Phytoparasitica DOI 10.1007/s12600-016-0529-y

Pomegranate arthropod pests and their management in the Mediterranean area Giuseppe E. Massimino Cocuzza & Gaetana Mazzeo & Agatino Russo & Vittorio Lo Giudice & Salvatore Bella

Received: 4 March 2016 / Accepted: 25 July 2016 # Springer Science+Business Media Dordrecht 2016

Abstract Here we review the arthropod pests most damaging to pomegranate cultivation in the main production regions of the Circum-Mediterranean area, and discuss the eventual phytosanitary risks linked to some newly introduced species in this geographical area. The arthropod species mentioned here are based on their occurrence and economic importance. These are either mites (Tenuipalpidae) or insects belonging to Hemiptera (Flatidae, Aphididae, Aleyrodidae, Coccidae, Diaspididae, and Pseudococcidae), Lepidoptera (Cossidae, Lycaenidae, Erebidae, and Pyralidae), Diptera (Tephritidae), and Coleoptera (Bostrichidae and Nitidulidae). In the Circum-Mediterranean area, the major pests are Aphis punicae, A. gossypii, Planococcus spp., Zeuzera pyrina, Apomyelois ceratoniae, Deudorix livia and Cryptoblades gnidiella. A nod is also given to those species normally considered as minor pests that, in some environment and under specific conditions, can be of major concern. Particular attention should be paid G. E. M. Cocuzza (*) : G. Mazzeo : A. Russo Di3A - Dipartimento di Agricoltura, Alimentazione e Ambiente, Università degli Studi di Catania, via S. Sofia 100, 95123 Catania, Italy e-mail: [email protected] V. L. Giudice Agronomist, via Calvario 45, 95030 Mascalucia, Catania, Italy S. Bella CREA-ACM – Consiglio per la Ricerca in Agricoltura e l’Analisi dell’Economia Agraria, Centro di Ricerca per l’Agrumicoltura e le Colture Mediterranee, Corso Savoia 190, 95024 Acireale, Catania, Italy

toward avoiding the introduction of two species that could become a serious problem for pomegranate that are Thaumatotibia leucotreta and Deudorix isocrates. The main morphological and biological characteristics of each pomegranate pest species and the tools available in their integrated and organic control are briefly presented. Keywords Punica granatum . Mediterranean basin . Insects . Mites . Natural enemies . Pest management options

Introduction The pomegranate (Punica granatum L.) is native to Central Asia. Subsequently, since ancient times, it has been cultivated throughout Middle Asia and North Africa. More recently, pomegranate has been cultivated in all continents. World pomegranate production is currently estimated at 1.5-2 million tonnes, 90 % of which is in Iran and India. The rest is distributed amongst various Mediterranean countries (mainly Spain, Turkey, and Israel), China, the United States, Armenia, Azerbaijan, Pakistan, and Argentina (CBI 2014). The consumption of pomegranate as fresh fruit or juice has recently increased due to its many recently discovered medicinal properties. Several studies have demonstrated its beneficial effects on health (e.g. the prevention of some cardiovascular diseases and prostate cancer) (Malik et al. 2005; Wang et al. 2011; Vilahur et al. 2013), due to its richness as an important source of phytochemicals

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and their derivatives (mostly polyphenols) and to its high content of antibacterial agents (Gil et al. 2000; Al-Zoreky 2009; Fischer et al. 2011). The cultivation of pomegranate has also recently been revaluated for the crop's positive agronomic characteristics, such as the high adaptability to various climatic or soil conditions and the limited water requirements that suit its cultivation on marginal land (Costa and Melgarejo 2000; Chandra and Jadhav 2008). Texeira da Silva et al. (2013) extensively review the main agronomic characteristics of the pomegranate (Table 1). The development of extensive pomegranate cultivation, especially in the Mediterranean area, has not been followed by adequate strategies of pest control, frequently due to the lack of information available for the pests that can attack the cultures. The pomegranate is also considered a Bminor crop^ in Europe, which has limited the availability of chemicals for use in programs of Integrated Pest Management (IPM). The pomegranate has many pests that, if not well managed can seriously affect commercial fruit production. Except the papers of Juan et al. (2000), Kozina et al. (2011) and Grafton-Cardwell (2013) that focus on pest species affecting pomegranate, to date, the key review articles on pomegranate deal with agronomic aspects of its cultivation, providing only few information on pests and the best strategies for their control (Holland et al. 2009; Glozer and Ferguson 2011). The present article reviews the pests of pomegranate in the Mediterranean area, describing their harmfulness, their main morphological and biological characteristics and the techniques used in their integrated and organic control. We also discuss the most damaging species occurring in the main pomegranate production areas of the world and the risks of their possible introduction to the Mediterranean area.

Hemiptera The citrus flatid planthopper Metcalfa pruinosa (Say) (Flatidae) is a polyphagous pest (recorded on more than 200 botanical species) that occasionally attacks pomegranate. The species is widespread in America (its area of origin) and across Europe to the Far East. The sides of the bodies of juvenile stages are covered with a white wax, but the adults (3 mm in length) appear whiter because the wax covers most of the body (Mead 1969), varying to greyish with age. M. pruinosa has one generation per year, with overwintering of the eggs

and occurrence of the young nymphs in spring. Damage is caused by the removal of sap, the large amount of honeydew produced, and wax that daub the vegetation with the subsequent development of sooty mould. Fruit covered by honeydew is greatly depreciated in value. In Europe, the insect is well controlled by Neodrynus typhlocybae (Ashmead) (Hymenoptera, Dryinidae), an introduced parasitoid (Lucchi 2000). Sporadic infestation is often a direct consequence of incorrect cultural practices or inappropriate use of non-selective insecticides that reduce populations of non-target beneficial insects. The best method of control is to restore the biological equilibrium. Several species of white flies (Aleyrodidae) can infest pomegranate. These insects are localised mainly on the underside of leaves. An infestation can be detected by foliar yellowing and abundant production of honeydew on which sooty mould develops, covering the plant, including fruits. Heavy attacks on pomegranate can cause defoliation and smaller fruit size. A sudden infestation by these insects is frequently due to improper agricultural practices or to the use of insecticides that eliminate natural enemies or alter the equilibrium of the agro-ecosystem, favouring the uncontrolled development of pest populations. Moreover, the exclusive use of insecticides is never fully effective for the control of whiteflies (Gyeltshen et al. 2014). The citrus whitefly, Dialeurodes citri (Ashmead), is primarily a pest of Citrus spp., and the attacks on pomegranate are rather episodic. This species probably originated in India but now it is almost cosmopolitan. The body and wings of adults (about 1 mm in length) are covered with a white, powdery wax. Nymphs are flattened, oval, light yellowish, and without a waxy secretion. D. citri develops 2–3 generations per year in Mediterranean areas and 5–6 in the tropical areas of origin. Numerous natural enemies can effectively control this pest on Citrus trees. Abd-Rabou and Simmons (2014) recorded 29 species of parasitoids and 15 of predators in Egypt, of which the parasitoid Encarsia lahorensis (Howard) (Hymenoptera, Aphelinidae) and the predator Clitostethus arcuatus (Rossi) (Coleoptera, Coccinellidae) were the most effective in control activity. Severe infestations on pomegranate by the ash whitefly, Siphoninus phillyreae (Haliday), have been reported in Greece and India (Balika et al. 1999; Tsagkarakis 2012). It is a cosmopolitan and polyphagous insect species reported on more than 50 botanical species in various families (Nguyen and Hamon 2011). Similarly

Citrus flatid planthopper Citrus whitefly Ash whitefly Spiny whitefly Pomegranate aphid Cotton aphis Citrus mealybug Hibiscus mealybug Japanese wax scale Chinese wax scale Florida wax scale Black scale Brown soft scale Grey citrus scale California red scale Olive scale Pomegranate scale Coconut scale Florida red scale Leopard moth Pomegranate butterfly Pomegranate fruit borer Passenger moth Honeydew moth Carob moth Quince moth False codling moth Dried fruit beetles Mediterranean fruit fly Black borer Grape borer Pomegranate mite False pomegranate mite Pomegranate leaf curl mite

Metcalfa pruinosa Dialeurodes citri Siphoninus phillyreae Aleurocanthus spiniferus Aphis punicae Aphis gossypii Planococcus citri Maconellicoccus hirsutus Ceroplastes japonicus Ceroplastes sinensis Ceroplastes floridensis Saissetia oleae Coccus hesperidum Coccus pseudomagnoliarum Aonidiella aurantii Parlatoria oleae Lepidosaphes granati Pinnaspis buxi Chrysomphalus aonidum Zeuzera pyrina Deudorix livia Deudorix isocrates Dysgonia algira Cryptoblades gnidiella Apomyelois ceratoniae Euzophera bigella Thaumatotibia leucotreta Carpophilus spp. Ceratitis capitata Apate monachus Amphicerus bimaculatus Tenuipalpus granati Tenuipalpus punicae Aceria granati

P O P P S P P P P P P P P O P P P P P O O O P P P P P P P P P P P O

+ + + + ++ ++ ++ + + + + + + + + + + + + +++ ++ ++ + ++ ++ + ++ + ++ + + + + +

Greece Everywhere Everywhere Spain, Turkey, Cyprus Spain, Turkey Greece, Italy, Spain, Israel, Portugal Turkey Turkey Turkey Greece Greece, Turkey Egypt, Turkey Everywhere Cyprus, Jordan, Tunisia Turkey Israel, Morocco, Tunisia, Turkey Israel Israel Turkey Italy, Turkey Greece, Turkey -

Countries with Degree of Degree of Specificity harmfulness recorded damages

+ + + + + + +

+ + +

+

+ + + + + + + + + + + + + + + +

+

+ +

+ + +

+ +

+ +

+ +

+ +

+ +

+ +

+ + +

+

+ +

+

+ +

+ + + + + + + + + + + +

+ + + + + + + + + + + + +

+

+

+

+ +

+

+ +

Foliage Green fruit Ripening fruit Shoot Twig Branch Trunk

Part attacked

S high specificity, O Oligophagous species; attacking pomegranate and a few of other plants, P Polyphagous species, attacking a wide range of plants.

Common name

Pest species

Table 1 Arthopod pests of pomegranate in the Mediterranean area, degree of harmfulness (+ less, +++ most) and preferred part of the plant

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to other whiteflies species, a white wax covers the body and wings of the adults. The nymphs are distinguished by the presence of two longitudinal tufts of white wax and by the production of typical droplets of a glassy wax that cover the body. S. phillyreae has numerous natural enemies, mainly C. arcuatus and Encarsia spp., which are capable of containing pest populations below the damage threshold (Abd-Rabou 2006; Nguyen and Hamon 2011). The orange spiny whitefly, Aleurocanthus spiniferus (Quaintance), is a serious pest of Citrus plants native to eastern Asia and it has recently been introduced in southern Italy (Apulia) (Porcelli 2008), where, within a few years, it has been found on 95 botanical species including pomegranate (Cioffi et al. 2013). The juvenile stages are oval-shaped, blackish, with a waxy white band visible along the edge. The adults are covered with a bluish powdery wax. In Swaziland, A. spiniferus may develop 4–6 generations per year depending on the climatic conditions. Several hymenopteran parasitoids (Aphelinidae) are natural enemies of this pest on Citrus, with Encarsia smithi (Silvestri) being the most effective in Micronesia and Swaziland (Muniappan et al. 1992; Van den Berg et al. 2000). The coccinellid predator C. arcuatus is the only effective biocontrol agent in the areas of recent spread in southern Italy (Cioffi et al. 2013). Worldwide, the most damaging aphids (Aphididae) of pomegranate are Aphis punicae Passerini (pomegranate aphid) and Aphis gossypii Glover (cotton aphid). The plant can also be rarely infested by Aphis spiraecola Patch (green citrus aphid or spirea aphid), Aphis craccivora Koch (cowpea aphid, groundnut aphid, or black legume aphid), Aphis fabae Scopoli (black bean aphid), Aphis achyranthi Theobald, and Toxoptera aurantii Boyer de Fonscolombe (black citrus aphid) (Blackman and Eastop 2006; Holman 2009). Aphis punicae is common in the Mediterranean area, Asia, Africa, and the Indian subcontinent (Swirsky 1954; Barbagallo and Stroyan 1982; Blackman and Eastop 2006; Sugimoto 2011; Bhagat 2012; Lee et al. 2015). This species is common on pomegranate but has also been recorded from Lawsonia inermis (Lythraceae), Duranta plumieri (=erecta), Lantana camara (Verbenaceae), Bignonia sp., Campsis radicans (Bignoniaceae), and Plumbago capensis (Plumbaginaceae) (Bodenheimer and Swirski 1957; Blackman and Eastop 2006; Holman 2009). The morphology and colour of A. punicae may vary with environmental conditions, as in many aphid species (Dixon et al. 1982; Helden et al. 1994). In spring, the

bodies of apterous viviparous females are green, 1.381.73 mm long, with blackish siphunculi and a tongueshaped pale brown to pale green cauda. In summer, the subsequent generations have pale green colour and generally significantly smaller bodies (0.80-1.17 mm), pale brown to pale green siphunculi with greyish brown apexes and pale green or yellowish cauda (Sugimoto 2011). Aphis gossypii is a cosmopolitan and polyphagous species recorded on more than 600 host plants (Holman 2009). The apterous form of this aphid has a smallmedium body (1.6-2 mm long) and a greenish colour in populations living on pomegranate. In Sicily, pomegranate plants grown in proximity to citrus groves are frequently infested by this aphid species. A. gossypii and A. punicae are not easily distinguished morphologically (Massimino Cocuzza and Lo Giudice 2014). The main distinctive morphological character is the siphunculus/ cauda ratio (1.22-1.50 in A. punicae and 1.50-2.00 in A. gossypii). The colour, which can vary in both species seasonally and with environmental conditions, is of little diagnostic value. Both species can be easily distinguished by their DNA barcodes (Cocuzza et al. 2009; Lee et al. 2015). In spring, appropriate scientific distinction between species should be performed to prevent subsequent infestations. Indeed, alatae A. gossypii leave definitively the plants with the hardening of the vegetation, whereas A. punicae populations remain on pomegranate during summer, infesting the fruits in late summer or in early autumn. This observation may leads to eventual considerations of using different pest control strategies. In Mediterranean area, both species begin infestation in spring coincident with the development of tender shoots. Field colonies of A. gossypii are established by alatae from other plants, but A. punicae colonies begin by fundatrixes born from overwintered eggs laid during the previous autumn on branches, close to dormant buds. The colonies of both species increase rapidly with increasing temperatures and invade all new vegetation. Colony population peak is reached during flowering period (first half of May), when buds, flowers, and young growing fruits are infested. The two species behave differently when the shoots harden and the temperatures rise further. The winged forms of A. gossypii abandon the pomegranate to search for new host plants. A. punicae mainly remains on the same plant during the summer, where colonies formed by small apterous viviparous females find refuge in the shoots of regrowth and survive the summer heat by reducing metabolic activity and reproduction (Patti 1985). The individuals

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described above, which leave the plant to establish summer colonies on secondary host plants represent exceptions. Colonies increase their growth rate in September as the temperature decreases and humidity increases, frequently developing large populations. The aphids settle on the underside of leaves or on fruits during this period. The amphigonic forms develop and produce the winter eggs from the second half of November. Damage derives from the considerable amount of sap consumed and from the abundant emission of honeydew on which sooty mould develops. The large amount of honeydew distributed on vegetation in very sunny areas can trigger a Blens effect^, which can cause burns in parts of the shoots. In late summer, A. punicae populations cause cosmetic damage to fruit epicarp with honeydew and by the formation of large discoloured areas due to the feeding pierces of the aphids, which depreciates the value of the product for fresh consumption. A. punicae and A. gossypii have many efficient natural enemies predators belonging to Coleoptera (Coccinellidae), Diptera (Syrphidae and Cecidomyiidae), Neuroptera (Chrysopidae), and Hymenoptera parasitoids (Lysiphlebus spp. and Aphidius spp.) that often fail to contain the damage in spring, but can later greatly reduce the aphid populations. In addition, in Sicily the activity of natural enemies is limited during late summer and early autumn, a time when the colonies of A. punicae are present on the fruits, causing considerable damages. The use of specific and authorised agrochemicals may be necessary for young plants, because an infestation can considerably delay plant development and the start of production. Nevertheless, these agrochemicals should not be used extensively to avoid affecting parasitisation/predatory activity of pest’s natural enemies, which would worsen infestations by other pests (Abd-Ella 2015). The excessive use of agrochemicals can also induce the occurrence of resistant pest populations, as reported on the specialised pomegranate crops in Alicante, Spain (Juan et al. 2000). Sixty-five species of scale insects (Coccoidea) have been recorded on P. granatum around the world (García Morales et al. 2016), but only a few of these sap-sucking insects species are capable to seriously reduce pomegranate yield. The commercial quality of pomegranate fruits in Spain and in other important producing areas of the Mediterranean basin is negatively affected by the citrus mealybug, Planococcus citri (Risso) (Pseudococcidae) (Bartual et al. 2012; Kahramanoglu and Usanmaz

2013). P. citri, generally known primarily as a citrus pest, is a polyphagous species that has been collected from 82 families and 191 genera of host plants (Daane et al. 2012; García Morales et al. 2016). The adult female body is oval (3–4 mm long) and covered by a powdery wax, with margins surrounded by 18 pairs of stout waxy filaments, of which the anal and the two preceding pairs are slightly longer than the others. Males are winged and have two long backwards-projecting white waxy threads (Gill et al. 2013). A fertilised female can lay 300–600 eggs inside white cottony ovisacs during her life. The first instars (crawlers) are yellow, oval-shaped with red eyes, and covered with white waxy particles (Gill et al. 2013). The citrus mealybug overwinters in different life stages inside shelters on various parts of plants, taking 6–10 weeks to reach maturity. Females can live for up to 1 month depending on the host plant. In citrus and other fruit crops, nymphs typically settle along the midribs and veins on the underside of leaves or on young twigs and fruit buttons. They tend to hide in crevices, and light infestations are often easily overlooked (Gill et al. 2013). The citrus mealybug has been found on the stems of young pomegranate trees and fruits and inside the fruit calyx (Wohlfarter et al. 2010). The pest develops 3–6 generations per year depending on the environmental and trophic conditions. P. citri can cause damage by settling between two fruits or inside the crown. It produces a sugary honeydew that falls on leaves and fruits below, resulting in the growth of sooty mould that may degrade fruit quality (Holland et al. 2009; Gill et al. 2013). In the inner valleys in Israel and in Turkey, P. citri has been replaced by the closely related mealybug species P. ficus (Signoret) (Zvi Mendel, personal communication). In Mediterranean areas, citrus mealybug is controlled by several natural enemies, such as the parasitic wasps Leptomastidea abnormis (Girault), Leptomastix dactylopii Howard, and Anagyrus pseudococci (Girault), predaceous lacewings of the genera Sympherobius and Chrysopa, and the lady beetles Cryptolaemus montrouzieri Mulsant and Scymnus sp. (Cravedi et al. 2008; Mani 2016). Several coccinellids have been collected in Turkey attacking the citrus mealybug in pomegranate orchards, such as C. montrouzieri and species of the genera Nephus, Chilocorus, and Clithostetus (Özturk and Ulusoy 2009). In Spain, biological control by natural enemies can help to decrease pest populations but cannot prevent fruit damage (Bartual et al. 2012). Pomegranate is considered a minor crop, and the chemical

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control of related pests is limited because of the scarcity of authorised and registered pesticides available for this crop (Bartual et al. 2012). The pink hibiscus mealybug, Maconellicoccus hirsutus (Green), is a polyphagous species considered a serious pest on many crops and ornamentals, infesting all parts of the plants and causing their mortality in the case of severe infestations (García Morales et al. 2016). M. hirsutus has been reported as a pest on pomegranate in India (Mani and Krishnamoorthy 1991) and Sri Lanka (Sirisena et al. 2013). In the Mediterranean Basin, the pink hibiscus mealybug is present in Lebanon, Egypt, Cyprus, and Tunisia (Ben Halima-Kamel et al. 2015; EPPO 2016); its polyphagia has favoured its rapid geographical expansion. The trade of infested plants and the dispersion of crawlers and egg sacks by wind have further promoted its diffusion. Considering the rapid spread of this invader in the Mediterranean Basin and the expansion of pomegranate cultivation, the species should be closely monitored especially in the areas of new introductions. Nineteen species of soft scales (Coccidae) and seventeen species of armoured scales (Diaspididae) have been recorded on pomegranate around the world (García Morales et al. 2016). Amongst the soft scales, Ceroplastes japonicus Green (japanese wax scale), Ceroplastes sinensis Del Guercio (chinese wax scale), and Ceroplastes floridensis Comstock (Florida wax scale) have been recorded on pomegranate in the Mediterranean Basin and are easily distinguishable among them using morphological characters of adult females. The female of the japanese wax scale is 2–2.5 mm long, with a reddish body coated with a thick layer of white-grey wax. The species is bisexual and develops one generation per year. It overwinters as young adult females that, in Italy, lay eggs in late spring or early summer (Pellizzari and Camporese 1994). The female of the chinese wax scale is larger (about 6 mm), with a reddish-brown body, elliptical and convex in lateral view, with a thick wax covering (Gimpel et al. 1974). It is a polyphagous, bisexual, and parthenogenetic scale, developing one generation per year and overwintering as females and third instar larvae (Pellizzari and Camporese 1994). Females of both species lay an average of 2000 eggs beneath their bodies (Cravedi et al. 2008). Females of the Florida wax scale have elongated reddish-brown bodies (2–4 mm long and 1–3.5 mm wide) with a short anal process and are covered with a pinkish-white wax

(Sharma and Buss 2014). It generally has two generations per year and is polyphagous, although it is considered a pest of citrus (Pellizzari and Camporese 1994; García Morales et al. 2016). The most common natural enemies in the Mediterranean area are Coccinellidae (Chilocorus spp. and Exochomus spp.), Noctuidae (Eublemma spp.), and Pteromalidae (Scutellista spp. and Moranila spp.) (Pellizzari and Camporese 1994). These three scale insect species are reported as pests of pomegranate in the Mediterranean area (Monaco and Sabatino 1980; Holland et al. 2009; Özturk and Ulusoy 2009) and China (Ma and Bai 2004). The black scale, Saissetia oleae (Olivier), is easily recognised by its round and convex body, brown or black in older females, and by the presence in all stages of raised areas forming an "H" on the dorsum. S. oleae occurs on leaves, stems, and produce honeydew that promotes the growth of sooty mould. It is polyphagous and has been recorded as a pest on pomegranate in Greece, Italy, Spain, and Portugal (Juan et al. 2000; Miller et al. 2014). Populations are reduced by high temperatures, mainly crawlers whose mortality can reach 90-95 % and by the predacious coleopteran Chilocorus spp., Exochomus spp., and by the hymenopteran parasitoids Scutellista spp., Moranila spp., Coccophagus spp. and Metaphycus spp. with the latter species representing the key natural enemies in many Mediterranean agro-ecosystems (Cravedi et al. 2008; Zvi Mendel, personal communication). The body of the adult female of Coccus pseudomagnoliarum (Kuwana) (grey citrus scale) is up to 7 mm long, elongate oval, slightly convex, and dark grey in older specimens; the dorsum of the young female is grey with dark-brown mottling (Miller et al. 2014). Females reproduce parthenogenetically and develop one generation yearly in Israel, Greece, and other countries around the world (Miller et al. 2014). The presence of C. pseudomagnoliarum and the similar Coccus hesperidum L. on pomegranate crops has been reported in Turkey by Özturk and Ulusoy (2009). The California red scale Aonidiella aurantii (Maskell), a worldwide pest of citrus, is among the most damaging armoured scales. It is a polyphagous species and has been recorded in Turkey as a pest of pomegranate (Özturk and Ulusoy 2009). Females have roundish covers and are firmly attached to the wood, fruit and/or leaves upon which they live. California red scales have long filamentous mouthparts that allow them to suck on twigs, leaves, branches, and fruit. This activity damages

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fruits and other parts of the plant, causing foliar yellowing and drop and occasionally the death of the tree (Grafton-Cardwell et al. 2015). Many natural enemies can control infestations of A. aurantii, such us coccinellids and wasps, particularly Aphytis melinus DeBach and Encarsia perniciosi Tower. The former species is an effective parasitoid of the scale and is used in biological control programmes, especially in Spain where it is well-adapted, and the latter species can be effective in controlling A. aurantii in areas where it has become established (García Morales et al. 2016). The females of Parlatoria oleae (Colvée) have whitish-grey ovate covers (0.69-85 mm long and 0.57-0.65 wide), with yellowish-brown, apical exuviae. This species develops two generations each year (up to four in some areas) (García Morales et al. 2016). P. oleae attacks olives, stone fruits, apples, pears, ornamentals (García Morales et al. 2016) and damages on pomegranate are reported in Greece (Argyriou et al. 1976). The species lives on branches, leaves, twigs and fruits, producing reddish spots, abnormalities, and deformations early during fruit development. This scale is usually under efficient biological control by its natural enemies, such us Aphytis paramaculicornis DeBach and Rosen, Coccophagoides utilis Doutt and Aphitis maculicornis (Masi) (Moursi et al. 2013; García Morales et al. 2016). Chemical control, whenever necessary, should be applied against crawlers in late spring (Cravedi et al. 2008). Lepidosaphes granati Koroneos (pomegranate scale) females have brown comma-like covers (2.0-2.2 mm long and 0.48-0.72 mm wide) (Kosztarab and Kozár 2012). The female body is characterised by typically shaped pygidial median lobes; the cover is more linear and smaller in males than females (Pollini 2013). This species has a Palearctic distribution and has been recorded on Eleagnus spp., Acacia cultriformis, Ficus carica, Rhamnus oleoides, Crataegus spp., Celtis, Ulmus, Zelkova and Platanus (Kaydan et al. 2013; García Morales et al. 2016). It has been recorded on P. granatum in Greece (Koroneos 1934), Italy (Balachowsky 1954), and Turkey (Kaydan et al. 2013). In the Mediterranean area, L. granati has one to two generations per year. It develops small populations on the branches and trunk of the host plant, but it is considered a pest (Kosztarab and Kozár 2012; García Morales et al. 2016) even if rarely needing control (Pollini 2013).

The covers of females of Pinnaspis buxi (Bouché) are elongated and variable in shape depending on the host plant, very small, pale brownish or nearly colourless, usually quite thin, flat, and translucent (McKenzie 1956; Pollini 2013; García Morales et al. 2016). Male covers have three strong carinae and are white (García Morales et al. 2016). Its distribution is not well known, however it has been recorded in many countries around the world, living in glasshouses in Europe (Pollini 2013). The scale lives on the above ground of plants of numerous genera, including Punica granatum in the Mediterranean Basin (Ferris and Rao 1947; Balachowsky 1954; Pollini 2013). Plants infested by P. buxi show loss of vigour, defoliation, deformations, and yellow spots on leaves, which become desiccated in case of severe infestations (Dekle 1965; Beardsley and Gonzalez 1975). Control measures are based on increasing plant spacing and pruning mature trees to prevent contact between canopies and thus the spread of scales between plants (Beardsley and Gonzalez 1975). Adopting strategies to preserve natural enemies is also recommended. In the Mediterranean area, the black circular scale, or Florida red scale, Chrysomphalus aonidum (L.), was initially recorded on Cycas in Sicily about twenty years ago (Longo et al. 1994) and is widespread in southern Italy on Citrus but has been recorded as a pest on pomegranate in Egypt and Turkey (Hall 1922; Özturk and Ulusoy 2009).

Lepidoptera Amongst the Lepidoptera, the leopard moth Zeuzera pyrina (L.) (Cossidae) is the most damaging pomegranate pest in the Mediterranean area, especially for young plants (1–3 years). The species is widely distributed in Europe, North Africa, Asia, and the USA. The moth is a polyphagous species and has been reported on several genera of host plants (e.g. Prunus, Malus, Pyrus, Olea, Acer, Fagus, Tilia, Platanus, Quercus, Salix, Populus, Ulmus, and Tamarix) (Gatwick 1992). The adults (about 3 cm long) have white forewings with metallic bluish spots of varying sizes. The thorax is white and tomentose with six large bluish spots, and the abdomen is dark. The females are larger than males (wingspans of 50– 70 mm in females and 35–50 mm in males) and have filiform antennae (the basal part is bipectinate in males). Larval colour varies with maturity from pinkish to yellowish, with small black spots (pinacula) in longitudinal

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rows along the body. Mature larvae are about 50–60 mm long. In South Italy, it was recorded that each female may lay up to 1000 eggs in groups of about a hundred in the more sheltered parts of the trunk or branches of 2–3 year-old-trees. The eggs are laid from late April to September, with a peak in late June and early July. The larvae, after eclosion, penetrate the plant tissue at the point of insertion of leaves or the axils of buds and begin to excavate ascending galleries. The larvae emerge and fall several times from plant tissues, attacking progressively larger twigs more suited to their growing size. The presence of larvae is revealed by sawdust and frass (as small cylinders) at the basis of the plant or around the exit holes from the galleries. The larval cycle is completed in 1–2 years, depending on whether the eggs hatched at the beginning or at the end of the summer, respectively (Giorgini et al. 1997). Adults live 8– 10 days, so mating and oviposition also occur during this brief period. Only a few eggs complete embryonic development, because most are eaten or are weakened by the high summer temperatures (Guario et al. 2001). Larval attacks may dry the buds, but more extensive damage in the branches is evidenced by the decay of the vegetation and loss of mechanical strength. The presence of the xylophagous form may often be unnoticed, and branches may suddenly break in strong winds. One larva can kill a 1-year-old tree, whereas a 3-year-old tree can easily lose some branches to larval activity. The leopard moth has numerous natural enemies that do not effectively control the moth populations. For example, in a study conducted in Egypt, only 1.2 % of the larvae was parasitized by Hyssopus sp. (Hymenoptera, Eulophydae), an ecto-parasitoid wasp (Hegazi et al. 2015). In North Italy, the parasitoids Neoxorides nitens (Gravenhorst), Dolichomitus messor (Gravenhorst), Pristomerus vulneratus (Panzer), Diasegma terebrans (Panzer) (Hymenoptera, Ichneumonidae), Dolichogenidea laevigatus (Ratzeburg) (Hymenoptera, Braconidae), Perilampus tristis Mayr (Hymenoptera, Perilampidae), and Megaselia praecusta (Schmith) (Diptera, Phoridae), were reported by Campadelli (1995). Similar percentages of natural activity have been recorded in Egypt for the entomopathogenic fungi Beauveria bassiana (Balsamo-Crivelli) Vuillemine and Metarhizium anisopliae (Metschnikoff) Sorokin (Hegazi et al. 2015). Nematodes of the genera Heterorhabditis and Steinernema can be effective in the control of the moth (Giorgini et al. 1997; Ashtari et al. 2011). The best control strategy, especially in areas

where Z. pyrina is present (i.e. near olive orchards), is the periodic visual inspection of the plants to promptly identify the penetration holes. Pruning and the subsequent destruction of the branches is effective if they are young. In larger branches, inserting a wire into the excavated galleries can kill the larvae. Spraying the galleries with authorised insecticides is an alternative. The holes must be cleaned, disinfected, and sealed with grafting mastic to avoid the stagnation of water or the entry of opportunistic fungi. In young and large orchards, pheromone traps can provide useful information on the seasonal flight of adults to identify the oviposition period and the most suitable time for treatment against the youngest larvae before they emerge from eggs (Natale and Pasqualini 1999). They can also be used for mass trapping or mating disruption, as demonstrated in olive orchards (Guario et al. 2001; Hegazi et al. 2009, 2010). The pomegranate butterfly, Deudorix (=Virachola) livia (Klug) (Lycaenidae), is amongst the most important and destructive pests of pomegranate worldwide. It is currently widespread in the Middle East, North Africa, and the Arabian Peninsula (Katbeh-Bader et al. 2003; Libert 2005). In Europe, D. livia has been recently reported in Greece (Müller et al. 2005) and Cyprus (Kahramanoglu and Usanmaz 2013). This pest has recently caused conspicuous losses of production in Tunisia (Ksentini et al. 2011; Moawad et al. 2011) and Cyprus (Kahramanoglu and Usanmaz 2013). The wings are bluish-brown in females and brown-orange in males. Colour, however, is highly variable in this species (Libert 2005). The larvae are reddish-brown. Under laboratory rearing conditions (27 °C and 70 % R.H.), the species can complete larval development in about 44 days when reared on pomegranate fruits and in 33 days when reared on acacia pods. The longevity of fertilised females is about 12 days when reared on either host; they lay about 42 eggs on pomegranate and about 50 eggs on the pods of acacia (Gharbi 2010). Blumenfeld et al. (2000) reported that D. livia lays eggs in the crown of the developing fruit, and damage appears during the ripening period or in storage. The neonate larva bores into the fruit to feed on the ripening seeds until maturity and then exits from a hole to pupate in the soil. The feeding activity of the larvae leads to the development of rot, which can later fall (Braham 2015). Ksentini et al. (2011) reported that the damage caused by D. livia in varieties of pomegranate grown in Tunisia was estimated at 5-52 %. In another study, Moawad

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et al. (2011) recorded that the percentage of damaged fruits varied from about 3 % (cv Al-Taif) to 60 % (cv Hegazi-Bathan). In Jordan, D. livia has 2–3 generations on pomegranate fruit, beginning in summer at 4 % and gradually increasing to 48 % infestation by early October (Obeidat and Akkawi 2002). In Cyprus and Tunisia, some research studies suggest that B. thuringiensis and spinosad are effective alternative biological control agents for D. livia and can be used in organic-farming systems and in IPM practices (Kahramanoglu and Usanmaz 2013; Sayed et al. 2015). A further study carried out in Saudi Arabia showed the efficacy of Trichogramma turkistanica Meyer (Hymenoptera, Trichogrammatidae) in the control of the pest (Sayed et al. 2015). The honeydew moth, or pomegranate moth, Cryptoblabes gnidiella Millière (Pyralidae), is native to the Mediterranean area and is an introduced species in South and Central America, New Zealand, SouthEast Asia, and some African countries. This moth is an important pest of citrus, grapes, and pomegranates in the Mediterranean area. It is a pest of wild, cultivated, or ornamental plants belonging to various families, e.g. Malus, Persea, Punica, Gossypium, Annona, Feijoa, Ceratonia, Vitis, Citrus, Actinidia, Eriobotrya, Ficus, Zea, Prunus, Pyrus, Cydonia, Oryza, Sorghum, Triticum, Daphne, Nerium, Paspalum, and Ricinus (Leraut 2014). The eggs are oval and irregularly reticulate. The body is yellowish, olivaceous, reddish, or brownish-grey with longitudinal stripes and measure at maturity about 12 mm. The adult wingspan is 11– 20 mm. Forewings are greyish-brown with a variable amount of whitish suffusion, and scattered reddishbrown scales give a purplish appearance. Hindwings are shiny white (Goater 1986). Adults are active at night and are attracted to sweet substances, including the honeydew excreted by mealybugs, and to fruits such as grapes and pomegranates that have been injured by other insects. Females lay their eggs on fruit, usually singly or in small batches, with an average of 150 eggs during their lives. The larvae will initially feed solely on the honeydew produced by aphids and mealybugs and are found in sheltered places amongst the fruits or between fruits and leaves (Ben Yehuda et al. 1991). The species has five larval instars and pupates close to the larval feeding site, either on the host plant or on the ground. This species has 3–4 generations per year, from May to October in Mediterranean climates, and up to five in North Africa, depending on the climate and host

plants used (Bagnoli and Lucchi 2001). Özturk and Ulusoy (2009) state that this species is a serious pest of pomegranate in Turkey. The management of this species must focus on controlling the primary pest that allows infestation by C. gnidiella. Many countries use chemical control to lessen the effects caused by the primary pest (Harari et al. 2007). Other control methods include biological control and mating disruption (Ben Yehuda et al. 1991, 1993; Sellanes et al. 2010). This species has been intercepted in material imported to the USA and the British Isles, especially on infested pomegranate fruits (Carter 1984). Wysoki et al. (1988) found that C. gnidiella larvae in Israel were highly susceptible to B. thuringiensis var. kurstaki, with 80-100 % mortality of the first and second larval instars (between 24 h and 4 days after treatment) on avocado fruits in the field. The carob moth, Apomyelois ceratoniae Zeller (Pyralidae), is a polyphagous fruit pest widespread in many tropical and subtropical regions. It is a pest of citrus, dates, figs, carob, pomegranate, pistachio, and almonds in Mediterranean countries (Gothilf 1984; Navarro et al. 1986). It is also found in the USA, Central and South America, and North Africa (Carpenter and Elmer 1978). The body of the moth is 8–10 mm in length, and the wingspan is 22–24 mm. The colour is creamy white to grey, brownish, or even dark brown. Two bright stripes with dark margins span their width. The rear wings are white-grey with light-brown veins. The larva is 12–15 mm long, pink, with a brown head and front dorsum and small dark-brown bumps on its back. The eggs hatch in 3–7 days. The development of larval stages may last 1–8 months, and pupation usually occurs at the feeding sites of the larvae. The females may lay 60–120 eggs during their lives (3–6 days). The eggs are laid in the calix of developing fruits and the larvae, after hatch, enter inside the endocarp, where their feeding activity cause rot and quality decay (Braham 2015). Three to four generations are developed yearly, from April to November, before the cooler weather induces diapause in the remaining larvae (Carpenter and Elmer 1978). Mean development time from egg to adult ranges from 45 to 62 days depending on the fruit attacked (Navarro et al. 1986). A. ceratoniae is a major problem for pomegranates in some countries. This species causes economic losses in Tunisia, especially in the South, with infestation rates as high as 90 %, it is also a major field pest of pomegranate in Iraq (Al-Izzi et al. 1985; Norouzi et al. 2008; Braham 2015), and a serious pest in date plantations in Morocco and Israel

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(Blumberg et al. 2001). Moawad et al. (2011) recorded that the percentage of damaged fruits varied from about 0 to 2.4 % (cv Mongaloty-Wonderful) to 31-42 % (cultivars Magrabi Abu-Halgon and Sweet-Banati, respectively). A. ceratoniae is the most important pomegranate pest in the Iranian province of Isfahan where an annual average of 30-40 % of the pomegranate production is destroyed or rendered unusable while in storage or on the trees. A. ceratoniae causes less fruit damage than C. gnidiella in Turkey (Yıldırım and Başpınar 2015) but it can develop in dried fruits in storage, with serious losses of product. In Morocco, it is parasitized by the hymenopterans (Braconidae) Phanerotoma ocuralis Kohl on date bunches and Bracon hebetor Say on fallen fruits (Hassan et al. 2001). The parasitoids Apanteles myeloenta Wilkinson, Bracon hebetor (Braconidae) and Brachymeria minuta (L.) (Chalcididae) have been found in parasitized larvae collected from pomegranate in Iran (Nobakht et al. 2015). In Saudi Arabia, the use of the egg parasitoid Trichogramma turkistanica and Bacillus can be an effective alternative to control the moth (Sayed et al. 2015). Populations are monitored using pheromone traps (Kehat et al. 1995), which have recently been successfully developed after many years of studies (Baker et al. 1991; ISCA 2008). The traps are placed in orchards in early March, and catches are recorded weekly. Practical experience in Turkey found that cleaning and removing the mass of old stamens after flowering could deter oviposition. The insecticide spinosad is the best option for IPM, however fenoxycarb or similar Insect Growth Regulators are likely to be effective. Synthetic pyrethroids (e.g. cypermethrin, lambda-cyhalothrin and bifenthrin) are probably effective, but are not recommended for IPM. Dysgonia algira (L.) (Erebidae) ranges from North Africa and Asia Minor in the Mediterranean area to southern Russia, Iran, Afghanistan, Turkmenistan, and Kyrgyzstan (Hacker 1989). Adults fly from April to October and develop 2–3 generations per year. The moths have a wingspan of 38–45 mm. The head and body are dark brown, and the eggs are greyish-brown. Mature caterpillars are about 42–48 mm long and brown, with reddish-brown tops and light-brown sides. The head is brown with yellow markings. The pupae are reddish-brown. The eggs are laid singly on the host plants. The caterpillars feed mainly on Rubus fruticosus but also on Salix, Genista, Lythrum, Punica granatum, Prunus, Ricinus communis, Cytisus, Epilobium, and

Parietaria. The pupa overwinters in a loosely woven cocoon. Dysgonia torrida (Guenée) share the same areas with D. algira. The patterns and colours of both species are very similar and can be distinguished only by comparing the genitalia. Numerous D. torrida larvae have been collected from pomegranate leaves in Sicily in the last decade (Salvatore Bella, unpublished data). This species, originating of sub-Saharan area, probably benefits from global warming in expanding its distribution in northern mediterranean basin (Goater et al. 2003; Bertaccini et al. 2008). Euzophera bigella (Zeller) (=E. punicaella) (Pyralidae) is a polyphagous species that occasionally can be harmful to pomegranate (Mehrnejad and Ebrahimi 1993; Atay and Öztürk 2010). The larvae develop in the cortical tissue of the trunk or branches taking advantages of the opening caused by hail, grafting or parasites, digging tunnels that can reach the cambium area. Sometimes, the attack can also affect the fruits of pomegranate that penetrate inside it through the calix. Adults have a wingspan of 15–18 mm with the front wings brown greyish in color, crossed by two lighter transverse strips (Zangheri et al. 1992). E. bigella rarely assume economic importance and usually their attack follow exceptional events (hail), graft made not properly or attack by other parasites (Zangheri et al. 1992; Simoglou et al. 2012).

Diptera The mediterranean fruit fly, Ceratitis capitata (Wiedemann) (Tephritidae), can occasionally cause serious damage to pomegranate and, especially in some conditions, it can become a key pest (Holland et al. 2009; Özturk and Ulusoy 2009; Braham 2015). Females lay eggs in small crevices in the epicarps of fully mature fruit. The larvae develop while feeding on the pulp and this activity, combined with the subsequent development of rot, render the fruit unmarketable (Braham 2015). The intensity of an infestation depends on various factors, including the susceptibility of the pomegranate variety, the seasonal climatic trend, and the presence of other suitable fruit crops in the cultivated area. Management strategy using trimedlure baited traps may serve to efficient monitoring of the medfly. Products containing a mixture of attractants and insecticides served for Blure and kill^ or Battract and kill^ approach.

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For products containing spinosad, the insecticide may be incorporated in attractive panels or applied directly to spots on plants. Low residue organophosphate insecticides (etofenprox) can be used against the medfly on pomegranate, close to ripening.

Coleoptera The genus Carpophilus (Nitidulidae), commonly known as the dried fruit beetle, includes several species that, in some areas, can be harmful to the ripe fruit. These insects are polyphagous and very common in fruit crops where they attack prevalently decaying fruits and sometimes the ripe ones still hanging on trees. In Mediterranean areas, the most common species are Carpophilus hemipterus L. and Carpophilus mutilatus Erichson, while less frequent are Carpophilus dimidiatus (F.), Carpophilus freemani Dobson (probably of South American origin) and Carpophilus quadrisignatus Erichson (Pollini 2014). Carpophilus spp. are small in size (1–5 mm long), with the body suboval and flattened. In many species, the elytra are shorter than abdomen. The background color is darkbrown; however, some species (for example C. hemipterus and C. quadrisignatus) presents on elytra roundish patches yellowish or light brown. Damages on fruits of pomegranate caused by Carpophilus spp. are reported in Israel (Zvi Mendel, personal communication) and Italy (Nuzzaci 1968). On pomegranate fruits, the attack originates from the chalice through which the larvae, emerged from eggs laid in its vicinity, penetrate into the endocarp causing burnishing and subsequent fall. As observed for peaches, probably, these latter consequences are caused by the spores of fungi that adhere to the insect body and are carried inside the fruits (Tremblay et al. 1984). The control is achieved through the immediate destruction of fallen fruit to prevent the growth of beetle population. The use of aggregationpheromone is effective in monitoring the sap beetles (Blumberg et al. 2005; Hossain et al. 2013). The use of appropriate insecticide just after varaison can prevent the oviposition or the attack by larvae. Powder post beetles (Bostrichidae) can also attack pomegranate. The black borer, Apate monachus (F.), has long been known attacking grapevines, peaches, apples, pears, avocados, citrus, and ornamental plants. Recently, damages of A. monachus on pomegranate plants were reported in a nursery on the Ionian coast of Calabria in

southern Italy (Bonsignore 2012) and in Turkey (Özturk and Ulusoy 2009). The various xylophagous life stages of the insect feed and lay eggs in holes of various sizes on the branches and trunks. The branches of the plants may be mechanically weakened, which can then be easily broken by particularly violent winds. Control is exclusively preventive and is achieved by maintaining healthy plants and continuously monitoring susceptible plant parts, from late spring to early summer, to detect the eventual presence of holes. The infested branches should be removed and destroyed (Bonsignore 2012). Chemical control is possible against adults of A. monachus by spraying the trunk and branches with long-lasting insecticides. For biological control, there are no specific studies on the black borer. However, as proven for other similar coleopteran borers, the use of Metarhizium anisopliae Metschnikoff or Beauveria bassiana (Bals. & Criv.) Vuillemin could be effective against A. monachus (Bonsignore 2012). On pomegranate, damages have also been recently reported for the insidious dog grape borer Amphicerus (=Schistoceros) bimaculatus (A.G. Olivier) in Turkey (Tezcan 2008) and Greece (Andreadis et al. 2016). Adult and larvae of this beetle attack the plants by boring holes in the branches, causing their wilt or die in the most severe infestations (Andreadis et al. 2016).

Mites The mites Tenuipalpus granati Sayed (pomegranate mite) and Tenuipalpus punicae Pirtchard & Baker (pomegranate false mite) (Prostigmata, Tenuipalpidae) and Aceria granati Canestrini & Massalongo (pomegranate leaf curl mite) (Prostigmata, Eriophyidae), can occasionally reach pest status on pomegranate (Jeppson et al. 1975; Al-Gboory et al. 1984; Döker et al. 2013). These species are largely distributed in the Mediterranean area and Middle East. Both Tenuipalpidae can also infest Vitis vinifera, Pistacea vera, Prunus armeniaca, Ficus carica and Olea europea (Jeppson et al. 1975; AlGboory and El-Haidani 1989). They are active year round, but their population reach the highest density in spring and early summer, and the females overwinter under the bark of trunk and branches (Al-Gboory and El-Haidani 1989). Both species infest preferably pomegranate leaves that became first yellowish and then dry up (Jeppson et al. 1975; Al-Gboory et al. 1984). These species cause rarely serious damage to pomegranate,

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because they are well controlled by numerous natural enemies, mainly predatory mites (Phytoseiidae). The rare infestation of A. granati can be easily noticed for the evident leaf roll on shoots. Its infestation requires no control (Vacante 2016).

Potential pest introductions in the Mediterranean area The false codling moth, Thaumatotibia leucotreta (Meyrick) (Lepidoptera, Tortricidae), was first found in 1984 in Israel on macadamia nuts, Gossypium and Ricinus crops and since then it has been repeatedly reported on imported plant material in some European countries (Mazza et al. 2014; EPPO 2015). T. leucotreta was detected in the Netherlands in 2009 (in glasshouses on Capsicum chinense) and was subsequently eradicated. The moth has occasionally been noticed in several countries in Europe (e.g. the Netherlands, Sweden, and the UK), but these specimens very unlikely came from already established populations, but from infested plants or imported fruits. This pest is a polyphagous species reported from more than 70 host plants in 40 families. It is considered a key pest of citrus and pomegranate in South Africa, and as reported in EPPO (2015) Bif there is poor orchard sanitation, this pest can cause serious crop losses up to complete fruit loss^. The damage is caused by larvae that penetrate inside the fruit by digging tunnels, which irreparably deteriorate its market value. Eggs are laid on the fruit surface, singly or in small numbers. Newly hatched larvae enter the fruit and feed internally. Fully grown mature larvae (about 15 mm long and pinkish-red) emerge from the fruit and pupate in the soil (EPPO 2015).The species has several generations per year without diapause in tropical and subtropical areas (Gilligan et al. 2011). Larvae are identified by a combination of molecular and morphological analyses (Mazza et al. 2014). The pomegranate fruit borer, or anar or common guava blue butterfly, Deudorix (=Virachola) isocrates (F.) (Lepidoptera, Lycaenidae) is considered one of the most harmful species to pomegranate in India where it can hamper planting in some districts (Bagle 2009). The same author also reported that all pomegranate varieties were susceptible to attack by D. isocrates, although some were more resistant than others. Thirty-five to 42 % of the fruit can be attacked in unprotected crops during development and can reach 90 % at fruit

maturity. This lepidopteran is an oligophagous species that can also infest Tamarindus indica, Psidium guajava, and Citrus spp. (Bhakare 2015; Chhetry et al. 2015). D. isocrates is widely distributed in Asia. The adults are mostly brown with reflex bluish in males and orange in females. The larvae (15–20 mm long at maturity) are dark brown with short hairs and white patches on the body. The eggs are laid singly on various parts of the plant, including flower buds. The pre-imaginal period is completed in 18–47 days, whereas the total life cycle lasts 1–2 months, depending on the seasonal climatic trend. Damage is caused by the activity of the larvae, which bore into the fruit and feed on the pulp and seeds originating fruit rot and, in some cases, fruit drop (Kakar et al. 1987). Infestations can be controlled by the cultivation of less susceptible varieties, the early collection and destruction of damaged fruits (easily recognised by the holes made by the larvae), and promoting the activity of the natural enemies through selective application of pesticides. The most promising natural enemies are the egg parasitoid wasps Trichogramma chilonis Ishii (Karuppuchamy et al. 2001), Trichogramma mani Nagaraja and Gupta (Hymemoptera, Trichogrammatidae) (Nagaraja and Gupta 2007), Ooencyrtus papilionis Ashmead (Hymenoptera, Encyrtidae), and Telenomus sp. (Hymenoptera, Scelionidae) (Mani and Krishnamoorthy 2002). Bagging the fruit can significantly reduce the damage (Bagle 2009) but increases production costs and favours infestations by mealybugs (Shevale 1994).

Final considerations An increase in the demand for pomegranates has led to the establishment of new plantations around the world. Pests and diseases are the most important problems that decrease pomegranate yield and quality. This review article emphasizes what is currently known about the pests of pomegranate trees and fruits in Mediterranean area and presents the most successful pest management strategies developed and implemented until recently. The correct management of pomegranate pests is crucial for the production of marketable fruits. In Europe, pomegranate is considered a minor crop, so the chemical control of pests is limited due to the scarcity of registered pesticides (Bartual et al. 2012). Alternative control tactics are becoming more important for pomegranate growers as the concerns of consumers and health

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organisations about pesticide residues increase. Pest management requires a greater commitment to the study of pomegranate pests, especially in the Mediterranean area. The increased attention to this crop must lead to the progressive development of an IPM programme against the most insidious pests. Appropriate agricultural techniques and crop management combined with newly developed biotechnological tools could optimise IPM strategies. The future management of some of the most injurious pomegranate pests might include systems involving the use of pheromones for mating disruption and attract-and-kill techniques, as well as the application of microbial products such as B. thuringiensis and augmentative release of parasitoid eggs. Further attention, especially for imported plant material, should be given to prevent the introduction in the Mediterranean area of some pests (such as T. leucotreta and V. isocrates) that potentially can establish in the southern part of the EPPO regions. Acknowledgments We are truly grateful to the reviewer for their critical reviews, their valuable comments as well as suggestions provided during the drafting of the text.

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