True bugs (Hemiptera, Heteroptera) as psyllid predators (Hemiptera, Psylloidea)

Abstract Data on natural enemies of psyllids are rare and can usually be found in papers about economically significant species. During an investigation of psyllid fauna in Serbia, natural enemies were investigated, too. True bugs were the most numerous among them. From 28 psyllid species, 21 species of true bugs from families Anthocoridae and Miridae were reared. Seven species of Anthocoridae were identified: Anthocoris amplicollis (Horváth, 1839), Anthocoris confusus Reuter, 1884, Anthocoris nemoralis (Fabricius, 1794), Anthocoris nemorum (Linnaeus, 1761), Orius majusculus Reuter, 1884, Orius minutus (Linnaeus, 1758) and Orius niger Wolff, 1811. The following 14 species of Miridae were identified: Atractotomus mali Meyer-Dür, 1843, Campylomma verbasci (Meyer-Dür, 1843), Deraeocoris flavilinea (A. Costa, 1862), Deraeocoris ruber (Linnaeus, 1758), Deraeocoris lutescens (Schilling, 1836), Heterocordylus genistae (Scopoli, 1763), Hypseloecus visci (Puton, 1888), Malacocoris chlorizans Panzer, 1794, Miris striatus (Linnaeus, 1758), Orthotylus marginalis Reuter, 1884, Psallus assimilis Stichel, 1956, Psallus quercus Kirschbaum, 1856, Psallus flavellus Stichel, 1933 and Pseudoloxops coccinea (Meyer-Dür, 1843). The aim of the research was to provide list of true bugs recorded as predators of psyllids in order to preserve their diversity and significance, especially on cultivated plants.

There is no data on other predatory psyllid species in Serbia.

Methods
Insect material was collected from 419 localities within the whole territory of the Republic of Serbia. Investigations were carried out in the period from 2005 to 2010, in field conditions and in the laboratory of the Faculty of Agriculture in Zemun, University of Belgrade. Locality mapping was carried out in World UTM (Universal Trans-verse Mercator) cartographic projection. Determination of coordinates of investigated localities in the field was carried out using GPS devices Geoexplorer 3 (Trimble) and E-trex Vista Hcx (Garmin), with an accuracy of 3 to 5 meters. Adults of predatory true bugs were collected from psyllid colonies by an aspirator and their larvae were collected together with plant material and psyllids and further reared to adults in laboratory conditions in Petri dishes.
A part of the material is deposited in the first author's collection in the Faculty of Agriculture, University of Belgrade, and another part, in the second author's collection in Natural History Museum, Belgrade.

Results and discussion
We collected and reared 21 true bug species predating on 28 psyllid species (Table  1) from 44 localities ( Fig. 1 and Table 2). The identified true bugs belong to families Anthocoridae and Miridae. A. amplicollis was already reported in Serbia (Protić and Stojanović 2003) but the above mentioned record is the first one in Serbia as a psyllid predator. In Switzerland, it was registered by Wyniger and Burckhardt (2003) in galls of Psyllopsis fraxini. According to available literature data, A. amplicollis has not been published as a predator of P. buxi.  (Wyniger and Burckhardt 2003) and aphids (Herard 1986). In the present paper, reported for the first time as a psyllid predator in Serbia. A. nemoralis is an important component of the natural enemy community in pear and apple orchards where it provides biological control against arthropod pests, particularly psyllids (Horton et al. 2004). Investigating the predator-prey complex of C. pyri in a pear orchard in France, Herard (1986) found that A. nemoralis was the most efficient enemy against this pest. A. nemoralis is mentioned in many papers as a permanent member of biocomplexes of pear psyllids in Europe (Wheeler 2000b, Erler 2004, Sigsgaard et al. 2006. In Turkey, A. nemoralis was an equally present and efficient predator of pear psyllid C. pyri, both in treated and untreated orchards, but still insufficient for its full control (Erler 2004). In Spain, Jauset et al. (2006) determined A. nemoralis as a very efficient predator of C. pyri, both in treated and untreated pear orchards. Now, there is a mass production of A. nemoralis in companies specialized for biological control of harmful insects (Sigsgaard et al. 2006). The same authors reported that A. nemoralis mostly prefers C. pyri to aphids, and that it prefers laying eggs on pear to apple. A. nemoralis is a polyphagous predatory species having psyllids as a usual prey.

2) Anthocoris confusus
It is distributed in Europe and the Mediterranean. From Europe it was introduced into North America in 1963 in order to control pear psyllid C. pyricola, giving satisfactory results (Horton et al. 2004). This species has adapted to this region so well that it has suppressed autochthonous predatory species A. antevolens and A. melanocerus (Herard 1986, Horton et al. 2004). In Serbia, in a pear orchard, Pavićević (1977), Grbić et al. (1989) and Jerinić-Prodanović (2010) note a permanent presence of A. nemoralis, both during vegetation and winter period together with an overwintering adult of C. pyri. A. nemoralis was also reported as a predator of Psyllopsis repens in Serbia (Malenovský and Jerinić-Prodanović 2011). A. nemorum is noted as a predator of many insect species, in the first place Hemiptera, Diptera, eggs of Lepidoptera and mites (Herard 1986, Wheeler 2000b, Sigsgaard et al. 2006, already registered as a predator of both C. pyri and Ps. fraxini (Herard 1986). It is also largely reported as an efficient predator of apple psyllid Cacopsylla mali in Norway (Jonsson 1983). In England, Hodkinson and Flint (1971) determined A. nemorum as a predator of Psyllopsis fraxini collected from ash, while in Germany Novak and Achtziger (1995) registered it as a predator of hawthorn psyllids Cacopsylla melanoneura and C. peregrina. Sigsgaard et al. (2006) note A. nemorum as a more polyphagous species than A. nemoralis. They also determined in experimental conditions that A. nemorum prefers aphids to psyllids, and has a preference for laying eggs on apple rather than on pear.
A. nemorum is an Eurosiberian species, introduced to North America in order to control C. pyricola just like A. nemoralis, but without satisfactory results (Herard 1986).
A. nemorum is reported here for the first time as a predator of psyllids in Serbia.
O. majusculus was registered as a predator of psyllids (Herard 1986). It is noted as a predator of aphids, such as Diuraphis noxia and Schizaphis graminum in Russia, mites in France, whiteflies in greenhouses in Italy and pear psyllid Cacopsylla pyri in France (Péricart 1972, Herard 1986 O. minutus is an extremely polyphagous species distributed in Europe, Siberia, China and Mediterranean region. Many authors determined it as a predator of harmful insect species from a number of orders (Thysanoptera, Diptera, Lepidoptera, Coleoptera and Hemiptera Homoptera). Already reported as a psyllid predator (Herard 1986). In France, Herard (1986) determined O. minutus as a predator of pear psyllids, primarily C. pyri, and hawthorn psyllids. Also in Slovenia, Vrabl and Matis (1977) register it as a predator of C. pyri and C. pyrisuga. In Serbia, Pavićević (1977) and Jerinić-Prodanović et al. (2010) determined O. minutus as a predator of C. pyri in pear orchards. Malenovský and Jerinić-Prodanović (2011) also found it as a predator of Ps. repens. In Croatia, Arčanin and Balarin (1972)  O. niger is widespread in Western Palaearctic, very rare in the Mediterranean region, also reported from China. It is a very polyphagous species, preying on aphids, psyllids, whiteflies, thrips, larvae of noctuids, mites (Péricart 1972, Herard 1986, Protić 1993. In south France, Herard (1986) determined Orius niger on pears as a predator of Cacopsylla pyri, but also collected it in a large number from Trioza urticae from nettle, which was surrounding the pear orchards. In Croatia, O. niger was determined along with O. minutus on Panonychus ulmi in an apple orchard (Arčanin and Balarin 1972).

8) Atractotomus mali
First record of A. mali as a predator of C. picta. The above mentioned data are the first ones for A. mali as a psyllid predator in Serbia. (Meyer-Dür, 1843 C. verbasci is a zoophytophagous species preying on apple aphids, pear psyllids, codling moth, thrips and mites (Wheeler 2000b). Its most common prey among insects are Aphis pomi and Cacopsylla mali, and among mites Panonychus ulmi and Tetranychus urticae (Hagen et al. 1999, Wheeler 2000b, Bradley 2007.

9) Campylomma verbasci
However, if there is a lack of prey, it can feed on apple fruits, rarely pear, causing the harm to their aesthetic value. Therefore, C. verbasci is a significant fruit pest in Canada (Hagen et al. 1999, Wheeler 2000a, Bradley 2007. Erler (2004) reported the presence of C. verbasci as a predator of C. pyri in treated and untreated pear orchards in Turkey, and Harizanova et al. (2012) mentioned it on Acizzia jamatonica in Bulgaria.
Already known in Serbia (Protić 1993) but in our investigations registered for the first time as a predator of psyllids in this country. D. flavilinea is reported so far as a predator of psyllids (Jerinić-Prodanović and Protić 2011, Simov et al. 2012). Until 1980's, it was known only from Sicily, from where it has spread to Central Europe where it is now considered as an invasive species (Rabitsch 2008). As a predator of psyllids, it has been known in Serbia since 2011 (Jerinić-Prodanović and Protić 2011). Already mentioned as a predator of C. pyri (Herard 1986). It also preys on younger caterpillar instars of some butterflies, mites and various other small insects in apple orchards, on Rubus spp. and Urtica spp. as well as on aphids on Corylus spp. (Herard 1986).

11) Deraeocoris
Reported as a predator of A. jamatonica (Harizanova et al. 2012) in Bulgaria and C. pyri in Serbia (Jerinić-Prodanović et al. 2010). D. lutescens is a Mediterranean species, distributed also in small numbers in Central Europe. Known mainly as an egg predator of pear psyllid C. pyri and hawthorn psyllid C. crataegi (Herard 1986). It is also reported as a predator of aphids and mite Panonychus ulmi in apple orchards in Croatia (Arčanin and Balarin 1972) and in pear orchards as a predator of C. pyri in France and Turkey (Herard 1986, Erler 2004.

12) Deraeocoris
D. lutescens has been already registered in Serbia (Protić 1993) but here is reported for the first time as a predator of psyllids in this country.
H. genistae is mentioned in the literature as a beneficial insect being a predator of psyllids both in larval and adult stage. It is registered as a predator of various other insects (Protić 1993(Protić , 1998. In the present paper, we report H. genistae for the first time as a predator of psyllids in Serbia. A general predator on aphids, psyllids, eggs and larvae of leaf miner moths (Wheeler 2000b, Wyniger andBurckhardt 2003). In Croatia, it is registered as a predator of Panonychus ulmi in apple orchards by Arčanin and Balarin (1972).

14) Hypseloecus visci (Puton
Malacocoris chlorizans has been already registered in Serbia (Protić 1998) but in the present paper is reported for the first time as a predator of psyllids in this country. O. marginalis is registered as a predator of aphids and psyllids (Wheeler 2000b). In Finland and Russia, it was mentioned as a predator of C. mali (Jonsson 1983).

16)
Registered in Serbia (Protić 2011) but here reported for the first time as a psyllid predator.   So far known as a predator of aphids, psyllids, thrips, spiders and eggs of various insects (Protić 1998).

18) Psallus (Hylopsallus) assimilis
Registered in Serbia (Protić 2011) but here reported for the first time as a psyllid predator in this country. Most of predatory true bugs are registered on deciduous perennial plants. We found the highest number of predatory true bugs on psyllids which overwinter on host plant and have more than one generation per year, e.g. Cacopsylla pyri, Psyllopsis fraxinicola and Ps. discrepans. On each of them, seven predatory true bugs were registered. Species from the genus Psallus were registered as predators only of psyllid genus Psyllopsis.

21) Pseudoloxops coccinea
Further investigations are necessary for the preservation of known beneficial predatory true bugs and finding of new ones, potentially usable for biological control on economically significant psyllid species.