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Pomegranate arthropod pests and their management in the Mediterranean area

Article in Phytoparasitica · July 2016 DOI: 10.1007/s12600-016-0529-y

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Giuseppe E. Massimino Cocuzza, Gaetana Mazzeo, Agatino Russo, Vittorio Lo Giudice & Salvatore Bella

Phytoparasitica

ISSN 0334-2123

Phytoparasitica DOI 10.1007/s12600-016-0529-y

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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 toward avoiding the introduction of two species that damaging to pomegranate cultivation in the main pro- could become a serious problem for pomegranate that duction regions of the Circum-Mediterranean area, and are Thaumatotibia leucotreta and Deudorix isocrates. discuss the eventual phytosanitary risks linked to some The main morphological and biological characteristics newly introduced species in this geographical area. The of each pomegranate pest species and the tools available arthropod species mentioned here are based on their in their integrated and organic control are briefly occurrence and economic importance. These are either presented. mites (Tenuipalpidae) or insects belonging to Hemiptera (Flatidae, Aphididae, Aleyrodidae, Coccidae, Keywords Punica granatum . Mediterranean basin . Diaspididae, and Pseudococcidae), Lepidoptera Insects . Mites . Natural enemies . Pest management (Cossidae, Lycaenidae, Erebidae, and Pyralidae), Dip- options tera (Tephritidae), and Coleoptera (Bostrichidae and Nitidulidae). In the Circum-Mediterranean area, the ma- jor pests are Aphis punicae, A. gossypii, Planococcus Introduction spp., Zeuzera pyrina, Apomyelois ceratoniae, Deudorix livia and Cryptoblades gnidiella. A nod is also given to The pomegranate (Punica granatum L.) is native to those species normally considered as minor pests that, in Central Asia. Subsequently, since ancient times, it has some environment and under specific conditions, can be been cultivated throughout Middle Asia and North Af- of major concern. Particular attention should be paid rica. More recently, pomegranate has been cultivated in all continents. World pomegranate production is cur- rently estimated at 1.5-2 million tonnes, 90 % of which G. E. M. Cocuzza (*) : G. Mazzeo : A. Russo Di3A - Dipartimento di Agricoltura, Alimentazione e Ambiente, is in Iran and India. The rest is distributed amongst Università degli Studi di Catania, via S. Sofia 100, 95123 Catania, various Mediterranean countries (mainly Spain, Turkey, Italy and Israel), China, the United States, Armenia, Azerbai- e-mail: [email protected] jan, Pakistan, and Argentina (CBI 2014). The consump- V. L. Giudice tion of pomegranate as fresh fruit or juice has recently Agronomist, via Calvario 45, 95030 Mascalucia, Catania, Italy increased due to its many recently discovered medicinal properties. Several studies have demonstrated its bene- S. Bella ficial effects on health (e.g. the prevention of some CREA-ACM – Consiglio per la Ricerca in Agricoltura e l’Analisi dell’Economia Agraria, Centro di Ricerca per l’Agrumicoltura e le cardiovascular diseases and prostate cancer) (Malik Colture Mediterranee, Corso Savoia 190, 95024 Acireale, Catania, et al. 2005;Wangetal.2011; Vilahur et al. 2013), due Italy to its richness as an important source of phytochemicals Author's personal copy

Phytoparasitica and their derivatives (mostly polyphenols) and to its and occurrence of the young nymphs in spring. Damage high content of antibacterial agents (Gil et al. 2000; is caused by the removal of sap, the large amount of Al-Zoreky 2009; Fischer et al. 2011). The cultivation honeydew produced, and wax that daub the vegetation of pomegranate has also recently been revaluated for the with the subsequent development of sooty mould. Fruit crop's positive agronomic characteristics, such as the covered by honeydew is greatly depreciated in value. In high adaptability to various climatic or soil conditions Europe, the insect is well controlled by Neodrynus and the limited water requirements that suit its cultiva- typhlocybae (Ashmead) (Hymenoptera, Dryinidae), an tion on marginal land (Costa and Melgarejo 2000; introduced parasitoid (Lucchi 2000). Sporadic infesta- Chandra and Jadhav 2008). Texeira da Silva et al. tion is often a direct consequence of incorrect cultural (2013) extensively review the main agronomic charac- practices or inappropriate use of non-selective insecti- teristics of the pomegranate (Table 1). cides that reduce populations of non-target beneficial The development of extensive pomegranate cultiva- insects. The best method of control is to restore the tion, especially in the Mediterranean area, has not been biological equilibrium. followed by adequate strategies of pest control, fre- Several species of white flies (Aleyrodidae) can in- quently due to the lack of information available for the fest pomegranate. These insects are localised mainly on pests that can attack the cultures. The pomegranate is the underside of leaves. An infestation can be detected also considered a Bminor crop^ in Europe, which has by foliar yellowing and abundant production of honey- limited the availability of chemicals for use in programs dew on which sooty mould develops, covering the plant, of Integrated Pest Management (IPM). The pomegran- including fruits. Heavy attacks on pomegranate can ate has many pests that, if not well managed can seri- cause defoliation and smaller fruit size. A sudden infes- ously affect commercial fruit production. Except the tation by these insects is frequently due to improper papers of Juan et al. (2000), Kozina et al. (2011)and agricultural practices or to the use of insecticides that Grafton-Cardwell (2013) that focus on pest species af- eliminate natural enemies or alter the equilibrium of the fecting pomegranate, to date, the key review articles on agro-ecosystem, favouring the uncontrolled develop- pomegranate deal with agronomic aspects of its cultiva- ment of pest populations. Moreover, the exclusive use tion, providing only few information on pests and the of insecticides is never fully effective for the control of best strategies for their control (Holland et al. 2009; whiteflies (Gyeltshen et al. 2014). Glozer and Ferguson 2011). The present article reviews The citrus whitefly, Dialeurodes citri (Ashmead), is the pests of pomegranate in the Mediterranean area, primarily a pest of Citrus spp., and the attacks on pome- describing their harmfulness, their main morphological granate are rather episodic. This species probably origi- and biological characteristics and the techniques used in nated in India but now it is almost cosmopolitan. The their integrated and organic control. We also discuss the body and wings of adults (about 1 mm in length) are most damaging species occurring in the main pome- covered with a white, powdery wax. Nymphs are flat- granate production areas of the world and the risks of tened, oval, light yellowish, and without a waxy secre- their possible introduction to the Mediterranean area. tion. D. citri develops 2–3 generations per year in Med- iterranean areas and 5–6 in the tropical areas of origin. Numerous natural enemies can effectively control this Hemiptera pest on Citrus trees. Abd-Rabou and Simmons (2014) recorded 29 species of parasitoids and 15 of predators in The citrus flatid planthopper Metcalfa pruinosa (Say) Egypt, of which the parasitoid Encarsia lahorensis (Flatidae) is a polyphagous pest (recorded on more than (Howard) (Hymenoptera, Aphelinidae) and the predator 200 botanical species) that occasionally attacks pome- Clitostethus arcuatus (Rossi) (Coleoptera, Coccinellidae) granate. The species is widespread in America (its area were the most effective in control activity. of origin) and across Europe to the Far East. The sides of Severe infestations on pomegranate by the ash white- the bodies of juvenile stages are covered with a white fly, Siphoninus phillyreae (Haliday), have been reported wax, but the adults (3 mm in length) appear whiter in Greece and India (Balika et al. 1999; Tsagkarakis because the wax covers most of the body (Mead 2012). It is a cosmopolitan and polyphagous insect 1969), varying to greyish with age. M. pruinosa has species reported on more than 50 botanical species in one generation per year, with overwintering of the eggs various families (Nguyen and Hamon 2011). Similarly Phytoparasitica Table 1 Arthopod pests of pomegranate in the Mediterranean area, degree of harmfulness (+ less, +++ most) and preferred part of the plant

Pest species Common name Degree of Degree of Countries with Part attacked Specificity harmfulness recorded damages Foliage Green fruit Ripening fruit Shoot Twig Branch Trunk

Metcalfa pruinosa Citrus flatid planthopper P + - + + + Dialeurodes citri Citrus whitefly O + - + + Siphoninus phillyreae Ash whitefly P + Greece + + + Aleurocanthus spiniferus Spiny whitefly P + - + + Aphis punicae Pomegranate aphid S ++ Everywhere + + + Aphis gossypii Cotton aphis P ++ Everywhere + + + + Planococcus citri Citrus mealybug P ++ Spain, Turkey, Cyprus + + + + + Maconellicoccus hirsutus Hibiscus mealybug P + - + + + + Author's Ceroplastes japonicus Japanese wax scale P + - + + + Ceroplastes sinensis Chinese wax scale P + Spain, Turkey + + + Ceroplastes floridensis Florida wax scale P + - + + + Saissetia oleae Black scale P + Greece, Italy,Spain,Israel,Portugal + + + Coccus hesperidum Brown soft scale P + Turkey + + Coccus pseudomagnoliarum Grey citrus scale O + Turkey + + personal Aonidiella aurantii California red scale P + Turkey + + + + + Parlatoria oleae Olive scale P + Greece + + + + + Lepidosaphes granati Pomegranate scale P + Greece, Turkey + + Pinnaspis buxi Coconut scale P + - + + +

Chrysomphalus aonidum Florida red scale P + Egypt, Turkey + copy Zeuzera pyrina Leopard moth O +++ Everywhere + Deudorix livia Pomegranate butterfly O ++ Cyprus, Jordan, Tunisia + + + + + Deudorix isocrates Pomegranate fruit borer O ++ - + + Dysgonia algira Passenger moth P + - + Cryptoblades gnidiella Honeydew moth P ++ Turkey + + + Apomyelois ceratoniae Carob moth P ++ Israel, Morocco, Tunisia, Turkey + + + Euzophera bigella Quince moth P + Israel Thaumatotibia leucotreta False codling moth P ++ - + + + Carpophilus spp. Dried fruit beetles P + Israel + + Ceratitis capitata Mediterranean fruit fly P ++ Turkey + + Apate monachus Black borer P + Italy, Turkey + + Amphicerus bimaculatus Grape borer P + Greece, Turkey + + Tenuipalpus granati Pomegranate mite P + - + Tenuipalpus punicae False pomegranate mite P + - + Aceria granati Pomegranate leaf curl mite O + - +

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

Phytoparasitica to other whiteflies species, a white wax covers the body bodies of apterous viviparous females are green, 1.38- and wings of the adults. The nymphs are distinguished 1.73 mm long, with blackish siphunculi and a tongue- by the presence of two longitudinal tufts of white wax shaped pale brown to pale green cauda. In summer, the and by the production of typical droplets of a glassy wax subsequent generations have pale green colour and gener- that cover the body. S. phillyreae has numerous natural ally significantly smaller bodies (0.80-1.17 mm), pale enemies, mainly C. arcuatus and Encarsia spp., which brown to pale green siphunculi with greyish brown apexes are capable of containing pest populations below the and pale green or yellowish cauda (Sugimoto 2011). damage threshold (Abd-Rabou 2006; Nguyen and Aphis gossypii is a cosmopolitan and polyphagous Hamon 2011). species recorded on more than 600 host plants (Holman The orange spiny whitefly, Aleurocanthus spiniferus 2009). The apterous form of this aphid has a small- (Quaintance), is a serious pest of Citrus plants native to medium body (1.6-2 mm long) and a greenish colour in eastern Asia and it has recently been introduced in south- populations living on pomegranate. In Sicily, pomegran- ern Italy (Apulia) (Porcelli 2008), where, within a few ate plants grown in proximity to citrus groves are fre- years, it has been found on 95 botanical species including quently infested by this aphid species. A. gossypii and pomegranate (Cioffi et al. 2013). The juvenile stages are A. punicae are not easily distinguished morphologically oval-shaped, blackish, with a waxy white band visible (Massimino Cocuzza and Lo Giudice 2014). The main along the edge. The adults are covered with a bluish distinctive morphological character is the siphunculus/ powdery wax. In Swaziland, A. spiniferus may develop cauda ratio (1.22-1.50 in A. punicae and 1.50-2.00 in 4–6 generations per year depending on the climatic con- A. gossypii). The colour, which can vary in both species ditions. Several hymenopteran parasitoids (Aphelinidae) seasonally and with environmental conditions, is of little are natural enemies of this pest on Citrus,withEncarsia diagnostic value. Both species can be easily distinguished smithi (Silvestri) being the most effective in Micronesia by their DNA barcodes (Cocuzza et al. 2009; Lee et al. and Swaziland (Muniappan et al. 1992; Van den Berg 2015). In spring, appropriate scientific distinction be- et al. 2000). The coccinellid predator C. arcuatus is the tween species should be performed to prevent subsequent only effective biocontrol agent in the areas of recent infestations. Indeed, alatae A. gossypii leave definitively spread in southern Italy (Cioffi et al. 2013). the plants with the hardening of the vegetation, whereas Worldwide, the most damaging aphids (Aphididae) A. punicae populations remain on pomegranate during of pomegranate are Aphis punicae Passerini (pomegran- summer, infesting the fruits in late summer or in early ate aphid) and Aphis gossypii Glover (cotton aphid). The autumn. This observation may leads to eventual consid- plant can also be rarely infested by Aphis spiraecola erations of using different pest control strategies. Patch (green citrus aphid or spirea aphid), Aphis In Mediterranean area, both species begin infestation craccivora Koch (cowpea aphid, groundnut aphid, or in spring coincident with the development of tender black legume aphid), Aphis fabae Scopoli (black bean shoots. Field colonies of A. gossypii are established by aphid), Aphis achyranthi Theobald, and Toxoptera alatae from other plants, but A. punicae colonies begin aurantii Boyer de Fonscolombe (black citrus aphid) by fundatrixes born from overwintered eggs laid during (Blackman and Eastop 2006;Holman2009). the previous autumn on branches, close to dormant Aphis punicae is common in the Mediterranean area, buds. The colonies of both species increase rapidly with Asia, Africa, and the Indian subcontinent (Swirsky 1954; increasing temperatures and invade all new vegetation. BarbagalloandStroyan1982;BlackmanandEastop2006; Colony population peak is reached during flowering Sugimoto 2011; Bhagat 2012; Lee et al. 2015). This spe- period (first half of May), when buds, flowers, and ciesiscommononpomegranatebuthasalsobeenrecorded young growing fruits are infested. The two species from Lawsonia inermis (Lythraceae), Duranta plumieri behave differently when the shoots harden and the tem- (=erecta), Lantana camara (Verbenaceae), Bignonia sp., peratures rise further. The winged forms of A. gossypii Campsis radicans (Bignoniaceae), and Plumbago abandon the pomegranate to search for new host plants. capensis (Plumbaginaceae) (Bodenheimer and Swirski A. punicae mainly remains on the same plant during the 1957; Blackman and Eastop 2006;Holman2009). The summer, where colonies formed by small apterous vi- morphology and colour of A. punicae may vary with viparous females find refuge in the shoots of regrowth environmental conditions, as in many aphid species and survive the summer heat by reducing metabolic (Dixon et al. 1982; Helden et al. 1994). In spring, the activity and reproduction (Patti 1985). The individuals Author's personal copy

Phytoparasitica described above, which leave the plant to establish 2013). P. citri, generally known primarily as a citrus summer colonies on secondary host plants represent pest, is a polyphagous species that has been collected exceptions. Colonies increase their growth rate in Sep- from 82 families and 191 genera of host plants (Daane tember as the temperature decreases and humidity in- et al. 2012; García Morales et al. 2016). The adult creases, frequently developing large populations. The female body is oval (3–4 mm long) and covered by a aphids settle on the underside of leaves or on fruits powdery wax, with margins surrounded by 18 pairs of during this period. The amphigonic forms develop and stout waxy filaments, of which the anal and the two produce the winter eggs from the second half of No- preceding pairs are slightly longer than the others. Males vember. Damage derives from the considerable amount are winged and have two long backwards-projecting of sap consumed and from the abundant emission of white waxy threads (Gill et al. 2013). A fertilised female honeydew on which sooty mould develops. The large can lay 300–600 eggs inside white cottony ovisacs amount of honeydew distributed on vegetation in very during her life. The first instars (crawlers) are yellow, sunny areas can trigger a Blens effect^,whichcancause oval-shaped with red eyes, and covered with white waxy burns in parts of the shoots. In late summer, A. punicae particles (Gill et al. 2013). The citrus mealybug over- populations cause cosmetic damage to fruit epicarp with winters in different life stages inside shelters on various honeydew and by the formation of large discoloured parts of plants, taking 6–10 weeks to reach maturity. areas due to the feeding pierces of the aphids, which Females can live for up to 1 month depending on the depreciates the value of the product for fresh host plant. In citrus and other fruit crops, nymphs typi- consumption. cally settle along the midribs and veins on the underside A. punicae and A. gossypii have manyefficientnatural of leaves or on young twigs and fruit buttons. They tend enemies predators belonging to Coleoptera to hide in crevices, and light infestations are often easily (Coccinellidae), Diptera (Syrphidae and Cecidomyiidae), overlooked (Gill et al. 2013). The citrus mealybug has Neuroptera (Chrysopidae), and Hymenoptera parasitoids been found on the stems of young pomegranate trees (Lysiphlebus spp. and Aphidius spp.) that often fail to and fruits and inside the fruit calyx (Wohlfarter et al. contain the damage in spring, but can later greatly reduce 2010). The pest develops 3–6 generations per year de- the aphid populations. In addition, in Sicily the activity of pending on the environmental and trophic conditions. natural enemies is limited during late summer and early P. citri can cause damage by settling between two fruits autumn, a time when the colonies of A. punicae are present or inside the crown. It produces a sugary honeydew that on the fruits, causing considerable damages. The use of falls on leaves and fruits below, resulting in the growth specific and authorised agrochemicals may be necessary of sooty mould that may degrade fruit quality (Holland for young plants, because an infestation can considerably et al. 2009;Gilletal.2013). In the inner valleys in Israel delay plant development and the start of production. Nev- and in Turkey, P. citri has been replaced by the closely ertheless, these agrochemicals should not be used exten- related mealybug species P. ficus (Signoret) (Zvi Men- sively to avoid affecting parasitisation/predatory activity del, personal communication). In Mediterranean areas, ofpest’snaturalenemies,whichwouldworseninfestations citrus mealybug is controlled by several natural ene- by other pests (Abd-Ella 2015). The excessive use of mies, such as the parasitic wasps Leptomastidea agrochemicals can also induce the occurrence of resistant abnormis (Girault), Leptomastix dactylopii Howard, pest populations, as reported on the specialised pomegran- and Anagyrus pseudococci (Girault), predaceous lace- ate crops in Alicante, Spain (Juan et al. 2000). wings of the genera Sympherobius and Chrysopa,and Sixty-five species of scale insects (Coccoidea) have the lady beetles Cryptolaemus montrouzieri Mulsant been recorded on P. granatum around the world (García and Scymnus sp. (Cravedi et al. 2008;Mani2016). Morales et al. 2016), but only a few of these sap-sucking Several coccinellids have been collected in Turkey insects species are capable to seriously reduce pome- attacking the citrus mealybug in pomegranate orchards, granate yield. such as C. montrouzieri and species of the genera The commercial quality of pomegranate fruits in Nephus, Chilocorus,andClithostetus (Özturk and Spain and in other important producing areas of the Ulusoy 2009). In Spain, biological control by natural Mediterranean basin is negatively affected by the citrus enemies can help to decrease pest populations but can- mealybug, Planococcus citri (Risso) (Pseudococcidae) not prevent fruit damage (Bartual et al. 2012). Pome- (Bartual et al. 2012; Kahramanoglu and Usanmaz granate is considered a minor crop, and the chemical Author's personal copy

Phytoparasitica control of related pests is limited because of the scarcity (Sharma and Buss 2014). It generally has two genera- of authorised and registered pesticides available for this tions per year and is polyphagous, although it is consid- crop (Bartual et al. 2012). ered a pest of citrus (Pellizzari and Camporese 1994; The pink hibiscus mealybug, Maconellicoccus García Morales et al. 2016). The most common natural hirsutus (Green), is a polyphagous species considered a enemies in the Mediterranean area are Coccinellidae serious pest on many crops and ornamentals, infesting all (Chilocorus spp. and Exochomus spp.), Noctuidae parts of the plants and causing their mortality in the case (Eublemma spp.), and Pteromalidae (Scutellista spp. of severe infestations (García Morales et al. 2016). and Moranila spp.) (Pellizzari and Camporese 1994). M. hirsutus has been reported as a pest on pomegranate These three scale insect species are reported as pests of in India (Mani and Krishnamoorthy 1991) and Sri Lanka pomegranate in the Mediterranean area (Monaco and (Sirisena et al. 2013). In the Mediterranean Basin, the Sabatino 1980; Holland et al. 2009; Özturk and Ulusoy pink hibiscus mealybug is present in Lebanon, Egypt, 2009) and China (Ma and Bai 2004). Cyprus, and Tunisia (Ben Halima-Kamel et al. 2015; The black scale, Saissetia oleae (Olivier), is easily EPPO 2016); its polyphagia has favoured its rapid geo- recognised by its round and convex body, brown or graphical expansion. The trade of infested plants and the black in older females, and by the presence in all stages dispersion of crawlers and egg sacks by wind have of raised areas forming an "H" on the dorsum. S. oleae further promoted its diffusion. Considering the rapid occurs on leaves, stems, and produce honeydew that spread of this invader in the Mediterranean Basin and promotes the growth of sooty mould. It is polyphagous the expansion of pomegranate cultivation, the species and has been recorded as a pest on pomegranate in should be closely monitored especially in the areas of Greece, Italy, Spain, and Portugal (Juan et al. 2000; new introductions. Miller et al. 2014). Populations are reduced by high Nineteen species of soft scales (Coccidae) and sev- temperatures, mainly crawlers whose mortality can enteen species of armoured scales (Diaspididae) have reach 90-95 % and by the predacious coleopteran been recorded on pomegranate around the world (García Chilocorus spp., Exochomus spp., and by the hymenop- Morales et al. 2016). teran parasitoids Scutellista spp., Moranila spp., Amongst the soft scales, Ceroplastes japonicus Coccophagus spp. and Metaphycus spp. with the latter Green (japanese wax scale), Ceroplastes sinensis Del species representing the key natural enemies in many Guercio (chinese wax scale), and Ceroplastes Mediterranean agro-ecosystems (Cravedi et al. 2008; floridensis Comstock (Florida wax scale) have been Zvi Mendel, personal communication). recorded on pomegranate in the Mediterranean Basin The body of the adult female of Coccus and are easily distinguishable among them using mor- pseudomagnoliarum (Kuwana) (grey citrus scale) is up phological characters of adult females. The female of the to 7 mm long, elongate oval, slightly convex, and dark japanese wax scale is 2–2.5 mm long, with a reddish grey in older specimens; the dorsum of the young fe- body coated with a thick layer of white-grey wax. The male is grey with dark-brown mottling (Miller et al. species is bisexual and develops one generation per year. 2014). Females reproduce parthenogenetically and de- It overwinters as young adult females that, in Italy, lay velop one generation yearly in Israel, Greece, and other eggs in late spring or early summer (Pellizzari and countries around the world (Miller et al. 2014). The Camporese 1994). The female of the chinese wax scale presence of C. pseudomagnoliarum and the similar is larger (about 6 mm), with a reddish-brown body, Coccus hesperidum L. on pomegranate crops has been elliptical and convex in lateral view, with a thick wax reported in Turkey by Özturk and Ulusoy (2009). covering (Gimpel et al. 1974). It is a polyphagous, The California red scale Aonidiella aurantii bisexual, and parthenogenetic scale, developing one (Maskell), a worldwide pest of citrus, is among the most generation per year and overwintering as females and damaging armoured scales. It is a polyphagous species third instar larvae (Pellizzari and Camporese 1994). and has been recorded in Turkey as a pest of pomegran- Females of both species lay an average of 2000 eggs ate (Özturk and Ulusoy 2009). Females have roundish beneath their bodies (Cravedi et al. 2008). Females of covers and are firmly attached to the wood, fruit and/or the Florida wax scale have elongated reddish-brown leaves upon which they live. California red scales have bodies (2–4mmlongand1–3.5 mm wide) with a short long filamentous mouthparts that allow them to suck on anal process and are covered with a pinkish-white wax twigs, leaves, branches, and fruit. This activity damages Author's personal copy

Phytoparasitica fruits and other parts of the plant, causing foliar The covers of females of Pinnaspis buxi (Bouché) are yellowing and drop and occasionally the death of the elongated and variable in shape depending on the host tree (Grafton-Cardwell et al. 2015). Many natural ene- plant, very small, pale brownish or nearly colourless, mies can control infestations of A. aurantii, such us usually quite thin, flat, and translucent (McKenzie 1956; coccinellids and wasps, particularly Aphytis melinus Pollini 2013; García Morales et al. 2016). Male covers DeBach and Encarsia perniciosi Tower. The former have three strong carinae and are white (García Morales species is an effective parasitoid of the scale and is used et al. 2016). Its distribution is not well known, however in biological control programmes, especially in Spain it has been recorded in many countries around the world, where it is well-adapted, and the latter species can be living in glasshouses in Europe (Pollini 2013). The scale effective in controlling A. aurantii in areas where it has lives on the above ground of plants of numerous genera, become established (García Morales et al. 2016). including Punica granatum in the Mediterranean Basin The females of Parlatoria oleae (Colvée) have (Ferris and Rao 1947; Balachowsky 1954; Pollini whitish-grey ovate covers (0.69-85 mm long and 2013). Plants infested by P. buxi show loss of vigour, 0.57-0.65 wide), with yellowish-brown, apical exu- defoliation, deformations, and yellow spots on leaves, viae. This species develops two generations each which become desiccated in case of severe infestations year(uptofourinsomeareas)(GarcíaMorales (Dekle 1965; Beardsley and Gonzalez 1975). Control et al. 2016). P. ole ae attacks olives, stone fruits, measures are based on increasing plant spacing and apples, pears, ornamentals (García Morales et al. pruning mature trees to prevent contact between cano- 2016) and damages on pomegranate are reported in pies and thus the spread of scales between plants Greece (Argyriou et al. 1976). The species lives on (Beardsley and Gonzalez 1975). Adopting strategies to branches, leaves, twigs and fruits, producing reddish preserve natural enemies is also recommended. spots, abnormalities, and deformations early during In the Mediterranean area, the black circular scale, or fruit development. This scale is usually under effi- Florida red scale, Chrysomphalus aonidum (L.), was cient biological control by its natural enemies, such initially recorded on Cycas in Sicily about twenty years us Aphytis paramaculicornis DeBach and Rosen, ago (Longo et al. 1994) and is widespread in southern Coccophagoides utilis Doutt and Aphitis Italy on Citrus but has been recorded as a pest on maculicornis (Masi) (Moursi et al. 2013;García pomegranate in Egypt and Turkey (Hall 1922; Özturk Morales et al. 2016). Chemical control, whenever and Ulusoy 2009). necessary, should be applied against crawlers in late spring (Cravedi et al. 2008). Lepidosaphes granati Koroneos (pomegranate scale) Lepidoptera females have brown comma-like covers (2.0-2.2 mm long and 0.48-0.72 mm wide) (Kosztarab and Kozár Amongst the Lepidoptera, the leopard moth Zeuzera 2012). The female body is characterised by typically pyrina (L.) (Cossidae) is the most damaging pomegran- shaped pygidial median lobes; the cover is more linear ate pest in the Mediterranean area, especially for young and smaller in males than females (Pollini 2013). This plants (1–3 years). The species is widely distributed in species has a Palearctic distribution and has been re- Europe, North Africa, Asia, and the USA. The moth is a corded on Eleagnus spp., Acacia cultriformis, Ficus polyphagous species and has been reported on several carica, Rhamnus oleoides, Crataegus spp., Celtis, genera of host plants (e.g. Prunus, Malus, Pyrus, Olea, Ulmus, Zelkova and Platanus (Kaydan et al. 2013; Acer, Fagus, Tilia, Platanus, Quercus, Salix, Populus, García Morales et al. 2016). It has been recorded on Ulmus,andTamarix) (Gatwick 1992). The adults (about P. granatum in Greece (Koroneos 1934), Italy 3 cm long) have white forewings with metallic bluish (Balachowsky 1954), and Turkey (Kaydan et al. spots of varying sizes. The thorax is white and tomen- 2013). In the Mediterranean area, L. granati has one to tose with six large bluish spots, and the abdomen is dark. two generations per year. It develops small populations The females are larger than males (wingspans of 50– on the branches and trunk of the host plant, but it is 70 mm in females and 35–50 mm in males) and have considered a pest (Kosztarab and Kozár 2012; García filiform antennae (the basal part is bipectinate in males). Morales et al. 2016) even if rarely needing control Larval colour varies with maturity from pinkish to yel- (Pollini 2013). lowish, with small black spots (pinacula) in longitudinal Author's personal copy

Phytoparasitica rows along the body. Mature larvae are about 50–60 mm where Z. pyrina is present (i.e. near olive orchards), is long. In South Italy, it was recorded that each female the periodic visual inspection of the plants to promptly may lay up to 1000 eggs in groups of about a hundred in identify the penetration holes. Pruning and the subse- the more sheltered parts of the trunk or branches of 2–3 quent destruction of the branches is effective if they are year-old-trees. The eggs are laid from late April to young. In larger branches, inserting a wire into the September, with a peak in late June and early July. The excavated galleries can kill the larvae. Spraying the larvae, after eclosion, penetrate the plant tissue at the galleries with authorised insecticides is an alternative. point of insertion of leaves or the axils of buds and begin The holes must be cleaned, disinfected, and sealed with to excavate ascending galleries. The larvae emerge and grafting mastic to avoid the stagnation of water or the fall several times from plant tissues, attacking progres- entry of opportunistic fungi. In young and large or- sively larger twigs more suited to their growing size. chards, pheromone traps can provide useful information The presence of larvae is revealed by sawdust and frass on the seasonal flight of adults to identify the oviposi- (as small cylinders) at the basis of the plant or around the tion period and the most suitable time for treatment exit holes from the galleries. The larval cycle is com- against the youngest larvae before they emerge from pleted in 1–2 years, depending on whether the eggs eggs (Natale and Pasqualini 1999). They can also be hatched at the beginning or at the end of the summer, used for mass trapping or mating disruption, as demon- respectively (Giorgini et al. 1997). Adults live 8– strated in olive orchards (Guario et al. 2001;Hegazi 10 days, so mating and oviposition also occur during et al. 2009, 2010). this brief period. Only a few eggs complete embryonic The pomegranate butterfly, Deudorix (=Virachola) development, because most are eaten or are weakened livia (Klug) (Lycaenidae), is amongst the most impor- by the high summer temperatures (Guario et al. 2001). tant and destructive pests of pomegranate worldwide. It Larval attacks may dry the buds, but more extensive is currently widespread in the Middle East, North Afri- damage in the branches is evidenced by the decay of the ca, and the Arabian Peninsula (Katbeh-Bader et al. vegetation and loss of mechanical strength. The pres- 2003; Libert 2005). In Europe, D. livia has been recently ence of the xylophagous form may often be unnoticed, reported in Greece (Müller et al. 2005) and Cyprus and branches may suddenly break in strong winds. One (Kahramanoglu and Usanmaz 2013). This pest has re- larva can kill a 1-year-old tree, whereas a 3-year-old tree cently caused conspicuous losses of production in Tu- can easily lose some branches to larval activity. nisia (Ksentini et al. 2011;Moawadetal.2011)and The leopard moth has numerous natural enemies that Cyprus (Kahramanoglu and Usanmaz 2013). The wings do not effectively control the moth populations. For are bluish-brown in females and brown-orange in males. example, in a study conducted in Egypt, only 1.2 % of Colour, however, is highly variable in this species the larvae was parasitized by Hyssopus sp. (Hymenop- (Libert 2005). The larvae are reddish-brown. Under tera, Eulophydae), an ecto-parasitoid wasp (Hegazi et al. laboratory rearing conditions (27 °C and 70 % R.H.), 2015). In North Italy, the parasitoids Neoxorides nitens the species can complete larval development in about (Gravenhorst), Dolichomitus messor (Gravenhorst), 44 days when reared on pomegranate fruits and in Pristomerus vulneratus (Panzer), Diasegma terebrans 33 days when reared on acacia pods. The longevity of (Panzer) (Hymenoptera, Ichneumonidae), fertilised females is about 12 days when reared on either Dolichogenidea laevigatus (Ratzeburg) (Hymenoptera, host; they lay about 42 eggs on pomegranate and about Braconidae), Perilampus tristis Mayr (Hymenoptera, 50 eggs on the pods of acacia (Gharbi 2010). Perilampidae), and Megaselia praecusta (Schmith) Blumenfeld et al. (2000)reportedthatD. livia lays eggs (Diptera, Phoridae), were reported by Campadelli in the crown of the developing fruit, and damage ap- (1995). Similar percentages of natural activity have been pears during the ripening period or in storage. The recorded in Egypt for the entomopathogenic fungi neonate larva bores into the fruit to feed on the ripening Beauveria bassiana (Balsamo-Crivelli) Vuillemine and seeds until maturity and then exits from a hole to pupate Metarhizium anisopliae (Metschnikoff) Sorokin in the soil. The feeding activity of the larvae leads to the (Hegazietal.2015). Nematodes of the genera development of rot, which can later fall (Braham 2015). Heterorhabditis and Steinernema can be effective in Ksentini et al. (2011) reported that the damage caused the control of the moth (Giorgini et al. 1997;Ashtari by D. livia in varieties of pomegranate grown in Tunisia et al. 2011). The best control strategy, especially in areas was estimated at 5-52 %. In another study, Moawad Author's personal copy

Phytoparasitica et al. (2011) recorded that the percentage of damaged plants used (Bagnoli and Lucchi 2001). Özturk and fruits varied from about 3 % (cv Al-Taif) to 60 % (cv Ulusoy (2009) state that this species is a serious pest Hegazi-Bathan). In Jordan, D. livia has 2–3generations of pomegranate in Turkey. The management of this on pomegranate fruit, beginning in summer at 4 % and species must focus on controlling the primary pest that gradually increasing to 48 % infestation by early Octo- allows infestation by C. gnidiella. Many countries use ber (Obeidat and Akkawi 2002). In Cyprus and Tunisia, chemical control to lessen the effects caused by the some research studies suggest that B. thuringiensis and primary pest (Harari et al. 2007). Other control methods spinosad are effective alternative biological control include biological control and mating disruption (Ben agents for D. livia and can be used in organic-farming Yehuda et al. 1991, 1993;Sellanesetal.2010). This systems and in IPM practices (Kahramanoglu and species has been intercepted in material imported to the Usanmaz 2013; Sayed et al. 2015). A further study USA and the British Isles, especially on infested pome- carried out in Saudi Arabia showed the efficacy of granate fruits (Carter 1984). Wysoki et al. (1988)found Trichogramma turkistanica Meyer (Hymenoptera, that C. gnidiella larvae in Israel were highly susceptible Trichogrammatidae) in the control of the pest (Sayed to B. thuringiensis var. kurstaki, with 80-100 % mortal- et al. 2015). ity of the first and second larval instars (between 24 h The honeydew moth, or pomegranate moth, and 4 days after treatment) on avocado fruits in the field. Cryptoblabes gnidiella Millière (Pyralidae), is native The carob moth, Apomyelois ceratoniae Zeller to the Mediterranean area and is an introduced species (Pyralidae), is a polyphagous fruit pest widespread in in South and Central America, New Zealand, South- many tropical and subtropical regions. It is a pest of East Asia, and some African countries. This moth is an citrus, dates, figs, carob, pomegranate, pistachio, and important pest of citrus, grapes, and pomegranates in the almonds in Mediterranean countries (Gothilf 1984; Mediterranean area. It is a pest of wild, cultivated, or Navarro et al. 1986). It is also found in the USA, Central ornamental plants belonging to various families, e.g. and South America, and North Africa (Carpenter and Malus, Persea, Punica, Gossypium, Annona, Feijoa, Elmer 1978). The body of the moth is 8–10 mm in Ceratonia, Vitis, Citrus, Actinidia, Eriobotrya, Ficus, length, and the wingspan is 22–24 mm. The colour is Zea, Prunus, Pyrus, Cydonia, Oryza, Sorghum, creamy white to grey, brownish, or even dark brown. Triticum, Daphne, Nerium, Paspalum,andRicinus Two bright stripes with dark margins span their width. (Leraut 2014). The eggs are oval and irregularly reticu- The rear wings are white-grey with light-brown veins. late. The body is yellowish, olivaceous, reddish, or The larva is 12–15 mm long, pink, with a brown head brownish-grey with longitudinal stripes and measure at and front dorsum and small dark-brown bumps on its maturity about 12 mm. The adult wingspan is 11– back. The eggs hatch in 3–7 days. The development of 20 mm. Forewings are greyish-brown with a variable larval stages may last 1–8months,andpupationusually amount of whitish suffusion, and scattered reddish- occurs at the feeding sites of the larvae. The females brown scales give a purplish appearance. Hindwings may lay 60–120 eggs during their lives (3–6days).The are shiny white (Goater 1986). Adults are active at night eggs are laid in the calix of developing fruits and the and are attracted to sweet substances, including the larvae, after hatch, enter inside the endocarp, where their honeydew excreted by mealybugs, and to fruits such feeding activity cause rot and quality decay (Braham as grapes and pomegranates that have been injured by 2015). Three to four generations are developed yearly, other insects. Females lay their eggs on fruit, usually from April to November, before the cooler weather singly or in small batches, with an average of 150 eggs induces diapause in the remaining larvae (Carpenter during their lives. The larvae will initially feed solely on and Elmer 1978). Mean development time from egg to the honeydew produced by aphids and mealybugs and adult ranges from 45 to 62 days depending on the fruit are found in sheltered places amongst the fruits or attacked (Navarro et al. 1986). A. ceratoniae is a major between fruits and leaves (Ben Yehuda et al. 1991). problem for pomegranates in some countries. This spe- The species has five larval instars and pupates close to cies causes economic losses in Tunisia, especially in the the larval feeding site, either on the host plant or on the South, with infestation rates as high as 90 %, it is also a ground. This species has 3–4 generations per year, from major field pest of pomegranate in Iraq (Al-Izzi et al. May to October in Mediterranean climates, and up to 1985; Norouzi et al. 2008; Braham 2015), and a serious five in North Africa, depending on the climate and host pest in date plantations in Morocco and Israel Author's personal copy

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(Blumberg et al. 2001). Moawad et al. (2011)recorded Parietaria. The pupa overwinters in a loosely wo- that the percentage of damaged fruits varied from about ven cocoon. 0 to 2.4 % (cv Mongaloty-Wonderful) to 31-42 % (cul- Dysgonia torrida (Guenée) share the same areas with tivars Magrabi Abu-Halgon and Sweet-Banati, respec- D. algira. The patterns and colours of both species are tively). A. ceratoniae is the most important pomegranate very similar and can be distinguished only by compar- pest in the Iranian province of Isfahan where an annual ing the genitalia. Numerous D. torrida larvae have been average of 30-40 % of the pomegranate production is collected from pomegranate leaves in Sicily in the last destroyed or rendered unusable while in storage or on decade (Salvatore Bella, unpublished data). This spe- the trees. A. ceratoniae causes less fruit damage than cies, originating of sub-Saharan area, probably benefits C. gnidiella in Turkey (YıldırımandBaşpınar 2015)but from global warming in expanding its distribution in it can develop in dried fruits in storage, with serious northern mediterranean basin (Goater et al. 2003; losses of product. In Morocco, it is parasitized by the Bertaccini et al. 2008). hymenopterans (Braconidae) Phanerotoma ocuralis Euzophera bigella (Zeller) (=E. punicaella) Kohl on date bunches and Bracon hebetor Say on fallen (Pyralidae) is a polyphagous species that occasionally fruits (Hassan et al. 2001). The parasitoids Apanteles can be harmful to pomegranate (Mehrnejad and myeloenta Wilkinson, Bracon hebetor (Braconidae) and Ebrahimi 1993; Atay and Öztürk 2010). The larvae Brachymeria minuta (L.) (Chalcididae) have been found develop in the cortical tissue of the trunk or branches in parasitized larvae collected from pomegranate in Iran taking advantages of the opening caused by hail, (Nobakht et al. 2015). In Saudi Arabia, the use of the grafting or parasites, digging tunnels that can reach the egg parasitoid Trichogramma turkistanica and Bacillus cambium area. Sometimes, the attack can also affect the can be an effective alternative to control the moth fruits of pomegranate that penetrate inside it through the (Sayed et al. 2015). Populations are monitored using calix. Adults have a wingspan of 15–18 mm with the pheromone traps (Kehat et al. 1995),whichhaverecent- front wings brown greyish in color, crossed by two ly been successfully developed after many years of lighter transverse strips (Zangheri et al. 1992). studies (Baker et al. 1991;ISCA2008). The traps are E. bigella rarely assume economic importance and usu- placed in orchards in early March, and catches are ally their attack follow exceptional events (hail), graft recorded weekly. Practical experience in Turkey found made not properly or attack by other parasites (Zangheri that cleaning and removing the mass of old stamens after et al. 1992;Simoglouetal.2012). flowering could deter oviposition. The insecticide spinosad is the best option for IPM, however fenoxycarb or similar Insect Growth Regulators are likely to be Diptera effective. Synthetic pyrethroids (e.g. cypermethrin, lambda-cyhalothrin and bifenthrin) are probably effec- The mediterranean fruit fly, Ceratitis capitata tive, but are not recommended for IPM. (Wiedemann) (Tephritidae), can occasionally cause se- Dysgonia algira (L.) (Erebidae) ranges from North rious damage to pomegranate and, especially in some Africa and Asia Minor in the Mediterranean area to conditions, it can become a key pest (Holland et al. southern Russia, Iran, Afghanistan, Turkmenistan, 2009; Özturk and Ulusoy 2009;Braham2015). Females and Kyrgyzstan (Hacker 1989). Adults fly from lay eggs in small crevices in the epicarps of fully mature April to October and develop 2–3 generations per fruit. The larvae develop while feeding on the pulp and year. The moths have a wingspan of 38–45 mm. this activity, combined with the subsequent develop- Theheadandbodyaredarkbrown,andtheeggs ment of rot, render the fruit unmarketable (Braham are greyish-brown. Mature caterpillars are about 2015). The intensity of an infestation depends on vari- 42–48 mm long and brown, with reddish-brown ous factors, including the susceptibility of the pome- tops and light-brown sides. The head is brown with granate variety, the seasonal climatic trend, and the yellow markings. The pupae are reddish-brown. presence of other suitable fruit crops in the cultivated The eggs are laid singly on the host plants. The area. Management strategy using trimedlure baited traps caterpillars feed mainly on Rubus fruticosus but may serve to efficient monitoring of the medfly. Prod- also on Salix, Genista, Lythrum, Punica granatum, ucts containing a mixture of attractants and insecticides Prunus, Ricinus communis, Cytisus, Epilobium,and served for Blure and kill^ or Battract and kill^ approach. Author's personal copy

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For products containing spinosad, the insecticide may southern Italy (Bonsignore 2012) and in Turkey (Özturk be incorporated in attractive panels or applied directly to and Ulusoy 2009). The various xylophagous life stages spots on plants. Low residue organophosphate insecti- of the insect feed and lay eggs in holes of various sizes cides (etofenprox) can be used against the medfly on on the branches and trunks. The branches of the plants pomegranate, close to ripening. may be mechanically weakened, which can then be easily broken by particularly violent winds. Control is exclusively preventive and is achieved by maintaining Coleoptera healthy plants and continuously monitoring susceptible plant parts, from late spring to early summer, to detect The genus Carpophilus (Nitidulidae), commonly the eventual presence of holes. The infested branches known as the dried fruit beetle, includes several species should be removed and destroyed (Bonsignore 2012). that, in some areas, can be harmful to the ripe fruit. Chemical control is possible against adults of These insects are polyphagous and very common in A. monachus by spraying the trunk and branches with fruit crops where they attack prevalently decaying fruits long-lasting insecticides. For biological control, there and sometimes the ripe ones still hanging on trees. In are no specific studies on the black borer. However, as Mediterranean areas, the most common species are proven for other similar coleopteran borers, the use of Carpophilus hemipterus L. and Carpophilus mutilatus Metarhizium anisopliae Metschnikoff or Beauveria Erichson, while less frequent are Carpophilus bassiana (Bals. & Criv.) Vuillemin could be effective dimidiatus (F.), Carpophilus freemani Dobson (proba- against A. monachus (Bonsignore 2012). bly of South American origin) and Carpophilus On pomegranate, damages have also been recently quadrisignatus Erichson (Pollini 2014). Carpophilus reported for the insidious dog grape borer Amphicerus spp. are small in size (1–5 mm long), with the body (=Schistoceros) bimaculatus (A.G. Olivier) in Turkey suboval and flattened. In many species, the elytra are (Tezcan 2008) and Greece (Andreadis et al. 2016). shorter than abdomen. The background color is dark- Adult and larvae of this beetle attack the plants by brown; however, some species (for example boring holes in the branches, causing their wilt or die C. hemipterus and C. quadrisignatus)presentsonelytra in the most severe infestations (Andreadis et al. 2016). roundish patches yellowish or light brown. Damages on fruits of pomegranate caused by Carpophilus spp. are reported in Israel (Zvi Mendel, personal communica- Mites tion) and Italy (Nuzzaci 1968). On pomegranate fruits, the attack originates from the chalice through which the The mites Tenuipalpus granati Sayed (pomegranate larvae, emerged from eggs laid in its vicinity, penetrate mite) and Tenuipalpus punicae Pirtchard & Baker into the endocarp causing burnishing and subsequent (pomegranate false mite) (Prostigmata, Tenuipalpidae) fall. As observed for peaches, probably, these latter and Aceria granati Canestrini & Massalongo (pome- consequences are caused by the spores of fungi that granate leaf curl mite) (Prostigmata, Eriophyidae), can adhere to the insect body and are carried inside the fruits occasionally reach pest status on pomegranate (Jeppson (Tremblay et al. 1984). The control is achieved through et al. 1975; Al-Gboory et al. 1984; Döker et al. 2013). the immediate destruction of fallen fruit to prevent the These species are largely distributed in the Mediterra- growth of beetle population. The use of aggregation- nean area and Middle East. Both Tenuipalpidae can also pheromone is effective in monitoring the sap beetles infest Vitis vinifera, Pistacea vera, Prunus armeniaca, (Blumberg et al. 2005; Hossain et al. 2013). The use Ficus carica and Olea europea (Jeppson et al. 1975;Al- of appropriate insecticide just after varaison can prevent Gboory and El-Haidani 1989). They are active year the oviposition or the attack by larvae. round, but their population reach the highest density in Powder post beetles (Bostrichidae) can also attack spring and early summer, and the females overwinter pomegranate. The black borer, Apate monachus (F.), has under the bark of trunk and branches (Al-Gboory and long been known attacking grapevines, peaches, apples, El-Haidani 1989). Both species infest preferably pome- pears, avocados, citrus, and ornamental plants. Recently, granate leaves that became first yellowish and then dry damages of A. monachus on pomegranate plants were up (Jeppson et al. 1975; Al-Gboory et al. 1984). These reported in a nursery on the Ionian coast of Calabria in species cause rarely serious damage to pomegranate, Author's personal copy

Phytoparasitica because they are well controlled by numerous natural maturity. This lepidopteran is an oligophagous species enemies, mainly predatory mites (Phytoseiidae). The that can also infest Tamarindus indica, Psidium rare infestation of A. granati can be easily noticed for guajava,andCitrus spp. (Bhakare 2015; Chhetry et al. the evident leaf roll on shoots. Its infestation requires no 2015). D. isocrates is widely distributed in Asia. The control (Vacante 2016). adults are mostly brown with reflex bluish in males and orange in females. The larvae (15–20 mm long at ma- turity) are dark brown with short hairs and white patches Potential pest introductions in the Mediterranean on the body. The eggs are laid singly on various parts of area the plant, including flower buds. The pre-imaginal peri- od is completed in 18–47 days, whereas the total life The false codling moth, Thaumatotibia leucotreta cycle lasts 1–2 months, depending on the seasonal cli- (Meyrick) (Lepidoptera, Tortricidae), was first found in matic trend. Damage is caused by the activity of the 1984 in Israel on macadamia nuts, Gossypium and larvae, which bore into the fruit and feed on the pulp and Ricinus crops and since then it has been repeatedly seeds originating fruit rot and, in some cases, fruit drop reported on imported plant material in some European (Kakar et al. 1987). Infestations can be controlled by the countries (Mazza et al. 2014;EPPO2015). T. leucotreta cultivation of less susceptible varieties, the early collec- was detected in the Netherlands in 2009 (in glasshouses tion and destruction of damaged fruits (easily on Capsicum chinense) and was subsequently eradicat- recognised by the holes made by the larvae), and pro- ed. The moth has occasionally been noticed in several moting the activity of the natural enemies through se- countries in Europe (e.g. the Netherlands, Sweden, and lective application of pesticides. The most promising the UK), but these specimens very unlikely came from natural enemies are the egg parasitoid wasps already established populations, but from infested plants Trichogramma chilonis Ishii (Karuppuchamy et al. or imported fruits. This pest is a polyphagous species 2001), Trichogramma mani Nagaraja and Gupta reported from more than 70 host plants in 40 families. It (Hymemoptera, Trichogrammatidae) (Nagaraja and is considered a key pest of citrus and pomegranate in Gupta 2007), Ooencyrtus papilionis Ashmead (Hyme- South Africa, and as reported in EPPO (2015) Bif there noptera, Encyrtidae), and Telenomus sp. (Hymenoptera, is poor orchard sanitation, this pest can cause serious Scelionidae) (Mani and Krishnamoorthy 2002). Bag- crop losses up to complete fruit loss^. The damage is ging the fruit can significantly reduce the damage caused by larvae that penetrate inside the fruit by dig- (Bagle 2009) but increases production costs and favours ging tunnels, which irreparably deteriorate its market infestations by mealybugs (Shevale 1994). 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 Final considerations long and pinkish-red) emerge from the fruit and pupate in the soil (EPPO 2015).The species has several gener- An increase in the demand for pomegranates has led to ations per year without diapause in tropical and sub- the establishment of new plantations around the world. tropical areas (Gilligan et al. 2011). Larvae are identified Pests and diseases are the most important problems that by a combination of molecular and morphological anal- decrease pomegranate yield and quality. This review yses (Mazza et al. 2014). article emphasizes what is currently known about the The pomegranate fruit borer, or anar or common pests of pomegranate trees and fruits in Mediterranean guava blue butterfly, Deudorix (=Virachola) isocrates area and presents the most successful pest management (F.) (Lepidoptera, Lycaenidae) is considered one of the strategies developed and implemented until recently. most harmful species to pomegranate in India where it The correct management of pomegranate pests is crucial can hamper planting in some districts (Bagle 2009). The for the production of marketable fruits. In Europe, same author also reported that all pomegranate varieties pomegranate is considered a minor crop, so the chemical were susceptible to attack by D. isocrates, although control of pests is limited due to the scarcity of regis- some were more resistant than others. Thirty-five to tered pesticides (Bartual et al. 2012). Alternative control 42 % of the fruit can be attacked in unprotected crops tactics are becoming more important for pomegranate during development and can reach 90 % at fruit growers as the concerns of consumers and health Author's personal copy

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