HORTICULTURE AND FORESTRY - REVIEW

Aceria kuko : a Comprehensive Review of their Phytosanitary Risk, Pathways and Control

Roxana CICEOI

*, Elena Ștefania MARDARE

University of Agronomic Sciences and Veterinary Medicine of Bucharest, Laboratory of Diagnosis and *) Protection of Research Center for Studies of Food Quality and Agricultural Products, Bd. Marasti, no.59, 011464, Bucharest, Romania Corresponding author, e-mail: [email protected] BulletinUASVM Horticulture 73(2) / 2016 Print ISSN 1843-5254, Electronic ISSN 1843-5394 DOI:10.15835/buasvmcn-hort:12264

Abstract

Aceria kuko The present review aims to identify the phytosanitary risk, the dissemination pathways and the possible control methods of , the goji-berries gall , which was imported to Europe from China via orders by mail in 2007. Despite the first eradicativeSolanaceae measures taken by the UK in 2008 and Germany in 2011, the was found again in Germany (2012), in Slovenia (2012), in Cyprus (2013), in Romania (2013), in Hungary (2014) and in Serbia (2015). Although the import of Aceria kuko intended for planting is prohibited in Europe, the parcels ordered by mail escape the pest and disease control services. Our field observations regarding the attack frequency, attack intensity and the losses indicate that is a potential threat for goji growers. Monitoring the presence of the mite in the Romanian Goji plantations should therefore be regarded as a biosafety measure not only for Romania,Keywords but forAceria entire kuko,Europe. biosafety, Lycium barbarum, nonindigenous pest, pest risk assessment

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INTRODUCTION Aceria kuko TheAceria goji berries gall mite, (Kishida, Global trade has been widely acknowledged 1927) belongs to the family and its as one of the leadinget al. causes of the introductionmo- etgenus, al. , includeset overal. 900 species which are netaryof invasive impacts alien of species IAS in Europe(IAS) on amount a new toterritory a total known to be taxonomically problematic (Magud of(Colunga-Garcia 12.5 billion EUR/year , 2013) and theet totalal. “ , 2007). Navia , in 2009, conclude that because of their veryEriophyid small size, that makes them ” (Kettunen , 2008). difficult to be detected and so easily distributed All around the globe, the Internet sales represent by world trade, mites have a high a serious threat, as the undetected, alien species potential as invasive alien species. The new goji may bypass the pest quarantine and control ser- pest had been for the first time reported on the vices. As example, in UK, the purchasing of European territory of United Kingdom, in April from larger traders who have their own websites, 2008, and was discovered by chance, following from the small companies or nurseries that pro- one regular inspection of some goji plants in a mote their products on E-commerce websites, nursery in Guernsey. Following this inspection, from the private persons who uses the sharing/ an entire businesset al. of illegal import of goji plants trading websites or from national newspapers and was discovered (Anderson and Ostoja-Starzewski, magazines that runs special promotionet al.for plants 2009; Giltrap , 2009). The European and supplying is considered an increasing trend, but in Mediterranean Plant Protection Organization the same time a major threat (Giltrap , 2009). (EPPO) mentioned the new finding and the actions 90 CICEOI

& MARDARE chinense in August and September 2008, samplestaken by ofthe severely UK authorities distorted in leaves EPPO ofRS ‘Goji’ 2008/222, plants (Huang, 2008). The same doubt had had werestating received that “by the Central Science Laboratory also the first researchers who hadet al. identified the (CSL) from 3 geographically distant parts of onepest inLycium the UK barbarum (Ostoja-Starzewski, 2009). In the England The infested plants were destroyed paper published in 2014, Balanto the Aceria mention kuko thatgall and further surveillance will be carried out by mite’s attack, the degree biotypeof attack wasbeing vulnerable 41%. The phytosanitary (…) inspectors. Publicity and advice will miteto powdery is specific mildew to Lycium and “ species and probably continue to be given to attract the attention of the came with the biological material, although it was general public to the risks presented by these illegal not observed at planting. However, it should be imports of Lycium spp. plants noted that neither fruit quantity nor quality was Aceria kuko negatively affected .” Following this first record, was reported again in 2011 in et al. .” Our field observation depicts Germany (EPPO RS 2011/218; Steinmöller and a different situation, as it will be further presented. Unger, 2012), then again in 2012 in Germany (EPPO Chireceanu , in 2015, mentions the European RS 2012/233),et al. in Slovenia (Seljak, 2013), in 2013 countries were the pest had been reported till etin al. Cyprus (Seraphides, 2014), in Serbia in 2014 L.2015 chinense, - United L. Kingdom, barbarum, Netherlands, Solanum nigrum Greece and (Vidović , 2015), in Hungary in 2015 (Ripka CapsicumSlovenia andannuum the fact that the pests develop on , 2015). Despite the first eradicative measures and taken by the UK in 2008 and Germany in 2011, the . The authourswith affirm the thatinfested the pest was found againAceria in these kuko countries. It has to plantpest wasmaterial identified brought in from a research China experimental be said that in the EPPO Global Database, EPPO field and that it was introduced “ code ACEIKU, the mite distribution could be a threat to the”, insisting cultures onof was last updated on 14 January 2013, when only economicthe fact that interest the plants of Solanaceae were heavily family affected and two European countries – Germany and the United that the pest “ Kingdom, mentioned to have identified the pest on Aceria kuko ”. their territory. Germany appears with the status A complete overview of the threats that “transient, under eradication” while in the United Lycium might barbarumraise for Europe would not be Kingdom the pest status is “absent, intercepted complete without analysing the situation of its only”. Those statuses are justified by the intensive host plant. , popularly known as eradication measures taken by the two countries wolfberry or “goji” from the Chinese “gou qi”, had at that time, to eliminate the new alien pest. been extensively advertisedet al. as the “superfruit” of It has neither been proved that the undertaken the century, having major sanogenic properties eradication measures in those two countries were (Mencinicopschi L., 2012).barbarum In their review effective, nor that the illegal import of plants has from 2011, aging, Amagase neuroprotection, and Farnsworth general mention well- stopped in other European countries. Aceria kuko, being,that the fatigue/endurance, studies on metabolism/energy indicate its In Romania, until the present moment there expenditure,effects on “ glucose control in diabetics, glaucoma, are only 3 mentions ofet theal. presence of anti-oxidant properties, immunomodulation, one in 2013 (Mencinicopschiet al. and Balan, 2013b), antitumor activity and cytoprotection” one in 2014 (Balan , 2014) and the last one in 2015 (Chireceanu Aceria, 2015), kuko all three being . Having presumptively from the same place in Bucharest. this said, it is understandable why the imports of The possibility to have in our country goji plants intendedLycium for barbarum planting have increased even before this date is high, as imports of Goji dramatically in the recent years (Potterat, 2009). plants originated from China started long before In the same time, grows wild into this date. Actually, the pest had been identified on etEurope al. and is considered by some scientist either imported goji plants, planted in 2010 for a field trial eta sub-spontaneous,al. naturalized plant (Doroftei of a doctoral thesis (Mencinicopschi and Balan, , 2005) either an invasive plant (Anastasiu 2013 a,c). The author only mentions that the pest , 2005, Paukovaet al. 2013). It is a hemerophyte had been reportedAceria kuko in UK, Japan and Holland,Lycium but plant (introduced from elsewhere cultivated states that the data are uncertain, as some authors plant) (Ferus , 2015) neophyte plant (recently

Bulletinaffirm UASVM that Horticulture 73(2) / is2016 monophagous on introduced plant in an area), initially introduced Aceria kuko 91

Research About Improvement the Aromatique Mites: a Comprehensive Review of their Phytosanitary Risk as ornamental, although the first mention as a Oxford Journals, CAB Abstracts, Google Scholar, wild plant dates since 1842-1848 in Moldova AgrisFao, simple google research. (Culita S, 2007), both an anthropochorous Although the present article is a review, (seeds transported by human actions, typically considering the fact that we did not publish inadvertent, into new geographicalet al. areas) and yet our own research results, we will also use endozochorus plantSolanaceous (seed dispersal realized by some unpublished pictures and data, as they are ingestion) (Ferus 2015). Goji plants considered necessary to demonstrate the actual belong to the family, which means situation in Romania. Our observations were made they are susceptible to certain dangerous pests in the experimental field of USAMV Bucharest, both and diseases common with plants of economic on potted (one-year-old plants) and planted in the importance, such as potato, pepper or tomato and field goji-berries plants (six years old plants). Our as they are perennials and relatively winter hardy research focused on the determinations regarding Lyciumplants, theybarbarum have the potential to be a major source the attack frequency, attack intensity and the of pest and diseases for a long time. Because attack degree caused by the goji gall mite. For our grows wild, its infestation with calculation, we used the following formulas: a new pathogen could act as a secondary source of The attack frequency F(%) infectionAceria for kuko subsequent years. In the present review, we aim to demonstrate that represents a potential threat and N = the number of plants observed and n = the should be considered as the starting point for the number of plants showing specific attack elaboration of preventive and eradicative control symptoms; measures for the living plant material importedAceria kukoby mail from third countries. The lack of scientific evidence about the damages produced by on different Solanaceae plants should not The attack intensity, i= % of plants presenting the be used by Romanian authorities as a reason for attack symptoms, f= the number of plants with postponing the appropriate containment and the specific % of attack, n= the total number of control measures. In Cyprus case, the discovery of plants attacked; the pest in 2013 lead to financial support coming from EU Commission, for the eradicative measures taken by Cyprus in 2014 (EU Commission, 2016). Until the present moment, from Romania, no The attack degree, F(%) = attack frequency and I information has been transmitted to the EPPO (%)PHYTOSANITARY = the attack intensity RISK services, either no eradicative, curative or preventive measure has been mentioned. As the imports via internet from China increases in the AceriaThe kuko bibliographical references state that the last years, especially for living plants and the phytosanitary risk associated with the presence of mailed parcels are usually inadequately verified, is low, as there are no knownLycium databarbarum about the risk of introducing other non-native pests in the damagesLycium andchinense economic losses caused by the pest on other crops, other than EuropeMATERIALS is very high. AND METHODS et al. and , crops that are specific to China. Despite this, Hong (2006) have For the present paper were used all the available included the mite in the list of invasive eriophyid online and offline bibliographical references we mites of economic importance in China. Analysing could find, using the following international the potential threats, we could summarize that databases: Web of Science - Core Collection there are four major types of phytosanitary risk, (Journal Citation Reports, Derwent Innovations of which1. The three risk havefor goji been berries already producers documented Index, Thomson Reuters), SpringerLink Journals (figure 1). (Springer), Scopus (Elsevier), ScienceDirect . In Freedom Collection (Elsevier), PROQUEST Central, Europe, the risk for the goji berries producers is considered small, as there is no economic goji Bulletin UASVM Horticulture 73(2) / 2016 92 CICEOI

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Fig. 1. Aceria kuko

The four possible different types of phytosanitary risk associated with the presence of mite in Europe production in the area, the majority of producers of the plants, were the flower and future fruit being amateurs. On the other hand, goji had occurs, were completely damaged. become extremely popular in the recent years, and In 2016, in the UASVM Bucharest experimental a growing number of people are living from selling fields, the attack frequency was 100% on goji the goji berries or goji plants. Not many data biotypes V1 and V2, the attack intensity on leaves are available about the goji producers in Europe vary between 45% and 85% and the production and there is also a scarcity of data relatedet al. to the losses in the month of June were estimated number of goji growers and the entire cultivated between 80% and 100%, as the majority of flowers goji area in Romania. Danaila-Guidea , 2015, buds were distorted by galls (figure 3). mention that a manufacturer in Ciuperceni village The observations made in July and August on (15 kilometres away from Satu Mare, in northern the fruits could not conclude to a clear comparison Romania) has set up the first organic goji plantation of the quantitative losses, as all the plants were in Europe, on an area of 2 hectares and from public infested and the majority of fruit A. stalks kuko had at TV and other internet sources we found out that least 1 to 4 galls on them (figure 4). he extend it to 12 ha (www.gojilandromania.eu). Up to now, we knew that is a Agrointel website, 2013, mention that Ms. Erzsebet thermophile species, having optimal development Kolbaszer from Carei had in 2013 an area of 2.5 ha at temperature between 25 – 35°C. For the of goji and wanted to extend to 5 ha until the end of necessary minimum temperature for survival, an the year. On YouTube website, the keywords “goji activity of the gall mites below 0°C was described and Romania” bring about 4730 results, and quite (Anderson and Ostoja-Starzewski, 2010). It was a few videos mentionet al.commercial goji plantations assumed by Ostoja-Starzewski, 2009 that also an with a surface between 0.2 and 2 ha. overwintering below bud scales and bark pieces In 2014 Balan concluded that either the is common and our observations show that the fruit quantity and quality was negatively affected, goji gall mites survives at least at temperatures but our observations depict a different situation of -25°C, which is a major adaptation at the new and indicate either a change in pestAceria virulencekuko on climatic factors and proves the species adaptability. its host plant either a better adaptation to the We consider that the presence of galls on new climatic conditions that led to `s stalks may interfere with the sap exchanges with population proliferation. Despite the fact that the the plant and presumptively can lead to qualitative degree of attack might be appreciated below 50% and quantitative losses. The fact that the presence for one of the plants, as the lower leaves of the of galls on plants may lead, in the case of severe shrub have fewer galls (figure 2), the young shoots infestation, to the death of the plant, indicate Bulletin UASVM Horticulture 73(2) / 2016 the necessity of chemical intervention when the Aceria kuko , Pathways and Control 93

Mites: a Comprehensive Review of their Phytosanitary Risk

Fig. 2.

Comparison between a heavily infested goji branches and one only with few galls (14.06.2016)

Fig. 3 Aceria kuko

. The flower buds completely destroyed by the galls formed by (14.06.2016). economic damage threshold is reached. Other stopped their shoot development and the apical Aceria specieset al. have been and are still used as growth and the adjacent stems were distorted, Aceriabiological chondrillae agents for weeds control (Lipa, 1978; leading to the death of the young plant (Cullen and McClay , 2013; Vacante, 2016). For example, Moore, 1983). Further research is necessary to is often used as a biological identify the modifications in the plant metabolism, control for the perennial herbA. malherbae skeleton weed induced by the feeding process. ( ) present in Europe,Convolvulus North Theet goji al. plants produce the fruit continuously arvensisAmerica and Australiaet al. while was during the summer, from June to November successfully used for the control of (Balan , 2014) and the application of systemic (McClay , 2013). It was introduced acaricides make the fruits improperAceria guerreronis for human to Australia in 1971 as part of a program to consumption, from one day to another. For suppress skeleton weed in infested areas. The galls example, Griffith, 1985, for the induced by the gall mites impede the growth and mite indicate the fact that a 5-month period is reproduction abilities of the plant by destroying required for the fruits to be free of all pesticide the flower buds in gall formation, reducing or residues (from treatment to harvest). For the goji suppressing seed production and destroying the producers, the necessity of using chemical plant apical shoots. Kim, 1965, demonstrate that starting protection products represents a serious problem, with the 15th day of their life, the mites feeding on first because the majority of the goji producers the leaves galls destroy the chloroplasts from the prefer to be certified as organic farms, to obtain a leaves cells. The plants infested in an early stage higher income and secondBulletin because UASVM Horticulture the producers 73(2) / 2016 94 CICEOI

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Fig. 4 Aceria kuko

.The galls formed on fruit stalks (02.08.2016). might lose a part of their production, because of be considered insignificantAceria cajani and should be the pause time imposed by each chemical product. further investigated.Aceria kuko Pallavi and Ramappa, 2014, Another aspect to be considered is the possible demonstrate that , another mite dissemination pathway represented by seeds. The related to , is the vector of pigeonpea presence of mites on stalks of the fruit indicate also sterility mosaic virus (PPSMV), so further studies the possibility that the mite is disseminated easily should be conducted on the mite on the possibility by fruit2. The and risk seeds, for the as insweet only pepper one gall producers. hundreds to of beingDISSEMINATION a vector for viruses PATHWAYS or other diseases. thousands individuals may be observed. Aceria kuko The Aceria kuko literature and the artificial infestation tests proved The bibliographical references states that that produce damages on sweet the pathways for the introduction of pepper (Kim, 1968; Ostoja-Starzewski 2009). In mite (its first mention) in Europe are represented the period 2011-2013, the EU produced 2 259 by illegal imports, as orders by mail, of dormant thousand tonnes of sweet peppers per year (on goji berry plants from China,et al. via Netherlands average): three countries, Spain, the Netherlands (Ostojá-Starzewski,goji 2009; gall Andresonmite, a species and Ostojá- never and Italy, concentrated 69% of the total production beforeStarzewski, recorded 2009; in Europe Giltrap , 2009). The (43%, 15% and 11%, respectively), while Romania discovery of the “ produced on average 147,2 thousands of tones, ” happened accidentally, representing 6,5 % from the total EU production when a Plant Healthet al. and Seeds Inspector was (EU, 3.2014; The faostat, risk for 2016). other A newspecies eriophyid belonging pest forto performing a routine control on some goji plant in Solanaceaesweet pepper family. would lead to great economic losses. a nursery (Giltrap , 2009) so more attention should be given to the multiple ways that should Until the present moment,Aceria the be considered as possible pathways (figure 5). kukorisk for other important Solanaceous crops is The present geographical distribution of this considered low, as no known data mentions pest is believed to be limited to south-east Asia, damaging other crops. Ostoja-Starzewski, mainly China, Korea, Japan, Taiwan (Andreson and 2009, in their tests, concluded that no transfer to Ostojá-Starzewski,Dissemination 2009). over long distances tomato (‘Moneymaker’),Solanum petunianigrum (‘Crown mix’) and tobaccoCapsicum (‘White burley’)annuum was successful. On the other hand, , a well-known From a country A. to kuko another, the mites are weed and , are mentioned as dispersed only with their host. According to Kim being4. aThe host risk for for the other goji species, gall mite besides since Solanaceae 1968, Kim (1968) the adults of overwinters in theA. family.CH, so the mite it is not a “devoted” monophagous. leaf galls, but all the observations made in Europe since 2008 demonstrate that the populations of Bulletin UASVM As Horticulture no record 73(2) exists/ 2016 so far, this risk may Aceria kuko , Pathways and Control 95

Mites: a Comprehensive Review of their Phytosanitary Risk

Fig. 5 Aceria kuko kuko .The possible pathways of mite spreading on European territory. et al. 1. also The overwinter trade of infested on buds Solanaceous and bark (Ostojá- plants 2009, Andreson and Ostojá-Starzewski, 2009 intendedStarzewski, for 2009). planting from third countries other and Giltrap , 2009 mention, the infested than European and Mediterranean countries plants have been imported in the UK from the Netherlands. As the internet trade for plants for et al. . planting is increasingly popular (Giltrap, 2009), Ostojá-Starzewski, 2009, Andreson and Ostojá- the intracommunity trade is not regulated and Starzewski, 2009 and Giltrap , 2009 illustrate the mailed parcels are not subject to appropriate the case study of illegal import in the UK of goji control measures, it is predictable that the spread berry plants from China via the Netherlands. In of the mite will continue around EU countries. The Europe, the import of Solanaceous plants intended presence of the pest in Greece in mentioned as for planting is prohibited according to Dir. result of imported plant material from Germany 2000/29/EC, in order to protect the other main (Bardas, 2012) while in Serbia it is not stated the Solanaceous crops of high economicet al. importance source of the plants, but given the fact that the mite (tomatoes, pepperin 2007, etc.) 38 to 000 be goji infected plants by had newly been was found in a 0.5 ha plantation, it is reasonable to sentalien by pests. mail Despiteto 8000 customersthis, Giltrap (...) while, 2009 in 2008, states 45 assume that the plant material was bought from 000that plantsin the UK,had “ been supplied to 19 000 customers Europe. Although there is no information about the phytosanitary condition of the plants, on a website ”. named agrointel, in 2012, there is a mention about An importantA. aspect kuko that deserves attention is a Romanian researcher and goji producer that the fact that although Kim (1968) concluded that sold 3.in Trade 2012 with goji infested plants forseeds 40 and ha fruitsgoji plantation from third the adults of overwinter in the leaf galls, countries,in Greece. other than European and Mediterranean the mites found in Europe overwinter under the countries A.buds kuko or bark crevices, as the imported plants had no leaves. Our own observations show that . The plants from the experimental field produces gals also on young branches from Romania were produced also from seeds (figure2. The4), an trade important of infested key factor Solanaceous for rapid, plantsvisual imported from China, so this pathway is totally intendedidentification for of plantingdefoliated plants.from European and valid. Considering the fact that the adult mites Mediterranean countries are extremely small, measuring between 0.17- 0.25 mm in length by 0.055 mm in width and also . As Ostojá-Starzewski, have a very difficult colourBulletin UASVM to see Horticulture (pale 73(2) salmon / 2016 96 CICEOI

& MARDARE et al. A. kuko pink) (Ostojá-Starzewski, 2009; Pipka 2015) of et by al. Kim in 1968), either by phoresy they are very difficult to see in the field or on on insects and birds (Ostojá-Starzewski, 2009). the planting material or seeds. This pathway is Michalska , 2009 cites leafhoppers as general not documented4. Trade with for infested the moment seeds and itfruits has tofrom be carriers of Aceria species while ambulatory and insidefurther the investigated. EU borders rain mode of dispersal was observed only in few Aceria kuko AceriaCONTROL species. . Our observations show that the mite can survive on the fruits and eventually infest the newly grown plants. This The identification of alien pests into a new pathway5. The is alsotrade not of documentedinfested Solanaceous for the moment plants territory must always be treated with precaution, intendedand it has for to planting be further inside investigated. of a country especially when the respective pest representsthe laack threat of in scientific its native certaintyabout location. According the various to the . The plants implicationsConvention onof an biological invasion diversity, should not 2002, be used “ presenting the distorted by galls leaves were as a reason for postponing or failing totake bought from the UK, after they were imported appropriate eradication, containment and control from Netherlands, from Guernsey, Channel Islands. measures In Romania, the number of goji plants imported from China is practically impossible to be stated, ”. The general term of control integrates as no evidence seems to be held by Romanian in the present review all three components of authorities. By reading the forums of goji amateurs the 1. precautionary Eradication. approach, the eradication, and producers, some information can showLycium out. containment and control measures respectively. barbarumIn one conversation, a goji nurseryman states In UK, the Plant Health that he had imported from China seeds of Authorities took all the necessary measures to , var. Ningxia nq1 (actually Ning Qi 1, a.n.) eradicate the mite populations identified in the and that he had sent plants in Romania, Republic 3 different regions of the country, among which of Moldova, Greece, Spain, Italy, Poland and only in withdrawing from sale of all known illegally 20136. he Accidental had produced contamination more than as a200000 result of plants trade imported ‘goji berry’ plants from plant nurseries exchanges(Marin, 2013) et al. and garden centres and followed either by their Lycium barbarum destruction or re-export (defra 2008), media . Ferus , 2015 demonstrates that publicity about the risk of having infested goji seeds and fruits of arrived on plants, sending informing lettersAceria tokuko all customers Slovakian territory, in a study about reciprocalLycium who bought directly from a mail order companies. barbarumcontamination of invasive plants in the period In all the places where mite was 2006-2010. The theoretical quantities of identified, the plants were voluntarily destroyed Lycium seeds exportedbarbarum into Slovakia into the 5 by owners and the Solanaceous plants around years of study exceeded 35 t. If we consider that them were carefully checked. The Plant Health fruits of may be infested, the Authorities carry out continuous surveillance and possibility of spreading into Europe by export is supplement the publicity and advice for all the proven. potential goji owners. The destruction of the plants AccordingAceria to kukothe bibliographical records that that were illegally imported is still recommended, could have been found until august 2016, the considering the potential threat (Anderson and history of on European territory can Ostoja-Starzewski, 2009). be summarizedDissemination as illustrated in the surroundings in table 1. In Germany, all known infested sites were subject to an intensive eradication programme, after the first finding, in Baden-Württemberg, in While the pathways to introduce the pest 2011. After the official inspections of nurseries on a new territory had been presented above, that were conducted in most German regions the dissemination of the existing populations in in 2012, the mite was found again in Berlin, the surroundings happens by passive dispersal Bayern, NordrheinWestfalen, Rheinland-Pfalz, either by wind currents (it was proved that wind Sachsen, and Schleswig-Holstein. In all sites, Bulletindirection UASVM influences Horticulture 73(2) the / 2016 migration and dispersal official control measures were taken during 2012 Aceria kuko , Pathways and Control 97

Mites: a Comprehensive Review of their Phytosanitary Risk Tab. 1. Aceria kuko

The presence of on European territory and the control action taken

Region, place Country Year Control action taken Bibliographical source

Ostoja-Starzewski (2008) United York in North Yorkshire, Selsey in West All infested plants EPPO RS (2008/222) 2008 Kingdom Sussex and Reading in Berkshire were destroyed Anderson and Ostoja- Starzewski(2009) Baden-Württemberg, in orchard for fruit Germany 2011 Under eradication EPPO RS (2011/218) production Berlin, Baden-Württemberg, Bayern, Transient, actionable, Germany 2012 Nordrhein-Westfalen, Rheinland-Pfalz, EPPO RS (2012/233) under eradication Sachsen, Schleswig-Holstein Transitional, no actions Slovenia 2012 Maribor and Ljubljana Seljak (2013) mentioned Mencinicopschi 2013b,c, No action taken until Romania 2013 Bucharest Balan 2014 2016 Chireceanu 2015. Hungary 2014 Heves, Budapest and Sasad Not stated Ripka (2015) Eradication and Cyprus 2014 Nicosia L. chinense Seraphides 2014 containment Sombor in a private orchard Serbia 2015 Not stated Vidovik 2015 area of 0.5 ha. including the destruction of infested plants (in In the same time attention should be drawn Bayern, Schleswig-Holstein, Rheinland-Pfalz), on the fact that in the UK, the most of those goji chemical treatments with acaricide, quarantine plants that were sold by mail order between May measures,2. Containment. official inspections in nurseries (EPPO and October 2007 and during April 2008 were RS 2012/233). not identified, only a few individual plants being As the goji gall mite continued reported after the public queries of Plant Health its spread in other countries in 2013 and 2014, Authorities and media publicity. All the ones who EU Aceria started kuko to take special measures. The fact purchased plants via a newspaper were either not that EU authorities admit the threat represented contacted or identified. The large numbers of goji by is proven by the fact that EU plantsAceria involved kuko (83.000 plants) and potentially Commission awarded financial support to Cyprus, widespread around the country suggests that for the measures taken by this country to control if was present on those plants, pest the mite in the Nicosia area in the year 2014. establishing is undergoing and without knowledge TheMeasures Commission against pests Implementing of the types the Aceria Decision kuko, of the3. locationsControl ofmeasures. all the goji berry plants, the UK Anoplophoraof 18.03.2016 chinensis, (Brussels, Anoplophora 2016) glabripennis, states that cannot guarantee that they eradicate the pest. and“ Bursaphelenchu sxylophilus may qualify for In the US, Maughan grants pursuant to Article 17 of Regulation (EU) and Black, 2015 states that as goji is stillA. akuko new No 652/2014 Cyprus submitted an application crop, the pest information is limited and the for Union funding on 18 September 2014 in relation only pest reported on goji in Utah is . to the measures.” As implemented “ in 2014 to eradicate Their recommended control measures include or contain Aceria kuko in Nicosia area” sulphur, insecticidal soap or horticultural oil (0.5% solution), only under the limit of 32°C or Aceria, kuko the EU horticultural oil 2%, either in the fall, just before decided that Cyprus will receive EUR 32 983 for leaves drop) or in the spring (just as leaves the measures implemented against in emerge). the area of Nicosia. Bulletin UASVM Horticulture 73(2) / 2016 98 CICEOI

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There were noAceria scientific kuko studies found for biodiversity monitoring but also in matters regarding either mechanical, chemical or biological concerningREFERENCES alien pest species. controlCONCLUSIONS methods of in Europe.

1. Amagase H Farnsworth NRLycium (2011). barbarum A review of botanical characteristics, phytochemistry, clinicalrelevance in Currently, the trade barriers and sanitary and efficacy and safety of fruit (Goji). phytosanitary measures (SPS measures) are of Food Research Int., 44(7) 1702–1717, DOI:10.1016/j. great interest worldwide. The trade-offs between foodres.2011.03.027. economic profitability and the risks raised by 2. Anastasiu P, Negrean G, Pascale G, Litescu S (2005). new invasive alien species into Europe are to be Naturalized and invasive ornamental plants present in Romanian flora. Sci. Papers IonIonescu de la Brad, Iaşi, addressed in future studies. Horticulture, 48(1) 619–624. Upon our knowledge, at this moment there is 3. Anastasiu P, Negrean G (2006). Alien vascular plants in no implemented and functional service to prevent Dobrogea (Romania) and their impact on different types the intrusion of nonindigenous species by mail in of habitats Plant, fungal and habitat diversity investigation Romania, although for example, the Dir. 2000/29/ and conservation. Proceedings of IV Balkan Botanical EC regulates the import of living plant material Congress, Sofia,Aceria 20-26 kuko June 2006, pg. 590-596. belonging to Solanaceous family. 4. Anderson H, Ostoja-Starzewski J (2010) Fera Pest Risk Analysis for .The Food and Environment The overwintering at -25°C, a major Research Agency.https://secure.fera.defra.gov.uk/phiw/ adaptation at the new climatic factors, proves the riskRegister/plant-health/ documents/Aceriakuko.pdf. species adaptability and should be regarded as an 5. Anonim, Defra, (2008).Prohibited import of goji additional warning sign. plants, 2008, http://webarchive. nationalarchives. Considering the phytosanitary risk, pathways gov.uk/20130822084033/http://www.defra.gov.uk/ news/2008/080430b.htm. and the difficult control methods for the plants 6. Balan V, Tudor V, Mencinicopschi OI, Manole C, imported via orders by Internet, integrating Stefan E(2014).Suitability for urban agriculture and invasive alien species prevention measures into permaculture of some biotypes and new varieties of the international trade rules should be considered species with sanogene characteristics and qualities,Aceria a must. National, regional and international kukoAgrolife Scientific Journal, 3(1): 15-24. precaution and prevention measures should be 7. Bardas GA (2012) The first record of the species implemented and awareness among the passionate in Goji berry cultivation in Greece http://plantdirect. blogspot.ro/2012./08/aceria-kuko-goji-berry.html, gardeners or small agricultural producers who accesed on 30.08.2016. regularly order from internet or newsletters 8. Chireceanu C, Chiriloaie A, Teodoru A, Sivu C (2015). campaigns should be raised. Contribution to knowledge of the gall insects and mites We appreciate that (minimum) 3 years associated with plants in southern Romania. Scientific without any control measures in Romania were Papers. Series B, Horticulture. Vol. LIX:27-36, http:// long enough to help the dissemination of the pest in horticulturejournal.usamv.ro/pdf/2015/art4.pdf. the country and we consider that field inspections 9. Colunga-Garcia M, Haack RA, Magarey RD, Borchert A. DM (2013). Understanding trade pathways to target kukoof all major Goji growers and in their nurseries biosecurity surveillance, NeoBiota 18:103–118(2013), are mandatory for monitoring the occurrence of DOI:10.3897/neobiota.18.4019. in Romania (both on goji berries plants and 10. Culita S (2007). Considerations regarding the alien plants on the Solanaceous plants). And, as many other from moldavian flora (Romania), deliberately introduced plants are coming from China by mail, we state by man, Buletinul Grădinii Botanice Iaşi, 14 41–50. http:// that there was enough time for the new adventive www.plant-journal.uaic.ro/docs/2007/8.pdf. species (also known as invasive alien species) 11. CullenChondrillajuncea JM, Moore AD, Journal (1983).The of influenceApplied ofEcology, three A. kuko populations of on three forms to adapt to our climatic conditions. We consider of the study of biology and ecology features Vol. 20, No. 1, pp. 235-243, http://www.jstor.org/ in Romanian environment to be the promoter of stable/2403389?seq=1#page_scan_tab_contents. a new step in plant protectionAceria kuko against new alien 12. Danaila-GuideaLycium barbarum SM, Dobrinoiu RV, Visan L, Toma RC species. (2015). Protocol for efficient in vitro multiplication We consider the case study as a of L. (goji) by direct organogenesis, Scientific Bulletin. Series F. Biotechnologies, Vol. XIX: 34- substantiation of using citizen science not only 38. Bulletin UASVM Horticulture 73(2) / 2016 Aceria kuko , Pathways and Control 99

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13. Doroftei M, Mierla M, Marinov M (2005). Ecology of some 25. Huang KW (2008).Zootaxa (Acarina: ) in alien plant species in Danube Delta, Ovidius University Taiwan: five new species and plant abnormalities caused Annals of Natural Sciences, Biology-Ecology 9(1) 33-40. by sixteen species 1829: 1–30. 14. European Commission, Health and consumers directorate 26. Kettunen M, Genovesi P, Gollasch S, Pagad S, Starfinger (2012). Summary report of the meeting of the standing U, ten Brink P, Shine C (2008). Technical support to EU committee on plant health, Brussels, ARES(2012) strategy on invasive species (IS)—assessment of the 1444026, available online at http://ec.europa.eu/food/ impacts of IS in Europe and the EU (Final module report plant/docs/sc_plant-health_20120918_sum.pdf. for the European Commission). Institute for European 15. 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Aceria kuko Central Science Laboratory, 39. DefraOstoja-Starzewski, J (2009) Plant Pest Notice: Goji gall dokumente/upload/2a4e7_aceria_kuko_express_pra_ mite, (Kishida). en.pdf; . Available online at: http://ofi.openfields.org. 47. Vacante V (2016). The handbook of mites of economic uk/1.13080156. Aceria plants: identification, bio-ecology and control. Mites as 40. cajani,Pallavi MS, RamappaHK(2014). Population Dynamics of biocontrol agents of weeds. Available online on google Pigeonpea Sterility Mosaic Virus Disease Vector Aceriabooks. kuko Mysore J. Agric. Sci.,48 (3): 394-399. 48. Vidović B., Vajgand D, Marinković S, Petanović R (2015). 41. Paukova Z (2013). Invasive plant species in the three (Kishida) (Acari: Eriophyoidea) – Nova microregions of Nitra region, South-west Slovakia Štetočina U FauniSrbije, Xiii Savetovanje O ZaštitiBilja, Ekologia, Vol. 32, No. 2, p. 262–266,Lycium barbarum DOI:10.2478/eko-L. Zlatibor, 23-26. chinense2013-0022. 49. *** UNEP (2002). Report of the sixth meeting of the 42. Potterat O (2009). Goji ( and conference of the parties to the convention on biological ): Phytochemistry, Pharmacology and Safety in diversity, The Hague, 7-19 April 2002, page 257. the Perspective of Traditional Uses and Recent Popularity, 50. ***http://www.digi24.ro/Stiri/Regional/ Planta Med 2010; 76: 7–19, DOI: 10.1055/s-0029- Digi24+Oradea/Stiri/ingura+plantatie+bio+de+goji+din 1186218. Aceria +Europa+se+afla+in+judetul+Satu. 43. kukoRipka G, Érsek L, RózsahegyiP, Vétek G (2015). First 51. ***https://gd.eppo.int/taxon/ACEIKU. occurrence of an alien eriophyoid mite species, 52. ***http://www.gojilandromania.eu/forum/aboutus.php. (Kishida) (: Eriophyidae) in Hungary, Növényvédelem2015 Vol. 51 No. 7 pp. 301-307. 53. *** http://faostat3.fao.org/browse/Q/QC/E. 44. Seljak G (2013). The dynamics of introduction of 54. *** http://www.plantatiegoji.ro/goji-media.html. alien phytophagous insects and mites into Slovenia. 55. ***(2012). Cel mai mare cultivator de cătină din România AceriaActaEntomologicaSlovenica kuko 21(2):85-122. câştigă peste 10.000 de euro la hectar. Secretele lui 45. Seraphides NA (2014). First record of the Goji gall mite, Alexandru Vulpe http://agrointel.ro/3240/cel-mai-mare- (Acari: Eriophyidae), The Review of the cultivator-de-catina-din-romania-castiga-peste-10-000- Agricultural Research Institute for 2012-2013, p. 42, de-uro-la-hectar/ AceriaLEFKOSIA, kuko ISSN 1018-9475. 46. Steinmöller S, Unger JG, (2012). Express – PRA for , http://pflanzengesundheit.jki.bund.de/

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