Intenzivan uzgoj agruma u Republici Hrvatskoj započinje u drugoj polovici 20. stoljeća, a danas su prema uzgojnim površinama i prinosima u domaćoj proizvodnji treća voćna kultura. Kao i sve kultivirane biljke, agrumi su podložni napadu entomofaune. Podredu Sternorrhyncha koji obuhvaća lisne buhe, štitaste moljce, lisne i štitaste uši pripadaju neki od najštetnijih kukaca koji su u prošlosti prouzročili propadanje čitavih plantaža agruma diljem svijeta. Razvojem svjetskih tržišta raste i međunarodna trgovina poljoprivrednim proizvodima. Kukci iz ovog podreda se lako prenose sadnim materijalom. S obzirom da je u posljednjih 20 godina i u Hrvatskoj otkriveno nekoliko novih štetnih organizama koji su regulirani EU zakonodavstvom, potpuno je jasno da niti naš teritorij nisu zaobišle ove negativne posljedice globalizacije. Stoga je cilj ovog rada bio pregledom literature istražiti koje su sve vrste kukaca iz podreda Sternorrhyncha štetnih na agrumima prisutne u Republici Hrvatskoj i usporediti ga sa zemljama s najvećom proizvodnjom agruma u svijetu, a nakon toga nadopuniti popis nalazima vlastitog faunističkog istraživanja u nasadima agruma u Republici Hrvatskoj, s posebnim osvrtom na novoutvrđene i karantenske vrste te izdvojiti potencijalno najštetnije. Faunističko istraživanje je provedeno u razdoblju od 2015. do 2020. godine u šest obalnih županija od Dubrovačko-neretvanske do Istarske županije. Ukupno je prikupljeno 1.495 uzoraka biljnog materijala iz kojih je izrađeno 1.416 trajnih mikroskopskih preparata. Determinirane su 22 vrste kukaca iz podreda Sternorrhyncha kojima domaćini mogu biti agrumi, od toga pet vrsta štitastih moljaca, sedam vrsta lisnih uši i deset vrsta štitastih uši. Utvrđena je prisutnost karantenske vrste štitastog moljca Aleurocanthus spiniferus Quaintance, 1903 i regulirane nekarantenske vrste Parabemisia myricae (Kuwana) 1927. U različitim tipovima nasada prvi put je na agrumima pronađeno pet vrsta lisnih uši i jedna vrsta štitaste uši. Aphis craccivora Koch, 1854, Aphis fabae Scopoli, 1763, Aphis gossypii Glover, 1877, Aphis neri Boyer de Fonscolombe, 1841, Aulacorthum solani Kaltenbach, 1843 i Pulvinaria floccifera (Westwood, 1870) su duže vremena prisutne u hrvatskoj entomofauni, ali su sada prvi put nađene na agrumima. Najveći broj vrsta (17) pronađen je u Dubrovačko-neretvanskoj i Splitsko-dalmatinskoj županiji (16) u kojima se nalazi glavnina proizvodnje agruma u Hrvatskoj, stoga je i statistička obrada podataka ograničena na ove dvije županije. Veći intenzitet šteta u proizvodnim nasadima agruma zabilježen je na tri lokacije u kojima je izostala primjena agrotehničkih mjera i mjera zaštite. U jednom od takvih nasada u Dubrovačko-neretvanskoj županiji prvi put je otkriven i štitasti moljac A. spiniferus. Za vrijeme istraživanja ovaj štitasti moljac se konstantno širio te je otkriven i u Splitsko-dalmatinskoj županiji. Provedeno istraživanje je prvi put objedinilo rezultate prisutnosti i raširenosti kukaca iz podreda Sternorrhyncha na agrumima u Hrvatskoj.
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Introduction: Citrus plants have been grown on the Croatian side of the Adriatic since the Middle Ages but intensive production started in the second half of 20th century. Satsuma mandarin is the 3rd important fruit culture in Croatia, following apple and olive with total growing areas of 2.100 hectares and annual fruit production from 20.000-65.000 tones in five year period. As all cultivated plants, species belonging to genus Citrus L. and Poncirus Raf. are susceptible to impact of entomofauna. Suborder Sternorrhyncha within the Hemiptera order comprises of four Superfamilies: Psylloidea, Aleyrodoidea, Aphidoidea and Coccomorpha. Many insects which may feed on citrus plants fall within the said superfamilies. Their direct damages on plants are manifested as vigour deteriorating and late tree dying. Indirect damage is pour commercial value of fruits due to sooty mold settled on honeydew excreted by these insects. On the other hand, more harmful to plants are insects which, apart from ability to cause direct and indirect damage, are vectors of plant diseases like Citrus tristeza virus, Citrus greening disease or Huanglongbing and virus like disease Citrus chlorotic dwarf. Former records show that vectors of the mentioned plant diseases like aphid Aphis (Toxoptera) citricidus (Kirkaldy) 1907, psyllid Trioza erytreae (Del Guercio 1918) and whitefly Parabemisia myricae (Kuwana) 1927 are already present in the Mediterranean part of EU in countries with considerable citrus production. It is important fact because planting material of host plants, although accompanied by plant passport, may freely circulate through EU territory and represent a potential source of infection. Up to now, several faunistic researches were conducted and check lists in Croatia were made for aphids, whiteflies and scale insects. There were no complete faunistic research for psyllids and its general status in Croatia is still unknown. Furthermore, previous faunistic research of insects from the suborder Sternorrhyncha only partially covered plants belonging to genus Citrus and Poncirus. Therefore the aim of this research was to make the inventory of insects from the suborder Sternorrhyncha in citrus production areas in Croatia in order to gain complete status of distribution of these insects and to provide scientific and sound support in case of accidentally imported quarantine pests.
Materials and methods: Literature research was done to gain image about distribution of the 73 chosen important insects from the suborder Sternorrhyncha that may feed on citrus plants. These insects (11 psyllids, 14 whiteflies, 19 aphids i 29 scale insects), according to the literature data, are classified as a quarantine, economic or secondary pests on citrus plants. Research was conducted for 15 countries which, according to FAO, have the biggest production and export of citrus fruits in the Mediterranean, Asia, South Africa, North and South America. Research was also done for Croatia and neighbouring countries Slovenia and Montenegro. In addition, six year faunistic research (2015-2020) in citrus production areas in Croatia was done. During that period 266 sites in total were inspected, of which 181 orchards, 69 backyards and 16 nurseries and garden centres. Visual inspections and sampling were conducted from April till November in six counties in coastal part of Croatia on ten plant species belonging to genus Citrus and Poncirus. Targeted psyllids were investigated on 105 locations. Whiteflies were found on 112 locations where 289 samples were taken. Aphids were found on 228 locations where 639 samples were taken and scale insects were found on 185 locations where 518 samples were taken. Host plants in orchards, backyards and nurseries and garden centres were visually inspected with help of 10x hand magnifier. Vast majority of locations were inspected at least two times during the six year period. Due to presence of planting material of citrus and ornamental plants originating in other EU countries, nurseries and garden centres were inspected at least once every year. In case of suspected infestation, sample of infested plant material or insects were taken for laboratory slide preparation. Methods of sampling nymphs and adults of psyllids are described by Hodkinson and White (1979) and Ossiannilsson (1992). Infested plant material with puparium and pupal case of whiteflies were taken according to the methods described by Martin (1987, 1999) and Hodges and Evans (2005). Infested plant material and adults of aphids were taken according to the method described by Blackman and Eastop (2000). Infested plant material with adult females of scale insects were taken according to the methods described by McKenzie (1967), Kosztarab and Kozár (1988), Gill (1988, 1997) and Watson and Chandler (1999). For slide preparation of psyllids modified method by Watson and Chandler (1999) was used. Whiteflies were slide mounted according to modified method by Šimala (2008) with individual phases described in method by Watson and Chandler (1999). For slide preparation of aphids methods described by Martin (1983) and Blackman and Eastop (2000) were used. Scale insects were slide mounted according to modified method by Masten Milek (2007) with individual phases described in method by Watson and Chandler (1999). After that microscopic identification according to relevant morphological keys for every group of insects was done. In case of finding of Trioza species, identification key by Hollis (1984) would be used. Since at the moment there is no relevant key for Diaphorina species, identification is done according to description by Yang (1984). For identification of puparium and pupal case of whiteflies, identification keys by Martin et al. (2000), Suh (2010), Dubey and Ko (2012) and Wang et al. (2014) were used. Identification of aphids were done according to keys by Blackman and Eastop (2000). For identification of scale insects identification keys by Gill (1988, 1997), Camporese and Pellizzari (1994), Williams and Watson (1990), Williams and Granara de Willink (1992) were used. For all species found during faunistic research, dominance, constancy and ecological significance indices were calculated for orchards, backyards and nurseries and garden centres in every county. Biodiversity for every locality was calculated using biodiversity indices (Shannon-Wiener Index, Simpson Index, and Sörenson Index). In order to determine if there is a difference between type of growing site (orchards, backyards and nurseries and garden centres) and county (only for Dubrovačko-neretvanska and Splitsko-dalmatinska), number of species in every group of insects and number of individuals from every group of insects were subjected to analysis of variance. Mean values were ranked based on Duncan's Multiple Range test with the protection level of 95% (p<0.05). Using factorial analysis and three factors: locality (county), superfamily and type of growing site, it was determined which of the mentioned factors and/or its interactions have most impact on number of species and number of individuals. In addition, using factorial analysis and three factors: locality (county), type of growing site and species founded, it is determined which of the mentioned factors and/or its interactions had most impact on dominance, constancy and ecological significance. In order to determine if there is a difference between type of growing site and county (only for Dubrovačko-neretvanska and Splitsko-dalmatinska), biodiversity indices were subjected to analysis of variance. Mean values were ranked based on Duncan's Multiple Range test with the protection level of 95% (p<0.05). Using factorial analysis and two factors: locality (county) and type of growing site, it was determined which of the mentioned factors and/or its interactions had most impact on biodiversity indices. All indices in Dubrovačko-neretvanska and Splitsko-dalmatinska county were calculated for individual localities and presented as its average (every locality counts 3-104 locations). For Šibensko-kninska, Zadarska, Primorsko-goranska and Istarska county, calculations were made only at county level while due to fewer number of localities and locations, statistical analysis has not been done.
Results and conclusions: Literature research showed that most of investigated insects are present in selected countries. Many of them are of Asian or African origin and from their natural habitat through international trade they have spread to another continents and caused huge damages in citrus industries. 11 psyllids that may feed on citrus are recorded in selected countries and quarantine species T. erytreae is present in EU. No psyllids that may feed on citrus have been recorded in Croatia. Eight out of 14 investigated whiteflies have been recorded in Croatia, five of them on citrus plants. Quarantine whitefly A. spiniferus was found once in 2012 in nursery and eradicated. 13 out of 19 aphids have been recorded in Croatia and only two on citrus plants. The most important aphid on citrus A. citricidus is present in EU. 25 out of 29 investigated scale insects have been recorded in Croatia, whereof 3 species were found only on imported fruits from South America. Most of them are present in selected countries and two quarantine species Unaspis citri (Comstock, 1883) i Lopholeucaspis japonica (Cockerell, 1897) are present in EU without recorded damages in citrus groves so far. During faunistic research (2015-2020) in six coastal counties 1.495 samples of plant material was collected. In total, 22 insects from suborder Sternorrhyncha were determined, five whiteflies, seven aphids and ten scale insects. The highest number of species was recorded in Dubrovačko-neretvanska (17) and Splitsko-dalmatinska (16) county and the least number in Istarska (8) and Primorsko-goranska (4) county. According to analysis of variance and factorial analysis, average number of determined species depends solely on type of growing site while county and superfamily has no influence on the number of determined species. It is also determined that average number of findings per one inspection is significantly influenced by interaction of county, superfamily and type of growing site. Conducted factorial analysis of dominance, constancy and ecological indices confirms significant influence of insect species and type of growing site as well as interaction between type of growing site and insect species on the said indices. As for biodiversity indices, no significant differences in all types of growing sites between Dubrovačko-neretvanska and Splitsko-dalmatinska were determined. Seven insects are new on citrus flora in Croatia. Aphids Aphis craccivora Koch, 1854, Aphis fabae Scopoli, 1763, Aphis gossypii Glover, 1877, Aphis neri Boyer de Fonscolombe, 1841, Aulacorthum solani Kaltenbach, 1843 as well as scale insect Pulvinaria floccifera (Westwood, 1870) were found for the first time on citrus plants but no significant damages were recorded. Furthermore, P. myricae is new recorded non quarantine regulated whitefly found on citrus plants in Dubrovačko-neretvanska (2015 and 2019) and in Splitsko-dalmatinska county (2018). No significant damages were recorded and the whitefly is still under control although climatic and environmental conditions are fulfilled for further spread. In addition, quarantine species A. spiniferus, after eradication in 2012, was found in natural habitat (orchards and backyards) in Dubrovačko-neretvanska (2018-2020) and Splitsko-dalmatinska (2019-2020). Taking into account its polyphagous nature, ideal climatic and environmental conditions and infested area, eradication of A. spiniferus in Croatia is no more possible. Conditions for outbreak of other investigated insects in Croatia are also fulfilled and imminent danger present specially those already present on EU territory like psyllid T. erytreae, aphid A. citricidus or scale insects A. citrina, U. citri, L. japonica and P. nigra. On the other hand, only wider scientific study may confirm if they are capable to cause serious damages in citrus groves in EU and Croatia. This thesis is contribution in knowing insects from the Sternorrhyncha suborder on citrus plants in Croatia. Taking into account serious damages that these insects may cause, it is important to know which species are present in Croatia and due to international trade with planting material it is also important to have image of its distribution within the EU.