Phytoseiid mites under environmental stress

Biological Control xxx (2016) xxx–xxx

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Biological Control journal homepage: www.elsevier.com/locate/ybcon

Review

Phytoseiid mites under environmental stress Noureldin Abuelfadl Ghazy a,b,c,⇑, Masahiro Osakabe a, Mohamed Waleed Negm d, Peter Schausberger e, Tetsuo Gotoh f, Hiroshi Amano a a

Laboratory of Ecological Information, Graduate School of Agriculture, Kyoto University, Kyoto, Kyoto 606-8502, Japan Agriculture Zoology Department, Faculty of Agriculture, Mansoura University, 35516 El-Mansoura, Egypt c Japan Society for the Promotion of Science, Chiyoda, Tokyo 102-0083, Japan d Department of Plant Protection, Faculty of Agriculture, Assiut University, 71526 Assiut, Egypt e Group of Arthropod Ecology and Behavior, Department of Crop Sciences, University of Natural Resources and Life Sciences, Peter Jordanstrasse 82, 1190 Vienna, Austria f Laboratory of Applied Entomology and Zoology, Faculty of Agriculture, Ibaraki University, Ami, Ibaraki 300-0393, Japan b

h i g h l i g h t s  We present an overview of the effect of environmental stressors on phytoseiid mites.  We discuss the strategies used by phytoseiid mites to avoid or tolerate environmental stress.  The factors that either promote or depress stress tolerance in phytoseiid mites are emphasized.

a r t i c l e

i n f o

Article history: Received 31 August 2015 Revised 30 December 2015 Accepted 28 February 2016 Available online xxxx Keywords: Abiotic Biocontrol Biotic Environment Predators Stressor

a b s t r a c t Predatory mites of the family Phytoseiidae are important natural enemies of phytophagous mites and small insects. Phytoseiid mites often experience a variety of stresses brought about by changing or fluctuating environmental factors in the field or laboratory or during their commercial production. These factors include abiotic stressors such as extreme temperature and humidity, ultraviolet radiation, and pesticides, and biotic stressors such as cannibalism, intraguild predation, food shortage, and pathogens, all of which affect the biocontrol potential of phytoseiid mites. The extent to which an environmental stressor may affect the biocontrol efficacy of phytoseiid mites depends on the characteristics of the species and on other concurrent stresses. In this review, we discuss the effects of environmental stressors on various biological and ecological aspects of phytoseiid mites, such as development, survival, reproduction, and predation, and the mites’ adaptation strategies to these stressors. Ó 2016 Elsevier Inc. All rights reserved.

Contents 1. 2.

3.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Abiotic stressors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1. Temperature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1.1. Cold . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1.2. Cold storage . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1.3. Heat . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2. Humidity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3. Ultraviolet radiation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.4. Pesticides . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Biotic stressors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1. Cannibalism . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2. Intraguild predation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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⇑ Corresponding author at: Laboratory of Ecological Information, Graduate School of Agriculture, Kyoto University, Kyoto, Kyoto 606-8502, Japan. E-mail address: [email protected] (N.A. Ghazy). http://dx.doi.org/10.1016/j.biocontrol.2016.02.017 1049-9644/Ó 2016 Elsevier Inc. All rights reserved.

Please cite this article in press as: Ghazy, N.A., et al. Phytoseiid mites under environmental stress. Biological Control (2016), http://dx.doi.org/10.1016/j. biocontrol.2016.02.017

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N.A. Ghazy et al. / Biological Control xxx (2016) xxx–xxx

3.3. 3.4.

4.

Food shortage . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Pathogens. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4.1. Fungi . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4.2. Protozoa . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4.3. Viruses. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4.4. Bacteria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1. Introduction No living organisms live alone or without environmental stress. This holds true for predatory phytoseiid mites (the family Phytoseiidae of the order Mesostigmata), which are well known natural enemies of spider mites and small insects. The potential of these predatory mites is always suppressed, and their performance lowered, by environmental stress. Phytoseiid mites are important natural enemies of several agricultural pests such as spider mites, thrips, and scale insects. Applied research on this group of mites started in 1839 with C.L Koch (Chant, 1992) and showed great progress in the 1960s when chemical control of spider mites was jeopardized by acaricide resistance in the field. There are currently 2709 described species of phytoseiid mites within 91 genera, although this species number includes 273 synonyms (Demite et al., 2014). There is no question that phytoseiid mites play a key role in the population dynamics of herbivorous prey species in the field, and this ability is taken advantage of in agricultural pest management. Commercial production of phytoseiid mites (as biological control agents) began in 1968, and 25 commercial products (species) were available by 2010 (van Lenteren, 2012). Attention is now focused on not only expanding the commercial production of these beneficial mites but also enhancing product quality. Phytoseiid mites are small, with a body shorter than half a millimeter long. Their biological potential is assured by high rates of development and reproduction, which are basically regulated by temperature and prey availability. Under favorable environmental and biological conditions, mites grow rapidly through four immature stages (egg, larva, protonymph, and deutonymph), and mated females, which have a pseudo-arrhenotokous reproductive system (Sabelis and Nagelkerke, 1988), produce several eggs per day. Thus, commercial mass production in the laboratory is relatively easy once the biological requirements of the mites have been met. However, in the field, it is uncommon to see large populations of phytoseiid mites, suggesting that a number of factors influence their abundance in the natural environment (Ferragut et al., 1987; Duso and Pasqualetto, 1993). Changing or fluctuating environments provoke a range of stresses in phytoseiid mites that adversely affect development, reproduction, survival, and overall biocontrol potential. Environmental stressors that affect phytoseiid mites may be broadly categorized as (1) abiotic stressors, which include temperature, humidity, ultraviolet radiation, and pesticides, and (2) biotic stressors such as cannibalism, intraguild predation within phytoseiid guilds, food shortage and pathogens. Also non-phytoseiid predators, such as non-phytoseiid mite predators, insect predators or spiders, may be important biotic stressors, which may exert both lethal and non-lethal effects (MacRae and Croft, 1996; Venzon et al., 2001; for overviews Gerson et al., 2003a, and Hoy, 2011). However, the knowledge on non-phytoseiid predators of phytoseiid mites is too scarce to account for it in a meaningful way in this review.

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The extent to which an environmental stressor influences the potential of phytoseiid mites is coupled with the magnitude and duration of the stress and the concurrency of one or more other stresses (i.e. interaction). Moreover, an environmental stress may be highly species-specific and may vary depending on developmental stage, physiological status (i.e. diapause capability), and sex. For instance, phytoseiid mites may tolerate extremely high or low temperatures or food shortages if the ambient humidity is high (Mori and Chant, 1966a; Stenseth, 1979; Gaede, 1992). Likewise, low humidity may be better tolerated if the temperature is modest and food is available (Walzer et al., 2007). Limited access to food increases the tendency of phytoseiid mites to cannibalize each other or renders them vulnerable to, and easily affected by, pesticides or attack by pathogens (Croft and van de Baan, 1988; Lighthart et al., 1988; Schausberger, 2003). However, phytoseiid mites may perceive environmental cues and exhibit a range of behavioral and physiological phenotypic plasticity (i.e. diapause, acclimatization, anti-predation behavior, or dispersal) in response to stressful conditions. In this review, we will discuss the different aspects of environmental stress and the strategies used by phytoseiid mites to avoid or tolerate stress. 2. Abiotic stressors 2.1. Temperature Temperature is perhaps the most important abiotic factor controlling the behavioral and physiological parameters of animals. Each phytoseiid mite performs optimally in terms of survival, development, and reproduction in a specific temperature range. However, because the mites are poikilotherms, their body temperature is influenced largely by, and varies with, the ambient temperature. Extremely low or high temperatures provoke stress and could have detrimental effects on phytoseiid mite populations; these effects can range from reduced survival and interrupted development and reproduction to death under chronic exposure. Nevertheless, some species of phytoseiid mites—if not all of them—have evolved adaptation measures such as hibernation to survive harsh temperature conditions. They may also recognize environmental cues early, before the harsh conditions begin, to enter a state of arrested activity such as reproductive diapause (Veerman, 1992). Here, we consider the responses, adaptation strategies, and factors that enable phytoseiid mites to cope with cold stress, including cold storage used for augmentation purposes in commercial enterprises, as well as heat stress. 2.1.1. Cold Cold stress is caused by the suboptimal temperatures like for instance during winter; it can be divided into chilling stress (from temperatures above zero) and freezing stress (from temperatures below zero) (Salt, 1961). Cold hardening is among the mechanisms used by arthropods to increase their cold tolerance. It is an inher-

Please cite this article in press as: Ghazy, N.A., et al. Phytoseiid mites under environmental stress. Biological Control (2016), http://dx.doi.org/10.1016/j. biocontrol.2016.02.017

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ent genetic trait and is triggered by environmental stimuli (mainly decreasing temperature and shortening day length), and it may require an extended period of weeks to months to fully develop (Salt, 1961; Teets and Denlinger, 2013). Cold hardening may occur as part of the diapause program for overwintering (in diapausing species) or independently (in nondiapausing species) (Denlinger, 1991). Cold-hardy arthropods are categorized as either freezing tolerant or freezing avoidant (Salt, 1961). Freezing-tolerant species rely on protective extracellular freezing at temperatures above their supercooling point (discussed below) and are found mostly in places with the harshest winters (Bale, 1996). Freezing-avoidant species (also known as freezing intolerant or susceptible) enhance their tolerance at subzero temperatures by removing icenucleating agents (e.g. by evacuating their gut contents), overwintering in protected microhabitats, or producing and accumulating antifreeze or cryoprotectant substrates such as polyols and sugars in order to increase their supercooling ability (Bale, 2002; Zachariassen and Kristiansen, 2003). According to published studies, phytoseiid mites are considered freezing avoidant (Morewood, 1992a, 1993; Broufas and Koveos, 2001a). The capability of arthropods to maintain their body fluids unfrozen is known as supercooling, and the lower limit of this process is called the supercooling point (SCP), the temperature at which body fluids spontaneously freeze (Salt, 1961; Sømme, 1982). Spontaneous freezing is a function of time and temperatures, meaning that ice may start to form at temperatures higher than the SCP if the exposure time is long and vice versa (Sømme, 1982). Phytoseiid mite species vary in their ability to supercool, and the SCP is profoundly affected by physiological status, body size, life stage, and the season in which the mites are collected. Phytoseiid mites diapausing or overwintering in the field have high supercooling abilities (i.e. lower SCP). Diapausing females of Euseius finlandicus (Oudemans) collected in winter had a SCP of 26.8 °C, whereas nondiapausing individuals collected in summer had a SCP of 20.1 °C (Broufas and Koveos, 2001a). Females of Typhlodromus pyri Scheuten, Typhlodromus (Anthoseius) rhenanus (Oudemans), and E. finlandicus overwintering in an apple orchard in Nova Scotia had SCPs between 29.05 °C and 31.39 °C (MacPhee, 1963). Likewise, females of T. pyri collected between July and September had SCPs of 17 °C to 19 °C, whereas those collected between October and March had SCPs ranging from -23 to 29 °C (Moreau et al., 2000). However, differences in SCPs between diapausing and nondiapausing phytoseiid mites were not evident when diapause was artificially induced in the laboratory (Morewood, 1992a; Broufas and Koveos, 2001a). This could be due to the fact that temperature fluctuation or gradual cooling occurs over an extended period under natural environmental conditions, whereas in the laboratory constant temperatures (usually <20 °C) are used for diapause induction (see Veerman, 1992). An inverse relationship between body size and SCPs has been observed in several species of phytoseiid mites; eggs and larvae had the highst supercooling abilities (Morewood, 1992a; Broufas and Koveos, 2001a; Coombs and Bale, 2014). Thus the small volume of eggs and larvae (which, in most phytoseiids, rarely feed) and the absence of ice-nucleating agents, which are common in other active stages, might contribute to these improved supercooling abilities (Leather et al., 1993). Acclimatization at mild low temperatures (a few degrees above zero) has no marked effect on the SCPs of phytoseiid mites, but it does enhance survival at temperatures above the SCP (Morewood, 1992a; Hart et al., 2002; Hatherly et al., 2004; Bale, 2005; Gotoh et al., 2005a). Tolerance to cold temperatures above the SCP is also enhanced in diapausing mites. Diapausing females of Phytoseius finitimus Ribaga, Neoseiulus umbraticus (Chant), and Amblysieus andersoni (Chant) tolerate cold temperatures two-to-

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three times greater than nondiapausing ones (Knisley and Swift, 1971; Wysoki, 1974; van der Geest et al., 1991). Acclimatization of diapausing mites further enhances their cold stress tolerance (van der Geest et al., 1991; Morewood, 1992a; Broufas and Koveos, 2001a; Hart et al., 2002). Although the SCP represents the lower temperature limit for survival of a freezing-avoidant organism, such organisms can be injured or killed if directly exposed to a temperature that is above their SCP—for example, if there is a sudden drop in temperature during late autumn or early spring (Lee et al., 1987; Broufas and Koveos, 2001b). The ability of an organism to increase its cold tolerance upon exposure to sudden changes in environmental temperature is known as rapid cold hardening (Chen et al., 1987; Lee et al., 1987). Rapid cold hardening (RCH) may be induced through brief exposure (minutes to hours) to sublethal stress conditions such as modest low temperature, high temperature, anoxia, or desiccation (Chen et al., 1987; Coulson and Bale, 1991; Nunamaker, 1993; Levis et al., 2012). This protection is accomplished by stimulating the synthesis of cryoprotective substrates such as glycerol and amino acids, as well as by changes in membrane fluidity (Chen et al., 1987; Lee et al., 1987; Overgaard et al., 2005; Michaud and Denlinger, 2006, 2007). Protection gained through RCH is lost shortly upon return to normal conditions (Lee, 2010). Unlike seasonal cold hardening, which is restricted to a specific life stage (i.e. the overwintering stage), RCH can occur in the developmental and nondiapausing stages (Denlinger, 1991; Lee, 1991). To date, RCH has been investigated in only two phytoseiid mite species, E. finlandicus and Neoseiulus californicus (McGregor) (Broufas and Koveos, 2001b; Ghazy and Amano, 2014). In E. finlandicus, exposure of nondiapausing females to 10 °C and diapausing females to 11.5 °C for 2 h resulted in 10% and 20% survival, respectively. Acclimatization of diapausing females at 0 °C to 10 °C and nondiapausing females at 5 °C for 4 h or by gradual cooling (0.4 °C per min) resulted in nearly 90% survival. In N. californicus, 62% of adult females survived 10 °C for 2 h, but the survival rate reached 75% when acclimatized first at 5 °C for 1 h. Also, immature stages of N. californicus exhibited RCH capability, with the egg stage being the most tolerant. Induction of RCH was also possible by acclimatization at 30 °C for 2 h or by anoxia (oxygen-free nitrogen) for 1–2 h. The mechanism by which exposure to high temperature or anoxia increases cold tolerance can be attributed to the accumulation or synthesis of polyols (Coulson and Bale, 1991; Yoder et al., 2006). 2.1.2. Cold storage Phytoseiid mites and many other economically important natural enemies are short-lived. For them to be used efficiently in biocontrol, mass production techniques need to ensure their availability at times of high demand. Storage of natural enemies at low temperatures—often below the thermal developmental threshold—is a valuable tool that allows extension of their shelflife by minimizing metabolic activity (Leopold, 1998). In this manner, natural enemies can be accumulated in large numbers, thus increasing their availability to end-users. Chilling injury, desiccation, and starvation are major threats to organism survival during storage and to post-storage reproductive potential (De Bach, 1943). These injuries can be mitigated by supplying the proper prey prior to storage; optimizing temperatures, relative humidity (i.e. vapor pressure deficit VPD), and photoperiod; selecting the most tolerant life stage; and using mites in diapause when applicable. For instance, at a range of low temperatures (0 °C to 15 °C), markedly high survival of N. californicus was maintained when VPD kept as low as 0.0 kPa (Ghazy et al., 2012a,b,c, 2014a). The advantage of storing phytoseiid mites under saturated water vapor conditions has also been observed in Phytoseiulus persimilis AthiasHenriot and Neoseiulus cucumeris (Oudemans) (Gillespie and

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Ramey, 1988; Morewood, 1992b; Nicoli and Galazzi, 1998). Low VPD is reported to help avoid desiccation stress during prolonged storage. In N. californicus, survival is substantially longer for adult mated females than for other developmental stages, and survival is enhanced when the females are fed diapausing spider mites Tetranychus urticae Koch before cold storage (Ghazy et al., 2012a, 2013, 2014b). Likewise, Luczynski et al. (2008) reported that young females of P. persimilis tolerate prolonged cold storage without their quality being impaired. These observations suggest that nutrient content, such as eggs and sperm in the adult female’s body, might have a positive effect on their cold tolerance. Diapausing prey are rich in nutrients, cryoprotectants, and antioxidants that might also increase the tolerance of predators to stress conditions (Ghazy et al., 2014b, 2015). Diapause propensity controlled by photoperiod and low temperature, if it exists, is of great advantage for cold storage of phytoseiid mites (Broufas et al., 2006). Provision of food (prey or alternative food) during cold storage increases survival. Providing P. persimilis with T. urticae eggs, bean leaflets infested with T. urticae or Tetranychus kanzawai Kishida, or honey significantly improved survival during storage and poststorage reproduction (Hamamura et al., 1978; Morewood, 1992b). However, storage without food is more valued to avoid the introduction of undesired pest organisms (Suzuki, 2012). Spraying P. persimilis with cryoprotectant and carbohydrate chemicals before cold storage may be of limited value for long-term cold storage (Riddick and Wu, 2010). It is frequently reported that cold storage (particularly when the storage duration is long) reduces the predator’s post-storage reproduction and dispersal ability (Price et al., 2002; Takano-Lee and Hoddle, 2002). However, the extent to which cold storage impacts on the biological characteristics of phytoseiid mites depends not only on storage duration but also on the temperature used, together with other environmental factors (Fig. 1; Ghazy et al., 2012a,b,c, 2014a,b). 2.1.3. Heat Energy demand progressively increases as temperature increases. Predatory mites initially become more effective in terms of predation, dispersal, and oviposition under rising temperatures (Everson, 1980; Ferragut et al., 1987). The dispersal speed of N. californicus increases markedly at 35 °C compared to lower temperatures (Auger et al., 1999). However, at temperature extremes (>40 °C) the predatory mites P. persimilis and Phytoseiulus macropilis (Banks) cease movement and enter a heat coma (Coombs and Bale, 2013). Rising temperatures coupled with low relative humidity

Days in cold storage

80

80% survival

60

40

20

0 RH

RH & Temperature

RH & Temperature & Nutrition

Fig. 1. Schematic representation of the effects of optimizing the abiotic and biotic environments on survival (80%) of the adult females of the predatory phytoseiid mite Neoseiulus californicus during cold storage. Optimum conditions were 100% relative humidity, 7.5 °C during cold storage, and nutrition is diapausing T. urticae as prey for one generation prior to cold storage. Based on the work of Ghazy et al. (2012a, 2014a,b).

in summer cause a decrease in phytoseiid mite populations, suggesting that this period is critical to their survival, particularly when plants or protective areas are not available (Duso and Pasqualetto, 1993). Even though prey were abundant, a decline in the population of Euseius stipulatus (Athias-Henriot) was observed in a Spanish citrus-growing area when the temperature rose to 34 °C to 38 °C for a few days accompanied by low humidity (Ferragut et al., 1987). Species divergences also exist. High temperatures in Northern Italy from August onward caused a dramatic decline in the population of released T. (T.) pyri, whereas the population of Kampimodromus aberrans (Oudemans) released at the same time increased, replacing T. (T.) pyri (Duso and Pasqualetto, 1993). High temperatures can favor the rapid build-up of pest populations and limit the efficiency of phytoseiid mites, leading to instability in prey–predator systems (Ebssa et al., 2006). Ferragut et al. (1987) speculated that declining survival and reproduction due to high temperatures can be attributed to mortality or reduced motility of the sperm. Recently, Zhang et al. (2014) provided evidence that exposure to extreme temperatures enhances the accumulation of reactive oxygen species (ROS) as a result of antioxidant system deficiency. The use of selective pesticides (i.e. to compensate for predators declining) or native phytoseiid species that can tolerate high temperature and low humidity, or the introduction of natural enemies that are adapted to such conditions, may give better plant protection during periods of high temperature (Ferragut et al., 1987). 2.2. Humidity In order to maintain physiological integrity, arthropods must keep their body water content within tolerable limits (Hadley, 1994). Water constitutes about two-thirds of the body mass in mites (Yoder, 1998). Phytoseiid mites are tiny organisms (0.2– 0.5 mm long) and are characterized by a large surface area-tovolume ratio and water loss through transpiration is a function of temperature and saturation deficit (Arlian and Veselica, 1979; Yao and Chant, 1989; Gaede, 1992). Most phytoseiid mites are susceptible to dry conditions but are able to absorb water vapor from unsaturated air as long as the relative humidity is above their critical equilibrium activity (CEA) (i.e. the point at which water loss equals water gain) (Stenseth, 1979; Gaede, 1992; Bakker et al., 1993; Yoder, 1998). CEA values vary according to species. For instance, at 20 °C, the CEAs of Typhlodromus (=Galendromus,=Metaseiulus) occidentalis Nesbitt and P. persimilis are at 86% and 90% relative humidity, respectively (Gaede, 1992; Yoder, 1998), suggesting that T. occidentalis may preferentially be used in arid areas. Eggs are considered the life stage most sensitive to dry conditions, because mobile life stages are able to replenish their water content through feeding, drinking free water, or searching for favorable sites (van Dinh et al., 1988; Bakker et al., 1993; Walzer et al., 2007). The hatchability of phytoseiid mite eggs usually shows a sigmoidal response, being minimum at humidity near zero and maximum near saturation (Bakker et al., 1993). Variations in susceptibility to dry conditions exist among species and strains inhabiting different climatic regions. In species from humid zones, egg hatchability at relative humidities below 60% and temperatures ranging from 20 °C to 32 °C is zero or very poor, whereas eggs from species from dry zones hatch at relative humidities as low as 30% and temperatures ranging from 20 °C to 25 °C (Stenseth, 1979; Ferragut et al., 1987; van Dinh et al., 1988; Kramer and Hain, 1989; Perring and Lackey, 1989; Bakker et al., 1993; Croft et al., 1993; Negm et al., 2014). Larvae of phytoseiid mites are small, having limited ability to ingest free water or to search for a favorable habitat; they are therefore considered more susceptible to dry

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conditions than are other mobile life stages (Croft et al., 1993; Shipp and van Houten, 1997). Co-occurrence of high temperatures and limited access to prey can markedly increase the adversity of drought stress, whereby the mites lose water, dehydrate, and eventually die; on the other hand, high humidity may alleviate the severity of both temperatures and food shortages (Mori and Chant, 1966a; Stenseth, 1979; Gaede, 1992). Under conditions of abundant food, moderately low humidity may have only a minor effect on phytoseiid mite activity, because water loss is compensated for by liquid intake from their prey (Mori and Chant, 1966b; de Courcy Williams et al., 2004; Walzer et al., 2007). In this context, the predation rate may increase with decreasing relative humidity (Shipp et al., 1996). This response also remains temperature dependent. For instance, P. persimilis controls T. urticae at relative humidities as low as 40% and 21 °C but fails to do so at the same relative humidity and 27 °C (Stenseth, 1979). On plants, humidity at the microhabitat level (i.e. within the leaf boundary) is to some extent higher than the atmospheric humidity and is affected by plant water content, plant physical features, evapotranspiration, and irrigation. Relative humidity may, therefore, have little effect on phytoseiid mites (Ferro and Southwick, 1984; Croft et al., 1993; Auger et al., 1999; Jones et al., 2005). However, van Dinh et al. (1988) suggested that plant evapotranspiration would be effective for improving egg hatching if the ambient humidity was intermediate (50–60% relative humidity). As with tolerance to other environmental stresses, drought tolerance depends on physiological adaptations, such as diapause (i.e. diapausing individuals have more tolerance to drought) and the composition of membrane lipids (i.e. species abundant in lipids have higher water loss resistance and often inhabit dry zones) (Hadley, 1994; Koveos and Broufas, 2001). It is therefore useful when planning an outdoor release program of phytoseiid mites to use natural enemies from a climatic zone that matches the climate of the intended release zone (van Dinh et al., 1988; Mangini and Hain, 1991; Bakker et al., 1993; Croft et al., 1993; Ferrero et al., 2010). 2.3. Ultraviolet radiation Although the effects of solar ultraviolet-B radiation (UVB; 280– 320 nm wavelength) on spider mites had been pointed out by Barcelo (1981) and evidence of the biological impact of UVB radiation was reported during the last decade (Santos, 2005; Suzuki et al., 2009), it was not until recently that this has been taken into serious account. Many plant-dwelling mites live primarily on the lower leaf surfaces of host plants (Sudo and Osakabe, 2011). Solar UVB radiation has a deleterious effect on mites on the upper leaf surfaces, decreasing survival rates of eggs and juveniles and reducing egg production (Ohtsuka and Osakabe, 2009; Sakai and Osakabe, 2010). Escaping from the biological impacts of solar UVB radiation may therefore be one reason why many mite species remain on the lower leaf surfaces. The finding that the citrus red mite, Panonychus citri (McGregor) (an upper-leaf-surface user) possesses higher tolerance to UVB radiation than does the two-spotted spider mite, T. urticae (a lower-leaf-surface user) supports this hypothesis (Fukaya et al., 2013). Because solar UVB irradiance is highest in summer, Barcelo (1981) estimated that the most serious impact would be in summer. However, the most deleterious effects of UVB radiation are observed in spring and the lowest in autumn (Sakai et al., 2012). This is caused by the fact that the extent of biological damage is determined by cumulative irradiance and not by the intensity of UVB (Murata and Osakabe, 2013). The lower temperature in spring prolongs development time and thus increases cumulative UVB irradiance, resulting in increasing mortality (Sakai et al., 2012).

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This suggests that there is potential for the combined effects of solar UVB radiation and temperature on seasonal and diurnal changes in the population dynamics of plant-dwelling mites. Phytoseiid mites are more vulnerable than spider mites to UVB radiation (Tachi and Osakabe, 2012), but the vulnerability of phytoseiid mites to UVB varies among species. Phytoseiulus persimilis possesses higher UVB tolerance than does N. californicus or Neoseiulus womersleyi Schicha (Tachi and Osakabe, 2012). According to Onzo et al. (2010), Amblydromalus (=Typhlodromalus) manihoti (Moraes) and Euseius fustis (Pritchard and Baker) can avoid the lethal effects of UVB irradiation by remaining on the lower leaf surfaces of cassava plants, whereas Typhlodromalus aripo De Leon still suffers UVB damage on the lower leaf surfaces and needs to hide inside domatia at the apex of cassava plants to avoid damage. UVB-absorbing compounds, including leaf phenolics (e.g. flavonoids), accumulate in leaves and act as selective sunscreens that reduce the penetration of UVB through the leaf epidermis, protecting sensitive targets in mesophyll cells (Rousseaux et al., 2004; Tegelberg et al., 2004). Therefore, leaves serve as shelter from solar UVB radiation to small arthropods on the lower leaf surfaces, and the protection may be more effective if individuals hide inside domatia. Phytoseiulus persimilis only rarely lays eggs within leaf domatia, whereas N. californicus frequently lays eggs there (Palevsky et al., 2008). Neoseiulus womersleyi, A. manihoti, and E. fustis have spatial distributions similar to that of N. californicus, whereas T. aripo remains inside the apex domatia during daytime (Onzo et al., 2003). Their spatial distributions are likely to be correlated with their vulnerability to UVB radiation (Table 1). Moreover, the most vulnerable T. aripo migrates from the apex domatia to leaf surfaces during the night to forage (Onzo et al., 2009). Although harsh climatic conditions such as low humidity, high temperature, and rain are factors that may confine T. aripo to their apex domatia during daytime, their diurnal migration between the apex domatia and leaves is also likely to be an adaptive response to solar UVB radiation. With regard to the spectrum-specific biological impact of UV radiation, bioassay using monochromatic UV radiation has revealed a drastic change in lethal effects between 300 and 310 nm: all eggs of N. californicus hatched after irradiation with UVB at >310 nm, whereas none hatched at <300 nm (Tachi and Osakabe, 2014). A similar change has also been observed in T. urticae between 300 and 320 nm (310 nm was not tested; Sakai and Osakabe, 2010). Sakai and Osakabe (2010) also found no behavioral avoidance of T. urticae from deleterious UVB radiation at 280 or 300 nm; however, the mites avoided UVA at 320 and 340 nm. Tetranychus urticae females may be incapable of recognizing UVB and may therefore exploit UVA as a source of information to avoid ambient UVB radiation (Suzuki et al., 2013). In contrast, N. californicus rapidly escapes from leaf areas irradiated with UV at shorter wavelengths ranging from 300 to 380 nm when there is no prey (T. urticae) or when only eggs of T. urticae without webs are present (Tachi and Osakabe, 2014). When both webs and eggs of T. urticae are present on the leaves, N. californicus does not escape from leaf areas irradiated with UV at 310–380 nm, but it still shows avoidance behavior if the area is irradiated with UVB at 300 nm (Tachi and Osakabe, 2014). The presence of spider mite webs is likely being a foraging cue and may act as a partial shelter from UV radiation for phytoseiid mites (Hoy and Smilanick, 1981; Sabelis and van de Baan, 1983; Dicke et al., 1990; Yano and Osakabe, 2009; Shinmen et al., 2010; Tachi and Osakabe, 2014); it also affects the prey preferences of phytoseiid mites (Furuichi et al., 2005). At safe wavelengths (>310 nm) the presence of intact prey residues acts to detain N. californicus and overcome its urge to escape from UV radiation, whereas when irradiated at 300 nm N. californicus disregards prey cues and escapes,

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Table 1 Tolerance of mite species to UV radiation, and distributions of species on leaves.

Based on the work of Onzo et al. (2010), Tachi and Osakabe (2012), and Fukaya et al. (2013)

maybe because of the harmfulness of this wavelength. Such a shift in behavioral response would affect the mite’s spatial distribution. Studies into the effects of solar UVB radiation on the long-term reactions of plant-dwelling mites are therefore also required to elucidate the mites’ spatiotemporal distribution. UVB-induced DNA damage in organisms, for example through the production of cyclobutane pyrimidine dimers (CPD) and 6,4photoproducts or 6,4 pyrimidine-pyrimidones, has been reviewed by many authors (e.g. Sinha and Häder, 2002; Häder and Sinha, 2005). Two major mechanisms are known to repair these DNA lesions in a wide range of taxa: photo-enzymatic repair (PER; Malloy et al., 1997; Weber, 2005) and excision repair (dark repair pathway: base or nucleotide excision repair; Sancar, 1996). The former is a simple repair system mediated by photolyase, whereas the latter is a complex pathway that replaces damaged DNA with new nucleotides (Sinha and Häder, 2002). Photoreactivation from UVB damage in spider mites was first reported by Santos (2005), and factors affecting photoreactivation effects were evaluated by Murata and Osakabe (2014). We have recently found photoreactivation in phytoseiid mites (unpublished data); however, the role of photoreactivation in plant-dwelling mites is still largely unknown. Overall, the influence of solar UVB radiation on phytoseiid mites and their interaction with prey mites is likely to be substantial. Solar UVB radiation may also affect community compositions of plants, herbivorous arthropods, and predators through the refuge provided by plant architecture or chemical components shielding against UV radiation and through variations in the UV vulnerability or tolerance of predators and prey. Solar UVB irradiance and temperature are roughly determined by solar elevation. However, the seasonal changes are not necessarily synchronized (Sakai et al., 2012), resulting in seasonal heterogeneity in interactive or integrated effects on mite communities. Therefore, the biological impact of solar UVB radiation may be an important stress in both spider mites and phytoseiid mites, and elucidating the effects of solar UVB radiation on plant-dwelling mite communities and their adaptive strategies is worthwhile. 2.4. Pesticides Synthetic pesticides have long been used for manipulating agricultural pest populations. Part of the negative environmental impact of pesticides is their side effects on natural enemies such as phytoseiid mites. This poses major limitations to the success of using phytoseiid mites as a component of integrated pest management (IPM) programs. Pesticide toxicity in phytoseiid mites has been extensively studied and reviewed, particularly from an ecological perspective (Croft, 1976; Croft et al., 1982; Croft and van de Baan, 1988; Gerson et al., 2003b; Hoy, 2011). The activities of predatory mites (e.g. behavior, development, fecundity, and survival) may be altered by the non-target effects of non-selective

pesticides used to manage pests (Croft, 1982). Pesticide application may remain species-specific but may still also affect the abundance and composition of naturally occurring or introduced phytoseiid mites (Amano et al., 2004; Szabó et al., 2014). Pesticide applications can affect phytoseiid mites in two ways: (1) by causing harmful side effects (Croft, 1990) and (2) by inducing pesticide resistance (Croft and Meyer, 1973; Croft et al., 1982; Hoy, 1984; Lee et al., 2002). Pesticide-induced side effects on phytoseiid mites include reduced consumption rate, developmental delay, reduced fecundity, egg non-viability, sex alteration, and population extinction (Croft, 1990; Stavrinides and Mills, 2009; Lima et al., 2015). Nevertheless, the extent to which pesticides induce negative impacts on phytoseiid mites depend on the exposure method and duration, the pesticide group and concentration, and the phytoseiid species, population, and strain (Zhang and Sanderson, 1990; Nadimi et al., 2008; Talebi et al., 2008; Pozzebon and Duso, 2010; Hoy, 2011). For example, an application of imidacloprid to control major pests in clementine plants did not affect the efficacy of P. persimilis to control T. urticae but it did affect N. californicus (Argolo et al., 2013). Differential susceptibility to pesticides were also observed between Galendromus occidentalis (Nesbitt) and Amblydromella caudiglans (Schuster) exposed to carbaryl, azinphosmethyl, and bifenazate where the latter experienced higher mortality (Schmidt-Jeffris and Beers, 2015). An increased mortality and decreased fecundity of Amblyseius swirskii Athias-Henriot was associated with increased concentration of fenpyroximate (Lopez et al., 2015). Broad-spectrum pesticide may lead to outbreaks of pest mites due to extinction of phytoseiid mites (Funayama, 2015). Ambient abiotic conditions such as the temperature during and after treatment affect pesticide toxicity. Pesticide toxicity to adult females of P. persimilis is positively correlated with temperature (Everson and Tonks, 1981). High temperatures apparently exacerbate the toxic effects of pesticides, but this association remains poorly understood, at least in mites. Resistance to pesticides is a favorable feature in integrated pest management. The factors that either promote or depress the evolution of pesticide resistance in phytoseiid mites may include: (1) dispersal and gene flow among populations (resistance is slowed/ reversed when pesticide-susceptible individuals move from untreated areas to treated areas); (2) reproduction rate (species with high reproduction rates have many generations per year, and resistance develops faster); and (3) prey availability (limited prey availability as a result of killing of prey by pesticides leads to starvation) (Croft and van de Baan, 1988; Dunley and Croft, 1992). The ability of a predatory mite to feed on alternative diets, particularly pollen can alleviate the sublethal effects of pesticides (Pozzebon et al., 2014). Specialist phytoseiid mites commonly demonstrate stronger resistance to pesticides than generalists, likely reflecting stronger selection pressure on specialists than

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generalists (Downing and Moilliet, 1967, 1972; Argolo et al., 2013; Schmidt-Jeffris and Beers, 2015). An exception to this general pattern is the recently reported stronger pesticide resistance of E. stipulatus and N. californicus, compared to P. persimilis, in citrus orchards (Argolo et al., 2014). Argolo et al. (2014) further suggested the use of P. persimilis, instead of E. stipulatus, as indicator species for non-target effects of pesticides in citrus, to prevent T. urticae control failure. It is also recommended that when synthetic pesticides are integrated with specialist predators, the synthetic pesticides should not kill all the prey, to allow persistence of the predator population (Amin et al., 2009). Interaction between the acute effects of pesticides and other stressors may synergistically affect mortality rates in phytoseiid mites, but this effect has yet to be comprehensively documented. Although many studies have investigated the side effects of pesticides on phytoseiid mites, the major evaluation criterion has been mortality. Behavioral and physiological consequences are also important to understand the fundamentals of resistance or susceptibility (Desneux et al., 2007). In a recent study, Beers and SchmidtJeffris (2015) reported that certain pesticides are not necessarily toxic to the phytoseiid mite G. occidentalis but may induce negative behavioral effects (e.g. repellency). To entirely assess risks before pesticide registration, the relationship between laboratory experiments (usually performed under ideal conditions) and exposure under field conditions (fluctuating conditions) should be considered. The compatibility between phytoseiid mites and pesticides is of great importance in IPM. Selective or reduced-risk pesticides that can be used to control mite pests and promote balanced predator–prey ratios in agro-ecosystems without adversely affecting the potential of phytoseiid mites are of prime importance (Villanueva and Walgenbach, 2005; Döker et al., 2015). Any IPM program should involve the use of resistant strains of predators in combination with the use of selective acaricides applied at less harmful concentrations, monitoring of predator–prey ratios, and spot treatments of small portions of the field early in the season (Hoy, 2011).

3. Biotic stressors 3.1. Cannibalism Environmental stressors experienced during early life commonly have significant effects on phenotypic development and on key life-history traits such as survival, growth, development, body size, and/or reproduction (e.g. Stearns, 1992; Nylin and Gotthard, 1998; Monaghan, 2008). An important context in early life of many animals is the social environment, and an associated stressor is the risk of cannibalism. Cannibalism is a widespread phenomenon in animals and an important selective force shaping prey morphology, physiology, and behavior (Fox, 1975; Elgar and Crespi, 1992). Similar to classical and intraguild predation and apart from lethal effects, the risk of cannibalism alone may exert non-lethal, non-consumptive effects on potential prey, such as changing activity levels, changing residence sites, retarding development, etc. and may thus result in stress-related individual phenotypic alterations (Lima, 1998). The effects of cannibalism risk not only apply directly to potential prey but also extend to the parents of potential prey, which are themselves not at risk but are caring for their offspring. While pertinent population and community models commonly account for the cascading effects of cannibalism per se (e.g. Claessen et al., 2004; Rudolf, 2007a), the implications of non-consumptive effects (i.e. cannibalism risk–induced changes in behavior and life history) at the population and community levels are by far less well studied and understood (Rudolf, 2007b). This is

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also and particularly true for plant-inhabiting predatory mites of the family Phytoseiidae (Schausberger, 2003). Albeit the level and intensity of cannibalism vary under the influence of intrinsic factors (such as species, life stage and phase, or physiological and motivational state) and extrinsic factors (such as food availability, habitat heterogeneity, presence of other predators, or abiotic conditions), more or less every phytoseiid mite species looked at for cannibalism has proven to be potentially cannibalistic (Schausberger, 2003). As with many other animal taxa, small immature individuals are at risk of being preyed upon by larger, older, or more mature individuals (Elgar and Crespi, 1992; Schausberger, 2003). Accordingly, in most, if not all, phytoseiid species cannibalism risk is the highest, and represents an important environmental stressor, in the very early life stages and phases. Starved adult gravid females and protonymphs threatening larvae are the most frequently observed cannibalism-related pairings and events, respectively. Eggs are relatively well protected from cannibalism by their shape and chorion, making them difficult to rupture and pierce. However, the first mobile stage—the larva—is highly vulnerable. Compared with more advanced life stages, larvae are small and soft-bodied, have only six legs and are thus less well able to run away when detected and attacked (Schausberger, 2003). In terms of foraging and the associated ability to molt to the next stage (the protonymph), phytoseiid larvae can be assigned to three different types: non-feeding, facultative feeding, and obligatory feeding (Zhang and Croft, 1994; Schausberger and Croft, 1999a; Chittenden and Saito, 2001). Schausberger and Croft (1999a) suggested that these three feeding types may also correlate with the anti-cannibal strategies of the larvae. Larvae that do not feed usually move little until molting; they are relatively defenseless once detected and thus tend to hide and be cryptic. In contrast, larvae that have to feed (and to a lesser extent also those that can feed but do not need to do so) can move more quickly and tend to escape once detected; they are also stronger in self-defense when attacked because they are strengthened by the uptake of nutrients (Schausberger, 2003). Recent studies suggest that the anti-cannibal strategies of prey larvae may also depend on the hunting strategies of the cannibal, as has been shown for intraguild predation scenarios (Walzer and Schausberger, 2013). The occurrence and level of cannibalism also vary and interact with other environmental stressors such as, for example, general food availability, the presence of heterospecific competitor mites, or abiotic conditions. Abundant food commonly lowers food stress and consequently also the propensity for cannibalism (e.g. Schausberger, 2003; Zhang et al., 2015). If species share (micro)habitats and/or prey, species discrimination abilities may function as mechanism to avoid kin cannibalism and allow going for another similarly nutritious meal and at the same time removing a competitor (Schausberger, 1997; Schausberger and Croft, 1999b; Zhang et al., 2015). Different stressors are interdependent and, depending on the context and species, one and the same stressor may either aggravate or relax a given cannibalism risk. For example, in species with social recognition abilities, such as in P. persimilis (Schausberger and Croft, 2001; Schausberger, 2004), food stress arising from low local prey availability may induce premature dispersal, thereby relaxing local competition and reducing the risk of cannibalism on familiar, possibly kin, individuals staying behind (Zach et al., 2012). In contrast, in species without social recognition, food stress may locally increase the risk of cannibalism and intensify its occurrence. Abiotic stress, such as that arising from low relative humidity, may, for example, intensify cannibalism risk because of increasing individual needs to obtain liquids for internal water balance (e.g. Croft et al., 1993). Also, maternal behavior and effects may play roles in cannibalism stress management, for example by reducing the risk of sibling and/or group-member

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cannibalism by selective egg placement (Schausberger and Hoffmann, 2008) or via the provisioning of offspring with certain hormones or nutrients (Vangansbeke et al., 2014). Cannibalism is more of a risk in species living in groups because of high frequencies of intraspecific encounter, which is common in species adapted to exploit ephemeral food patches, for example in Phytoseiulus spp. adapted to exploiting colonies of their spider mite prey. Within these patches, individuals compete for food, mates, and/or space. In such scenarios, cannibalism may be considered an extreme form of exploitation competition, but it can additionally be seen as a way of obtaining nutrients that provide behavioral and life-historical advantages unobtainable for non-cannibals. Group-living, and when young tend to stay at their natal sites, entails a high risk of kin cannibalism, selecting for social recognition abilities (Schausberger and Croft, 2001; Schausberger, 2007). These abilities may primarily evolve for the sake of cannibalism avoidance but can then affect, and have relevance in, many other life activities and contexts, such as mate choice (Enigl and Schausberger, 2007), foraging (Strodl and Schausberger, 2012a, 2013), anti-predator behavior (Strodl and Schausberger, 2012b), and/or dispersal and dispersion (Zach et al., 2012; Muleta and Schausberger, 2013). Individuals deprived of any social contact early in life may experience higher stress levels and become more aggressive cannibals later in life than those growing up in groups (Schausberger, 2004). In species with a more scattered distribution or in which the young move away from their natal sites soon after hatching (e.g. in species that have obligatory feeding larvae such as Euseius spp.), dispersal and the need to search for food, respectively, can function as anti-cannibalism mechanisms (Schausberger and Croft, 1999a; Chittenden and Saito, 2001). Overall, a host of pertinent studies suggests that the risk of cannibalism is an important stressor for immature phytoseiid mites and their parents. Studies on the genetic basis and phenotypic plasticity of the response to this stressor, its interrelations with and modifiability by other stressors, and the cascading effects of individual responses to stress, emanating from cannibalism risk, at the population and community levels are currently underrepresented but promising areas for future research. 3.2. Intraguild predation Intraguild predation (IGP) refers to the phenomenon of killing and eating potential competitors (Polis et al., 1989; Rosenheim et al., 1995). In phytoseiid mites, IGP mainly occurs by adult female predators (intraguild predator) on mobile immature stages, or rarely eggs, of another phytoseiid mite species (intraguild prey), most likely when primary prey is absent or low (Schausberger, 2003; Hatherly et al., 2005; Hoy, 2011). Predator-predator interactions incl. IGP are receiving increasing attention due to their predicted effects on pest control (Schausberger and Walzer, 2001; Onzo et al., 2005). Studies on predator-predator interactions where phytoseiid mites are killed and eaten by non-phytoseiid predators, such as insects or spiders, are too scarce to be accounted for in this review. From the perspective of a superior IG predator, IGP can be advantageous because it may allow to persist periods of food scarcity (Polis et al., 1989). Under some circumstances, IGP interactions may disrupt the biological control efficacy of phytoseiid mites. For example, population growth decline of P. persimilis was attributed to IGP by N. californicus and even happened if Tetranychus prey was available, albeit the decline was more severe under conditions of prey scarcity (Schausberger and Walzer, 2001; Walzer et al., 2001). In some circumstances and predator-predator combinations, IG-predators may even display a preference for IG-prey over the shared extraguild (pest) prey. For instance, A. swirskii showed a

high predation rate and a preference for immature of N. cucumeris over thrips (Buitenhuis et al., 2010). Habitat heterogeneity, such as leaf structures and webbing, may affect the strength of IGP (Roda et al., 2000; Janssen et al., 2007; Seelmann et al., 2007). For instance, the predatory mite N. californicus and E. stipulatus are known as biocontrol agents against persea mite Olygonychus perseae; the former predator is able to enter inside intact nests of the shared prey whereas the latter feeds only on mobile stages outside the nests (González-Fernán dez et al., 2009). Seelmann et al. (2007) reported from field observations that the phytoseiid K. aberrans was abundant on apple cultivars with strongly pubescent leaves while E. finlandicus was predominant on cultivars with little pubescent or glabrous leaves. This distribution was also attributed to mutual IGP, because the development and survival of K. aberrans immatures in presence of E. finlandicus is higher on pubescent leaves while E. finlandicus immatures survived and developed better on glabrous leaves. Other factors such as predator body size and the degree of polyphagy may affect the strength of IGP (i.e. predator that is larger in size and more polyphagous outcompete the others) (Zhang and Croft, 1995). Generalist phytoseiid mites tend to get more nutritional advantages from engaging in IGP in terms of enhancing survival, development and oviposition as compared to diet specialists (Walzer and Schausberger, 1999a). Schausberger and Croft (2000a) reported that generalist phytoseiid mites gain equal or more nutritional benefits from feeding on heterospecific than conspecific prey whereas specialist phytoseiids gain equal or more nutritional benefits from conspecific than heterospecific prey (Schausberger, 2003). Generalist phytoseiid mites are commonly more aggressive against heterospecific phytoseiids and prefer heterospecific to conspecific prey when having a choice (Schausberger and Croft, 2000b). This behavior of selecting heterospecific instead of conspecific prey may be due in part to the avoidance of conspecific, possibly genetically closely related, prey and/or the nutritional quality of heterospecific prey (Montserrat et al., 2006). Nevertheless, numerous differences in predation or IGP behavior also exist between generalist phytoseiid mites (Hatherly et al., 2005; Meszaros et al., 2007). The propensity to, and intensity of, IGP is tightly linked to the availability of extraguild food. Under natural conditions, the availability of shared food is temporally and spatially variable. Thus, there will be times and places where IGP is highly likely and intense and others where it is negligible. For example, GonzálezFernández et al. (2009) speculated that predatory mites will only engage in IGP only under shared food scarcity. They reported that presence of alternative non-prey food (pollen) reduces IGP stress. Similarly, Onzo et al. (2005) observed that interspecific competition and IGP between T. manihoti and E. fustis increased when shared prey mites, Mononychellus tanajoa, and alternative food (maize pollen) were absent or scarce, while presence of abundant prey/food reduced IGP to very low levels (though T. manihoti does not feed on pollen). The occurrence and intensity of IGP under field conditions is only poorly documented. Sabelis and Van Rijn (1997) speculated that, under field conditions, IGP may be less intense due to in part to one or several of the following reasons: (1) high density of shared prey, (2) plant structures providing refuges for predators, (3) availability of structures created by the prey such as webs and galls, and (4) availability of alternative food. Regarding biological control, in general combined release may result in rapid suppression of pest population at least as long as prey density is sufficient, but the generalist will displace the specialist under low prey level (Walzer and Schausberger, 1999b; Schausberger and Walzer, 2001). Release of combinations of phytoseiid mites is a matter of considerable debate and will depend on good under-

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standing of the nature of involved species through long-term studies (Schausberger and Walzer, 2001; Lawson-Balagbo et al., 2008).

3.3. Food shortage Phytoseiid mites may experience periods of limited access to food or inadequate intake of nutrition (e.g. during winter or during transportation from production site to release site). In nature, nondiapausing phytoseiid mites survive winter as long as their prey is available, but reductions in population have been observed in late winter as a result of prey depletion (McMurtry and Johnson, 1966; Penman and Chapman, 1980). The coincidence of food shortage and other environmental stressors such as exposure to excess temperatures, dehydration, or cannibalism during transportation may result in failure of released phytoseiid mites to become established (Drukker et al., 1993; de Courcy Williams et al., 2004; Toyoshima et al., 2009). It is therefore believed that the ability of phytoseiid mites to maintain their populations under unfavorable environments or to endure periods of food shortage is an important feature for their integration in biological control programs (Greco et al., 2006; Ji et al., 2013). Differences in ability to tolerate food shortage-induced stress are attributed to species differences, life stage, physiological status, water availability, and temperature. Generalist species may avoid starvation by exploiting alternative food resources (Greco et al., 2006). Food shortage is more problematic for specialist species because the absence of their prey may lead to extinction upon the failure to disperse or emigrate (Blommers and van Arendonk, 1979). Variation in gut capacity and metabolic rate may also affect species starvation tolerance (i.e. species with larger gut capacity or lower metabolic rate survive longer and vice versa) (Yao and Chant, 1989; Croft et al., 1995). Among life stages, adult females are more starvation tolerant and their tolerance is much higher when in diapause (Knisley and Swift, 1971; Blommers and van Arendonk, 1979; Croft and Blyth, 1979; Ivancich Gambaro, 1990). Food shortage rapidly affects mite survival if it is accompanied by low humidity and rising temperatures or lack of access to free water (Schausberger, 1997; Ji et al., 2013). Survival is at least doubled in starved N. californicus, N. cucumeris, P. persimilis, and Iphiseius degenerans (Berlese) when access to free water is available (Mori and Chant, 1966b; de Courcy Williams et al., 2004). Females of P. persimilis starved at 50–100% relative humidity survived longer (approx. 8 days) than those starved at 0–50% relative humidity (<2 days) (Bernstein, 1983). Blommers et al. (1977) found that 50% of starved females of Neoseiulus bibens (Blommers) given access to water could survive 18.8 days at 22 °C and 5.1 days at 28 °C, whereas those without access to water survived 6.8 days at 22 °C and 2.1 days at 28 °C. Adult females of Neoseiulus fallacis (Garman) that were starved without water survived longer at 15.5 °C than at 26.6 °C, but providing water or plant leaves improved survival at both temperatures (Croft and Blyth, 1979). Besides having a direct effect on survival, starvation affects foraging, dispersal, reproduction, sex ratio, and mating behavior. Whereas short-term starvation may have only a small impact on foraging behavior, longer-term starvation affects prey selection and prey-stage preferences (Sabelis, 1981; Zhang and Sanderson, 1992; Blackwood et al., 2001; Xiao and Fadamiro, 2010). The dispersion or walking speed may initially increase, but longer starvation leads to more energy exhaustion and the predators fail to disperse (Blommers et al., 1977; Bernstein, 1983; Auger et al., 1999; Palevsky et al., 1999). Starving of phytoseiid mites as adults—particularly for long periods—reduces egg production, and some authors have reported a shift toward the production of more males (Elsawi and Abou-Awad, 1992; Momen, 1994; Greco et al., 2006; Gotoh and Tsuchiya, 2009). This could be due to

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irreversible damage to the reproductive organs (Toyoshima and Amano, 1998; Gotoh and Tsuchiya, 2009). Starvation or poor prey conditions during the immature stages may have minor effects on female reproduction (particularly if females are mated with unstarved males) and on the male’s willingness to mate, but it has also been found to affect sex ratio and the male’s copulation time (Chant, 1961; Amano and Chant, 1978; Blommers and van Arendonk, 1979; Elsawi and AbouAwad, 1992; Momen, 1994; Zaher et al., 2007). Modest starvation (of hours to a few days) may not hinder the reproduction ability of phytoseiid mites, but total egg production will decrease as starvation time increases (Amano and Chant, 1978; Blommers and van Arendonk, 1979; Sabelis, 1981; Mégevand and Tanigoshi, 1995; Zaher et al., 2007). 3.4. Pathogens Several pathogenic microorganisms have been reported infecting phytoseiid mites and may induce a decrease in their overall fitness and biocontrol efficiency (Bjørnson, 2008). Reported pathogens include fungi, protozoa, viruses and bacteria. Pathogenicity of those microorganisms may be enhanced by other environmental stressors such as temperature, humidity, starvation and cannibalism and are frequently observed in mass-reared phytoseiid mites (Lighthart et al., 1988; Beerling and van der Geest, 1991a,b). Here, we will briefly highlight recent reports on phytoseiid mite-associated pathogens, their infection symptoms, transmission and management measures when available (but see Bjørnson (2008), Schütte and Dicke (2008) and van der Geest (2010) for further details). 3.4.1. Fungi Fungi of the family Entomophthoraceae (Order Entomophthorales) cause epizootic diseases that often devastate arthropod populations (van der Geest et al., 2000). Fungi of Neozygites sp., Hirsutella sp., Lecanicillium sp. and unidentified fungi were reported infecting phytoseiid mites and the infection may be promoted under high relative humidity (Furtado et al., 1996; Keller, 1997; Schütte et al., 2005; Bałazy et al., 2008). The entomopathogenic fungi used against pest mites may also exert stress on phytoseiid mites. For instance, the prey handling time and overall feeding rate of P. persimilis is negatively affected when the predator offered T. urticae treated with Beauveria bassiana (Seiedy et al., 2012, 2013). Typical fungal infection symptoms may include: coloration of the body surface of the host due to the presence of fungal hyphae and reproductive structures; foraging of the host may be reduced; general weakness and partial paralysis (Boucias and Pendland, 1998; Schütte and Dicke, 2008). 3.4.2. Protozoa Protozoa known from phytoseiid mites belong to the phylum Microspora and they are small, spore-forming, and obligate intracellular parasites (Tanada and Kaya, 1993; Schütte and Dicke, 2008). Microsporidia reported from phytoseiid mites include species of genera Microsporidium, Oligosporidium and Nosema and unidentified microsporidia (Hunger, 1988; Beerling and van der Geest, 1991a,b; Bjørnson et al., 1996; van der Geest et al., 2000; Becnel et al., 2002; Olsen and Hoy, 2002). Microsporidia may be transmitted from parent to offspring through eggs or through direct contact between infected and healthy individuals such as by cannibalism and grooming (van der Geest et al., 2000; Bjørnson, 2008). Infected individuals are characterized by shortened longevity, reduced fecundity, reduction in predation and movement, and male-biased sex ratios (Bjørnson and Keddie, 1999; van der Geest et al., 2000). Heat treatments (33 °C for 7 days)

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are partly successful for reduction of microsporidia infection (Olsen and Hoy, 2002). 3.4.3. Viruses There are four reports on viral infection of phytoseiid mites (Šutáková and Rüttgen, 1978; Steiner, 1993; Bjørnson et al., 1997; Poinar and Poinar, 1998). Viral infection may occur through ingestion, via eggs, through body opening or wounds (Tanada and Kaya, 1993; Schütte and Dicke, 2008). Unidentified non-occluded viruses have been observed in egg yolks in gravid females of N. cucumeris and P. persimilis (Steiner, 1993; Bjørnson et al., 1997), but their effects on the hosts are unknown. Virus-like particles have been observed in the cytoplasm of cells of P. persimilis infected with Rickettsiella phytoseiuli (Šutáková and Rüttgen, 1978). However, the authors considered that the viruses were merely carried by R. phytoseiuli and may not have been associated with the phytoseiid mites. Three types of virus-like particles (classified based on their diameter and electron-dense core) have been detected by transmission electron microscopy in T. occidentalis (Poinar and Poinar, 1998; Hoy and Jeyaprakash, 2008). Although, diseased females of T. occidentalis showed lowered fecundity and reduced longevity and died suddenly, it is not clear whether these viruses were the cause of these symptoms (Hoy and Jeyaprakash, 2008). 3.4.4. Bacteria Bacteria reported from phytoseiid mites include species of genera Rickettsiella, Wolbachia, Cardinium, Spiroplasma, Acaricomes and Serratia. The genus Rickettsiella comprises intracellular, rickettsialike entities, and all species are exclusively arthropod pathogens. Rickettsiella phytoseiuli is found in only one phytoseiid mite species, P. persimilis, in the Ukraine (Šutáková and Rüttgen, 1978). This pathogen may be transmitted through feeding or through wounds (Bjørnson, 2008; Schütte and Dicke, 2008). Infected mites show no developmental and morphological changes, or mortality (Šutáková and Rüttgen, 1978; Šutáková, 1988). Šutáková and Rüttgen (1978) recorded a coincidence infection of P. persimilis with R. phytoseiuli and virus-like particles and they speculated that R. phytoseiuli may be decisive for establishment of viral infection. Wolbachia are maternally inherited alphaproteobacteria that infect a broad array of arthropods (Werren et al., 1995; Bouchon et al., 1998). Wolbachia infection to phytoseiid mites is widely reported (Breeuwer and Jacobs, 1996; Johanowicz and Hoy, 1996; Weeks et al., 2003; Corpuz-Raros, 2005; Famah Sourassou et al., 2014). They are transovarially transmitted from parents to offspring and manipulate hosts in the way that the infected host produces more female offspring (i.e. parthenogenesis), male embryos develop as females (i.e. feminization of genetic males), male killing (male embryos die during the embryonic or immature stages), beside cytoplasmic incompatibility (CI) between uninfected females and infected males that result in high mortality among offspring or male-biased sex ratios, or both (Stouthamer and Kazmer, 1994; Werren, 1997; Stouthamer et al., 1999; Hong et al., 2002; Gotoh et al., 2005b; van der Geest, 2010). Antibiotics (rifampicin, tetracycline hydrochloride) or temperature treatment (ca. 32 °C to 35 °C) are known to successfully reduce or eliminate Wolbachia from infected mites (Johanowicz and Hoy, 1996; Breeuwer, 1997; van Opijnen and Breeuwer, 1999; Gotoh et al., 2003, 2005b). Cardinium is a symbiotic bacteria that manipulates hosts in a way similar to that of Wolbachia to ensure their widespread and are transmitted maternally (Hunter et al., 2003; Wu and Hoy, 2012). Cardinium infection in phytoseiid mites was first reported in T. occidentalis by Hoy and Jeyaprakash (2005); the bacteria have since been found in E. finlandicus and N. paspalivorus (Enigl and Schausberger, 2007; Famah Sourassou et al., 2014). Crosses between Cardinium-uninfected females and Cardinium-infected males in T. occidentalis result in reduced fecundity in parental

females and reduced survival rate and male-biased sex ratio of F1 progeny (Wu and Hoy, 2012), showing that Cardinium infection of T. occidentalis induces non-reciprocal cytoplasmic incompatibility. Similar observation was reported for the Ghanaian population of N. paspalivorus by Famah Sourassou et al. (2014). Treatment with antibiotics (penicillin G, tetracycline hydrochloride) or temperature (ca. 35 °C to 40 °C) are successful for reducing or eliminating Cardinium infection in mites (Gotoh et al., 2007; Zhu et al., 2012). Spiroplasma was detected in N. californicus (Enigl and Schausberger, 2007). However, the precise biological effects that Spiroplasma may have on N. californicus remain unclear. Acaricomes phytoseiuli is another bacterium isolated from P. persimilis and can be transmitted from diseased to healthy individuals via feces and debris (Pukall et al., 2006; Schütte et al., 2006a,b, 2008b). Infected mites exhibit a lower degree of attraction to plant volatiles (mainly those emitted by plants in response to herbivore feeding), which predatory mites use to locate their prey, the socalled ‘‘non-responding syndrome” (Sabelis et al., 1999; Schütte et al., 2006a). As a consequence, infected females show reduced fecundity, reduced longevity and high mortality (Schütte et al., 2006a, 2008b; Bjørnson, 2008). All infected populations originate from European countries, while P. persimilis populations from outside Europe and other phytoseiid species tested negative for A. phytoseiuli (Gols et al., 2007; Schütte and Dicke, 2008). Possible methods of eliminating A. phytoseiuli are antibiotic treatments and surface sterilizing eggs with bleach (Schütte et al., 2008a,b). Serratia marcescens is a bacterial pathogen of various insect species. When T. occidentalis was kept at a high temperature before being exposed to this bacterium, the mites became more sensitive to the bacterium than when there were no such pre-existing stress factors (Lighthart et al., 1988; van der Geest et al., 2000). Unidentified bacteria and unidentified pathogens have been reported in several phytoseiid mites (Steiner, 1993; Bjørnson et al., 1997; Schütte et al., 2005), but as yet little is known about their roles or systematic status. 4. Conclusion No environmental stressor can be seen in isolation but interacts with others, possibly resulting in overshadowing, additive, subtractive, or synergistic effects. As living organisms, phytoseiid mites are frequently exposed to a range of environmental stressors. We have shown in this review that the tolerance of phytoseiid mites to an environmental stressor is highly variable and depends on a species’ life history traits and the concurrence or interactions of other stressors. The majority of the information presented in this review refers to laboratory results; little is yet known about the responses of phytoseiid mites to environmental stressors under natural or field environments. Furthermore, our knowledge of the physiological and genetic mechanisms underpinning the tolerance or susceptibility of phytoseiid mites to an environmental stressor remains poor. Extensive future research into these issues is necessary if we are to develop a more comprehensive knowledge of the responses and strategies that phytoseiid mites use to cope with environmental stresses. Only then we will be having sufficient information for effective decision-making with respect to integrating specific phytoseiid mites into biological control programs for specific habitats. Acknowledgments This study was supported by JSPS Grants-in-Aid for Scientific Research (25660276 and 25450069) and for JSPS Fellows (2503084).

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Please cite this article in press as: Ghazy, N.A., et al. Phytoseiid mites under environmental stress. Biological Control (2016), http://dx.doi.org/10.1016/j. biocontrol.2016.02.017