Plant damage to vegetable crops by zoophytophagous mirid predators

Biological Control 59 (2011) 22–29

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Plant damage to vegetable crops by zoophytophagous mirid predators Cristina Castañé ⇑, Judit Arnó, Rosa Gabarra, Oscar Alomar IRTA-Entomology, Ctra. Cabrils Km 2, 08348-Cabrils, Spain

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Article history: Available online 24 March 2011 Keywords: Biological control Tomatoes Generalist predators Omnivory Feeding injuries

a b s t r a c t The use of plant-feeding predators for biological pest control has traditionally been neglected, mainly due to the risk of them feeding on crop plants and causing economically significant damage. Yet, these predators offer advantages for biological pest control. They are mostly generalist predators that have an impact on several crop pests. They may also be able to establish on crops early in the growing season, when pests colonize them, and can remain on the target crop when prey is scarce. Therefore, management programs must seek to minimize risks while maximizing benefits. In vegetable crops, most of the literature on zoophytophagous predators has focused on four species: Dicyphus tamaninii, Dicyphus hesperus, Macrolophus pygmaeus and Nesidiocoris tenuis (Heteroptera, Miridae). The capacity of these species to produce crop damage in tomatoes varies. This damage has been related to relative predator-toprey abundance, with damage increasing at high predator abundances and low prey densities. In this review, we analyze the use of these species in biological control programs and the associated benefits and risks. The differences in the damage caused by the four predatory species examined could not be attributed to either stylet morphology or saliva composition. However, feeding on specific plant structures where they may find the resources required for their development is what probably determines feeding damage. Understanding when and why these predators increase their feeding on plants or on certain plant parts is of crucial importance for integrating them in biological control programs. Ó 2011 Elsevier Inc. All rights reserved.

1. Introduction Insect feeding studies increasingly show that many insect species are omnivores: they can use food from more than one trophic level (Pimm and Lawton, 1978; Coll and Guershon, 2002). Zoophytophagy is a special case of omnivory in which insects can feed on both plants and prey at the same developmental stage. These predators are called zoophytophagous, plant-feeding predators or facultative predators (Albajes et al., 2006) and have received attention due to their increasing role in the biological control of agricultural pests (Alomar and Wiedenmann, 1996; Coll and Ruberson, 1998). Biological control refers to the action of parasites, predators or pathogens in maintaining the insect population density at a lower average level than would occur in their absence (DeBach, 1964). It includes methods that combine pests with their natural enemies or that make modifications to the environment (or to the natural enemy itself) that favor natural enemy population growth and its impact on pest dynamics (Rubertson et al., 1999). The potential use of plant-feeding predators for biological pest control has traditionally been neglected. The main reason for this is the risk of their feeding on crop plants which may result in economically ⇑ Corresponding author. Fax: +34 937533954. E-mail addresses: [email protected] (C. Castañé), [email protected] (J. Arnó), [email protected] (R. Gabarra), [email protected] (O. Alomar). 1049-9644/$ - see front matter Ó 2011 Elsevier Inc. All rights reserved. doi:10.1016/j.biocontrol.2011.03.007

significant damage, either as a direct consequence of the injuries that they cause to plant tissue or as an indirect effect associated with the inoculation of pathogens that cause crop diseases. Although the herbivory of natural enemies may injure plants and result in economic losses, significant plant damage is relatively rare, despite the fact that many biological control agents regularly feed on plants (Albajes and Alomar, 2008). In a thorough review of the majority of predatory groups conducted by Hagen et al. (1999), plant feeding was mentioned several times since various species of mites, thrips, earwigs and Heteroptera suck plant juices and pollen; even so, crop damage was rarely noticed. Crop damage is often the result of complex interactions between the morphological, physiological and behavioral traits of the natural enemy, plant, crop type, and certain environmental factors. Another reason for the traditional neglect of plant-feeding predators is the fact that they are mostly generalist predators. Zoophytophagous predators are generally perceived as being less effective at maintaining pest levels below economic thresholds because plant consumption may reduce prey ingestion. There is experimental evidence, though further investigation is required, to suggest that plant-feeding predators are able to establish themselves on crops early in the growing season together with pests. This evidence was shown by Gabarra et al. (2004) in commercial tomato greenhouses, indicating that the crop was simultaneously colonized by whiteflies and their mirid predators. This trait would be particularly positive in the case of annual crops that need to be

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recolonized every season. In such crops, predators feeding on plant tissues would be able to remain on the target crop even in the absence, or shortage, of prey. Predator establishment would depend on the characteristics of the plant, since predators may avoid foraging or ovipositing on certain plant species or varieties. The experimental data suggest that even if plant feeding by predators may imply certain inherent problems, it also offers some advantages, and management programs must seek to minimize risks while maximizing benefits. The objective of this review is to analyze the benefits and risks associated with the use of predatory mirids which have a zoophytophagous feeding regime in biological control programs applied to vegetable crops. We first describe four examples of zoophytophagous predators that have been or are still used in biological control programs. We then examine several factors that are implicated in the appearance of crop damage associated with predator and plant characteristics or their relationship with prey abundance. 2. Zoophytophagous mirid predators Several mirid species are known on account of the injuries and damage that they cause to crops, but many of them are also predacious (Wheeler, 2001). For instance, Lygus hesperus (Knight), a key phytozoophagous pest affecting cotton, had recently been recognized as also being an important predator in that crop (Hagler and Naranjo, 2005). In other species, this predatory action is known, but it has not yet been considered by Integrated Pest Management (IPM) programs. This is the case of Dicyphus errans Wolff, (Quaglia et al., 1993), and Creontiades pallidus (Rambur) (Urbaneja et al., 2001). In vegetable crops, the management of zoophytophagous predators has mainly focused on four species: Dicyphus tamaninii Wagner, Dicyphus hesperus (Knight), Macrolophus pygmaeus (Rambur) and Nesidiocoris tenuis (Reuter), all belonging to the same subfamily Dicyphinae. They are important generalist predators that regulate arthropod populations such as whiteflies, but also other pests like aphids, spider mites and leafminers. Conservation of native populations of three of these predatory mirid species is a pest management strategy that has been successfully used in the Mediterranean region. 2.1. D. tamaninii D. tamaninii was first reported as an active predator of whiteflies along the north-east coast of Spain where it was very abundant in a wide range of cultivated and non-cultivated plants, and spontaneously colonized tomato crops when no broad-spectrum insecticides were applied (Gabarra et al., 1988; Alomar et al., 2002). In the 1980s and 1990s, a novel pest management strategy was developed based on the conservation of populations of this species on field tomatoes. This IPM program was extensively applied by growers and contributed to a significant reduction in the number of pesticide sprays used on this crop (Albajes and Alomar, 1999). However, since the mid 1990s, we observed a decrease in its abundance and it has since been replaced by M. pygmaeus. The role of D. tamaninii as predator of some key pests that affect vegetable crops was documented in laboratory studies that showed its voracious capacity for consuming whiteflies, aphids and thrips (Alvarado et al., 1997; Barnadas et al., 1998; Montserrat et al., 2000; Sengonça and Saleh, 2002; Blaeser et al., 2004). Cage trials also showed its efficacy for the control of whiteflies and thrips on tomato and cucumber crops (Gabarra et al., 1995; Castañé et al., 1996, 2009; Blaeser et al., 2004; Ghabeish et al., 2008). However, several types of injuries produced by the predator were described. On tomatoes, visible injuries were produced on

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green fruit, including small blemishes, scars and deformations (Alomar and Albajes, 1996). On zucchinis and cucumbers, dimples and pits of various sizes were produced and fruits may become malformed (Castañé et al., 2003). On melons, minor spots were observed on very young melon fruitlets, though these tended to disappear with fruit maturation (Alomar et al., 2006). The appearance of crop damage was related to relative predator-to-prey abundance. Laboratory and cage experiments with tomato plants confirmed that the number of punctures in fruit tended to significantly decline when prey was present. This decline in the number of punctures indicated that predators preferred prey over plants and also that damage to fruit was more likely to occur when there was a shortage of prey. During periods of prey scarcity, predator nymphs tended to survive better when fruit was available because tomato fruit had a higher nutritional quality than leaves (Salamero et al., 1987; Lucas and Alomar, 2002). Similar experiments with cucumber and zucchini showed that the number of punctures on fruit also declined in the presence of prey on the leaves (Castañé et al., 2003; Sengonça et al., 2003). Nevertheless, no economically significant damage was reported on commercial cucumbers or zucchinis, perhaps because predator populations in these crops were lower than in tomato crops. In experimental and commercial tomato fields and greenhouses, damage appeared at high predator abundances and when whitefly prey had already been controlled (Gabarra et al., 1988). This observation led to the implementation of the mentioned IPM program by means of a decision-chart, which aimed to prevent the coincidence of high predator populations with low prey densities (Alomar and Albajes, 1996). The use of this decision-chart with field tomatoes successfully contributed to the management of both D. tamaninii and whitefly populations and made it possible to prevent crop damage. The use of D. tamaninii provided a good example of successful management of naturally colonizing populations of a zoophytophagous predator that offered the advantages of predation while minimizing the risk of crop damage. However, this risk dissuaded us from recommending the commercial release of this predator. 2.2. D. hesperus The use of this predator began when the Canadian greenhouse industry sought to apply similar biocontrol alternatives to those developed in Europe with M. pygmaeus, a Palaearctic species that could not be imported. D. hesperus was selected after screening several native mirid species. As this species does not spontaneously migrate to greenhouses under Canadian conditions, it was commercially produced and released for the biological control of whiteflies or thrips in greenhouse-grown tomatoes. Releases of this predator took place in both Canada and northern Europe (Gillespie et al., 2007; Arnó et al., 2009a), but its commercial production has now been discontinued. On tomato plants, this predator was able to complete its development with a diet of whiteflies, spider mites and/or thrips. Releases in experimental tomato greenhouses resulted in the effective control of all these pest species (McGregor et al., 1999; Gillespie et al., 2001; Shipp and Wang, 2006). However, while the control of whiteflies and thrips proved effective in commercial settings that of spider mites did not. Introductions of D. hesperus also proved effective in the control of gerbera pests and of aphids in pepper crops (Gillespie et al., 2007). As already mentioned for D. tamaninii, the main type of damage produced by this predator consisted of blemishes on tomato fruit which were characterized by feeding punctures surrounded by a yellowish, bleached area (Shipp and Wang, 2006). On gerbera, feeding injuries may cause deformations of blossom and the downgrading of flowers (Gillespie et al., 2007).

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In laboratory experiments, McGregor and Gillespie (2000) concluded that the potential damage on tomato fruit was low because D. hesperus preferred tomato leaves to ripe tomato fruit. Observed blemishing was primarily caused by feeding on young, green fruit whereas the predator tended not to feed on ripe fruit (Gillespie et al., 2007). Nevertheless, the use of this predator on tomato crops was not constrained by blemishing. In fact, substantial fruit damage to greenhouse tomatoes was only described when excessive predator populations coincided with controlled whitefly or thrips infestations (Gillespie et al., 2001, 2007; Shipp and Wang, 2006). 2.3. M. pygmaeus Two species, M. pygmaeus and M. caliginosus Wagner (a junior synonym of M. melanotoma (Costa)), have been cited as efficient biological control agents on vegetable crops. However, due to their great morphological similarity, these two species have often caused confusion among researchers (Martinez-Cascales et al., 2006; Perdikis et al., 2003). Based on this available information, we assume that publications referring to Macrolophus in vegetable crops should have referred to M. pygmaeus. Since the mid 1990s, M. pygmaeus has been the predominant species colonizing tomato crops in the north-east of Spain (Alomar et al., 2002; Castañé et al., 2004; Gabarra et al., 2004). The IPM program originally developed for D. tamaninii was easily adapted for M. pygmaeus and is still applied by growers in that area. M. pygmaeus has been commercially available since 1994 and its use as generalist predator has steadily increased in European tomato greenhouses (Malausa and Trottin-Caudal, 1996; van Lenteren, 2003; Arnó et al., 2009a). This is a well-known predator and is used for controlling several vegetable crop pests including the whiteflies Trialeurodes vaporariorum Westwood and Bemisia tabaci Gennadius (Fauvel et al., 1987; Barnadas et al., 1998), thrips, leafminers, aphids, mites and the eggs of lepidopteran pests (Alvarado et al., 1997; Riudavets and Castañé, 1998; Hansen et al., 1999; Arnó et al., 2003; Margaritopoulos et al., 2003). It had also been recently shown to be a predator of the South American tomato pinworm, Tuta absoluta (Meyrick), (Arnó et al., 2009b; Urbaneja et al., 2009). There are few reports of plant damage caused by this predator and its use is generally considered safe. Plant damage has mainly been described under experimental conditions with high predator densities and low prey availability. The types of injuries observed in these cases were: feeding marks on vegetative organs and fruit, on tomatoes; dimples, pits and fruit distortion, on zucchinis; and discoloring spots on gerbera flowers. However, these kinds of injuries had not generally been observed on commercial crops (Malausa and Trottin-Caudal, 1996; Van Schelt et al., 1996; Castañé et al., 2003). Only Sampson and Jacobson (1999) reported distorted tomato leaf growth, necrotic spots on leaves, scars on fruit and fruit drop in a field survey conducted in the UK; they also recorded extremely high predator densities (50–300 individuals per plant) with very low prey abundance. As previously mentioned, M. pygmaeus has been widely released and conserved in greenhouses and on outdoor tomato crops in continental Europe for more than 15 years without any major complaints about crop damage. 2.4. N. tenuis N. tenuis is the predominant species colonizing tomato crops in some Mediterranean areas. It is a cosmopolitan species whose status as either a pest or a beneficial insect remains a matter for debate. On tomato crops, it had been mentioned as a pest in Egypt and in the south of France, while it was generally regarded as a beneficial predator in Sicily and Spain, although there had been a concern about some crop damages that have been observed.

In addition to feeding on whiteflies and other pests that affect vegetables, this generalist predator also consumed lepidopteran eggs. Both in exclusion cages and in commercial fields, it effectively controlled B. tabaci and was responsible for a significant reduction in T. absoluta populations (Castañé et al., 2008; Sanchez, 2008; Arnó et al., 2009b; Calvo et al., 2009a,b; Urbaneja et al., 2009; Belda et al., 2010). This predator can feed on all the aerial parts of tomato plants but has a strong preference for the three uppermost leaves and the apical bud, which is where up to 80% of the predator population is found. The feeding activities of both nymphs and adults produced different types of damage that include: necrotic rings on the main stems, shoots, leaf petioles and flower stalks; the abortion of flowers and small fruits; and the reduced growth of stems and leaves which causes stunted plant growth (El-Dessouki et al., 1976; Vacante and Tropea-Garzia, 1994; Sanchez and Lacasa, 2008; Calvo et al., 2009a; Arnó et al., 2010). In laboratory and field tests, an inverse relationship had been observed between prey availability and the abundance of necrotic rings and aborted flowers. Even so, the appearance of these necrotic rings and aborted flowers was not correlated with any yield reduction. The appearence of necrotic rings was more clearly related to the abundance of nymphs than to adults (Arnó et al., 2006; Calvo et al., 2009a; Perdikis et al., 2009; Sanchez, 2009). As with D. tamaninii, the damage that N. tenuis causes to tomato crops was described at high predator densities and with low prey availability and was related to the duration of predator/plant interaction. When the infestation of N. tenuis persisted 1–4 weeks, the number of necrotic rings on the stem and shoots was closely related to the abundance of the predator. However, most lesions disappeared after a few days and no negative effects were observed in terms of plant growth, the number of flowers or fruit set per truss, or the average weight of the fruits (Arnó et al., 2010). Although Sanchez and Lacasa (2008) found an increase in the number of aborted fruits, this was compensated by an increase in the final average weight of each harvested fruit. When the infestation of N. tenuis persisted more than 6 weeks, insect feeding altered both plant growth and the quantity and quality of the yield. There was a significant reduction in the total growth of the plant, including leaf length, number of trusses, number of fruits per truss and average size of the fruits. When the mirid continued to feed on the plant and no prey was present, this produced a cumulative loss of assimilates that caused a sudden loss of both plant growth and yield (Arnó et al., 2010). Sanchez and Lacasa (2008) proposed a mathematical model when prey is scarce that predicted yield loss from 187 cumulative Nesidiocoris-days onwards. However, in a crop cage experiment with a similar prey density, no fruit abortion or loss of fruit weight was found by Arnó et al. (2010) after reaching the double of that threshold. Although it would be desirable to have a threshold capable of determining the risk of yield loss, thresholds vary and depend on such factors as plant nutrition, plant variety, crop cycle, weather conditions, etc. They are, therefore, only applicable under the specific conditions for which they were calculated. In spite of the risk of crop damage, N. tenuis is being broadly released in tomato greenhouses in southern Spain, which is an important production area (van der Blom et al., 2009). The predator is being released because the risk associated with its management is perceived as being lower than that associated with virus vectors like B. tabaci. The risk of using this predator is also perceived as being smaller than the potential disruption of IPM programs if growers revert to the use of pesticides against new invasive pests like T. absoluta. It is important to note that, under greenhouse conditions, N. tenuis populations descended rapidly when numbers of whitefly and other prey decreased (Sanchez, 2008). This reduction was mainly due to the predator migrating to other crops or host

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plants, which prevented any potential plant damage. However, when this migration is blocked, the risk of crop damage increases. This crop damage occurre in greenhouses that have all their ventilation openings covered with mesh to prevent the entry of pests, a practice which is common in many production areas.

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shown to enhance plant-feeding, and previous access to prey also increased the amount of subsequent plant-feeding. However, this behavior had not been confirmed in other mirid species such as D. tamaninii and M. pygmaeus. These predators spent the same amount of time feeding on leaves when they did not consume prey as when they consumed up to 5 whitefly pupae (Montserrat et al., 2004).

3. Resources obtained from plants by plant-feeding predators 4. Types of plant damage To understand the extent of plant feeding by zoophytophagous predators and therefore the associated risk of damage, it is important to know which type of resources are obtained when they feed on plants. It has been widely reported that predators that are able to complement or supplement carnivorous diets with plant materials enhance one or more of their fitness components: developmental rate, survival, fecundity or longevity (e.g., Maleki et al., 2006; Lemos et al., 2009a,b). For example, D. tamaninii and M. pygmaeus were able to develop and reproduce on a beef meat diet without access to any plant material for several generations, but they then had a considerably longer preimaginal developmental time and adults were significantly smaller than those fed with Ephestia kuehniella eggs on tobacco plant (Iriarte and Castañé, 2001; Castañé and Zapata, 2005). Although the main protein source differed from the control to the beef meat diet treatment, and this may have accounted for part of the difference observed, the absence of a plant source was probably the main reason for the observed reduction in fitness. In the case of D. hesperus, nymphs were able to complete their development when prey was combined with water, but in a lower proportion than when this prey was combined with a plant leaf (Gillespie and McGregor, 2000). What facultative predators obtain from plants depends to a great extent on the predator species, the plant species and the part of the plant, since different plant organs have different nutritional values. Whereas certain plant food could sustain predator development and even some reproduction in the absence of prey, other plants or plant parts were only able to keep adults alive for a limited time (Naranjo and Gibson, 1996). While M. pygmaeus was able to complete its immature development when only tomato, eggplant, cucumber, pepper, or green bean leaves were available (Perdikis and Lykouressis, 2000), neither D. tamaninii nor N. tenuis nymphs were able to develop to adults when only feeding on tomato, pepper or eggplant leaves (Lucas and Alomar, 2001; Urbaneja et al., 2005). Although D. hesperus could not develop on the leaves of several plant species, it could develop and reproduce on mullein plants (McGregor et al., 1999; Sanchez et al., 2004). On the other hand, D. tamaninii could complete preimaginal development when green or red tomato fruit were offered (Lucas and Alomar, 2001), suggesting that tomato fruit contains enough nutrients to sustain the development of this predator. Predaceous Heteroptera need a substantial amount of water to feed on their prey due to their extra-oral digestion. These insects inject considerable amounts of digestive enzymes into their prey from their salivary glands. These enzymes are diluted in water and used in combination with their stylets as they pierce prey tissue and macerate them, producing a liquid that is ingested and finally digested in the gut (Cohen, 1995). Water is also needed to maintain the physiological status of these predators. Due to this high demand of water, which zoophytophagous heteropteran predators mainly take from plant tissues, phytophagy in these predators should probably be considered essential rather than facultative. Water consumption by D. hesperus has been studied in detail by Gillespie and McGregor (2000) and Sinia et al. (2004). These authors showed that this insect needed to ingest water to consume its prey and that the water required was primarily obtained from plant tissues. Previous water deprivation was

As stated in Section 2, damage by zoophytophagous predators can affect growing plant tissues, stems, leaves and/or fruits, and is species-crop specific; in other words, a given predatory species may damage certain crops, or cultivars or even crop growth stages but it may not affect others. Injuries caused by plant feeding predators may be due to the mechanical action of their stylets when they penetrate plant tissues. The type of injury that is externally observed varies from simple punctures, in the case of green fruit, which then become discolored spots in mature fruit (as occurs in tomatoes), to a variety of depressions (pits) and scars. However, the importance of the damage depends on where the bugs feed; while feeding on the mesophyll causes simple lesions, feeding on meristematic tissues produces malformations of the stem, leaves and fruit (Hori, 2000). In the case of heteropterans, the mouthpart that penetrates the prey or the plant consists of the stylet bundle with two external mandibular stylets and two internal maxillary stylets (Wheeler, 2001) whose morphology had been related to predator’s feeding regime: in predacious families, (e.g., Reduviidae) barbs on the mandibular stylets were generally more numerous than in phytophagous families (e.g., Lygaeidae, sensu lato) (Cohen, 1990). In the case of maxillary stylets, the inner surface of the right maxilla ranged from moderately serrated, in predatory families (e.g., Anthocoridae, Nabidae), to smooth, in strictly phytophagous families (e.g., Tingidae), while the Miridae represented an intermediate situation (Cobben, 1978). In a more specific study of this family, Boyd (2003) showed that the serrations on the right maxillary stylet were deeper in strictly zoophagous species than in phytophagous ones. Other than this general trend for the two extremes of the zoophytophagous spectrum, both within the Heteroptera and the Miridae, there is little information available about the stylet morphology of plant-feeding predators that are present in vegetable crops. We examined the mandibular and maxillary stylets of D. tamaninii, N. tenuis and M. pygmaeus with Scanning Electron Microscopy images and concluded that they were similarly shaped. The mandibular stylets of all three species had between 10 and 12 teeth and their maxillary stylets had at least 4 strongly recurved teeth. It does not therefore seem that the differences observed in the types and intensities of the damage produced by each of these three species could be directly related with the morphologies of their respective stylet bundles (Fig. 1). In other cases, damage is not primarily produced mechanically but is the result of a chemical process by which the affected cells are killed by salivary enzymes. The damage caused by this saliva and the process involved had been described in detail for L. hesperus on cotton: nymphs and adults produced minute injections of macerating watery saliva which were deeply drilled into all parts of the developing cotton boll at the square stage. After injecting its saliva, the insect waited for the square’s cell content to solubilize and then quickly ingested the resulting slurry (Backus et al., 2007). Polygalacturonase, a specific type of pectinase, had been postulated as the main cause of damage by L. hesperus rather than mechanical damage caused by the insect’s stylet (Shackel et al., 2005). Differences in the composition of plant and prey-based diets are particularly related to the carbohydrate-protein ratio, which is

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Fig. 1. Stylet bundles. Mandibular (A) and maxillary (B) stylets of the mirid bugs Nesidiocoris tenuis, Macrolophus pygmaeus and Dicyphus tamaninii as seen under a Scanning Electronic Microscope at magnifications of 1500–3000.

estimated as 6.0 for plants and 0.5 for animals, including insects (Vonk and Western, 1984). A diverse range of enzymes should therefore be expected in phytophagous and carnivorous heteropterans and especially in those of salivary origin. Pectinases and amylases are more likely to be found in plant feeders, whereas proteases (e.g., trypsin, chymotrypsin and cathepsin) and phospholypases are characteristic digestive enzymes in zoophagous species (Cohen, 1996, 1998). The simultaneous occurrence of both types could be expected in omnivores. In the case of the phytozoophagous mirids, L. hesperus and L. lineolaris, protease, amylase and pectinase activity was detected in their salivary gland complexes. The presence of both types of enzymes suggests that these mirids should be able to access structural insoluble animal proteins and plant tissues (Agustí and Cohen, 2000). A certain ratio of amylase to protease activity (A/P ratio) had been proposed to reflect the relative dependence of a given species on starch as opposed to protein, since a greater ability to digest starch than protein would be congruent with the proportions of these substrates found in plants and animals (Zeng and Cohen, 2000). In the case of the Miridae family, pectinase had been postulated as a major component in the watery saliva of most species (Hori, 2000) and the presence of this enzyme had been confirmed in the salivary gland complex of both D. tamaninii and M. pygmaeus (C. Castañé unpublished results). Another type of damage is that caused by insects feeding on plant vascular tissues. Although this type of feeding is unusual among zoophytophagous mirids, it has been described that N. tenuis and Engytatus modestus (Distant) mainly fed on the vascular bundles of tomato plants (Tanada and Holdaway, 1954; Raman and Sanjayan, 1984; Wheeler, 2001). The continuous extraction of assimilates by large populations of N. tenuis under conditions of low prey availability may explain the important loss of yield that was observed as these assimilates were impeded from reaching the developing fruits (Arnó et al., 2010). The appearance of necrotic rings on stems, leaves and flower petioles caused by N. tenuis was the result of the mechanical destruction of cells by the stylet when the insect fed on the vascular tissues, the action of the salivary enzymes on the tissues and the response reaction of the plant (toxemia). Tissue damage by insect feeding initiated a series of wound-response reactions (the Phenol-PhenolOxidase PPO cascade) that produced the characteristic brown discoloration of injured tissues (Raman et al., 1984). The feeding of heteropterans can also produce hormonal imbalances as the result of a mechanical and/or chemical action

and induce such plant responses as the abscission of organs and/ or disturbances of the physiological condition (Hori, 2000). The abscission of flower and fruit clusters and reductions in plant height caused by N. tenuis has also been described in tomato (see Section 2.4). Reductions in plant height and the development of secondary stems due to damage to apical meristematic tissue by Lygus bugs had been described in Hibiscus cannabinus L. (Conti and Bin, 2001). One further aspect that has not yet been investigated is how improvements in plant defensive mechanisms could modulate the extent of the injuries that these zoophytophagous predators cause to the crop. The application of jasmonic acid on tomato plants reduced the amount of damage that several pests caused to leaves by up to 60% (Stout et al., 2002). Therefore, applying elicitors that temporarily activate plant resistance mechanisms may offer an effective way to reduce the amount of damage produced by zoophytophagous predators.

5. Functional relationships between prey consumption and plant damage Three models had been proposed to explain the functional relationships between the amount of plant and prey consumed by omnivorous predators (Gillespie and McGregor, 2000; Albajes et al., 2006). In one, predators switched between plant and prey as alternative food sources (e.g., plants are exploited when suitable prey cannot be found) and as a result plant feeding decreased with increased prey feeding. In the second, plant feeding occurred independently of the amount of prey feeding as the predator needed critical elements of plants that were not available from their prey. In the third, plant feeding increased with prey feeding, since plants provided elements that were needed for prey consumption. These models were appropriate for studying the behavior of individual predators in relation to plant feeding but were not all mutually exclusive: individuals may behave according to one model or another depending on the specific crop circumstances that they find. As previously mentioned, the acquisition of water seems to be a primary function in which plant feeding plays a central role. Since water is needed for prey feeding but also to maintain the physiological status of the insect, a certain amount of plant feeding is essential rather than facultative and occurs independently of prey abundance. In fact, several studies have shown that plant feeding tends to be constant, even when prey is abundant (Salamero

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et al., 1987; Gillespie and McGregor, 2000; Montserrat, 2001; Sanchez, 2008; Pumariño et al., 2010). However, predators did not seem to produce visible injuries during all the time that they spend feeding on their host plants. Similarly, not all predatory species caused the same amount of injury and – at least in the four species that we have examined in detail – the observed differences in plant damage could not be attributed to stylet morphology (Sections 2 and 4). It is probable that feeding on specific plant structures is what determines feeding-associated damage. For example, D. tamaninii may remain on leaves when prey is abundant but it feeds on fruit – where they may find the resources required for nymphal development – when prey is scarce. Conversely, M. pygmaeus may not exhibit such a behavioral shift and, as a result, may not cause as much damage to crops, except when there are very high populations and an absence of prey. If most of the plant feeding events on fruit by a given species were likely to cause plant injuries, we would expect to observe some low level lesions even when predators are less abundant. This had been described for both D. tamaninii and D. hesperus (Alomar and Albajes, 1996; Shipp and Wang, 2006). For predators that may damage crops, we should expect an increase in crop damage as their establishment on crops increases, as a result of the numerical response of predator-to-prey abundance. This response produces a reduction in prey abundance which, in turn, forces predators to increase their plant feeding, increasing crop damage. According to the specific crop-predator setting, damage may be considerable and require the use of control spraying, as reported for D. tamaninii and N. tenuis with tomatoes. In such situations, we would predict most of the damage to be caused by nymphs, as adults would tend to leave the crop once prey became depleted, under both open field conditions and in greenhouses with open ventilation windows (Gabarra et al., 2004; Montserrat et al., 2004; Sanchez, 2008). A decision chart based on predators switching from prey feeding to injuring plants according to predator and prey abundance had already been used to satisfactorily manage Dicyphus spp. populations, as explained in Section 2.1. (Alomar and Albajes, 1996; Shipp and Wang, 2006). This biocontrol practice prevented high predator-to-prey ratios at susceptible crop growth stages.

6. Discussion Although the use of zoophytophagous predators for pest control in vegetable crops may initially be considered too risky, both M. pygmaeus and N. tenuis are not only conserved, but also released in greenhouse crops across extensive geographical areas, particularly in the Mediterranean basin. Their advantages as efficient generalist predators tend to counterbalance the risk of their causing crop damage. The biocontrol industry is also now interested in the use of generalist entomophagous insects that could be used to control both current and new exotic pest. The case of N. tenuis is a good example. Based on a thorough analysis of the potential risks of its use, it would probably not be recommended for release. However, due to its high predation capacity on some tomato devastating pests that limit crop production, such as virus vectors and invasive pests, it has been proven to be an efficient control agent and is now commercially produced and released. On the other hand, the fact that most of these species occur spontaneously and that growers already have to deal with them if they do not heavily spray their crops means that managing their presence is not an option but a necessity. The importation of plant-feeding predators as exotic biocontrol agents is not recommended. When a plant-feeding predator is considered for introduction into a new area, the risk of crop damage must be analyzed (Albajes et al., 2006). If a risk exists, there is no

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point in continuing with the process of evaluating the possibility of importing that natural enemy (Van Lenteren and Loomans, 2006). In conclusion, some of these predators are being used not only in conservation but also in augmentation biological control programs. A low level of crop damage would not be a major obstacle to the use of these predators as long as they offer net benefits in terms of pest control and reductions in insecticide sprayings. The risks associated with their use are a function of various different factors that need to be well known in order to predict potential damage. This knowledge should be integrated into management programs in order to minimize risks and to take the fullest advantage of the use of these predators as biocontrol agents.

Acknowledgments We thank our colleagues from IRTA, Jordi Riudavets and Nuria Agustí, for their suggestions on the manuscript and two anonymous reviewers for their wise comments on an early draft of this review. This work was funded by the Spanish Ministry of Science and Innovation (MICINN) (projects AGL2007-60371 and AGL2008-00546).

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