A wide-diversity of horticultural crops are grown simultaneously in greenhouse production systems including ornamentals and vegetables [1] [2] . Greenhouse producers strive to maintain plant quality for consumer satisfaction and consequently economic benefits. However, there are challenges associated with growing horticultural crops in greenhouses, such as, dealing with insect and/or mite pests that can reduce aesthetic quality, marketability, and yield of a given crop [3] [4] . Therefore, greenhouse producers must provide inputs related to plant protection strategies in order to protect crops from damage affiliated with insect or mite pests. Furthermore, greenhouse producers typically deal with multiple pest complexes simultaneously [2] [5] [6] . Two major insect pests of greenhouse production systems are fungus gnats, Bradysia spp., (Diptera: Sciaridae), and western flower thrips, Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae). Both insect pests can cause direct damage by feeding on plant parts and indirect damage by transmitting plant pathogens, including soil-borne fungi and viruses [7] - [14] .

A plant protection strategy that can be implemented to manage insect or mite pest populations is biological control. Biological control entails periodic releases of natural enemies or biological control agents, such as parasitoids and predators in order to regulate or maintain insect or mite pest populations below damaging levels [4] [6] [15] . There are natural enemies commercially available for use against fungus gnats and western flower thrips including the following predatory mites: Stratiolaelaps scimitus (Womersley) (formerly = “Hypoaspis miles”) (Acari: Laelapidae) [16] [17] , Neoseiulus (formerly = Amblyseius) cucumeris Oudemans (Acari: Phytoseiidae) [18] [19] [20] , and Amblyseius swirskii Athias- Henriot (Acari: Phytoseiidae) [21] [22] . In addition, two generalist predators commercially available for use in greenhouse production systems are the rove beetle, Dalotia coriaria (Kraatz) (Coleoptera: Staphylinidae), and the insidious flower bug, Orius insidiosus (Say) (Hemiptera: Anthocoridae).

Dalotia (formerly = Atheta) coriaria adults are glossy, dark-brown, covered with a thick pubescence, and approximately 3 to 4 mm long [23] . Adults begin searching for food after emerging from pupae, and are mobile, flying long distances although they tend to spend most of their time in growing media. Larvae are white during the early instars whereas the later instars are yellow-brown [24] . The life history of D. coriaria has been studied under laboratory conditions with development time from egg to adult taking 17 days [25] although development time varies depending on temperature. For instance, development time from egg to adult is 21 to 22 days at 25˚C and 11 to 12 days at 30˚C [23] . Additional life history parameters that have been investigated include the following: egg, larval, and pupal development; male and female longevity; female fecundity; and number of adults per female in the F1 generation [25] . Adult longevity may influence effectiveness of D. coriaria when used as a biological control agent because adults prey and lay eggs for extended time periods, which may enhance their ability to regulate fungus gnat larval populations in greenhouses [25] . Dalotia coriaria is easy to rear under laboratory conditions using either live prey (fungus gnat larvae) or artificial diets, such as ground trout pellets, turkey starter crumbs, and/or oats, Avena sativa L. [25] [26] . In addition, greenhouse producers in the UK have experimented with “breeding boxes” or rearing-release boxes to establish populations of D. coriaria in poinsettia (Euphorbia pulcherrima Willd. ex Klotzsch) and cyclamen (Cyclamen persicum Mill.) crops [27] . However, cannibalism may occur under crowded conditions when rearing D. coriaria [23] .

Adults and larvae reside in the growing medium and feed on fungus gnat larvae [24] [28] [29] and western flower thrips pupae (Yinping Li, unpublished data). Rove beetle adults prefer fungus gnat, Bradysia sp. nr. coprophila (Lintner) larvae over oats in choice tests conducted under laboratory conditions [30] . However, rove beetle larvae do not develop into pupae in the absence of prey [23] . Total prey consumption of fungus gnat larvae by rove beetle adults increases as the number of rove beetle adults increases, reaching a maximum at four adult rove beetles per 473 mL deli container [29] . However, five rove beetle adults per 473 mL container were not effective in suppressing fungus gnat larval populations (20 fungus gnat larvae per 473 mL container) [31] . Dalotia coriaria can also feed on the eggs and first instar larvae of Duponchelia fovealis Zeller (Lepidoptera: Pyralidae) [32] . Since D. coriaria feeds on a wide-range of prey, the predator may be able to switch from preferred prey to non-preferred prey depending on changes in abundance [23] . Moreover, the ability of rove beetle adults to effectively regulate fungus gnat larval populations can be influenced by cultural practices, such as, growing medium type and watering practices [33] . Greenhouse producers throughout the USA are successfully using D. coriaria against fungus gnats (R. A. Cloyd; personal observation).

Orius insidiosus adults are black, 2 to 5 mm in length, and flattened with distinctively patterned black and white wings. Eggs are laid inside plant tissues and nymphs that emerge from eggs are light-brown [34] . Plant suitability may influence egg-laying by females, which may be affiliated with plant nutritional quality [35] . Under laboratory conditions, mean longevity of O. insidiosus females is 26.1 days [36] . Orius insidiosus is widely used to regulate pest populations in greenhouse production systems associated with ornamentals and vegetables [37] [38] [39] and is relatively easy to mass produce [39] [40] .

The insidious flower bug is a generalist predator. The nymphs and adults feed on a wide-range of arthropod pests including: thrips, whiteflies, aphids, and spider mites [41] [42] . Moreover, O. insidiosus can regulate populations of western flower thrips and the two spotted spider mite, Tetranychus urticae Koch (Acari: Tetranychidae), when these pests are present simultaneously [43] . Orius insidiosus will also feed on plant sap and pollen in the absence of prey [41] [42] . The insidious flower bug feeds on the larval and adult stages of western flower thrips [42] [44] [45] [46] located on plant leaves and flowers. Orius insidiosus can consume more than 20 western flower thrips per day [47] . The insidious flower bug is an effective natural enemy against western flower thrips, either individually or when combined with other natural enemies [48] [49] [50] . A major benefit of releasing O. insidiosus instead of the predatory mites, N. cucumeris and A. swirskii, is that the nymphs and adults of O. insidiosus feed on the mobile life stages (larvae and adults) of western flower thrips [45] , whereas the predatory mites primarily feed on the 1^st instars of western flower thrips [18] [51] [52] . Orius insidiosus can effectively regulate populations of western flower thrips in ornamental and vegetable production systems [38] [45] [53] .

During winter in the northern portions of the USA, the insidious flower bug undergoes reproductive diapause in response to short (<12 hours) photoperiods [54] , which impacts the ability of the predatory bug to effectively regulate western flower thrips populations from September through March [55] . However, extending the photoperiod (≥12 hours of light) and increasing temperature (30˚C) can inhibit O. insidiosus from entering diapause [54] [56] . In addition, diapause can be prevented by exposing O. insidiosus to an extended photoperiod with blue light (400 - 500 nm) [55] .

Banker plant systems consist of non-crop plants that provide alternative food sources (prey) for predators as well as pollen and nectar in order to enhance establishment [57] [58] . “Black Pearl” pepper (Capsicum annuum L. “Black Pearl”) plants provide sufficient pollen that enhances development, fitness, and abundance of O. insidiosus adults [59] . However, “Purple Flash” pepper plants have the highest population growth of O. insidiosus and may be a more suitable banker plant in commercial greenhouses [60] . The use of banker plants may improve the effectiveness of O. insidiosus in biological control programs designed to regulate western flower thrips populations [57] [58] .

Plants may influence the ability of predators to sufficiently regulate pest populations [61] [62] [63] [64] . For instance, O. insidiosus does not establish on tomato (Solanum lycopersicum L.) plants resulting in minimal regulation of western flower thrips populations [65] . The reason for this may be associated with inadequate functional and numerical responses possibly due to searching behavior hindered by glandular trichomes (hairs) on the leaves and stems of tomato plants [66] , which would reduce the ability of O. insidiosus to effectively regulate pest populations.

Since D. coriaria and O. insidiosus feed on different insect pests located either above-ground (western flower thrips) or below-ground (fungus gnats) there are opportunities to use both natural enemies together without the potential of intraguild predation [67] [68] . Both above and below-ground natural enemies may be used simultaneously to regulate populations of one insect pest [69] [70] [71] or even two different insect pests. However, no studies have been conducted to assess the potential of integrating two natural enemies that feed on different insect pests, such as, D. coriaria and O. insidiosus in greenhouse biological control programs. Research in this area may prove to be invaluable to greenhouse producers in regards to improving biological control programs designed to deal with multiple pest complexes.

The use of pesticides, including insecticides, miticides, and fungicides, is a common practice in greenhouse production systems to suppress insect and/or mite populations, and protect plants from plant-pathogenic fungi [72] . Therefore, pesticides may directly or indirectly affect natural enemies; thus potentially disrupting biological control programs and pest suppression. Studies have evaluated the direct and/or indirect effects of pesticides on O. insidiosus [73] [74] [75] [76] and D. coriaria [28] [77] [78] .

The interactions associated with integrating pesticides with natural enemies are more complex when using multiple natural enemies to regulate different insect and/or mite pest populations [79] . However, pesticide exposure may not directly or indirectly affect a natural enemy such as O. insidiosus inhabiting aboveground plant parts (e.g., leaves, stems, or flowers). Nonetheless, excess solution (“run-off”) from foliar spray applications may directly or indirectly affect a natural enemy residing in the growing medium like D. coriaria, thus compromising biological control programs targeting another insect pest [78] .

A number of pesticides are not directly harmful to rove beetle adults including: fungicides (azoxystrobin, fosetyl-aluminum, and mefenoxam), Bacillus thuringiensis subsp. israelensis, flonicamid, Metarhizium anisopliae, azadirachtin, and spinosad [77] . Furthermore, none of the pesticides impeded predation of rove beetle adults on fungus gnat (Bradysia sp. nr. coprophila) larvae. However, the pesticides clothianidin, dinotefuran, imidacloprid, chlorpyrifos, and chlorfenapyr are directly harmful to rove beetle adults. A follow-up study [78] reported that certain pesticides were directly harmful to rove beetle adults including: acetamiprid, lambda-cyhalothrin, and cyfluthrin whereas other pesticides such as, Beauveria bassiana, azadirachtin, and organic oils (cinnamon oils, rosemary oil, thyme oil, and clove oil) were not directly harmful to adult rove beetles.

A comprehensive study evaluated the effects (direct and indirect) of pesticides on O. insidiosus adults under laboratory conditions [76] . The findings indicated that fungicides (aluminum tris, azoxystrobin, fenhexamid, and kresoxim-me- thyl), insect growth regulators (azadirachtin, buprofezin, kinoprene, and pyriproxyfen), botanicals (Capsicum oleoresin extract, garlic oil, soybean oil; and rosemary, rosemary oil, peppermint oil, and cottonseed oil), and entomopathogenic fungi (Beauveria bassiana and Metarhizium anisopliae) are not directly harmful to O. insidiosus with 80% to 100% adult survival. However, the pesticides abamectin, spinosad, pyridalyl, chlorfenapyr, tau-fluvalinate, imidacloprid, dinotefuran, acetamiprid, and thiamethoxam were directly harmful to O. insidiosus after 96 hours (0% to 60% adult survival). Nevertheless, none of the pesticides indirectly affected predation of surviving adult O. insidiosus on western flower thrips adults [76] .

The fungicides myclobutanil and potassium bicarbonate are not directly harmful to O. insidiosus adults [80] . So, fungicides may be used in conjunction with both natural enemies. Insect growth regulators are presumed to have no direct or indirect effects on the adult stage of natural enemies since insect growth regulators are only active on the immature stage [72] [81] . Studies [77] [78] [82] support the presumption that insect growth regulators (e.g., azadirachtin, buprofezin, kinoprene, and pyriproxyfen), in general, are not directly or indirectly harmful to either natural enemy under laboratory conditions. In addition, the insect growth regulators, cyromazine, diflubenzuron, and novaluron are not directly harmful to D. coriaria adults after 96 hours of exposure [28] . Furthermore, entomopathogenic fungi including Beauveria bassiana and Metarhizium anisopliae are not directly harmful to D. coriaria and O. insidiosus [76] [77] . Therefore, the pesticide types described above may be integrated into plant protection programs for western flower thrips and fungus gnats that include D. coriaria and O. insidiosus. Furthermore, the pesticide mixture (combination of two active ingredients) of azadirachtin + B. bassiana is not directly harmful to D. coriaria and O. insidiosus [76] .

Dalotia coriaria and O. insidiosus are commercially available generalist predators that can effectively regulate populations of fungus gnats and western flower thrips. Therefore, greenhouse producers should consider releasing these natural enemies in greenhouse production systems in order to reduce inputs from pesticides and diminish the potential for resistance developing in pest populations.

The authors would like to thank Dr. Mary Beth Kirkham from the Department of Agronomy at Kansas State University (Manhattan, KS) for reviewing an initial draft of the manuscript.

Cloyd, R.A. and Herrick, N.J. (2017) Ecology and Role of the Rove Beetle, Dalotia coriaria, and Insidious Flower Bug, Orius insidiosus, in Greenhouse Biological Control Programs. Advances in Entomology, 5, 115-126. https://doi.org/10.4236/ae.2017.54012