (Wolff) (Hemiptera: Miridae) are naturally widespread in many crops with low-pesticide pressure, where they prey upon several arthropods, including the tomato pinworm Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). However, their efficacy as biological control agents (BCAs) of this pest needs further investigations. Therefore, in this study the predatory efficacy of D. bolivari and of D. errans on T. absoluta was evaluated on tomato in laboratory and greenhouse trials. Their functional response to different numbers of T. absoluta eggs (up to 350) offered to single females or 5th-instar nymphs for 24 h was assessed in laboratory. Females and nymphs of both predators showed a high voracity and a type II functional response, with an estimated maximum predation rate per day of 189 and 194 eggs for D. bolivari females and nymphs, respectively, and 197 and 179 eggs for D. errans females and nymphs, respectively. The predators showed similar predation rates of T. absoluta eggs on plants in cage trials. However, our greenhouse trial showed that the commonly used Macrolophus pygmaeus (Rambur) (Hemiptera: Miridae), which has a lower individual predation capacity than D. bolivari and D. errans, was more effective in controlling T. absoluta than D. errans and D. bolivari because of its stronger numerical response to densities of T. absoluta and supplemental food than the other two predator species. This shows that long-term greenhouse trials, which include functional and numerical responses to pest densities, are essential to evaluate the efficacy of an omnivorous predator.</p

Natural enemies of Tuta absoluta in the Mediterranean basin, Europe and South America

The tomato leafminer Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) represents a global threat to commercial tomato (Solanum lycopersicum L.) production, both in open field and greenhouse. Native to South America, it spread over the Mediterranean Basin, Europe, Africa and part of Asia in only 12 years, and currently it is reported in over 80 countries. Biological control is one of the options for its control and a large number of natural enemies has been reported in association with the pest, both in the areas of origin and of introduction. The egg parasitoid Trichogramma pretiosum, in South America, and the mirid predators Macrolophus pygmaeus and Nesidiocoris tenuis, in Europe and the Mediterranean basin, are used as commercial biocontrol agents. Even if several natural enemies might be promising candidates for biocontrol, their potential role in quantitative pest reduction has been seldom established under practical tomato production conditions. Since climatic suitability indices predict a high probability for continued invasion by T. absoluta, mainly in China and the USA, there is an urgent need for new control options. In order to minimise the use of broad spectrum insecticides, biocontrol techniques should be considered. As tomato is produced seasonally, augmentative biocontrol seems to be the most effective control option, but pest reduction might be optimised by adding conservation biocontrol, and by combining biocontrol within IPM programmes. Here, an overview of predators and parasitoids of T. absoluta in South American and Euro-Mediterranean regions, and their biological control efficacy under laboratory, semi-field and field conditions is provided