Eriophyoid (Acariformes: Eriophyoidea) and Phytoseiid (Parasitiformes: Phytoseiidae) Mite Fauna of Selected Rubus taxa (Rosaceae) with Re-description of Anthocoptes rubicolens Roivainen and Epitrimerus rubi (Domes)

Mite species (Acari: Parasitiformes, Acariformes) living on foliage of brambles (Rubus sp.) were collected in Hungary, Austria and Slovakia. Four eriophyoid mite species (Acariformes: Eriophyoidea) associated with 14 Rubus taxa were identified. Female of Anthocoptes rubicolens Roivainen, 1953 is re-described, the male is described and illustrated from Rubus praecox Bertol., and recorded for the first time from R.bifrons Vest, R.clusii Borbás, R.grabowskii Weihe, R.praecocifrons Király et Trávn., Rubus ser. Rhamnifolii (Bab.) Focke, R.slavonicus Király, Trávn. et Žila, and R. solvensis W. Maurer. Anthocoptes rubicolens is a new species for the fauna of Hungary. Female of Epitrimerus rubi (Domes, 1960) is re-described, male and nymph are described and illustrated from R.bertramii G. Braun. Morphological differences distinguishing these species from the similar Anthocoptes rubi Domes and Epitrimerus gibbosus (Nalepa) are discussed. Out of the four identified phytoseiid species, Phytoseius juvenis Wainstein et Arutunjan (Parasitiformes: Phytoseiidae) was the most frequent predatory mite on the leaves of studied Rubus spp.


Materials and Methods
During botanical excursions in 2019 eriophyoid mites were collected by the second author (G. Király) at localities in Austria, Hungary and Slovakia from bramble (genus Rubus) specimens that showed mite damage symptoms on the foliage (e.g. erineum, leaflet deformation, yellowing and galls). The sampling covered colline and submontane deciduous forest and forest fringes, in some cases coniferous plantations, between 190 and 370 m a.s.l. For each locality, the geo-coordinates were determined using a Garmin GPSMAP64 handheld device in WGS 84 projection. Altogether 12 species of bramble were included in the sampling; further two distinct Rubus taxa could be identified only on the rank of series (see Tables 1, 2 and 3). The nomenclature of Rubus taxa follows generally Kurtto et al. (2010), for some recently described or lectotypified species Király et al. (2015Király et al. ( , 2017 and Sochor et al., (2019). The botanical voucher specimens collected during the studies were generally deposited in the collection of the Hungarian Natural History Museum (BP) and/or in the private herbarium of G. Király. In the course of sampling leaves of brambles were placed in paper and polythene bag and then posted to the corresponding author (G. Ripka) for identification. The leaves collected were examined under a stereo dissecting microscope (Zeiss Stemi 2000-C). All eriophyoid and phytoseiid mites were placed into 88% lactic acid with the aid of a bent insect pin. The clearing of these specimens in lactic acid took considerably longer time, about 2 months at room temperature to obtain the desired extent of clearing. The mites were mounted on microscope slides in Keifer's F-medium due to the superior contrast and longevity provided by this mounting medium (Keifer, 1975;Amrine and Manson, 1996). The slide-preparations were dried for about four weeks at room temperature and then sealed with commercial nail varnish (Upton, 1991). Specimens were examined with the aid of a compound microscope equipped with phase contrast (Nikon Eclipse E600) and a drawing tube (Nikon Y-IDT). A Zeiss Axio Imager.A2 phase-contrast microscope with differential interference contrast (DIC), connected to a computer using Axiovision image analysis software was used for making digital microscopic images on slide mounted specimens. In the supplementary descriptions of Anthocoptes rubicolens and Epitrimerus rubi, for females the measurement ranges and the mean of ten specimens, for males the measurement ranges of five specimens are given. All measurements are given in micrometers (μm) and are lengths except when mentioned otherwise. Classification and terminology of external morphology follow Amrine et al. (2003) and Lindquist (1996), respectively. Phytoseiid mites were identified by the third author, Á. Szabó.
Host plant -Rubus praecox Bertol. (Fam. Rosaceae). The species is one of the commonest brambles in warmer regions of the Carpathian Basin, it often occurs in sunny forest fringes, including plantations, and open scrublands.
Relationship to the host -Females and males of A. rubicolens were collected from the lower surface of the leaves, from the main and secondary veins. It is a less numerous vein-sucking leaf vagrant mite, which caused no damage symptoms on the host plants.
Host plant -Rubus bertramii G. Braun (Fam. Rosaceae). The host plant has a West and Central European distribution from the British Isles to Austria, it grows on acidic soils, mainly in hedges and forest fringes. The species was sampled in Upper Austria at the south-eastern border of the range.
Relationship to the host -Females, males and nymph of E. rubi were collected from the dirty light green erinea, found on the lower surface of the leaves. The mites caused typical erinea on the host plant.
Material examined -the re-described female and described males and nymph among 2 females and 2 males on one slide, 12 July 2019, slide # 1474a. Other specimens were collected -2 slides (# 1474b, # 1474c) from the same host, in the same locality and date, containing (# 1474b) 9 females, 5 males and one larva, and (# 1474c) 3 females and 7 males. They are in the collection of G. Ripka and deposited in the National Food Chain Safety Office, Directorate of Plant Protection, Soil Conservation and Agri-environment, Hungary.
Epitrimerus gibbosus is a similar refuge-inhabiting species causing greyish-white erineum along veins on leaf under and upper side, and leaf margin. E. gibbosus was first reported in Hungary, as Eriophyes gibbosus, by Ambrus (1958) from Rubus fruticosa, R. idaeus, R. sp. and R. thyrsoideus. These records were apparently based on observed host damage symptoms alone, e.g. erineum and gall morphology, and not on the morphological characteristics of the mite species itself, and cannot be verified. Farkas (1966) confirmed E. gibbosus, also as Eriophyes gibbosus, from Rubus spp., and reported it as being a frequent species in Hungary. In the present study it was not a frequent Rubus-dwelling species (Table 1). E. gibbosus was found in considerably high numbers on the underside of the leaves of Rubus ser. Subcanescentes H.E. Weber near Nemesvámos (Hungary). It was difficult to pick the light ochre mites out among the erineum trichomes. E. gibbosus caused mosaic-like greenish-yellow spots on the leaves between and along the veins.
Phyllocoptes gracilis -Roivainen, 1953: 26-27. Eriophyes gracilis -Farkas, 1966: 72. Phyllocoptes gracilis -Amrine and Stasny, 1994. Phyllocoptes gracilis was first reported in Hungary, as Eriophyes gracilis, by Farkas (1966). He described it, and mentioned the damage symptoms caused by the species as whitish spots and leaf torsion. According to Roivainen (1953) who transferred this species from the genus Eriophyes to Phyllocoptes, P. gracilis is a vagrant mite living on the under surface of the leaves. On the other hand Dobrivojević and Petanović (1985) and Domes (1957) gave detailed description of the female and the pronounced symptoms on raspberry caused by P. gracilis. Dobrivojević and Petanović (1985) reported the symptoms as light green to yellow spots, leaf discoloration, mottling, shoot proliferation, fruitfulness, and the natural pubescence was lost on the leaf underside. They stated that P. gracilis was a monophagous species. These leaf symptoms are often attributed to virus. In case of severe infestation the berries may ripen prematurely and dry up (Pye and de Lillo, 2010;Denizhan et al., 2015). Farkas (1966) reported a similar Rubus-inhabiting species, Phyllocoptes rubi Roivainen, 1950 from Hungary, as well, which caused no damage on the leaves of the host. It has 4-rayed empodium, whereas P. gracilis has 5-rayed empodium.
To the authors' knowledge, in Central Europe the present work represents the first attempt to discover the eriophyoid mite fauna having limited ambulatory dispersal capabilities of 14 Rubus taxa in different natural and seminatural habitats.

Family Phytoseiidae Berlese
The present study provides new data to the acarine biodiversity on the foliage of Rubus spp. excluding the cultivated fruit crops (e.g. European blackberry and raspberry). A total of four phytoseiid mite species (Acari: Parasitiformes: Phytoseiidae) were identified. On majority of our bramble leaf samples Phytoseius juvenis was present in considerably high numbers. It was identified from 12 Rubus taxa, while the other three species, Amblyseius andersoni, Anthoseius rhenanus and Neoseiulus cucumeris (Oudemans) were collected only from one Rubus species and in one locality (Tables 2 and 3). In Hungary A. andersoni had been recorded from raspberry (Komlovszky and Jenser, 1987). Szabó et al. (2010Szabó et al. ( , 2013 reported P. juvenis with the highest population density from Rubus spp. in Eger and Badacsony wine growing regions. (Figs 12,13,14,15,16
Besides, tetranychid, tydeid, cunaxid and tarsonemid mites (all Acari: Acariformes) were also collected in our survey, which will be reported in a separate paper.