Deuterogyny and the Association of Two Vagrant Eriophyoid Mites (Acariformes, Eriophyoidea) with the Host-plant Generative Organs of Two Broad-leaved Trees in North-West Russia

© 2023 Academia Sinica, Taiwan Open Access Deuterogyny and the Association of Two Vagrant Eriophyoid Mites (Acariformes, Eriophyoidea) with the Host-plant Generative Organs of Two Broad-leaved Trees in North-West Russia Philipp E. Chetverikov1,2,* , Alexey G. Desnitskiy2, Pavel B. Klimov3, Sebahat K. OzmanSullivan4, Anna E. Romanovich2, and Sogdiana I. Sukhareva2 1Zoological Institute, Russian Academy of Sciences, Universitetskaya nab. 1, 199034, St. Petersburg, Russia. *Correspondence: E-mail: [email protected] (Chetverikov) 2Saint-Petersburg State University, Universitetskaya nab. 7/9, 199034, St. Petersburg, Russia. E-mail: [email protected] (Desnitskiy); [email protected] (Romanovich); [email protected] (Sukhareva) 3X-BIO institute, Tyumen State University, 6 Volodarskogo Str. Tyumen, Russia 625003. E-mail: [email protected] (Klimov) 4Ondokuz Mayis University, Faculty of Agriculture, Department of Plant Protection, 55139 Samsun, Turkey. E-mail: [email protected] (Ozman-Sullivan) Received 5 August 2022 / Accepted 4 May 2023 / Published 21 July 2023 Communicated by Benny K.K. Chan Phytoparasitic mites of the superfamily Eriophyoidea Nalepa live and feed on mature leaf surfaces, between leaf bud scales, and (though less commonly) on flowers or fruits. In this study, we focused on the seasonal associations of two eriophyoid species, Shevtchenkella serrata (Nalepa 1892) with the Norway maple tree (Acer platanoides L.), and Brevulacus reticulatus Manson 1984 with the common oak (Quercus robur L.). These species have complex life cycles with two morphologically different, seasonal female forms, the protogyne and deutogyne. In B. reticulatus, both forms retain all the major generic characteristics but in S. serrata only the protogynes conform to the diagnosis of Shevtchenkella, whereas the deutogynes have the typical traits of Anthocoptes. We confirmed the conspecificity of the protogynes and deutogynes of both eriophyoid species by sequencing a barcode fragment of the Cox1 gene from which we obtained four pairwise identical sequences: ON920305/ON920306 (S. serrata) and ON920307/ ON920308 (B. reticulatus). In addition, taxonomical studies on Shevtchenkella and Brevulacus resulted in new synonymies and combinations: (1) Oxypleurites obtusus Roivainen 1947 is considered a deutogyne of S. serrata and treated as a junior synonym of S. serrata; (2) two rhyncaphytoptine species from North America are transferred from the genus Rhyncaphytoptus to Brevulacus: B. albus (Keifer 1959) comb. nov. and B. atlanticus (Keifer 1959) comb. nov.; and (3) one species, B. salicinus Soika et al. 2017, is excluded from Brevulacus and transferred to Rhyncaphytoptus: Rhyncaphytoptus salicinus (Soika et al. 2017) comb. nov. Apart from distinct morphological deuterogyny in S. serrata and B. reticulatus, we observed the persistent association of S. serrata with the generative organs of the maple tree, A. platanoides, leading to transmission to the next host generation via the seed-containing winged fruits (samaras) and subsequent colonization of seedlings. In B. reticulatus, similar synchronization with host-plant dispersal was not detected; however, in mid-summer, temporary colonization of immature acorns and feeding was observed. Additional studies conducted in various ecosystems and including different ecological groups of plants, especially anemochorous plants, are needed to estimate the frequency of the association of eriophyoids with plant generative organs, seeds and seedlings to better understand what role in mite ecology such associations may play. Key words: Seasonal dimorphism, Herbivore, Dispersal, Phytophagy Citation: Chetverikov PE, Desnitskiy AG, Klimov PB, Ozman-Sullivan SK, Romanovich AE, Sukhareva SI. 2023. Deuterogyny and the association of two vagrant eriophyoid mites (Acariformes, Eriophyoidea) with the host-plant generative organs of two broad-leaved trees in North-west Russia. Zool Stud 62:35. doi:10.6620/ZS.2023.62-35. Zoological Studies 62:35 (2023) doi:10.6620/ZS.2023.62-35 1 © 2023 Academia Sinica, Taiwan BACKGROUND The superfamily Eriophyoidea is a highly diverse, ancient lineage of phytoparasitic acariform mites (Lindquist 1996; Sidorchuk et al. 2015). They are the most difficult group of mites for taxonomists to classify due to their microscopic size (most species 200‒300 µm), greatly simplified morphology and numerous undescribed species (Nuzzaci and Alberti 1996; Amrine et al. 2003). An additional complication comes from a type of seasonal dimorphism, seen in ~65 of the ~4800 total described eriophyoid species, known as deuterogyny, a complex life cycle with two morphologically different forms of female, a protogyne and a deutogyne (Keifer 1942; Hall 1967; Manson and Oldfield 1996; Guo et al. 2015; Marini et al. 2021). Morphologically these two forms can appear nearly indistinguishable in some taxa, or so divergent that some have been assigned to different genera and even subfamilies, and only with the use of molecular data were they resolved as seasonal morphotypes of the same species (Guo et al. 2015; Druciarek et al. 2016; Chetverikov et al. 2018; Yin et al. 2020). Most species of eriophyoid mites are obligate symbionts of plant leaves or buds, with only a small proportion of their contemporary diversity strongly associated with flowers and fruits (Oldfield 1996; Amrine et al. 2003). Chetverikov et al. (2022) showed that in the system comprising the phytoparasite, Shevtchenkella serrata Nalepa (Eriophyidae) on the Norway maple, Acer platanoides L., the association of the eriophyoid with maple fruits facilitated the eriophyoid’s vertical transmission. That is, it allowed the eriophyoid to exploit the host’s dispersal mechanism and colonize the next generation of hosts. In this paper, we report advances in the same line of research by complementing our previous findings on the ecology of S. serrata on A. platanoides with new data on seasonal changes in populations of B. reticulatus from Q. robur. More specifically, we present novel data on seasonal morphological dimorphism in Shevtchenkella and Brevulacus species collected from North-West Russia, report new synonymies for several species in these two genera, and discuss the ecological role of the association of eriophyoid mite species with the plant generative organs of broad-leaved, boreal trees. MATERIALS AND METHODS Morphology Eriophyoid mites were collected from Acer platanoides and Quercus robur from 2018 to 2022 in Saint-Petersburg and Vyritza (Leningrad Prov.) in North-West Russia. All eriophyoids were removed from separately bagged, freshly collected plant material using a fine minuten pin and a dissecting microscope, then placed in Eppendorf tubes filled with 96% ethanol. The mites were mounted in a modified Berlese medium with iodine (Amrine and Manson 1996) and cleared on a heating block at 90°C for 3–5 hours. Slide-mounted specimens were examined with a Leica DM2500 light microscope (LM) equipped with differential interference contrast (DIC) and phase contrast (PC), and photographed with a ToupCam (UCMOS09000KPB) digital camera. Images and specimens were analyzed and measured using ToupTek ToupView software. In the mite descriptions, the measurements are given as ranges in micrometers (μm) except when mentioned otherwise. Classification and terminology of external morphology follow Amrine et al. (2003) and Lindquist (1996). Drawings of mites were sketched in pencil using a video projector (Chetverikov 2016), then scanned and finalized in Adobe Illustrator CC 2014 using a Wacom Cintiq 16 (DTK1660K0B) interactive display and Wacom Pro Pen 2. DNA extraction and sequencing For DNA extraction, 1‒3 specimens of each species were crushed with a fine pin in a 2 μl drop of distilled water on a cavity well microscope slide. The drop was then pipetted into a thin-walled PCR tube with 30 μl of 5% solution of Chelex® 100 Resin (Bio-Rad) before being heated three times for 5 minutes at 95°C. The DNA in the solution above the settled Chelex® granules was used for PCR amplification of the fragment of mitochondrial cytochrome oxidase c subunit I gene (Cox1). The thermocycling profiles and primers for PCR were those specified by Chetverikov et al. (2021a). After amplification, 4 μl of each reaction product was mixed with 0.5 μl of SYBR Green I (Lumiprobe) and analyzed by electrophoresis on 1% agarose gel to assess the product size and concentration. DNA sequences were obtained using BigDye Terminator v.3.1 chemistry (Applied Biosystems, Foster City, CA, USA) and a 3500xl Genetic Analyzer (Applied Biosystems). Trace files were checked and edited using GeneStudioTM Professional 2.2.0.0. Field observations Every week from July 2020 to October 2021 (excluding the period from mid-December to March when night frosts were common, and the leaves and samaras (winged fruits) that had fallen on the ground page 2 of 18Zoological Studies 62:35 (2023) © 2023 Academia Sinica, Taiwan became embedded in the frozen leaf litter) (see Chetverikov et al. (2022) for the mite survey in 2020 to 2021), and every two weeks from March 2022 to August 2022, we sampled eriophyoid mites from 15 mature trees, saplings and samaras of Norway maple (A. platanoides) growing in a wooded area (59°23'43.5"N, 30°18'00.6"E) in the village of Vyritza in the Leningrad region of Russia. We also sampled eriophyoids from two oak trees (Q. robur) every 2–3 weeks during the warm seasons of 2021 and 2022, one growing in the same area in Vyritza from which the mites were collected from the maple trees, and the other (59°56'30.3"N 30°18'08.9"E) near the main building of the Zoological Museum in the center of Saint-Petersburg. We inspected both the vegetative and generative organs of the host plants, including both maple samaras and oak acorns attached to the trees as well as those found on the ground. Additionally, we partially uprooted seedlings that germinated in the springs of 2021 and 2022, and checked them for the presence of eriophyoid mites. RESULTS TAXONOMY Family Eriophyidae Nalepa Subfamily Phyllocoptinae Nalepa Tribe Anthocoptini Amrine & Stasny Genus Shevtchenkella Bagdasarian 1978 Shevtchenkella serrata (Nalepa 1892) (Figs. 1, 2, 3) Tegonotus serratus – Nalepa 1892: 333–335, pl. 13, figs. 7b, 8, 9. Oxypleurites serratus – Nalepa 1898: 68; Roivainen 1947: 39, fig. 22. Oxypleurites obtusus – Roivainen 1947: 38, fig. 21 (new synonymy). Shevtchenkella serrata – Petanović, Stanković 1999: 67. PROTOGYNE (n = 10), supplementary description (Fig. 1). Body fusiform, subtriangular, whitish or slightly yellowish, 180–207, 72–79 wide at the level of seta c2. Prodorsal shield semicircular, 49–56, 70–77 wide, with large apically rounded frontal lobe 10–12, 18–22 wide. Posterolateral margin of prodorsal shield with indistinct acuminate projection (Fig. 1C). Cuticle of prodorsal shield with numerous round microgranulations. Median line absent, two faint incomplete admedians and traces of putative incomplete submedians present on prodorsal shield (Fig. 1D). Epicoxal areas with microtubercules and thin striae. Scapular setae sc 5–8, 25–28 apart. Gnathosoma short, directed obliquely forward, 18–21, ep 2–3, d 5–7, ν 0.5–1; chelicera 13–15. Leg I 31–34, femur 10–12, bv 9–11; genu 5–6, l'' 17–22; tibia 7–8; l' 2–4; tarsus 5–6, u' 2–3, slightly angled, ft' 17–22, ft'' 25–29, solenidion ω 6–7 with spherical knob apically, empodium (em) 6–7, 4/4-rayed, each ray except of the rays of apical pair with one subray each (Fig. 1A). Leg II 30–33, femur 10–11, bv 8–11; genu 5–6, l'' 3–4; tibia 7–8; tarsus 5–6, u' 2–3, slightly angled, ft' 4–6, ft'' 20–24, solenidion ω 6–7 with spherical knob apically, empodium (em) 6–7, 4/4-rayed, similar to empodium I. Infracapitular plate rounded anteriorly, microtuberculated, 11–13, 15–18 wide; sternal line distinct, 10–12. Coxal plates with numerous microtubercles and thin striae. Setae 1b 6–8, 13–14 apart; 1a 16–19, 9–11 apart; 2a 31–38, 27–28 apart; 2–3 incomplete and 6–8 complete coxigenital annuli before epigynium. External genitalia. Genital coverflap rounded posteriorly, 10–13, 23–25 wide, with 10–12 longitudinal ridges; setae 3a 10–12, 16–18 apart; basal coverflap and adjacent area (homologous to the pregenital plate sensu Flechtmann et al. 2015) with short curved lines and microtubercles. Opisthosoma with 19–20 dorsal and 65–74 microtuberculated ventral annuli. Anterior 12–13 dorsal annuli with lateral spinelike projections; 2nd, 3rd, 4th, 5th, 7th and 9th dorsal annulus with a small subtriangular medial plate slightly overlapping next dorsal annulus. Dorsal annuli with numerous thin longitudinal ridges. Setal lengths: c2 23– 28, d 60–68 very thin in distal half, e 8–12, f 20–25, h1 about 0.5, h2 60–70; 11–12 annuli from the rear margin of coxa II to c2; 12–14 annuli between c2 and d; 17–20 annuli between d and e; 18–23 annuli between e and f; 5–6 annuli between f and h2. Male (n = 3): Body shaped similarly to protogynes but notably shorter, 141–152, 69–75 wide at the level of seta c2. Opisthosoma with 19–21 dorsal and 66–69 ventral annuli. Genital area 11–13, 20–22 wide; 3a 9–11, 16–17 apart. GenBank data (protogynes): ON920305 (Cox 1). Material examined: Numerous adults and immatures from the slide series E4701, E4702 and E4703 collected on 17 July 2021 from the lower leaf surfaces of Acer platanoides L. (Sapindaceae) in Russia: Leningrad Prov., Gatchina distr., vil. Vyritza, coll. P.E. Chetverikov, slide series, mites in vials with 96% ethanol. All slides and ethanol material (mites in vials filled with 96% ethanol) have been deposited in the Acarological Collection of the Zoological Institute of the Russian Academy of Sciences (ZIN RAS) in Saint-Petersburg, Russia. Remarks: The protogyne of S. serrata has been frequently reported as a vagrant on the lower leaf surface of various Acer spp. in different European countries (Petanović and Stanković 1999; Farkas 1965; Roivainen 1947; Skoracka et al. 2005). The protogynes from our material were very similar to those from page 3 of 18Zoological Studies 62:35 (2023) © 2023 Academia Sinica, Taiwan Finland (Roivainen 1947, p. 39, fig. 22), except that our specimens had a larger number of ventral annuli (65–74 vs. 50). DEUTOGYNE (n = 10, Figs. 2, 3): Body elongated, non-flattened, bright orange, 229–250, 62–67 wide at the level of seta c2. Prodorsal shield subtriangular 41–46, 53–58 wide, with acuminated frontal lobe 8–10, 10–12 wide. Cuticle of prodorsal shield with numerous tiny round cavities (putative pores leading to wax glands, Fig. 3A). Distinct curved transverse line resembling a flattened letter “U” present between tubercles of sc. Longitudinal lines (median, admedians and submedians) absent. Epicoxal areas smooth. Scapular setae sc 11–15, 24–27 apart. Gnathosoma directed obliquely forward, 19–21, ep 2–3, d 6–8, ν about 0.5; chelicera 15–17. In two specimens, the outlines of a short suboral fork (sensu Chetverikov and Bolton 2016) embedded in the ventral wall of the proboscis were discernible (Fig. 3F, G, H). The fork was comprised of a stalk about 3 (Fig. 3H, arrow) and two Fig. 1. DIC LM images of protogynes of Shevtchenkella serrata. A, empodium I. B, tarsal solenidion I. C, lateral view of opisthosoma. D, prodorsal shield. E, dorsal view of protogyne. F, dorsal view of male. G, ventral view of protogyne. Scale bars: A, B = 3 µm; C = 20 µm; D = 15 µm; E, F = 70 µm, G = 30 µm. page 4 of 18Zoological Studies 62:35 (2023) © 2023 Academia Sinica, Taiwan Fig. 2. Drawings of deutogyne of Shevtchenkella serrata. A, dorsal view of body. B, leg II. C, leg I. D, empodium I. E, tarsal solenidion I. F, internal genitalia. G, prodorsal shield. H, coxigenital area. Scale bars: A, H = 25 µm; B, C, D, E, F = 10 µm; G = 15 µm. page 5 of 18Zoological Studies 62:35 (2023) © 2023 Academia Sinica, Taiwan leaf-shaped plates about 2 × 1–1.5 wide (Fig. 3F, G, H, arrows), and similar to suboral forks described earlier in other eriophyoids (Chetverikov and Bolton 2016). Leg I 37–40, femur 11–12, bv 10–13; genu 5–6, l'' 12–18; tibia 8–9, l' 4–5; tarsus 6–8, u' 3–5, ft' 19–24, ft'' 23–28, solenidion ω 8–9 with spherical knob apically, empodium (em) 8–10, 4/4-rayed, rays and medial shaft of the empodium wide, flattened. Leg II 36–38, femur 10–12, bv 10–12; genu 5–6, l'' 7–9; tibia 7–9; tarsus 6–7, u' 3–4, ft' 5–7, ft'' 16–22, solenidion ω 8–9 with spherical knob apically, empodium (em) 8–10, 4/4-rayed, similar to empodium I. Infracapitular plate rounded anteriorly, smooth, 12–14, 15–17 wide; sternal line distinct, 10–12. Coxal plates without distinct ornamentation. Setae 1b 7–10, 12–14 apart; 1a 18–24, 10–11 apart; 2a 38–47, 26–28 apart; 2–3 incomplete and 5–6 complete coxigenital annuli before epigynium. External genitalia: Genital coverflap oblong, 12–14, 23–25 wide, with 10–11 longitudinal ridges; setae 3a 14–17, 14–16 apart; basal coverflap with round microtubercles. Internal genitalia (n = 4). Spermathecae globose, about 6–7 in diameter; spermathecal tubes short, subspherical, about 1.5–2; spermathecal process not apparent; longitudinal bridge 9–11, anterior Fig. 3. DIC LM images of deutogyne of Shevtchenkella serrata. A, prodorsal shield; B, empodium I; C, tarsal solenidion I; D, dorsal view of entire mite; E, ventral view of entire mite; F, G, H, gnathosoma shown in three different planes from dorsal (F) to ventral (H). White arrows in Fig. 3. F, G, H indicate putative suboral fork. Scale bars: A = 15 µm; B, C = 10 µm; D, E = 60 µm; F, G, H = 5 µm. page 6 of 18Zoological Studies 62:35 (2023) © 2023 Academia Sinica, Taiwan (transverse) genital apodeme bell-shaped, with 2–3 longitudinal ridges on each side. Opisthosoma with 15–18 dorsal and 64–73 ventral annuli. Dorsal annuli slightly curved and smooth. Ventral annuli in anterior half of opisthosoma smooth or with traces of very faint microtubercles, ventral annuli in posterior half of opisthosoma bearing more distinct subconical microtubercles; last 3–4 ventral telosomal annuli with elongate microtubercles. Setal lengths: c2 20–26, d 58–69 very thin in distal half, e 10–12, f 29– 35, h1 about 0.5, h2 85–98; 12–14 annuli from the rear margin of coxa II to c2; 13–15 annuli between c2 and d; 16–19 annuli between d and e; 18–22 annuli between e and f; and 4–5 annuli between f and h2. GenBank data (deutogynes): ON920306 (Cox 1). Material examined: Numerous females from the slide series E4677 and E4678, collected on 15 August 2021 from the lower leaf surface of Acer platanoides L. (Sapindaceae) in Russia: Leningrad Prov., Gatchina distr., vil. Vyritza, coll. P.E. Chetverikov. All slides and ethanol material (mites in vials filled with 96% ethanol) have been deposited in the Acarological Collection of ZIN RAS (Saint-Petersburg, Russia). Remarks: Using the morphological key of Amrine et al. (2003), rather than Shevtchenkella, the deutogyne conforms to Anthocoptes, a genus in the same subfamily, Phyllocoptinae. The tribes that Shevtchenkella and Anthocoptes belong to (Tegonotini and Anthocoptini, respectively) are primarily differentiated by the presence or absence of lateral lobes or spine-like projections, as shown in the protogyne of S. serrata (Fig. 1C, E, F), but absent in the deutogyne (Fig. 3). In contrast to the protogynes, the deutogynes have smooth dorsal annuli without lateral projections and medial plates, smooth prodorsal shield, flat paddle-like empodia, and more elongated body proportions. The deutogynes from our material very closely approximate Oxypleurites obtusus Roivainen 1947 which was described in sympatry with S. serrata from the lower leaf surface of A. platanoides in Finland, except that they were notably larger (229–250 vs. 160–175) and had an acuminated vs. blunt frontal lobe. We consider Oxypleurites obtusus Roivainen 1947 to be the deutogyne of S. serrata and treat it as a junior synonym of S. serrata (Nalepa 1892). Family Diptilomiopidae Keifer Subfamily Rhyncaphytoptinae Keifer Genus Brevulacus Manson 1984 Diagnosis: Mites of this genus have a complete set of all common opisthosomal, prodorsal, leg and gnathosomal setae, dorso-ventrally differentiated opisthosomal annuli, large anteriorly notched frontal lobe of prodorsal shield, and bushy undivided empodia with 3–7 well-developed secondary rays on all primary empodial rays, except the terminal pair. Remarks: Manson (1984) reported that the tarsal solenidia ω are displaced laterally in the type species, B. reticulatus. However, considering the artifact positions of setae u′ and empodium in the drawings from the original description (Manson 1984, fig. 36F, 43F), and the fact that different authors observed normal positioning of ω in this species (Pye 2012, this paper), we do not consider this trait to be either a true characteristic of B. reticulatus or a differentiating character of the genus Brevulacus. Species included: Brevulacus reticulatus Manson 1984 (type species) from Quercus sp. in New Zealand, B. jilinensis Xue et al. 2009a from Quercus sp. in China, B. carpathicus Ripka 2011 from Quercus petraea (Matt.) Liebl. in Hungary, B. extensus Pye 2012 from Quercus robur L. in Great Britain, B. albus (Keifer 1959) n. comb. from Quercus alba L. in USA, and B. atlanticus (Keifer 1959) n. comb. from Ulmus americana L. in USA. Remarks: Twenty five years before Manson (1984) erected the genus Brevulacus and described the type species, B. reticulatus, from Quercus sp., Keifer (1959) described two Rhyncaphytoptus species from the northern USA, R. albus from Quercus alba L. (Fagaceae) and R. atlanticus from Ulmus americana L. (Ulmaceae). These two Rhyncaphytoptus species are very close morphologically to B. reticulatus, having almost identical net-like ornamentation of the prodorsal shield (Fig. 4 A, B, E, F), and possessing large bushy empodia and a broad notched frontal lobe. We transfer these two species from g. Rhyncaphytoptus to g. Brevulacus because we consider them members of the same putatively monophyletic group of rhyncaphytoptines with a notched frontal lobe defined by Manson (1984) as the genus Brevulacus. Another Brevulacus species (B. salicinus) was described from Salix sp. (Salicaceae) from Iran (Soika et al. 2017). However, this species does not conform to the generic diagnosis of Brevulacus because it has an acuminate frontal lobe of the prodorsal shield (Fig. 4D). Additionally, it lives on Salix sp. (Salicaceae), in contrast to most other Brevulacus spp. that are associated with oaks (Fagaceae). Morphologically, this species fits the diagnosis of the genus Rhyncaphytoptus Keifer. Therefore, we propose a new combination, Rhyncaphytoptus salicinus (Soika et al. 2017) comb. nov. Seven Rhyncaphytoptus species are known from willows (Salix spp.) worldwide, including R. acilius Keifer 1939, R. alsasuensis Roivainen 1953, R. capreae Liro 1942, R. funali Xue et al. 2009a, R. salicifoliae Keifer 1939, R. salicis-glaucae Roivainen 1950 and R. tibetisalisis Song, Xue & Hong 2009. Future comparison is needed to determine if “salicinus” page 7 of 18Zoological Studies 62:35 (2023) © 2023 Academia Sinica, Taiwan is a junior synonym of one of these species or a true species. Hosts: Oaks (Fagaceae: Quercus) and elm (Ulmaceae: Ulmus). Relation to hosts: All known species of Brevulacus are vagrant and cause no visible damage to their hosts. Brevulacus reticulatus Manson 1984 Brevulacus reticulatus Manson 1984: 87–88, fig. 32–39 (protogyne), fig. 40–46 (deutogyne). B. reticulatus Skoracka et al. 2005: 25; Xue et al. 2009b: 33; Ripka 2011: 133; Pye 2012: 61. Remarks: Manson (1984) found the type species, B. reticulatus, on Quercus sp. in three cities of New Zealand (Levin, Upper Hutt and Christchurch) and reported on its seasonal dimorphism. Since then this species has been recorded many times on Quercus spp. in different European countries and in China. According to Breitwieser et al. (2010), all oak species currently known from New Zealand are non-indigenous. Colonists introduced them, presumably from Europe most likely along with different associated symbionts, including B. reticulatus. Below we give supplementary data on the protogyne and deutogyne of B. reticulatus, based on material collected from Q. robur in NorthWest Russia. PROTOGYNE (n = 10), supplementary description (Figs. 4B, 5, 6I, M–T). Body fusiform, yellowish, 238–255, 83–89 wide at the level of seta c2. Prodorsal shield subtriangular, 42–47, 63–70 wide, with large apically notched smooth frontal lobe 10–12, 15–19 wide. Prodorsal shield ornamentation net-like with distinct cells between median, admedian and submedian lines. Median line complete, entire (Figs. 4B, 5A, C). Scapular setae sc 25–29, 33–37 apart, directed up and forward. Gnathosoma large, directed obliquely downward, 41–50, ep 3–4, d 10–13, ν 5–7, angled. Leg I 43–46, femur 11–13, bv 12–16; genu 5–7, l'' 33–40; tibia 9–10, l' 9–12; tarsus 7–8, u' 4–6, ft' 24–30, ft'' 26–32, solenidion ω 9–10 with small knob apically, empodium (em), 7–9, 8-rayed, each ray, except of the rays of apical pair, with 3 to 7 subrays (Fig. 6M– T). Leg II 40–43, femur 10–12, bv 10–14; genu 5–6, l'' 17–22; tibia 8–10; tarsus 7–8, u' 4–6, ft' 9–13, ft'' 27–31, solenidion ω 9–11 with small knob apically, empodium (em) 7–9, 7-rayed, similar to empodium I. Infracapitular plate rounded anteriorly, smooth, 11–12, 22–25 wide; sternal line distinct 9–11. Coxal plates striated. Setae 1b 14–18, 11–13 apart; 1a 26–33, 10–12 apart; 2a 58–70, 27–31 apart; 12–17 incomplete coxigenital annuli bearing microtubercles before epigynium. External genitalia. Genital coverflap subtriangular, smooth, 9–11, 31–35 wide, preceded by distinct ribbon-shaped pregenital plate (sensu Flechtmann et al. 2015; Fig. 5D, arrow); setae 3a 34–45, 23–25 apart. Opisthosoma with 49–57 microtuberculated dorsal annuli forming three faint longitudinal ridges and 87–107 microtuberculated Fig. 4. Prodorsal shields in females of Brevulacus reticulatus Manson 1984 (protogyne, A, from original description. B, this paper), B. extensus Pye 2012 (C), Rhyncaphytoptus salicinus (Soika et al. 2017) n. comb. (D), B. albus (Keifer 1959) n. comb. (E), B. atlanticus (Keifer 1959) n. comb. (F), B. carpathicus Ripka 2011 (G), and B. jilinensis Xue, Song & Hong 2009 (H). All except figure 4B redrawn from original descriptions. page 8 of 18Zoological Studies 62:35 (2023) © 2023 Academia Sinica, Taiwan ventral annuli. Setal lengths: c2 36–43, d 46–52, e 29–34, f 46–52, h1 4–5, h2 70–85, all opisthosomal setae, except c2 and h1, very thin in distal half; 18–22 annuli from the rear margin of coxa II to c2; 16–22 annuli between c2 and d; 13–16 annuli between d and e; 35–41 annuli between e and f; 5–6 annuli between f and h2. Paired cuticular tubes associated with rectum (the elements of anal secretory apparatus, sensu Chetverikov et al. 2019) were clearly visible under the telosomal cuticle in all studied protogynes (not shown). Male (n = 6): Body shape similar to protogynes but notably shorter, 178–202, 70–73 wide at the level of seta c2. Prodorsal shield ornamentation similar to those in protogynes. Opisthosoma with 51–56 dorsal and 81–87 ventral annuli. Genital area 12–15, 20–24 wide; 3a 22–26, 17–19 apart; eu 0.5–1. Paired cuticular tubes associated with rectum (the elements of anal secretory apparatus sensu Chetverikov et al. 2019) were observed in all studied males (not shown). GenBank data (protogynes): ON920307 (Cox 1). Material examined: Numerous adults collected on 10 June 2022 from the lower surfaces of leaves of Quercus robur L. (Fagaceae) in RUSSIA: Leningrad Prov., Gatchina distr., vil. Vyritza, coll. P.E. Chetverikov, slide series, mites in vials with 96% ethanol. All slides and ethanol material have been deposited in the Acarological Collection of ZIN RAS (Saint-Petersburg, Russia). Remarks: The protogynes in our study are very similar to those described by Manson (1984) from New Zealand, except that our specimens have a larger number of ventral annuli (87–107 vs. 70–76, respectively) and longer prodorsal shield (42–47 vs. 31–39, respectively); the difference between the Fig. 5. DIC microphotographs of protogyne of Brevulacus reticulatus Manson 1984. A, dorsal view of body. B, ventral view of body. C, prodorsal shield. D, genital area (arrow indicates pregenital plate). Note: setae sc in live mites are directed anteriad (Fig. 5A), in contrast to many slide-mounted mites with artifact backward directed sc (Fig. 5C). Scale bars: A, B = 40 µm; C, D = 15 µm. page 9 of 18Zoological Studies 62:35 (2023) © 2023 Academia Sinica, Taiwan mandshuricum Maxim., A. campestre L., A. barbinerve Maxim., A. palmatum Thunb., A. tegmentosum Maxim., A. pseudosieboldianum (Pax) Kom.) and the other eight germinated in the spring of the first year (A. pseudoplatanus L., A. mono Maxim. ex Rupr., A. platanoides L., A. ginnala Maxim., A. saccharum Marshall, A. semenovii Regel & Herder, A. tataricum L., A. rubrum L.). The 14 tested maple species also differed in the proportion of successfully overwintered seeds, with the minimum values for seed germination about 50% in A. saccharum and A. rubrum. Apparently the host plant species with a single season dormancy period and a high germination rate are the most likely to support the development of overwintering associations of eriophyoids with seeds in regions with a cold climate. Besides maples, various deciduous broadleaf trees of the genera, Fraxinus, Tilia and Ulmus, possess samaras, and taxa with rapidly germinating seeds could have similar “mite-samara” associations to that we observed on A. platanoides. In S. serrata, the hibernation of deutogynes on seeds fallen on the ground is an additional diapause mode because typically eriophyoids on this host overwinter on the young twigs. Interestingly, hibernation on seeds implies a long period of survival in leaf litter on the soil and spring migration from the germinating samara to the developing seedling. Data from literature suggest that many eriophyoid species have a period in their life cycle when they are closely associated with soil or even live on the plant parts at the soil level. Although eriophyoids have not been reported as feeding on roots, they have been found feeding and overwintering on below-ground buds of stems and leaves on a rhizomatous perennial, or on modified leaves such as bulb scales (Krantz and Ehrensing 1990; Petanović et al. 1997; Asadi et al. 2014; Chetverikov et al. 2021b). These reports may indicate an underestimated role of the soil in the ecology of eriophyoid mites. Association with soil in extant eriophyoids could be some kind of an ecological throwback to when nematalycid-like ancestors of the eriophyoids started developing associations with the above-ground organs of plants (Bolton et al. 2017 2018; Klimov et al. 2018 2022). A search for eriophyoids in soil and leaf litter samples and careful investigations of the invertebrates associated with plant roots and mycorrhizae, especially in ancient intact biomes like the forests of Amazonia, Kalimantan and Australia, may result in the finding of unusual forms of eriophyoids or eriophyoid-like mites that could help clarify the evolutionary relationship between the ancestral soil mites and contemporary phytophagous eriophyoids. CONCLUSIONS The correct identification of phytophagous mites and fundamental knowledge about their life cycles are critical for pest management in agricultural crops. The eriophyoid mites (Acariformes, Eriophyoidea) are among the smallest known herbivores. They are highly host specific and include numerous economically important pests of both annual and perennial crop plants. Seasonal changes in populations of some eriophyoid species involve the co-occurrence of morphologically different, conspecific seasonal forms, the deutogyne and protogyne, a phenomenon termed deuterogyny. Although only a small proportion of currently known eriophyoids are proven to be deuterogynous, this phenomenon might be more common than currently understood and may have created a situation in which the same taxon could have been described under different names by different authors. DNA barcoding is the most effective tool for testing the conspecificity of eriophyoids collected from mixed populations. Therefore, the inclusion of barcode data in future descriptions of new taxa of eriophyoids is essential, especially when deuterogyny is suspected. In this study, we reported on seasonal dimorphism in eriophyoid mites of the genera Shevtchenkella and Brevulacus. Although the two studied species, S. serrata and B. reticulatus, both fed on the generative organs of their hosts in late summer, only one of them (S. serrata) dispersed with seed-containing winged fruits in autumn, overwintered on them in leaf litter and colonized the new seedlings emerging in spring. Various uninvestigated plant species could be appropriate hosts for eriophyoids adapted to exploit the seed dispersal abilities of their hosts in a similar way to S. serrata. Additional studies conducted in various ecosystems and including different ecological groups of plants, especially anemochorous plants, are needed in order to estimate the frequency of the association of eriophyoids with plant generative organs and to better understand the role of such associations in their ecology. Acknowledgments: The reported study was funded by the Russian Foundation for Basic Research (RFBR) under the research project #21-54-46003 and by the Scientific and Technological Research Council of Turkey (TUBITAK) under the research project #220N174. Mite collection was partially supported by the Zoological Institute of the Russian Academy of Sciences (RAS) under the research project #1021051603202-7. The PCR and sequencing were conducted with the equipment of the “Development of Molecular and Cellular Technologies” and “The Bio-Bank” Resource Centers of St. Petersburg State University. page 16 of 18Zoological Studies 62:35 (2023) © 2023 Academia Sinica, Taiwan Authors’ contributions: Chetverikov PE and Sukhareva SI designed the study, collected mites, analysed the DNA data, drafted the manuscript and submitted the manuscript. Chetverikov PE and Romanovich AE performed slide-mounting, PCR and DNA sequencing. Desnitskiy AG, Klimov PB and Ozman-Sullivan SK helped to revise the drafts of the manuscript. All authors are in agreement with the content of the manuscript. Competing interests: All authors declare that they have no competing interests. Availability of data and materials: Slide-mounted mites and ethanol material have been deposited at Acarological Collection of the Zoological Institute of the Russian Academy of Sciences. The DNA sequences have been uploaded to the GenBank database. Consent for publication: Not applicable. Ethics approval consent to participate: Not applicable. REFERENCES Amrine JW Jr, Manson DCM. 1996. Preparation, mounting and descriptive study of eriophyoid mites. In: Lindquist EE, Sabelis MW, Bruin J. (eds) Eriophyoid mites: their biology, natural enemies and control. World crop pests, vol 6. Elsevier Science B.V., Amsterdam, The Netherlands, pp. 383–396. doi:10.1016/ S1572-4379(96)80023-6. Amrine JW Jr, Stasny TAH, Flechtmann CHW. 2003. Revised keys to the world genera of the Eriophyoidea (Acari: Prostigmata). Indira Publishing House, Michigan, USA. Asadi G, Ghorbani R, Cristofaro M, Chetverikov P, Petanović R, Vidović B, Schaffner U. 2014. The impact of the flower mite Aceria acroptiloni on the invasive plant Russian knapweed, Rhaponticum repens, in its native range. BioControl 59:367–375. doi:10.1007/s10526-014-9573-z. Bagdasarian AT. 1978. A new genus of the Eriophyoidea. Zool Zh 57:936–939. Bolton SJ, Chetverikov PE, Klompen H. 2017. Morphological support for a clade comprising two vermiform mite lineages: Eriophyoidea (Acariformes) and Nematalycidae (Acariformes). Syst App Acarol 22:1096–1131. doi:10.11158/saa.22.8.2. Bolton SJ, Bauchan GR, Chetverikov PE, Ochoa R, Klompen H. 2018. A rudimentary sheath for the smallest of “biting” chelicerae: the mouthparts of Cunliffea (Nematalycidae) and a new hypothesis on the origin of the stylet sheath of Eriophyoidea (Acariformes). Int J Acarol 44:374–381. doi:10.1080/01647954.2018.1488274. Breitwieser I, Brownsey PJ, Nelson WA, Wilton AD (eds). 2010. Flora of New Zealand. http://www.nzflora.info. Accessed 2 July 2022. Chetverikov PE. 2016. Video projector: a digital replacement for camera lucida for drawing mites and other microscopic objects. Syst App Acarol 21:1278–1280. doi:10.11158/saa.21.9.10. Chetverikov PE, Bolton S. 2016. Suboral fork: a newly discerned gnathosomal structure from the proboscis of eriophyoid mites (Acari, Eriophyoidea). Exp App Acarol 70:137–153. doi:10.1007/s10493-016-0077-7. Chetverikov PE, Bolton SJ, Gubin AI, Letukhova VY, Vishnyakov AE, Zukoff S. 2019. The anal secretory apparatus of Eriophyoidea and description of Phyllocoptes bilobospinosus n. sp. (Acariformes: Eriophyidae) from Tamarix (Tamaricaceae) from Ukraine, Crimea and USA. Syst App Acarol 24:139–157. doi:10.11158/saa.24.1.11. Chetverikov PE, Craemer C, Neser S. 2018. New pseudotagmic genus of acaricaline mites (Eriophyidae, Acaricalini) from a South African palm Hyphaene coriacea and remarks on lateral opisthosomal spines and morphology of deutogynes in Eriophyoidea. Syst App Acarol 23:1073–1101. doi:10.11158/ saa.23.6.6. Chetverikov PE, Craemer C, Cvrković T, Klimov PB, Petanović RU, Romanovich AE, Sukhareva SI, Zukoff SN, Bolton S, Amrine J. 2021a. Molecular phylogeny of the phytoparasitic mite family Phytoptidae (Acariformes: Eriophyoidea) identified the female genitalic anatomy as a major macroevolutionary factor and revealed multiple origins of gall induction. Exp App Acarol 83:31–68. doi:10.1007/s10493-020-00571-6. Chetverikov PE, Fedorov DS, Romanovich AE, Sarratt JV. 2021b. Morphological descriptions and DNA barcodes of Oziella viscida n. sp. (Eriophyoidea, Phytoptidae) and two infrequently reported Trisetacus species (Nalepellidae) from Crimea. Syst App Acarol 26:1619–1635. doi:10.11158/saa.26.9.1. Chetverikov PE, Klimov PB, He Q. 2022. Vertical transmission and seasonal dimorphism of eriophyoid mites (Acariformes, Eriophyoidea) parasitic on the Norway maple: a case study. R Soc Open Sci 9:220820. doi:10.1098/rsos.220820. Cvrković T, Chetverikov PE, Vidović B, Petanović R. 2016. Cryptic speciation within Phytoptus avellanae s.l. (Eriophyoidea: Phytoptidae) revealed by molecular data and observations on molting Tegonotus-like nymphs. Exp App Acarol 68:83–96. doi:10.1007/s10493-015-9981-5. Druciarek T, Kozak M, Maroufpoor M, Lewandowski M. 2016. Morphological variability of Phyllocoptes adalius female forms (Acari: Eriophyoidea), with a supplementary description of the species. Syst App Acarol 21:181–194. doi:10.11158/saa.21.2.3. Farkas HK. 1965. Familie Eriophyidae, Gallmilben. Die Tierwelt Mitteleuropas 3:1–155. Flechtmann CH, Arana M, Ciarrocchi F, Chetverikov PE, Amrine JW Jr. 2015. Rediscovery and redescription of two eriophyid mites (Acari, Prostigmata, Eriophyidae) from Baccharis salicifolia (Asteraceae), from Argentina with remarks on the eriophyoid coverflap base. Acarologia 55:387–396. doi:10.1051/ acarologia/20152178. Gleiser G, Picher MC, Veintimilla P, Martinez J, Verdú M. 2004. Seed dormancy in relation to seed storage behaviour in Acer. Bot J Linn Soc 145:203–208. doi:10.1111/j.1095-8339.2003.00276.x. Guo JF, Li HS, Wang B, Xue XF, Hong XY. 2015. DNA barcoding reveals the protogyne and deutogyne of Tegolophus celtis sp. nov. (Acari: Eriophyidae). Exp App Acarol 67:393–410. doi:10.1007/s10493-015-9953-9. Hall CC Jr. 1967. A look at eriophyid life cycles (Acarina: Eriophyoidea). Ann Entomol Soc Am 60:91–94. doi:10.1093/ aesa/60.1.91. Hodgkiss HE. 1913. New species of maple mites. J Econ Entomol 6:420–424. Hong TD, Ellis EH. 1990. A comparison of maturation drying, germination, and desiccation tolerance between developing seeds of Acer pseudoplatanus L. and Acer platanoides L. New Phytol 116(4):589–596. doi:10.1111/j.1469-8137.1990.tb00543.x. page 17 of 18Zoological Studies 62:35 (2023) © 2023 Academia Sinica, Taiwan Keifer HH. 1939. Eriophyid Studies VII. Bulletin of the Calif Dep Agric 28:484–505. Keifer HH. 1942. Eriophyid Studies XII. Bulletin of the Calif Dep Agric 31:117–129. Keifer HH. 1959. Eriophyid Studies XXVIII. Occasional Papers, Calif Dep Agric 2:1–20. Keifer HH. 1975. Eriophyoidea Nalepa. In: Jeppson LR, Keifer HH, Baker EW (eds) Mites injurious to economic plants. University of California Press, Berkeley, pp. 327–533. Klimov PB, Chetverikov PE, Dodueva IE, Vishnyakov AE, Bolton SJ, Paponova SS, Lutova LA, Tolstikov AV. 2022. Symbiotic bacteria of the gall-inducing mite Fragariocoptes setiger (Eriophyoidea) and phylogenomic resolution of the eriophyoid position among Acari. Sci Rep 12:3811. doi:10.1038/s41598022-07535-3. Klimov PB, OConnor BM, Chetverikov PE, Bolton SJ, Pepato AR, Mortazavi AL, Tolstikov AV, Bauchan GR, Ochoa R. 2018. Comprehensive phylogeny of acariform mites (Acariformes) provides insights on the origin of the four-legged mites (Eriophyoidea), a long branch. Mol Phylogenet Evol 119:105– 117. doi:10.1016/j.ympev.2017.10.017. Krantz GW, Ehrensing DT. 1990. Deuterogyny in the skeleton weed mite, Aceria chondrillae (G. Can.) (Acari: Eriophyidae). Int J Acarol 16:129–133. doi:10.1080/01647959008683524. Lindquist EE. 1996. External anatomy and notation of structures. In: Lindquist EE, Sabelis MW, Bruin J. (eds) Eriophyoid mites: their biology, natural enemies and control. World crop pests, vol 6. Elsevier Science B.V., Amsterdam, The Netherlands, pp. 3–31. doi:10.1016/S1572-4379(96)80003-0. Liro JI. 1942. Neue finnische Eriophyiden (Acarina). Ann Entomol Fenn 8:71–79. Manson DCM. 1984. Eriophyoidea except Eriophyinae (Arachnida: Acari). Fauna of New Zealand, vol 4. Science Information Publishing Centre, DSIR, Wellington. Manson DCM, Oldfield GN. 1996. Life forms, deuterogyny, diapause and seasonal development. In: Lindquist EE, Sabelis MW, Bruin J. (eds) Eriophyoid mites: their biology, natural enemies and control. World crop pests, vol 6. Elsevier Science B.V., Amsterdam, The Netherlands, pp. 173–183. doi:10.1016/S15724379(96)80009-1. Marini F, Weyl P, Vidović B, Petanović R, Littlefield J, Simon S, de Lillo E, Cristofaro M, Smith L. 2021. Eriophyid mites in classical biological control of weeds: progress and challenges. Insects 12:1–25. doi:10.3390/insects12060513. Nalepa A. 1892. Tegonotus, ein neues Phytoptiden-Genus. In: Spengel JW (ed) Geographie und biologie der tiere. Zoologische jahrbücher abteilung für systematik, vol 6(2). Gustav Fischer Verlag Jena, Germany, pp. 327–337. Nalepa A. 1898. Eriophyidae (Phytoptidae). Das tierreich. Eine zusammenstellung und kennzeichnung der rezenten tierformen 4. Lieferung. Leopold Classic Library, Germany, pp. 1–74. Nuzzaci G, Alberti G. 1996. Internal anatomy and physiology. In: Lindquist EE, Sabelis MW, Bruin J (eds) Eriophyoid mites: their biology, natural enemies and control. World crop pests, vol 6. Elsevier Science B.V., Amsterdam, The Netherlands, pp. 101–150. doi:10.1016/S1572-4379(96)80006-6. Oldfield GN. 1996. Diversity and host plant specificity. In: Lindquist EE, Sabelis MW, Bruin J (eds) Eriophyoid mites: their biology, natural enemies and control. World crop pests, vol 6. Elsevier Science B.V., Amsterdam, The Netherlands, pp. 199–216. doi:10.1016/S1572-4379(96)80011-X. Ozman SK. 2001. The life history and population development of Rhyncaphytoptus negundivagrans Farkas (Acari: Diptilomiopidae). In: Halliday RB, Walter DE, Proctor HC, Norton RA, Colloff MJ (eds) Acarology: Proceedings of the 10th International Congress. CSIRO Publishing, Melbourne, Australia, pp. 352–354. Petanović R, Boczek J, Stojnić B. 1997. Taxonomy and bioecology of eriophyids (Acari: Eriophyoidea) associated with Canada thistle, Cirsium arvense (L.) Scop. Acarologia 38:181–191. Petanović R, Stanković S. 1999. Catalog of the Eriophyoidea (Acari: Prostigmata) of Serbia and Montenegro. The Entomological Society of Serbia, Beograd. Ponomareva PE. 1978. Chetyrehnogie kleshchi (Acarina: Tetrapodili) orekhovo-plodovykh lesov Kirghizii. Frunze: Ilim Publishing House, Kyrgyzstan. Poulin R. 2011. Evolutionary ecology of parasites, 2nd edn. Princeton University Press, Princeton. doi:10.1515/9781400840809. Putman WL. 1939. The plum nursery mite (Phyllocoptes fockeui Nal. & Trt.). The 70th Annual Report of the Entomological Society of Ontario, pp. 33–40. Pye D. 2012. New eriophyoid mites (Acari: Prostigmata: Eriophyoidea) in Britain: one new genus, four new species, 19 new records and two incursions. Zootaxa 3578:43–68. doi:10.11646/zootaxa.3578.1.3. Ripka G. 2011. New Quercus-feeding Brevulacus species, redescription of Rhyncaphytoptus cerrifoliae Farkas and new eriophyoid mite records from Hungary (Acari: Prostigmata: Eriophyoidea). Acta Phytopathol Entomol Hung 46:129–138. doi:10.1556/aphyt.46.2011.1.10. Roivainen H. 1947. Eriophyid news from Finland. Acta Entomol Fenn 3:1–49. Roivainen H. 1950. Eriophyid news from Sweden. Acta Entomol Fenn 7:1–51. Roivainen H. 1953. Some gall mites (Eriophyidae) from Spain. Archivos del Instituto de Aclimatación de Almeria 1:9–43. Sidorchuk EA, Schmidt AR, Ragazzi E, Roghi G, Lindquist EE. 2015. Plant-feeding mite diversity in Triassic amber (Acari: Tetrapodili). J Syst Palaeontol 13:129–151. doi:10.1080/147720 19.2013.867373. Skoracka A, Lewandowski M, Boczek J. 2005. A catalogue of eriophyoid mites (Acari: Eriophyoidea) of Poland. Natura optima dux Foundation, Warszawa. Soika G, Gol A, Honarmand A, Wozinska A, Sadeghi H. 2017. New records of eriophyoid mites from Iran (Acari: Trombidiformes: Eriophyoidea) and a description of a new Brevulacus Manson species. Zootaxa 4216:321–338. doi:10.11646/zootaxa.4216.4.2. Song ZW, Xue XF, Hong XY. 2009. Four new species of Rhyncaphytoptus from Tibet Autonomous Region, China (Acari: Eriophyoidea: Diptilomiopidae). Zootaxa 2196:31–47. doi:10.11646/zootaxa.2196.1.3. Sukhareva SI, Chetverikov PE. 2013. Morphological transformations in the course of transition from protogyne to deutogene form of female in eriophyoid mites (Acari: Eriophyoidea). Vestnik SanktPeterburgskogo Universiteta 3:3–15. (in Russian) Xue XF, Song ZW, Hong XY. 2009a. One new genus and five new species of Rhynacaphytoptinae from China (Acari: Eriophyoidea: Diptilomiopidae). Zootaxa 1992:1–19. doi:10.11646/ zootaxa.1992.1.1. Xue XF, Wang Z, Song ZW, Hong XY. 2009b. Eriophyoid mites on Fagaceae with descriptions of seven new genera and eleven new species (Acari: Eriophyoidea). Zootaxa 2253:1–95. doi:10.11646/zootaxa.2253.1.1. Yin Y, Yao LF, Zhang Q, Hebert PDN, Xue XF. 2020. Using multiple lines of evidence to delimit protogynes and deutogynes of fourlegged mites: a case study on Epitrimerus sabinae s.l. (Acari: Eriophyidae). Invertebr Syst 34:57–768. doi:10.1071/IS20014. page 18 of 18Zoological Studies 62:35 (2023)