Amblyseius swirskii in greenhouse production systems

Amblyseius swirskii in greenhouse production systems: a floricultural perspective Rosemarije Buitenhuis, Graeme Murphy, Les Shipp & Cynthia ScottDupree Experimental and Applied Acarology ISSN 0168-8162 Exp Appl Acarol DOI 10.1007/s10493-014-9869-9

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Author's personal copy Exp Appl Acarol DOI 10.1007/s10493-014-9869-9

Amblyseius swirskii in greenhouse production systems: a floricultural perspective Rosemarije Buitenhuis • Graeme Murphy • Les Shipp Cynthia Scott-Dupree

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Received: 20 January 2014 / Accepted: 2 December 2014 Ó Springer International Publishing Switzerland 2014

Abstract The predatory mite Amblyseius swirskii Athias-Henriot is a biological control agent that has the potential to play an important role in pest management in many greenhouse crops. Most research on this predatory mite has focused on its use and efficacy in greenhouse vegetables. However, an increasing number of growers of greenhouse ornamental crops also want to adopt biological control as their primary pest management strategy and find that biological control programs developed for vegetables are not optimized for use on floricultural plants. This paper reviews the use of A. swirskii in greenhouse crops, where possible highlighting the specific challenges and characteristics of ornamentals. The effects of different factors within the production system are described from the insect/mite and plant level up to the production level, including growing practices and environmental conditions. Finally, the use of A. swirskii within an integrated pest management system is discussed. Keywords Whiteflies

Phytoseiidae Integrated pest management Biological control Thrips

Introduction Acarid predators represent the second largest group of organisms (by species) used for biological control (13.1 %, or 30 species) after hymenopteran parasitoids (van Lenteren

R. Buitenhuis (&) Vineland Research and Innovation Centre, Vineland Station, ON L0R 2E0, Canada e-mail: [email protected] G. Murphy Ontario Ministry of Agriculture and Food and Ministry of Rural Affairs, Vineland Station, ON L0R 2E0, Canada L. Shipp Agriculture and Agri-Food Canada, Harrow, ON N0R 1G0, Canada C. Scott-Dupree School of Environmental Sciences, University of Guelph, Guelph, ON N1G 2W1, Canada

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Author's personal copy Exp Appl Acarol

2012). Six species of predatory mites rank among the most important biological control agents used in augmentative biological control against various pests, i.e., the laelapids Gaeolaelaps aculeifer (Canestrini) and Stratiolaelaps scimitus (Womersley) (formerly referred to as Hypoaspis miles) (against sciarids) and the phytoseiids Phytoseiulus persimilis Athias-Henriot, Neoseiulus californicus (McGregor), Neoseiulus fallacis (Garman) and Amblyseius andersoni (Chant) (against mites), Neoseiulus cucumeris (Oudemans) and Transeius montdorensis (Schicha) (against thrips) and Amblyseius swirskii Athias-Henriot and Amblydromalus limonicus (Garman and McGregor) (against whiteflies, thrips, mites) (Cock et al. 2010; Van Lenteren 2012). In greenhouse production systems, these predators often form the backbone of biologically-based integrated pest management (IPM) programs. A review of these species in protected culture is provided by Gerson and Weintraub (2007). Most research on predatory mites has focused on their use and efficacy in greenhouse vegetables. However, an increasing number of growers of greenhouse ornamental plants also want to adopt biological control as their main pest management strategy and find that biological control programs developed for vegetables are not optimized for use in floriculture crops (Brødsgaard et al. 2004). Most ornamentals have short production cycles and no or few food sources (e.g., pollen or alternative prey), so biological control agents do not have time to establish in the crop, necessitating frequent inundative releases. Complex growing procedures, different environmental requirements, and other factors like the presence of multiple plant species and varieties, plant ages and pest species in the same greenhouse, all require careful selection of compatible biological control agents. Finally, because ornamentals are sold for their aesthetic value and little cosmetic damage is tolerated, there is little margin for error, unlike in most greenhouse vegetables where some damage on leaves is acceptable as long as fruit quality is not compromised. As part of this special issue on A. swirskii, this review focuses on the use of this predatory mite in greenhouse ornamental crops. The efficacy of A. swirskii is influenced by various factors within the greenhouse system (Fig. 1). The effects of different pest/prey species, the presence of other biological control agents and crop species are discussed at a plant scale, whereas the impact of production practices and environmental factors on A. swirskii are discussed on a greenhouse scale. Finally, the integration of A. swirskii in an IPM strategy is addressed.

Pest prey species Most information on the host range of A. swirskii is obtained from experiments in greenhouse vegetables. There are very few peer-reviewed articles that document the efficacy of A. swirskii in ornamental crops. This section describes the host range of A. swirskii in general, whereas the influence of crop species is discussed in a following section. Amblyseius swirskii was originally investigated as a new biological control agent against whiteflies, and preys on the eggs and young nymphal stages of both Bemisia tabaci (Gennadius) and Trialeurodes vaporariorum Westwood (Nomikou et al. 2001, 2002; Messelink et al. 2008; Calvo et al. 2011). In addition, it has proven to be an effective predator of larvae of several thrips species, specifically Frankliniella occidentalis (Pergande), Scirtothrips dorsalis Hood and Thrips tabaci L. (Messelink et al. 2006; Pijnakker and Ramakers 2008; Gerson and Weintraub 2007; Arthurs et al. 2009; Wimmer et al. 2008). Although A. swirskii feeds on spider mite eggs and nymphs (Momen and El-Saway

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Fig. 1 Factors influencing Amblyseius swirskii in greenhouse floriculture crops. 1 Prey species, 2 interactions among prey species, 3 intra-guild predation, 4 hyperpredation, 5 plant characteristics, 6 environmental factors, 7 production practices, 8 other IPM strategies

1993), it is not considered a primary control agent of this pest because A. swirskii is not able to enter the webbing produced by spider mites (Messelink et al. 2010) and has a clear preference for thrips compared to spider mite nymphs (Xu and Enkegaard 2010). Amblyseius swirskii successfully controls broad mites, Polyphagotarsonemus latus (Banks), on pepper and eggplants (van Maanen et al. 2010; Stansly and Castillo 2009) and begonia (R. Buitenhuis, unpublished data). Although eriophyid mites are rarely a problem on greenhouse ornamentals, A. swirskii can feed on tomato russet mite, Aculops lycopersici (Massee) on greenhouse tomato (Park et al. 2010, 2011). Despite its broad host range, several economically important pest species are not suppressed by A. swirskii. It does not perform well on aphids, scales or mealybugs (Ragusa and Swirski 1977; Hoda et al. 1986; Swirski et al. 1967). Amblyseius swirskii can survive on honeydew, although it is a poor food source (Ragusa and Swirski 1977). Many of the pests that are consumed by A. swirskii can occur simultaneously in a crop. This could lead to potential control problems if the predator switches to the more preferred prey reducing the predation pressure on the less preferred prey. Short-term satiation of A.

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swirskii in the presence of high numbers of greenhouse whitefly (T. vaporariorum) eggs was observed to cause delays in the control of thrips, although eventually thrips suppression was achieved (Messelink and Janssen 2008; van Maanen et al. 2012). However, at more moderate infestation levels, a positive effect on pest control was observed because predator densities increased through a numerical response to the alternate prey species. For example, control of greenhouse whiteflies was improved when thrips were present at low densities (Messelink et al. 2008) and spider mite damage was lower in the presence of thrips and/or whiteflies (Messelink et al. 2010). In addition to an increased numerical response in the presence of two prey species, Messelink et al. (2008) observed a positive effect of a mixed diet of thrips and whiteflies on A. swirskii juvenile survival and development rate, but not on oviposition rate. Calvo et al. (2011) also found an increased numerical response of A. swirskii to mixed prey populations of thrips and B. tabaci. The predator provided good control of both pest species alone, but no increased control was observed in the mixed prey treatments (Calvo et al. 2011). In conclusion, one of the main reasons for the success of A. swirskii is that it is able to target more than one important prey at the same time. Still, in situations with multiple prey species, the outcome of these types of interactions most likely depends on initial prey and predator densities.

Intra-guild predation and hyperpredation A single biological control agent rarely provides satisfactory levels of control, especially in ornamental crops with very low threshold levels for pests and pest damage. For example, A. swirskii only preys on first instar thrips larvae, and pupal and adult stages of thrips are not attacked. Strategic selection of one or more additional natural enemies (e.g., predatory bugs, soil predatory mites, rove beetles and/or entomopathogenic nematodes or fungi) attacking other thrips stages may be needed to provide fast, reliable and effective control. One of the most important factors to consider when designing an IPM program is the compatibility of the different biological control agents that are used to manage the target pest, for example intra-guild predation (IGP), and the compatibility of those that are selected for control of other pests in the same crop or greenhouse (e.g., hyperpredation). As a generalist with a wide host range, A. swirskii has a high potential to prey on other biological control agents. Interspecific predation and cannibalism is common in several species of phytoseiid mites (e.g., McMurtry and Croft 1997; Montserrat et al. 2006). Amblyseius swirskii in particular has been shown to be a predator of N. cucumeris (Buitenhuis et al. 2010b), Euseius scutalis (Athias-Henriot) (Rasmy et al. 2004) and Gynaeseius liturivorus (Ehara) (Sato and Mochizuki 2011). In addition, it prefers and shows better performance on N. cucumeris immature stages compared to their target prey, thrips (Buitenhuis et al. 2010b). No references were found to determine whether A. swirskii can prey on P. persimilis or N. californicus and potentially disrupt control of spider mites, although spider mite webbing might serve as a refuge against A. swirskii predation. The laboratory experiments mentioned above suggest that A. swirskii has the potential to interfere with control by other predators, yet this does not mean that these interactions will occur or be significant in a commercial crop. Predators may be able to coexist if they have different foraging strategies, plant or habitat preference or defense/avoidance mechanisms (Seelmann et al. 2007; Gnanvossou et al. 2003; Janssen et al. 2006, 2007; Onzo et al. 2014).

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In other cases, the negative effect of predation of A. swirskii on other biological control agents is clearly demonstrated: in greenhouse experiments, both A. swirskii and N. cucumeris consumed eggs of the aphid predator Aphidoletes aphidimyza, which caused aphid densities to increase significantly (Messelink et al. 2011, 2013). Therefore, growers should consider replacing A. aphidimyza with a different biocontrol agent if they need to use predatory mites for thrips and/or whitefly control. Within a greenhouse crop ecosystem, several biological control agents may also prey on, and potentially affect the performance of A. swirskii. However, no evidence of any negative effects of IGP on A. swirskii was found in the literature. In roses, Orius insidiosus (Say) does not have a preference for thrips larvae or A. swirskii adults and tends to switch to the most abundant prey (Chow et al. 2010). In a study on greenhouse peppers, fewer A. swirskii were found in flowers in tunnels where O. laevigatus was released, but this did not result in faster establishment or larger numbers of O. laevigatus (Weintraub et al. 2011). In both studies, using Orius species together with A. swirskii did not have a negative effect, but neither did it reduce thrips populations more than using only one predator (Chow et al. 2010; Weintraub et al. 2011). However, this combined release strategy is still recommended because of the increased control of another pest, i.e., whiteflies to minimize virus transmission (Calvo et al. 2012). Entomopathogenic fungi can also infect a wide range of arthropod species. However, (Shipp et al. 2003, 2012) found no effect of Beauveria bassiana Vuillemin on A. swirskii or N. cucumeris and in greenhouse trials thrips control by N. cucumeris was not affected (Jacobson et al. 2001). Finally, one of the main target prey of A. swirskii in ornamentals, thrips, can also consume A. swirskii eggs and female predators were observed to preferentially oviposit at sites without thrips, or to kill more thrips at oviposition sites to presumably protect their offspring (de Almeida and Janssen 2013).

Influence of host plant species Amblyseius swirskii is successfully used in a wide variety of ornamental crops such as chrysanthemums, roses, bedding plants, gerberas and poinsettias. However, the host plant species can affect the performance and establishment of A. swirskii, because leaf characteristics, plant structural complexity, chemical and physical defenses and availability of pollen as supplemental food vary with crop species. The large range of plant species and cultivars cannot possibly be tested individually for intrinsic negative impacts on an individual basis, but there will almost certainly be effects on the performance of A. swirskii. Recent reviews on the effect of plant attributes on biological control agents demonstrate the need to consider these attributes as an essential and interactive component of biological control practices (Cortesero et al. 2000; Schmidt 2014). The choice of biological control agent and timing, method and rate of release may have to be adjusted according to crop species. Alternatively, plant breeding for certain attributes may enhance predator efficacy. Moreover, the use of companion plants with desirable characteristics within the crop may increase the densities of the biological control agent. In a meta-analysis, Schmidt (2014) shows that increasing complexity of plant structures benefits many phytoseiid mites, especially the presence of domatia that may provide a refuge from hyperpredators and adverse biotic conditions. In a greenhouse crop, small potted ornamental pepper plants can be used as banker plants to build up and support A. swirskii populations for control of multiple pests (Xiao et al. 2012), because A. swirskii prefers the tuft domatia on the leaves of these plants as an oviposition site, leading to a

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positive correlation between the number of domatia and the number of eggs, nymphs and adults per plant (Avery et al. 2014). Banker plants supported high populations of A. swirskii (ca. 1,000 individuals) and resulted in a significant reduction of B. tabaci and F. occidentalis populations in the crop (Xiao et al. 2012). Leaf pubescence or trichomes can also affect phytoseiid mites in multiple ways (summarized by Schmidt 2014). Trichomes can trap pollen or fungal spores, making them easily available to predatory mites as an alternative food source. Depending on predator and prey species and their adaptation to trichome-dense environments, leaf pubescence can decrease or increase encounters between (intra-guild/hyper) predators and prey. Many phytoseiids exhibit preferences for pubescent leaves, and trichome presence increases phytoseiid abundance; however, a metaanalysis also indicates that this does not result in lower pest populations (Schmidt 2014). There are few studies on the effect of plant structural characteristics on A. swirskii in particular. Increasing trichome density results in decreased walking speed, and predation rate varies among leaf disks of different plant species, but is not related to trichome density (Buitenhuis et al. 2014b). Applying artificial leaf hairs (low densities of tiny fibers) and/or pollen to the canopy of plants lacking these resources enhances the persistence and egg production of A. swirskii (Loughner et al. 2011; Adar et al. 2014). Predatory mites may experience a negative effect from glandular trichomes, which trap the mites in their sticky excretions (van Haren et al. 1987; Ce´dola et al. 2002), yet this does not seem to be an obstacle for A. swirskii on tomato (Buitenhuis et al. 2014b; Park et al. 2010). However, nothing is known about the effect of toxic exudates of glandular trichomes on A. swirskii or about glandular trichomes on crops other than tomato. The effects of other plant defenses on A. swirskii have not yet been explored, but potentially include physical characteristics such as waxes and plant architecture and chemical defenses like plant secondary metabolites and induced plant resistance. An increasing number of studies address the role of plants in providing A. swirskii with alternative food sources such as pollen or nectar, or how to add supplemental food to plants that are lacking these resources, such as most ornamentals during the production phase. Laboratory experiments show that thrips are not the best food source for juvenile A. swirskii (Wimmer et al. 2008; Buitenhuis et al. 2010b; Delisle et al. 2015) due to the aggressive defensive behaviour of thrips larvae (Bakker and Sabelis 1989). It is likely that in an ornamental crop environment, juvenile stages feed (if possible) on alternative food sources such as pollen or easier prey species, although juvenile A. swirskii and N. cucumeris can feed on thrips prey killed by adult predators (Cloutier and Johnson 1993; R. Buitenhuis, unpublished data). For an omnivorous predator such as A. swirskii, consuming pollen provides essential nutrients (e.g., sugars) that are low in prey, permitting the predator to balance nutrient intake and leading to higher performance (Coll and SalomonBotner 2013). In crops such as sweet pepper, where pollen is available naturally, predatory mites (including A. swirskii) persist and build up populations (van Rijn et al. 2002; Xiao et al. 2012; Calvo et al. 2012). In crops without pollen, frequent augmentative releases of A. swirskii are needed to ensure a constant presence of predators, or exogenous pollen can be added to the crop as a supplemental food source. Recent studies show that adding apple pollen to chrysanthemum plants improves the establishment and population growth of A. swirskii, leading to better thrips control (Delisle et al. 2015). In greenhouse cucumber, the control of whiteflies by A. swirskii is improved by supplementing the predators with Typha sp. pollen (Nomikou et al. 2010). A survey of the literature reveals that pollen of 46 plant species have been tested as food for A. swirskii. It shows that A. swirskii feeds on pollen of a wide range of plant species, but that some pollen species are better food sources than others (see Goleva and Zebitz 2013, and references therein; Delisle et al. 2015). Possible

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methods to apply pollen are through banker plants, spraying or dusting, or point source applications in the crop (Goleva and Zebitz 2013). For example, flowering ornamental pepper plants are used as banker plants for A. swirskii to successfully control western flower thrips (F. occidentalis), chilli thrips (S. dorsalis) and whitefly (B. tabaci) on surrounding bean plants (Xiao et al. 2012). More A. swirskii are recovered from crops dusted with pollen using an electrostatic device, but this method still requires large amounts of pollen (Weintraub et al. 2009). Finally, pollen provided on pieces of rayon jute twine attached to pepper plants double A. swirskii populations in 2–3 weeks by providing supplemental food and oviposition sites (Adar et al. 2014). Other, non-plant-related supplemental food sources include factitious prey such as the mites Suidasia medanensis and Carpoglyphus lactis, Artemia franciscana cysts or Ephestia kuehniella eggs (Midthassel et al. 2013; Nguyen et al. 2014; Hoogerbrugge et al. 2008; Delisle et al. 2015). Contrary to some other phytoseiid mites (e.g., Euseius scutalis), A. swirskii does not regularly feed on plant sap (Adar et al. 2012; Nomikou et al. 2003). In practice, the manipulation of plant characteristics such as the use of banker plants and supplemental food to promote preventative establishment of A. swirskii in greenhouse crops is promising and some of the above-mentioned research is now applied in commercial greenhouse production systems (e.g., application of cattail pollen).

Production practices The requirement for an aesthetically perfect product means that there is little margin for error in pest control in greenhouse ornamentals. In addition, in potted flowers, cycles can be as short as 10 weeks and crops often lack suitable food sources such as pollen or alternative prey. This means that predatory mites have little opportunity to establish and increase in numbers. Biological control programs in these crops therefore put the emphasis on preventative releases at relatively high rates. Because prey density is (ideally) low, predator survival is limited and regular repeated releases, or a breeding system such as slow-release sachets, are needed to maintain sufficient predators in the crop. In potted ornamentals, the different stages of a crop cycle represent very different environments; pest management strategies such as release frequency and number of release points have to be adjusted for optimal control. In propagation, newly germinated seedlings or unrooted cuttings are establishing under mist with very high humidity and high plant density. With no (or limited) spacing between individual plants (or their containers), this is an ideal situation for introduction of bulk A. swirskii, as there is little off-target wastage from broadcast product. The environment is excellent, not only for the predatory mite, but also for complementary IPM strategies such as the use of insect pathogenic fungi. As the seedlings establish, the mist is reduced, resulting in a reduction in humidity; however, the high plant density in this production area continues to provide a beneficial environment, encouraging the use of broadcast product. After transplanting or when individual pots are spaced, the ambient crop environment changes. Larger space between pots results in increased air movement and reduced humidity. More importantly, however, the foliage of adjacent plants may no longer be touching, limiting the inter-plant mobility of A. swirskii. Additionally, the spacing between containers can result in considerable wastage of broadcast product that would fall between plants. For example, 15 cm pots spaced at 10/m2 and with no foliage extending past the lip of the pot cover \20 % of the bench or floor surface area. More than 80 % of broadcast product would be wasted at this stage of production. Other crops such as spring baskets hanging from the greenhouse structure can

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be considered completely isolated, not allowing movement of A. swirskii among them. In these types of situations, slow-release sachets on every plant may be a preferable option. The biggest challenge when using predatory mites in potted plants is to get good coverage of the crop by the mites. Because they cannot fly and wind speed in greenhouses are too low for aerial dispersal (Zemek and Nachman 1999), their movement within a greenhouse crop relies completely on walking. Although some short-term learned attraction to prey volatile cues is observed, this response wanes quickly. Inexperienced and starved A. swirskii likely search randomly for prey until arrested by prey cues (Nomikou et al. 2005). The layout of the crop is therefore one of the most important factors to consider when choosing an A. swirskii introduction method in a greenhouse. Buitenhuis et al. (2010a) demonstrated that A. swirskii effectively stay on the potted ornamental plant on which they are released; approximately a quarter of the mites walked down the pot to the ground, but only a few individuals were recovered from adjacent pots. Only when plant canopies of adjacent pots were touching, A. swirskii freely moved between plants. In a study with N. cucumeris, similar results were obtained in trays containing 15 gerbera seedlings (Buitenhuis et al. 2014a). This clearly demonstrates that predatory mites should ideally be added to every plant early in the crop cycle. Effective coverage of all plants can be more difficult to achieve in ornamentals than in greenhouse vegetable crops, but it is nonetheless critical to ensure that such coverage is achieved. The availability of different product formulations of A. swirskii facilitates its use in different situations and environments. Loose product is suitable for broadcasting in situations where contiguous crop cover minimizes wastage. Slow-release sachets provide intensive release of large numbers of predatory mites over a sustained period of time where plants are isolated from each other, and where the use of broadcast product would result in significant loss of predators that do not reach their target.

Environmental factors In greenhouses, factors such as temperature, relative humidity or vapour pressure deficit, light intensity, photoperiod and CO2 level can be precisely regulated to provide crops with ideal growing conditions. These environmental conditions also affect pests and their natural enemies directly or indirectly through changes induced in their host plants (Va¨nninen et al. 2010; Johansen et al. 2011; Lindquist and Short 2004). Some crops have environmental requirements that could negatively affect biological control agents. For example, crops such as kalanchoe and Christmas cactus (Schlumbergera) are succulents and provide a drier environment compared with other crops. Also greenhouse design (e.g., concrete floors, sub-irrigation compared to overhead irrigation and open floors, polyethylene vs. glass covering) leads to big differences in ambient humidity. When considering the influence of environmental conditions on small plant-dwelling insects and mites, it should be noted that the microclimate at the phylloplane can be very different from ambient conditions (Jewett and Jarvis 2001; Boulard et al. 2004) so conditions measured at the leaf surface provide a much better indication of the environment of pests and biological control agents. As A. swirskii originates from humid coastal areas in the Mediterranean (Porath and Swirski 1965; de Moraes et al. 2004), it is adapted to high temperatures and relative humidity. It is classified as a drought sensitive species and needs humid conditions (63 %, 11.4 hPa) for egg hatch (Ferrero et al. 2010). Development takes place between 11.3 and 37.4 °C and population increase is highest at 32 °C (Lee and Gillespie 2011). No research has been done on the influence of temperature and humidity limits on predation rate and

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survival, but it can be assumed that older nymphal stages and adult A. swirskii can still control pests under somewhat more extreme conditions than noted above if no establishment and persistence is expected. If slow-release breeding sachets are used, care must be taken not to expose them to conditions that exceed the tolerance limits of the predator for breeding (e.g., full direct sunlight) (Buitenhuis et al. 2014a). Biological control agents are often observed to have decreased efficacy under winter greenhouse conditions in temperate climates, even if the species does not enter diapause (Shipp et al. 2009). When A. swirskii first became commercially available in 2005, it was expected that it would replace N. cucumeris as the predator of choice for thrips control. Now, 9 years later, it is clear that both species have their place in thrips IPM. In temperate climates, A. swirskii provides better thrips control than N. cucumeris in summer, whereas both predators show similar efficacy in winter. In growth chamber trials, predation and oviposition rates of both predator species showed no major differences between simulated summer and winter greenhouse conditions, so the difference in performance in summer is likely related to better survival of A. swirskii (Hewitt et al. 2015). However, as N. cucumeris is significantly less expensive than A. swirskii, this predator might be the better option in winter (Hewitt et al. 2015). Unfortunately, similar comparative greenhouse studies between A. swirskii and other recently commercialized phytoseiid predatory mites (e.g., A. limonicus and T. montdorensis) have not yet been done. However, based on life table studies at different temperatures, A. limonicus seems to have a lower optimum temperature than A. swirskii and T. montdorensis (Knapp et al. 2013). Recently, there is much interest in the effects of new greenhouse technologies (such as artificial lighting and elevated CO2 level) on biological control agents, but no studies have been published yet on how they affect predatory mites such as A. swirskii. Preliminary studies found that development of A. swirskii (egg–egg) is significantly faster under high pressure sodium supplemental lighting compared to red and blue light-emitting diode lights. Also, the predation rate of A. swirskii is significantly higher under red LED lights than under blue LED (L. Shipp, unpublished data).

Place in IPM strategy Integration with other IPM strategies is important in optimizing the benefits of biological control. As discussed above, A. swirskii can interact negatively with other biological control agents in the laboratory; in most cases, however, there is little evidence that such interactions affect the outcome of control programs in commercial greenhouses (for an exception, see Messelink et al. 2011). Pesticides remain an important management tool in greenhouse crops, especially for pests (and diseases) without effective biological control agents, or to bring pest populations down to a level where biological control agents can provide control. Forty two active ingredients were tested for their impact on A. swirskii, of which five are considered ‘toxic’ ([75 % mortality) and seven ‘moderately toxic’ (50–75 % mortality), including commonly used pesticides for mites, whiteflies and thrips such as abamectin, spinosad, imidacloprid (spray), pyridaben and insecticidal soap (spray) (Gradish et al. 2011; Cuthbertson et al. 2012; Biobest 2014). Still, several active ingredients are compatible with A. swirskii, including flonicamid, pymetrozine, and biopesticides (Biobest 2014; Colomer et al. 2011; Cuthbertson et al. 2012). In some cases, the timing or application method of pesticides may reduce the negative effect of incompatible pesticides. Finding compatible pesticides is complicated by the loss of registered pesticides and the development of pest resistance, so

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it is expected that biological control will play an increasingly important role in greenhouse pest management (Buitenhuis et al. 2013). In addition, most tests of side-effects only measure mortality, whereas sublethal effects (e.g., changes in longevity, development, fecundity and predation capacity) are known to affect the physiology and/or behaviour of biological control agents (Desneux et al. 2007).

Conclusions and future research needs Amblyseius swirskii plays an important role in biological control programs for greenhouse ornamental crops. It is an effective predator of thrips and whitefly, especially in situations where both pests occur simultaneously or where higher temperatures prevail, and it complements other natural enemies that target different life stages of the same pests. Several product formulations exist to optimize the release of A. swirskii in different crop stages and environments. Plant characteristics such as domatia, trichomes and the presence of pollen affect A. swirskii, so release strategies have to be adjusted depending on crop species. Other strategies such as banker plants and the use of supplemental food sources provide innovative opportunities to further the use of A. swirskii and improve its costeffectiveness. The current cost of A. swirskii for thrips control in greenhouse ornamentals may limit its use as a like-for-like replacement of cheaper alternatives such as N. cucumeris. However, its wider host range (including whiteflies) and greater efficacy under summer conditions ensure its value in a well-rounded biological control program. Specifically, its efficacy against thrips, which has long been a serious obstacle to greater adoption of biological control in ornamentals, has the potential to enhance and broaden the uptake and success of such programs. Further research is needed specifically for optimizing the use of A. swirskii in greenhouse ornamental crops. This review has identified several knowledge gaps. For example, studies comparing thrips control among a number of predatory mites exist (e.g., Messelink et al. 2006); however, similar work is needed to compare A. swirskii efficacy against whitefly with other biological control agents such as parasitoids. Additionally, its interactions with spider mite predators (i.e., P. persimilis, N. californicus) are not well documented, although spider mite webbing might serve as a refuge against A. swirskii predation. Also, the importance of IGP in commercial crops should be determined. The potential impact of crop species on predatory mites has been discussed, but with hundreds of ornamental species being grown, more information is needed on their use in individual crops, especially those grown in large volumes (e.g., poinsettia). Little is yet known about the influence of physical plant characteristics and architecture or chemical defenses such as secondary metabolites or induced plant resistance on A. swirskii. For crops lacking pollen or with other challenges that impede establishment or persistence of A. swirskii, research should investigate the development of an application strategy for alternative food (i.e., pollen) or a companion/banker plant strategy. The cost of A. swirskii (3–5 times more expensive than N. cucumeris) has been noted as an obstacle to its greater use and research into mass-rearing techniques (e.g., artificial food sources) that could lower production costs making it more economical, would be valuable. Finally, as new pesticides are developed and commercialized, it is imperative that research continues on the compatibility of these new control products with biological control agents with emphasis not only on lethal (acute) but also sublethal (chronic) toxicity.

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Author's personal copy Exp Appl Acarol Acknowledgments The authors thank their colleagues and three anonymous reviewers for their helpful comments and suggestions on the manuscript.

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