In October 2013, orange spiny whitefly Aleurocanthus spiniferus (Quaintance) (Hemiptera: Aleyrodidae) was detected for the first time in Montenegro. It was found in citrus orchards in Baošići (orange and mandarin), Herceg Novi (mandarin) and Kumbor (orange), in an area of Boka Kotor Bay on the Adriatic Sea (latitude 42° 26’ north). A. spiniferus is regulated in the European Union and therefore an immediate survey of the whole montenegrin coastal area, where citrus production occurs, was undertaken. The pest was additionally found in Djnovići, on a small number of mandarin and lemon trees. A. spiniferus is polyphagous and a major pest of citrus. It originated in southeast Asia and has spread widely in tropical and subtropical Asia, Africa and the Pacific Islands. In Europe it was first detected in Italy (2008) and subsequently in Croatia (2012). It presents a potential risk for citrus production in Montenegro, particularly for the important citrus producing areas of Bar and Ulcinj. These areas, geographically more southern than the area of first detection, are still free from the pest. Additionally, the whitefly presents a potential risk for other host plants grown in Montenegro where the climatic conditions are suitable for acclimatization of A. spiniferus

Hrncic, Snjezana

Malumphy, Chris

Radonjic, Sanja

English

CREA Journals (Consiglio per la ricerca in agricoltura e l’analisi dell’economia agraria)

REDIA, XCVII, 2014: 141-145(*) University of Montenegro, Biotechnical Faculty, Mihaila Lalića 1, 81000 Podgorica, Montenegro; e-mail: sanja_radonjic@t-com.me(**) The Food and Environment Research Agency, Sand Hutton, York, YO41 1LZ, United KingdomRadonjić S., Hrnčić S., Malumphy C. – First record of Aleurocanthus spiniferus (Quaintance) (HemipteraAleyrodidae) in Montenegro.In October 2013, orange spiny whitefly Aleurocanthus spiniferus (Quaintance) (Hemiptera: Aleyrodidae) wasdetected for the first time in Montenegro. It was found in citrus orchards in Baošići (orange and mandarin), HercegNovi (mandarin) and Kumbor (orange), in an area of Boka Kotor Bay on the Adriatic Sea (latitude 42° 26’ north). A.spiniferus is regulated in the European Union and therefore an immediate survey of the whole montenegrin coastalarea, where citrus production occurs, was undertaken. The pest was additionally found in Djnovići, on a smallnumber of mandarin and lemon trees. A. spiniferus is polyphagous and a major pest of citrus. It originated in south-east Asia and has spread widely in tropical and subtropical Asia, Africa and the Pacific Islands. In Europe it was firstdetected in Italy (2008) and subsequently in Croatia (2012). It presents a potential risk for citrus production inMontenegro, particularly for the important citrus producing areas of Bar and Ulcinj. These areas, geographicallymore southern than the area of first detection, are still free from the pest. Additionally, the whitefly presents apotential risk for other host plants grown in Montenegro where the climatic conditions are suitable foracclimatization of A. spiniferus.KEY WORDS: Aleurocanthus spiniferus, Montenegro, first record, citrus pest.SANJA RADONJIĆ (*) - SNJEŽANA HRNČIĆ (*) - CHRIS MALUMPHY (**)FIRST RECORD OF ALEUROCANTHUS SPINIFERUS(QUAINTANCE) (HEMIPTERA ALEYRODIDAE) IN MONTENEGROINTRODUCTIONAleurocanthus spiniferus (Quaintance) (Hemiptera:Aleyrodidae), commonly known as orange spiny whitefly,originated in south-east Asia and has spread widely intropical and subtropical Asia, into Africa and the PacificIslands (EPPO/CABI, 1997). It was recorded by Kuwana asthe most destructive whitefly attacking citrus in tropicalAsia (KUWANA, 1928; WEEMS, 1974). This is a quarantinepest for the European Union. The genus AleurocanthusQuaintance & Baker (A. spiniferus and A. woglumi Ashbyare specifically listed) is regulated by EU Annex II/A1Council Directive 2000/29/EC (ANONYMOUS, 2000). A.spiniferus is also listed by the European and MediterraneanPlant Protection Organization (EPPO) as a species reco -mmended for regulation as a quarantine pest; it has re centlybeen transferred from the A1 (absent from the EPPOregion) to the A2 (locally present in the EPPO region) list(ANONYMOUS, 2013). QUAINTANCE (1903) described thespecies under the name Aleurodes spiniferus from specimenscollected in Java (Indonesia) by Marlatt in 1901. A. spiniferus is a polyphagous pest that infests host plantsassigned to more than 30 botanical families includingEbenaceae, Lauraceae, Moraceae, Punicaceae, Rosaceae,Rutaceae and Vitaceae. CIOFFI et al. (2013) provided acomprehensive list of its host plants. The main hosts ofeconomic importance are Citrus spp.A. spiniferus has six developmental stages: the egg, fournymphal instars and the adult. In tropical conditions it hasoverlapping generations and all stages of A. spiniferus maybe found throughout the year, although little breedingoccurs during colder periods. The life cycle takes 2-4months depending on climatic conditions, and there can bebetween three to six generations per year (JANSEN, 2002).Each female lays 100+ eggs (WEEMS, 1974), and alldevelopmental stages and occur on the undersurfaces ofleaves. The adults fly actively when disturbed. A. spiniferus feeds on plant sap and excretes copiousamounts of sugary, sticky honeydew, which coats theleaves, branches and fruit surfaces. Black sooty moulddevelops on the honeydew, reducing the area ofrespiration and photosynthesis. A heavy infestation givesthe plants an almost completely black appearance. As aresult, contaminated foliage may drop, young leaf growthis damaged, fruit set may be reduced, and already formedfruits are unmarketable. Heavily infested plants sufferfrom general weakening, dieback of branches and twigs,deformed growth, and fruits are prematurely dropped(EPPO/CABI, 1997; CIOFFI et al., 2013).A. spiniferus was first detected in Europe in 2008 inthe Apulia region of Southern Italy on oranges(PORCELLI, 2008). Since then it has been spreading in theApulia Region, gradually invaded the whole LecceDistrict and expanding northward into Brindisi District(CIOFFI et al., 2013). A few years later, in May 2012, thepest was recorded in Croatia, on ornamental pottedorange seedlings (Citrus x aurantium L.) at one nurserygarden in Split, a city on the coast of the Adriatic Sea,and action was taken to eradicate it (ŠIMALA and MASTENMILEK, 2013). In October 2013, A. spiniferus wasdetected for the first time in citrus orchards inMontenegro and the purpose of this publication is toprovide details of this first incursion [an isolatedpopulation of a pest recently detected in an area, notknown to be established, but expected to survive for theimmediate future (FAO, 2010)] in Montenegro.– Received 10 June 2014     Accepted 30 September 2014      Published 10 December 2014SHORT NOTE MATERIALS AND METHODSIn October 2013, the presence of a new whiteflyspecies in Montenegro was recorded in citrus orchards inBaošići, Kumbor and Herceg Novi, in the area of theBoka Kotor Bay on the Adriatic Sea (latitude 42° 26’north) (Fig. I). The whitefly colonies looked unusual asthe nymphs were black, surrounded by a fringe of whitewax, and the adults were metallic grey-blue with whitemarkings on their wings. 142 S. RADONJIĆ ET AL. REDIA, Vol. XCVII, 2014Fig. I. – Distribution of Aleurocanthus spiniferus in Montenegro(in red).Samples of infested leaves were collected and taken tothe Entomology Laboratory of the Biotechnical Facultyin Podgorica (Montenegro) for examination. Identity ofthe whitefly species was confirmed at The Food andEnvironment Research Agency (FERA) (UnitedKingdom). A series of 10 puparia were slide mounted inCanada balsam according to the method by MALUMPHY(2004), examined using a Leitz Diaplan high powermicroscope (magnification x100-400) and identified onthe basis of morphological characters using thedescriptions and keys provided by MARTIN (1987),JANSEN (2002) and DUBEY and KO (2012). Voucherspecimens are deposited at FERA.The Phytosanitary Directorate of Montenegro wasofficially informed about the first detection of A.spiniferus and additional surveys of the citrus producingareas in Montenegro were carried out in October,November and December, 2013. RESULTS AND DISCUSSIONA. spiniferus adults, nymphs and eggs were recorded onthe undersurface of leaves of several trees in citrus orchardsin Baošići and Kumbor; in Kumbor it was found only onoranges while in Baošići it was found on both orange andmandarins (Fig. II). Several nymphs and eggs were alsofound on one mandarin tree in a citrus orchard in HercegNovi. After the initial finding of A. spiniferus an immediatesurvey of the whole Montenegro coastal region, wherecitrus production occurs, was undertaken in October, andrepeated during November and December. The pest wasadditionally found in Djenovići (near to where it was firstdetected), on a small number of mandarin and lemon trees.During these inspections it was observed that the nymphswere more frequent on the undersurface of the olderleaves, while the adults and eggs were more frequent on theundersurface of younger leaves.Fig. II. – Colony of Aleurocanthus spiniferus on undersurface oforange leaf: nymphs (1, 2); adults (3).123Fig III. – Aleurocanthus spiniferus: adult (1- resting pose, 2- female (left) and male (right)); elongate-oval to kidney-shaped eggs(3); eggs and young nymphs - 1st and 2nd instars (4); older nymphs 3rd and 4th instars and sooty mould (5); 4th instars - puparia (6)Colonies of A. spiniferus are highly conspicuous andunlikely to be confused with any other whitefly speciescurrently found in Europe. The field characteristics ofthe species are shown in Fig. III, 1-6. Adult female A.spiniferus are about 1.7 mm in length, and the males 1.35mm long: at rest, their general appearance is metallicgrey-blue, being the colour of their wings which covermost of the body; a pale transverse mark across themiddle of the wings is distinctive. The head and thoraxare dark red to brown, and the abdomen dark orange tored. The eyes are reddish-brown and the antennae andlegs are white with pale-yellow markings. The eggs areelongate-oval with the lower surface convex and uppersurface slightly concave, producing a kidney shape, 0.2mm long, and are usually laid in a characteristic spiralpattern, attached to the undersurface of the leaves by ashort, slender pedicel extending from the lower surfacenear the base of the egg. The chorion is covered with adistinct lattice with little evidence of wax. The eggs areyellowish when first laid, turning darker with maturity,becoming dark golden brown as the embryo develops.Hatched eggs are a translucent golden brown. The first-nymphal instar is elongate oval, with six well developedlegs, 0.30 x 0.15 mm, dusky in colour, with 2 pairs ofFIRST RECORD OF ALEUROCANTHUS SPINIFERUS (QUAINTANCE) (HEMIPTERA ALEYRODIDAE) IN MONTENEGRO 14345 61 23greatly enlarged dorsal setae (cephalic and firstabdominal). The second-nymphal instar is ovoid, slightlyconvex, with reduced, non-functional legs, 0.4 x 0.2 mm,dark-brown to pale-black with yellow markings, witheasily distinguished, radiating spines; the third-nymphalinstar is more ovate, 0.74-0.87 mm, generally black with arounded, greenish spot on the anterior part of theabdomen, the spines are well developed and obvious; thefourth-nymphal instar, or puparium, is ovate, shiny-black, with the females about 1.25 mm in length, and themales slightly smaller, about 1.0 mm in length. The dorsalsurface bears many stout, glandular spines and there is adistinct white wax marginal secretion. Exuviae of earlierinstars often remain stacked up on the median area of thepuparium (EPPO/CABI, 1997). Identification to species requires microscopicexamination of the derm (external surface) of slide-mounted puparia or empty pupal cases (as for allAleyrodidae) (JANSEN, 2002). Important diagnosticcharacters of the puparium of A. spiniferus include:puparium black; glandular spines present on all the dorsalareas, apex of spines acute, most of them reaching wellbeyond margin; female puparium with 30 pairs of dorsalspines, of which 11 pairs on submargin; all the submarginalspines placed singly; abdominal submedian spines vary inlength; vasiform orifice cordate with operculum almostfilling the orifice; margin coarsely toothed with seven tonine marginal teeth per 0.1 mm (Fig. IV, 1-2) (JANSEN,2002; DUBEY and KO, 2012). A. spiniferus puparia aremorphologically similar to those of the related citrusblackfly A. woglumi and may be separated using the keypresented by DUBEY and KO (2012).144 S. RADONJIĆ ET AL. REDIA, Vol. XCVII, 2014Fig. IV. – Aleurocanthus spiniferus: slide mounted femalepuparium (1); puparium margin showing the coarse marginalteeth (2)The pathway of introduction of this quarantine speciesinto Montenegro is unknown, as it has been recorded inestablished citrus orchards (older than 10 years), with norecent import connection. It is assumed that the infestationis likely to have originated from plant material importedfrom Italy or Croatia, where the pest has been found. Adultsof Aleurocanthus spp. are capable of limited down-windflight, but this is not a major means of long-range dispersal.The pest is most likely to be moved between countries onplanting material of citrus or other host species, or possiblyon fruits. Species of Aleurocanthus have been intercepted onthe leaves of infested host plants moving in internationaltrade (EPPO/CABI, 1997). REFERENCESANONYMOUS, 2000 - Council Directive 2000/29/EC of 8May 2000 on protective measures against theintroduction into the Community of organisms harmfulto plants or plant products and against their spreadwithin the Community + Annexes I-IX.- OfficialJournal of the European Communities, L 169/29.ANONYMOUS, 2013 - EPPO A2 List of pests recommendedfor regulation as quarantine pests (version 2013-09).[online] URL: http://www.eppo.int/QUARANTINE/listA2.htmCIOFFI M., CORNARA D., CORRADO I., JANSEN M. G. M.,PORCELLI F., 2013 - The status of Aleurocanthusspiniferus from its unwanted introduction in Italy todate.- Bulletin of Insectology, 66 (2): 273-281.DUBEY A.K., KO C.C., 2012 - Sexual dimorphism amongspecies of Aleurocanthus Quaintance & Baker(Hemiptera: Aleyrodidae) in Taiwan, with one newspecies and an identification key. - Zootaxa, 3177: 1-23.EPPO/CABI, 1997 - Aleurocanthus spiniferus. In: SMITHI.M., MCNAMARA D.G., SCOTT P.R., HARRIS K.M.,(Eds.), 1997 - Quarantine Pests for Europe, SecondEdition, CAB International, Wallingford: 21-24.F.A.O., 2010 - Glossary of phytosanitary terms.12International standards for phytosanitary measures 5:1–27.JANSEN M., 2002 - Diagnostic protocols for regulated pests.Aleurocanthus spiniferus. - Bulletin OEPP/EPPOBulletin, 32: 255-259.KUWANA, I., 1928 - Aleyrodidae or white flies attackingcitrus plants in Japan. - Ministry of Agriculture andForestry, Japan. Scientific Bulletin, 1:41-78.MALUMPHY C., 2004 - Diagnostic protocols for regulatedpests – PM7/35 Bemisia tabaci.  - BulletinOEPP/EPPO Bulletin, 34: 281-288.MARTIN J.H., 1987 - An identification guide to commonwhitefly pest species of the world (Homoptera,Aleyrodidae). - Tropical Pest Management, 33: 298–322.PORCELLI F., 2008 - First record of Aleurocanthusspiniferus (Homoptera: Aleyrodidae) in Apulia,Southern Italy. - Bulletin OEPP/EPPO Bulletin, 38:518-520.QUAINTANCE A. L., 1903 - New oriental Aleurodidae. -Canadian Entomologist, 35: 61-64.WEEMS H. V., 1974 - Orange spiny whitefly ,Aleurocanthus spiniferus (Quaintance) (Homoptera:Aleyrodidae). - The Florida Department of Agricultureand Consumer Services’ Division of Plant IndustryEntomology Circular, 151: 1-2.ŠIMALA M., MASTEN MILEK T., 2013 - First Record of theOrange Spiny Whitefly, Aleurocanthus spiniferusQuaintance, 1903 (Hemiptera: Aleyrodidae), in Croatia.- Zbornik predavanj in referatov 11. Slovenskegaposvetovanja o varstvu rastlin z mednarodno udeležbo,354-358.FIRST RECORD OF ALEUROCANTHUS SPINIFERUS (QUAINTANCE) (HEMIPTERA ALEYRODIDAE) IN MONTENEGRO 145

First record of Aleurocanthus spiniferus (Quaintance) (Hemiptera Aleyrodidae) in Montenegro

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First record of Aleurocanthus spiniferus (Quaintance) (Hemiptera Aleyrodidae) in Montenegro

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