An annotated update of the scale insect checklist of Hungary (Hemiptera, Coccoidea)

Abstract The number of scale insect species (Hemiptera: Coccoidea) known from Hungary has increased in the last 10 years by 39 (16.6 %), to a total of 274 species belonging to 112 genera in10 families. The family Pseudococcidae is the most species rich, with 101 species in 34 genera; Diaspididae contains 59 species in 27 genera; Coccidae contains 54 species in 27 genera; and the Eriococcidae contains 33 species in 8 genera. The other 6 coccoid families each contain only a few species: Asterolecaniidae (7 species in 3 genera); Ortheziidae (7 species in 4 genera); Margarodidae sensu lato (5 species in 5 genera); Cryptococcidae (3 species in 2 genera); Kermesidae (4 species in 1genus); and Cerococcidae (1 species). Of the species in the check list, 224 were found in outdoor conditions, while 50 species occurred only in indoor conditions. This paper contains 22 species recorded for the first time in the Hungarian fauna.


Introduction
Scale insects (Hemiptera: Coccoidea) live on a wide variety of plant species and many of them are important agricultural pests. Publication of new knowledge of this insect group is therefore very important from a practical viewpoint. The distribution data of different species may serve also as a reliable biodiversity indicator in different ter-ritories, such as nature reserves and agricultural or urban landscapes. The distribution data may also reflect the progress of climatic changes (Kozár 1997;2009;Kozár et al. 2004;Kozár et al. 2009).
The world distribution of insect pests has changed greatly in recent decades, mainly due to increasing international trade in plant material. Scale insects are particularly well adapted to accidental introduction because their habits are often cryptic, so they can escape detection during quarantine inspections (Muniappan et al. 2009). Specifically, in recent years intensive scale insect invasions have been observed in several parts of Europe. In parallel, the number of species detected in the continent increased substantially, both outdoors and in indoor conditions such as greenhouses, commercial fruit stores and nurseries (Ben-Dov et al. 2013;Fetykó and Kozár 2012;Fetykó and Szita 2012;Malumphy and Badmin 2012;Pellizzari and Germain 2010).
Early data on the distribution of scale insects in Hungary were summarized by Kosztarab and Kozár (1978;1988) and by Kozár (1998). The last check list of the scale insects of Hungary (Kozár 2005) reported 235 species and provided distribution maps. At the same time, the international ScaleNet database contained 206 scale insect species recorded from Hungary (Ben-Dov et al. 2013). Since the work of Kozár (2005), 17 new scale records from Hungary have been published Fetykó and Szita 2012;Klupács and Volent 2012;Kozár 2004;2009;Kozár et al. in preparation;Kozár et al. 2004;Kozár and Konczné Benedicty 2005;2007;Kozár et al. 2009). In the present paper we provide the latest checklist of scale insect species found in Hungary, and give a zoogeographic analysis of the known fauna of Central Europe and surrounding countries.
Scale insect species in Hungary are grouped into three categories. True members of the Hungarian fauna can be found regularly in outdoor habitats and typically overwinter outdoors. The second category of species is generally found in greenhouses or other buildings, mainly on ornamental plants. These introduced species are, in some cases, well-established in Hungary and may occur regularly, but are unable to overwinter outdoors. The third category consists of relatively few, introduced species that occur typically on imported tropical or subtropical fruits for consumption. Some of these species have not been able to establish at all, even in greenhouses, despite repeated introductions over several decades. All the species in the following checklist are assigned to one of these three categories.

Materials and methods
The list below is based on the collection data of the authors between 2003 and 2013 and includes earlier records from Kozár (2005). In this ten-year period, 4738 scale insect samples were studied (Kozár's collection index numbers 6097-0835). The samples originated from both outdoors and indoors, i.e. field trips, greenhouses, botanical gardens, nurseries, imported fruits and indoor ornamental plants.
The scales were mounted on microscope slides following the method described by Kosztarab and Kozár (1988). Voucher specimens, mainly in form of microscope slides, can be found in Kozár's collection in the Plant Protection Institute at the Centre for Agricultural Research of the Hungarian Academy of Science.
The nomenclature of the scale insects has frequently been changed, even within the last decade. The scientific names used below therefore are annotated to relate them to those that were used in earlier Hungarian publications. We have endeavoured to maintain conformity with our previous works, as well as with the international scale insect database on "ScaleNet" (Ben-Dov et al. 2013). The taxonomic status of the families Margarodidae and Pseudococcidae are subject to current research, so these families in their wider circumscription are dicussed here as Margarodidae sensu lato and Pseudococcidae sensu lato.

Results and discussion
The number of scale insect species in Hungary has increased by 39 (16.6 %) in the last ten years, and currently totals 274 species in ten families (Tables 1 and 2). The largest families in order of species richness are: Pseudococcidae with 101 species, Diaspididae (59 species), Coccidae (54 species) and Eriococcidae with 33 species. The new species to the Hungarian fauna recorded here belong to the Pseudococcidae, Diaspididae and Eriococcidae. Most of the species in the checklist (224; 81.75 %) are native and live outdoors. The check list contains 50 introduced (generally cosmopolitan) species, mainly occurring indoors in Hungary on ornamental plants in greenhouses and buildings. Of these indoor species, 33 occurred only in greenhouses or buildings (mainly on ornamental plants) and 7 were found exclusively on imported tropical/subtropical fruits for consumption. Four of the species living in greenhouses sometimes also occur outdoors. Four other species, which are typically found on imported fruit, also appear in greenhouses from time to time. Two of the newly recorded species were found on imported nursery plant material. In the present list, 22 species are new to the Hungarian fauna. According to these data, Hungary is the most scale-insect-species-rich country in in Central Europe (Fig. 1).
No species should be considered as truly endemic only on the basis of its presence in a checklist, because the lack of a species in the surrounding countries is most likely due to inadequate exploration of those areas (Fig. 1). Out of the above list,  Green, 1921 Found in Hungary in 2011 (Klupács and Volent 2012).
Trionymus thulensis Green, 1931Trionymus tomlini Green, 1925Volvicoccus stipae Borchsenius, 1949 Previously recorded as Mirococcopsis. Volvicoccus volvifer (Goux, 1945) New to the Hungarian fauna. Found in Hungary (Sashegy) by D-vac (leg: E. Botos) on Brometum. Probably native. Vryburgia brevicruris (McKenzie, 1960) Comments: i. The record of the presence of Acanthomytilus sacchari (Hall, 1923) in Hungary was given by Danzig and Pellizzari in Kozár (ed.) (1998), cited by ScaleNet, is not proven. ii. The presence of Lepidosaphes shanxiensis Shi, 1990 in Hungary, cited by ScaleNet, is not proven (error or misidentification). iii. The record of the presence of Parlatoria oleae (Colvée, 1880) in Hungary given by Kosztarab and Kozár (1988), based on US quarantine record cited by ScaleNet, is not proven. iv. The record of Kermes ilicis (Linnaeus, 1758) given by Sugonyaev (1965) as a host of a parasitoid, cited by ScaleNet as a scale distribution record, is a misunderstanding of the text; the distribution record concerns the parasitoid species, not the scale. v. The record of the presence of Luzulaspis frontalis Green, 1928, cited by ScaleNet as a scale distribution record for Hungary, is probably a misunderstanding of the text of Kosztarab and Kozár (1978), where it was mentioned as possibly present in Hungary. 106 (38.69%) species are considered as widely distributed Pan-Palaearctic species, 75 (27.37%) are widely distributed Euro-Siberian species, 91 (33.21%) are cosmopolitan, and only two species are known to originate from the Mediterranean subregion.
Our data from Hungary shows a substantially different picture from that of earlier analyses dealing with scale insect zoogeography (Danzig 1980;Kozár 1995;Kozár and Drozdják 1986), where most of the species were thought to be restricted to one of the special subregions of the Palaearctic Region. The high proportion of the Palaearctic and cosmopolitan species in our analysis shows some similarity with the fauna of Israel (Ben-Dov 2012). This may be explained by the special borderline situation of each of these countries. Both are situated on the borders between different zoogeographic regions: Hungary on the borders of the European-Siberian and Mediterranean subregions, with strong influence from Irano-Turanian subregions; while Israel is on the borders of the Palaearctic, Oriental and the Ethiopian regions. Hungary has a tem-perate climate, but with several submediterranean, xerophilous habitats. In addition, the Great Hungarian Plain belongs to the steppic province of the Palaearctic Region, which ranges from Hungary to China and the Far East (Emeljanov 1974). The importance of the steppic influence can be seen in that almost 50% of the species belong to the families Pseudococcidae and Eriococcidae, and most of them live on grasses and small herbaceous plants (Table 3).
In Central Europe in the wide bio-geographic sense of Emeljanov (1974), the Hungarian list of 274 species (Fig. 1) represents the greatest species-richness value among the component countries. Undoubtedly this is partly due to better exploration of Hungary. However, it is also due to the various climatic influences affecting the territory from different directions. Important differences in species richness values were found between the data on ScaleNet and the local checklists Foldi 2001;Gertsson 2001;Jansen 1999;Kozár 2005;Kozár et al. 1994;Kozár et al. in preparation;Lagowska 2001;Masten-Milek and Simala 2008;Pellizzari and Russo 2004;Schmutterer 2008;Seljak 2010;Tereznikova 1975;1981;1986, Tomov et al. 2009Trencheva 2012). The map shows that some countries, like Bosnia and Serbia, are inadequately represented in the ScaleNet database. The published check lists in general show a more reliable picture; however, in some cases we meet an opposite situation (for example, for Germany and France). These discrepancies need further study in the future.
A detailed study of the scale insects introduced into Hungary on tropical and subtropical fruits was published by Kozár and Kienitz (1979), whose list already contained 13 species shown in Table 5, only one species in this category is new record for the Hungarian fauna (Pseudococcus elisae Borchsenius, 1957). The number of species in this category is surprisingly low, compared to the number of pests living on various fruits exported from the different regions of production. The low species number reflects the efforts made by exporting countries to prevent the spread of invasive pests. It should be noted that most of these species were unable to establish in Hungary even indoors in greenhouses or on ornamental plants in buildings, despite repeated introductions over more than one hundred years. On the other hand, some of them have become regular pests in Hungary, which has lead to some overlap with the category in Table 4. Among these species, A. nerii, Pl. citri and Ps. viburni occur in greenhouses and buildings, while P. pentagona and C. carueli are found outdoors.