Situngu, Sivu ¹ ; Elhalawany, Ashraf Said ² ; Ngubane-Ndhlovu, Nompumelelo P. ³ and Chetverikov, Philipp E. ⁴

¹✉ School of Animal, Plant and Environmental Sciences, University of the Witwatersrand, Johannesburg, South Africa.
²Fruit Tree Mite Department, Plant Protection Research Institute, Agricultural Research Centre, Dokki, Giza, Egypt.
³Plant Health Diagnostic Services, Department of Agriculture, Land Reform and Rural Development (DALRRD), Private Bag X5015, Stellenbosch, 7599, South Africa.
⁴Department of Invertebrate Zoology, Saint-Petersburg State University, 199034 Saint-Petersburg, Russia & Zoological Institute of Russian Academy of Sciences, Universitetskaya Nab. 1, 199034 St. Petersburg, Russia.

2023 - Volume: 63 Issue: 4 pages: 1271-1303

ZooBank LSID: 451893E3-DCEB-45CC-8C31-D51150B867DE

Original research

Keywords

Abstract

Introduction

Four-legged or gall-mites (Acariformes, Eriophyoidea) belong to an ancient hyperdiverse lineage of basal acariform mites permanently associated with higher vascular plants (Lindquist 1996, Klimov et al. 2018, Bolton et al. 2023). Among three currently recognised families of eriophyoid mites (Phytoptidae, Diptilomiopidae and Eriophyidae), Eriophyidae is the largest one, comprising about 314 genera and over 4000 described species (Amrine et al. 2003; de Lillo and Skoracka 2010). Most eriophyoids are monophages and some of them are of high economic importance, especially those associated with crops (wheat, tomato, mango, etc.) and transmit phytoviruses (Petanović and Kielkiewicz 2010, de Lillo et al. 2018, 2021). Eriophyoid mites are distinct in that they have elongated bodies covered with annular cuticular folds, only two pairs of legs, a bunch of needle-like gnathosomal stylets, and a well-developed and typically bilobed anal sucker that they use to attach themselves to their host during feeding and winter diapause (Linquist 1996; Krantz and Walter, 2009; Chetverikov et al. 2019a,b, 2022). Eriophyoid mites usually feed on the plant epidermis often causing various growth abnormalities such as galls, russeting of leaves and shortening of shoots (Kiefer 1982; de Lillo et al. 2018). These abnormalities are initiated by unknown chemical compounds of the mite saliva injected within plant cells and used by mites for manipulating normal plant cell development processes and initiating gallogenesis (Desnitskiy et al. 2023). It is typically accompanied by a change of the cell's pH, suppression of photosynthesis, and changes in the expression levels of meristem-specific genes, and the genes determining adaxial–abaxial polarity and signalling of phytohormones (Petanović and Kielkiewicz 2010, Ivanova et al. 2022, Paponova et al. 2018, Klimov et al. 2022).

Tamarisk or salt-cyder, is a multi-branched evergreen shrub with specialised salt glands in its leaves (Bredenkamp 2003). Tamarix is the largest genus in Tamaricaceae comprising 57 species, of which only 57 are valid (The Plant List 2023). This notable bias between the numbers of the species names (204/57) occurred because many species of this genus are morphologically very similar and various botanists have described them under different names that were later synonymized. Tamarisks are widely distributed in temperate and subtropical regions in South Europe, Asia, and Africa, while only some introduced species are known in Northern America and Australia (Harms and Hiebert 2006). In Africa, eighteen species of Tamarix are found including those that are non-native (Baum 1978; Marlin et al 2017). Among them, Tamarix usneoides E. Mey. ex Bunge is the only one that is native to South Africa (Bredenkamp 2003). Twelve Tamarix species have been recorded in Egypt (Boulos 1999; Hosni 2000).

In different countries with dry climates, tamarisks are considered weeds and may become highly invasive due to their outstanding salt and water resistance and competition with local plants (Marlin et al 2017; Byrne et al 2021). Different phytophagous arthropods have been tested for biological control of tamarisks including several gall-forming species of eriophyid mites (Marlin et al 2017; Mayonde et al 2019). All currently known species of eriophyoids associated with Tamarix belong to four genera of the two subfamilies (Eriophyinae and Phyllocoptinae) of the family Eriophyidae (Table 1): Aceria (8 spp., including three new species described in this paper), Eriophyes (4 spp.), Phyllocoptes (2 spp.), and Dicruvasates (1 sp.). The species of the first two genera are capable of inducing various galls on twigs and buds, whereas all three phyllocoptine species are exclusively vagrant. Remarkably, one of them, Phyllocoptes bilobospinosus, possesses a well-developed anal secretory apparatus (ASA) that is homologous to ASA of the silk-producing eriophyoid mites of the genus Aberoptus living under web mats on leaves of their hosts (Chetverikov et al. 2023). Up to now, only five Aceria species have been recorded on Tamarix worldwide: A. amrini Joshi 2013, A. arbosti (Cotte 1924) A. dioicae (Keifer 1979), A. tamaricis (Trotter 1901), and A. tlaiae (Trabut 1917). In this paper, we describe three new Aceria species associated with Tamarix spp. in Egypt and South Africa and provide supplementary descriptions of A. amrini, A. dioicae, and A. tamaricis based on material from Egypt.

Material and methods

Collection and morphological measurements

Plant materials (branches of Tamarix spp.) were collected in South Africa (near Noorspoort farm in the Western Cape and near Dwayka River in the Eastern Cape), and in Egypt (in the Qalyubia governorate) in spring, summer and winter seasons in 2016 – 2022. Plant material was kept cool and shipped to the laboratory the day after collection. In the laboratory the mites were collected under a stereomicroscope with a fine minute pin and transferred (a) in Eppendorf tubes filled with 96% ethanol for molecular studies, (b) into a drop of sorbitol-isopropyl solution for slide mounting (Amrine and Manson 1996), or (c) directly onto a double-sided carbon taped stub for scanning electron microscopy (SEM). Later, sorbitol-isopropyl solution was dissolved with distilled water and mites from this solution were mounted without using fibers on slides in modified Berlese medium with Iodine and cleared on a heating block at 90° C for 3–5 hours (Amrine and Manson 1996).

External morphology of the slide-mounted specimens was studied under phase contrast (PC) and differential interference contrast (DIC) light microscopy (LM) using a Carl Zeiss Jena microscope connected with a camera Optika Optikam B3 (in Egypt), a Leica DM4B connected with a camera Leica MC170 HD (in South Africa), and a Leica DM2500 connected with a camera ToupCam E3ISPM05000KPA (in Russia). No fibre was used in the mounting of the SOUTH African specimens. Measurements were obtained using Las Core (LAS V4.12) and compuEye software (Bakr 2005). They are given in the descriptions in micrometres (µm) and are lengths except when stated otherwise. In the descriptions of new species the measurements of a holotype female followed by the ranges (in brackets) based on measurements of the paratypes and holotypes are given. In the descriptions of males and immatures as well as in the supplementary descriptions, only ranges are given. Terminology of eriophyoid morphology and classification of Eriophyoidea follow Lindquist (1996) and Amrine et al. (1996), respectively.

The type materials from Egypt were deposited at the mite reference collection of the Fruit Tree Mites Department, Plant Protection Research Institute, Agricultural Research Centre, Dokki, Giza governorate, Egypt (PPRI-ARC). Some paratypes have been deposited at the Mite Reference Collection of the Egyptian Society of Acarology Museum (ESAM), Zoology and Agricultural Nematology Department, Faculty of Agriculture, Cairo University, Giza governorate, Egypt; the Arthropod/Mite Collection of the Department of Entomology, Nanjing Agricultural University, Jiangsu Province (NJAU), China; College of Agriculture and Forestry, West Virginia University (WVU), USA.; and the mite collection of Department of Plant, Soil and Food Sciences (Di.S.S.P.A.), University of Bari Aldo Moro, Italy (UNIBA, formerly indicated as UBI by Zhang 2018). Type materials from South Africa were deposited in the Department of Agriculture, Land Reform and Rural Development at the Plant Quarantine Station in Stellenbosch, South Africa and paratypes were deposited in the Acarological Collection of Zoological Institute of RAS (ZIN RAS, Saint-Petersburg, Russia).

Scanning Electron microscopy (SEM)

For cryo-fixation and preparing the mite samples for imaging, we followed the methodology used by Rahbani et al. (2013). While viewing the mites under a stereomicroscope, live mites were collected from the fresh galls and bud scales with a trimmed paintbrush. They were then transferred to a stub with double-sided carbon tape and immediately frozen using liquid nitrogen at –210 °C for a few milliseconds to avoid ice crystal formation. The stub with the specimens was then heated to –100 °C for 3 to 5 min to sublimate any water condensed on the surface of the mites, and then cooled again to –140 °C. Thereafter, the mites were coated with platinum for 60s. The Zeiss Supra 55VP SEM equipped with a Gatan Alto cryo-stage (Gatan, Pleasanton, CA, USA) was used for viewing the mites and capturing images.

DNA extraction and sequencing

For DNA extraction, 1‒3 mite specimens of each species were crushed with a fine pin in a 1 μL drop of distilled water on a microscope slide. The drop was pipetted into a thin-walled PCR tube with 20 μL of 8% solution of Chelex® 100 Resin before being heated twice (10 min at 95 °C). The solution above the settled Chelex® granules was used as the DNA template for PCR to amplify a fragment of subunit I of Cox1 gene, D1D2 region of 28S rDNA gene, and ITS1-5.8S-ITS2 genes. Thermal cycling profiles and primers (for PCR and for sequencing) used were as specified by Klimov et al. (2018) and Chetverikov and Bertone (2022). After amplification, 3.5 μL of each reaction product was mixed with 0.5 μL of SYBR Green I (Lumiprobe, Hannover, Germany) and analyzed by electrophoresis in a 1% agarose gel to assess the product size and concentration. Sequences were obtained using BigDye Terminator v.3.1 chemistry in a 3500xl Genetic Analyzer (Applied Bio-systems, Foster City, CA, USA). New sequences were compared with the sequences of Eriophyoidea currently available in GenBank (23 June 2023) using different blast algorithms (http://blast.ncbi.nlm.nih.gov/Blast.cgi ). The voucher specimens were deposited in the Department of Agriculture, Land Reform and Rural Development at Plant Quarantine Station in Stellenbosch, South Africa.

Results

Eriophyidae Nalepa, 1898

Subfamily Eriophyinae Nalepa, 1898

Tribe Aceriini Amrine et Stasny, 1994

Genus Aceria Keifer, 1944

Aceria aegyptytamaricis Elhalawany n. sp.

ZOOBANK: 82CC1027-A40C-4009-8E32-085002CFFF45

(Figures 2–3)

Description

Female — (n=15). Body vermiform, 184 (150–190) including gnathosoma, 65 (50–67) wide, 65 (50–65) thick, yellowish.

Gnathosoma 21 (21–23), projecting obliquely downwards, ep 2 (2–3), d 6 (6–7), v 1–2, cheliceral stylets 17 (16–18). Prodorsal shield 25 (23–30) with short subtriangular frontal lobe 2 (2–4), 45 (42–55) wide. Prodorsal shield ornamentation faint. Median line short, present only near posterior shield margin as a short dark ridge, admedian lines very indistinct, complete; sub-median lines absent. Scapular tubercles on rear shield margin, 25 (23–27) apart, sc 40 (30–45), directed backward. Coxigenital area smooth, with 4-5 semiannuli between coxae and genitalia, prosternal apodeme 6 (5–6); 1b 7 (7–9), 13 (13–14) apart; 1a 25 (24–28), 9 (9–10) apart; 2a 35 (35–42), 27 (27–30) apart.

Leg I 28 (28–31), femur 9 (8–10), bv 13 (12–15); genu 4 (3–4), l″ 20 (18–25); tibia 4 (4–5), l′ 6 (6–8), located in ½ from dorsal base; tarsus 7 (7–8); tarsal empodium simple 7 (7–10), 8-rayed, tarsal solenidion ω tapered, 8 (7–9), ft′ 22 (22–24), ft″ 28 (26–28), u′ 3 (3–4). Leg II 24 (22–24), femur 7 (7–8), bv 13 (12–15); genu 3 (3–4), l″ 10 (10–12); tibia 4 (3–4); tarsus 5 (4–5); tarsal empodium simple 8 (7–9), 8-rayed, ω tapered 7 (7–9), ft′ 15 (15–17), ft″ 26 (25–28), u′ 3 (3–4).

Opisthosoma dorsally evenly flat, with 65 (64–75) dorsal semiannuli and 60 (60–65) ventral semiannuli. Dorsal semiannuli with linear elongate microtubercles on rear annular margins, 4–5 caudal annuli dorsally without microtubercles. Ventral semiannuli with elongate microtubercles on rear annular margins, microtubercles on the last 7-8 ventral semiannuli oval. Setae c2 25 (25–30), 45 (42–49) apart, on annulus 7 (7–7) from coxae II; d 45 (42–49), 35 (35–37) apart, on annulus 15 (14–15); e 40 (38–45), 19 (19–21) apart, on annulus 31 (30–33); f 42 (35–48), 25 (25–28) apart, on 8^th annulus from rear, h1 6 (6–7); h2 65 (65–86). External genitalia. Genital coverflap subtriangular, smooth, 11 (10–11), 17 (17–18) wide, 3a, 40 (35–48), 11 (11–12) apart. Internal genitalia. Spermathecae globose, oriented postero laterad; spermathecal tubes relatively short about one third of spermathecal diameter; oblique apodeme indistinct.

Male — (n=5). Similar to females, 153–175 including gnathosoma, 48–54 wide and 50–57 thick, whitish when alive.

Gnathosoma 17–20, cheliceral stylets 14–15, ep 2–3, d 5–6, v 1–2,. Prodorsal shield pattern similar to that of female, 23–25 including frontal lobe, 39–42 wide; Scapular tubercles on rear shield margin, 24–26 apart, sc 26–30, directed backward. Coxigenital area smooth, prosternal apodeme 5–6; 1b 7–8, 12–13 apart; 1a 25–28, 8–9 apart; 2a 30–35, 26–28 apart.

Leg I 20–22, femur 6–7, bv 8–12; genu 3–4, l″ 17–20; tibia 4–5, l′ 3–5; tarsus 5–6; empodium simple 5–6, 7-rayed, tarsal solenidion ω 7–8 tapered, ft′ 20–22, ft″ 20–25, u′ 3–4. Leg II 19–21, femur 6–7, bv 8–10; genu 2–3, l″ 6–9; tibia 3–4; tarsus 4–5; em 5–6, 7-rayed, ω 7–8 tapered, ft′ 7–10, ft″ 18–22, u′ 2–3.

Opisthosoma with 58–65 dorsal semiannuli and 58–61 ventral semiannuli, microtubercles shaped as in females. Setae c2 18–23, 43–49 apart, on annulus 7 from coxae II; d 28–33, 35–38 apart, on annulus 14–15; e 26–28, 20–21 apart, on annulus 27–28; f 25–28, 24–28 apart, on 8^th annulus from rear, h1 3–4; h2 55–60. External genitalia 12–14, 17–19 wide, genital cuticle behind the tubercles of eugenital setae with microgranulations, 3a 28–32, 13–14 apart.

Nymph — (n=3). Body vermiform, 145–150 including gnathosoma, 38–40 wide.

Gnathosoma 14–15, cheliceral stylets 12–13, ep 1–2, d 3–4. Prodorsal shield semicircular, smooth, 20–22, 21–23 wide. Scapular tubercles on rear shield margin 16–18 apart, sc 11–13, directed backward. Coxigenital area smooth; 1b 2–3, 10–11 apart; 1a 6–8, 6–7 apart; 2a 9–11, 19–20 apart; 3a 8–10, 6–7 apart.

Leg I 15–17, femur 3–4, bv 3–5; genu 2–4, l″ 5–7; tibia 3–3, l′ 2–3; tarsus 3–3; empodium simple 3–4, 4-rayed, solenidion ω 4–5 tapered, ft′ 8–10, ft″ 11–13, u′ 1–2. Leg II 13–14, femur 3–4, bv 4–5; genu 2–3, l″ 3–5; tibia 2–3; tarsus 3–3; empodium 3–4, 4-rayed, ω 4–5 tapered, ft′ 5–6, ft″ 6–10, u′ 1–2.

Opisthosoma with 45–48 smooth dorsal semiannuli and 40–42 smooth ventral semiannuli. Setae c2 10–11, 39–40 apart, on annulus 6–7 from coxae II; d 13–14, 31–32 apart, on annulus 14; e 8–9, 14–15 apart, on annulus 23; f 15–17, 22–24 apart, on 4–5^th annulus from rear, h1 1–2; h2 21–25.

Host plant

Tamarisk (athel), Tamarix senegalensis DC. (=Tamarix nilotica (Ehrenb.) Bunge) (Tamaricaceae).

Relation to the host plant — Mites cause green elongate galls on buds and twigs, about 4–6 mm long and 2.5–3.5 in diameter (Figure 1 C).

Etymology

The name ''aegypty'' refers to Egypt; ''tamaricis'' refers to the genus name of the host plant.

Type locality

Benha city (30°26′04.62″N, 31°11′24.22″E), Qalyubia governorate, Egypt, 9 March, 2021, coll. Ashraf Elhalawany.

Type material

Holotype: female (slide no. EGYErio55.1), deposited at ARC-PPRI, Egypt. Paratypes: ten females, five males and five nymphs on five slides (slides no. EGYErio55.2–55.6), 19 February 2021 deposited at ARC-PPRI, Egypt. Five paratypes females on two slides (slide no. EGYErio55.7–55.8), 10 January 2019, with the same data as holotype, deposited at ESAM, Egypt. Two slides (slides no. EgTT09-10), 10 January 2019, with the same data as holotype, deposited at UNIBA, Italy. Four slides, 9 March 2021, with the same data as holotype, deposited at Zoological Institute of the Russian Academy of Sciences (ZIN RAS), Russia. Two slides, 9 March 2019 with the same data as holotype, deposited at the College of Agriculture and Forestry, West Virginia University (WVU), USA.

Differential diagnosis

The new species is close to Aceria dioicae (Keifer, 1979) and A. tamaricis (Trotter, 1901) that are associated with different Tamarix spp. and cause galls resembling those caused by A. aegyptytamaricis sp. n These three species are similar in smooth coxae, and lengths of scapular setae sc, setae e and f but differ in ornamentation of prodorsal shield, shape of microtubercles on opisthosomal annuli, number of empodium rays, and lengths of c2 and 3a (Table 2).

Aceria amrini Joshi, 2013

(Figures 4–5)

Supplementary description

Female — (n=10). Body vermiform, 225 (150–235) including gnathosoma, 51 (42–52) wide, 49 (41–50) thick; yellowish.

Gnathosoma 26 (24–28), projecting obliquely downwards, ep 2 (2–3), d 7 (6–8), v absent, cheliceral stylets 20 (18–21). Prodorsal shield 31 (29–33), 43 (39–44) wide; subtriangular, smooth. Scapular tubercles on rear shield margin, 22 (20–23) apart, sc 37 (34–38), directed backward. Coxigenital area smooth, with three semiannuli between coxae and genitalia, prosternal apodeme 4 (4–5); 1b 10 (10–12), 12 (12–14) apart; 1a 25 (21–31), 8 (7–8) apart; 2a 43 (29–45), 23 (23–25) apart.

Leg I 25 (23–28), femur 7 (6–8), bv 13 (11–14); genu 4 (4–5), l″ 25 (25–27); tibia 4 (4–5), l′ 7 (7–8), located in the middle from dorsal base; tarsus 5 (5–6); tarsal empodium simple 9 (8–10), 6-rayed, tarsal solenidion ω tapered, 9 (8–9), pa ft′ 17 (15–20), ft″ 28 (27–33), u′ 7 (6–7). Leg II 24 (23–26), femur 6 (6–7), bv 13 (12–15); genu 4 (3–4), l″ 11 (11–13); tibia 4; tarsus 6 (5–7); tarsal empodium simple 9 (8–10), 6-rayed, ω tapered 8 (8–9), ft′ 15 (15–17), ft″ 30 (30–34), u′ 7 (6–7).

Opisthosoma dorsally evenly arched, with 53 (52–55) dorsal semiannuli and 58 (56–60) ventral semiannuli. Dorsal and ventral semiannuli smooth except the last 10–11^th ventral annuli bearing distinct pointed microtubercles. Setae c2 37 (35–45), 40 (39–50) apart, on annulus 8 (8–9) from coxae II; d 70 (45–70), 30 (29–36) apart, on semiannulus 15 (15–16); e 57 (35–58), 15 (14–18) apart, on annulus 31 (30–32); f 55 (38–55), 33 (33–35) apart, on 6–7^th annulus from rear, h1 6 (5–6), h2 100 (85–107). External genitalia. Genital coverflap subtriangular, smooth, 15 (15–16), 17 (16–17) wide, 3a, 45 (30–44), 11 (11–12) apart. Internal genitalia. Anterior genital apodeme trapezoidal, longitudinal bridge distinct; oblique apodeme non-apparent; spermathecal tubes short, directed laterad; spermathecae ovoid.

Male — (n=5). Similar to female, body vermiform, 185–215 including gnathosoma, 50–58 wide and 40–57 thick; whitish in life.

Gnathosoma 23–25, cheliceral stylets 16–20, ep 2–3, d 6–8, v absent,. Prodorsal shield smooth, 25–28, 34–38 wide; scapular tubercles on rear shield margin, 21–25 apart, sc 23–32, directed backward. Coxigenital area smooth, prosternal apodeme 3–5; 1b 7–8, 10–11 apart; 1a 14–16, 6–8 apart; 2a 19–27, 18–20 apart.

Leg I 24–26, femur 6–8, bv 13–14; genu 4–5, l″ 22–25; tibia 3–4, l′ 5–6; tarsus 5–6; empodium simple 6–7, 6-rayed, ω 6–7 tapered, ft′ 13–15, seta ft″ 20–27, u′ 5–6. Leg II 21–24, femur 6–8, bv 11–14; genu 3–4, l″ 10–12; tibia 3–4; tarsus 5–6; empodium 6–6, 6-rayed, ω 6–7 tapered, ft′ 12–15, ft″ 25–28, u′ 5–6.

Opisthosoma with 50–54 dorsal semiannuli and 53–57 ventral semiannuli, microtubercles shaped similar to those of female. Setae c2 27–35, 47–50 apart, on annulus 7–8 from coxae II; d 36–45, 31–40 apart, on annulus 15–16; e 25–45, 16–18 apart, on annulus 29–30; f 27–35, 32–35 apart, on 6^th annulus from rear, h1 4–6, h2 72–95. External genitalia 10–14, 17–19 wide, cuticle behind eugenital setae smooth, 3a 27–31, 15–16 apart.

Nymph — (n=3). Body vermiform, 148–160 including gnathosoma, 45–52 wide, 42–46 thick.

Gnathosoma 17–19, cheliceral stylets 14–16, ep 1–2, d 4–6. Prodorsal shield subtriangular, smooth, 24–25, 35–38 wide. Scapular tubercles on rear shield margin, 19–21 apart, sc 10–14, directed backward. Coxigenital area smooth; 1b 5–8, 9–11 apart; 1a 14–16, 6–8 apart; 2a 17–21, 19–20 apart; 3a 7–10, 8–9 apart.

Leg I 15–16, femur 3–4, bv 4–6; genu 2, l″ 10–12; tibia 2, l′ 2–3; tarsus 2; empodium simple 4–5, 5-rayed, ω 5–6 tapered, ft′ 11–14, ft″ 12–15, u′ 3–4. Leg II 15–16, femur 3–4, bv 4–6; genu 2, l″ 7–8; tibia 2; tarsus 2; em 4–5, 5-rayed, ω 5–6 tapered, ft′ 6–8, ft″ 10–13, u′ 3–4.

Opisthosoma with 44–47 smooth annuli. Setae c2 10–13, 40–42 apart, on annulus 7 from coxae II; d 20–22, 30–31 apart, on annulus 15–16; e 11–20, 20–22 apart, on annulus 27–28; f 20–22, 20–21 apart, on 4–5^th annulus from rear, h1 3–4, h2 29–33.

Host plant

Tamarix aphylla (L.) Karst. (Tamaricaceae).

Relation to the host plant — In Egypt, A. amrini causes large rounded brown galls about 30–52 mm diameter on twigs of Tamarix aphylla (Figure 1 E, F). In India, these mites were collected as vagrants from the stems, leaves, and buds on the same host with no apparent damage to plant observed (Joshi et al. 2013).

Distribution

India (New Delhi) and Egypt (first record for Africa).

Material examined

Fifteen females, five males and four nymphs on five slides (slide no. EGYErio40.1–40.5), from T. aphylla, deposited in the Plant Protection Research Institute collection, Giza, Egypt, 9 March, 2021, Qalyubia governorate (30°16′14.03″N, 31°14′07.28″E), coll. Ashraf Elhalawany. Four slides (slides no. EgTA01-04) with the same data, deposited at UNIBA, Italy. Four slides with the same data as holotype, deposited at Zoological Institute of the Russian Academy of Sciences (ZIN RAS), Russia. Two slides deposited at the College of Agriculture and Forestry, West Virginia University (WVU), USA. Five females on two slides (EGYErio40.6 and EGYErio40.7, collected on 28 January 2023), deposited at ESAM, Egypt.

Remarks

In comparison to specimens of A. amrini described by Joshi et al. (2013) from India, the specimens from Egypt have shorter opisthosomal setae c2 (35–45 vs 45–60) and h2 (85–107 vs 100–135).

Aceria benhaiensis Elhalawany, Ngubane-Ndhlovu et Situngu n. sp.

ZOOBANK: EAA146D6-487C-44F0-BB59-2A1088122FBC

(Figures 6–8)

Description

Female — (n=15). Body vermiform, 185 (170–195) including gnathosoma, 45 (40–46) wide, 42 (40–45) thick; light yellow.

Gnathosoma 23 (21–23), projecting obliquely downwards, ep 3 (3–4), d 6 (6–7), v 1–2, chelicerae 17 (14–17). Prodorsal shield 21 (21–22) with short anteriorly rounded subtriangular frontal lobe, 32 (30–33) wide; prodorsal shield ornamentation faint. Median line absent or very indistinct only in posterior ¼ of prodorsal shield, admedian lines very faint, complete, curved at base L-shaped; some dashes and short lines present in epicoxal areas. Scapular tubercles on rear shield margin, 22 (19–23) apart, sc 23 (22–25), projecting posteriorly. Coxigenital area smooth, with 2-3 annuli between coxae and genitalia, prosternal apodeme 4 (3–4); I 1b 5 (4–6), 8 (8–10) apart; I 1a 21 (19–24), 6 (6–7) apart; 2a 32 (30–35), 19 (19–20) apart.

Leg I 23 (21–23), femur 7 (7–8), bv 9 (5–9); genu 4 (3–4), l″ 22 (17–23); tibia 4 (4–6), l′ 4 (3–5), located in the middle from dorsal base; tarsus 5 (4–6); tarsal empodium simple 5 (5–6), 6-rayed, ω tapered, 6 (6–7), ft′ 17 (14–17), ft″ 20 (18–22), u′ 3 (3–4). Leg II 21 (18–21), femur 6 (5–6), bv 9 (7–10); genu 4 (3–4), l″ 10 (9–10); tibia 4 (3–4); tarsus 4 (4–5); tarsal empodium simple 5 (5–6), 6-rayed, ω tapered 6 (6–7), ft′ 10 (8–10), ft″ 20 (19–22), u′ 3 (3–4).

Opisthosoma dorsally with 41 (39–46) annuli, with linear elongate microtubercles on rear annular margins, last 6 annuli without microtubercles; ventrally with 42 (42–45) annuli, with more rounded microtubercles than on dorsal annuli. Setae c2 21 (20–22), 44 (44–45) apart, on annulus 7 from coxae II; d 32 (31–40), 30 (29–30) apart, on annulus 14 (14–15); e 30 (28–30), 16 (15–18) apart, on annulus 25 (24–25); f 30 (25–35), 31 (31–35) apart, on 6–7^th annulus from rear, h1 5 (5–6), h2 55 (49–70). External genitalia 10 (9–10), 17 (16–17) wide, coverflap smooth, subtriangular, 3a 25 (25–32), 10 (8–10) apart.

Male — (n=5). Similar to female, body vermiform, 149–175 including gnathosoma, 37–42 wide and 38–40 thick; whitish.

Gnathosoma 18–20, cheliceral stylets 16–18, ep 2–3, d 5–6, v 1–2. Prodorsal shield pattern similar to that of female, 18–20, 27–34 wide; Scapular tubercles on rear shield margin, 21–22 apart, sc 18–22, directed backward. Coxigenital area smooth, prosternal apodeme 3–4; 1b 4–5, 8–9 apart; 1a 16–18, 5–6 apart; 2a 25–28, 17–19 apart.

Leg I 17–19, femur 5–7, bv 6–9; genu 2–3, l″ 12–15; tibia 3–4, l′ 3–4; tarsus 4–5; empodium simple 4–5, 6-rayed, ω 5–6 tapered, ft′ 12–15, ft″ 17–21, u′ 2–4. Leg II 16–174, femur 5–6, bv 7–11; genu 3, l″ 8–10; tibia 3; tarsus 3–4; empodium 4–5, 6-rayed, ω 6–7 tapered, ft′ 7–9, ft″ 15–18, u′ 2–3. Opisthosoma with 38–40 dorsal semiannuli and 40–42 ventral semiannuli, microtubercles shaped similar to those of female. Setae c2 16–21, 41–43 apart, on annulus 7 from coxae II; d 24–27, 29–30 apart, on annulus 12–13; e 15–23, 16–17 apart, on annulus 21–22; f 26–30, 25–29 apart, on 5^th annulus from rear, h1 5–6; h2 49–70. Male genital area 10–12 long 13–15 wide, 3a 18–21, 11–12 apart, eu minute, surface below eugenital setae with short lines.

Larva — (n=3). Body vermiform, 130–139 including gnathosoma, 32–34 wide.

Gnathosoma 12–15, cheliceral stylets 10–11, ep 1–2, d 2–3. Prodorsal shield subtriangular, smooth, 12–14, 22–24 wide. Scapular tubercles on rear shield margin, 18–20 apart, sc 9–11, directed backward. Coxigenital area smooth; 1b 2–3, 5–6 apart; 1a 7–9, 3–4 apart; 2a 10–11, 13–14 apart; 3a 4–5, 4 apart.

Leg I 13–14, femur 2–3, bv 3–4; genu 2, l″ 9–10; tibia 2, l′ 1–2; tarsus 2–3; empodium simple 2–3, 3-rayed, ω 2–3 tapered, ft′ 5–7, ft″ 10–11, u′ 1–2. Leg II 10–12, femur 2–3, bv 3–5; genu 2, l″ 5–6; tibia 2; tarsus 2–3; empodium 2–3, 3-rayed, ω 2–3 tapered, ft′ 5–7, seta ft″ 11–13, u′ 1–2.

Opisthosoma with 30–35 smooth annuli. Setae c2 7–8, 30–31 apart, on annulus 5 from coxae II; d 9–10, 28 apart, on annulus 10; e 9–10, 16 apart, on annulus 17–18; f 11–13, 20–21 apart, on 4^th annulus from rear, h1 1–2; h2 15–22.

Host plant

Tamarix senegalensis DC. (=T. nilotica) in Egypt and T. usneoides E. May. ex Bunge. (Tamaricaceae) in South Africa.

Relation to the host plant — Mites were collected from leaf axils and twigs; they cause rusting symptoms and deformations on the plants.

Etymology

The name ''benhaiensis'' refers to the type location; Benha city, Qalyubia governorate, Egypt, where the type specimens were collected + suffix –iensis, meaning coming from.

Type locality

Benha city (30°26′04.62″N, 31°11′24.22″E), Qalyubia governorate, Egypt, 9 March, 2021, coll. Ashraf Elhalawany.

Type material

Holotype: female (slide no. EGYErio110.1), deposited at ARC-PPRI, Egypt. Paratypes: ten females, five males and five nymphs on five slides (slides no. EGYErio110.2–110.6), 10 January 2019, deposited at ARC-PPRI, Egypt. Five paratype females on two slides (slide no. EGYErio55.7–55.8), 14 November, 2017, with the same data as holotype, deposited at ESAM, Egypt. Two slides with the same data as holotype, 9 March 2021, deposited at Zoological Institute of the Russian Academy of Sciences (ZIN RAS), Russia. Two slides, 10 January 2019, deposited at the College of Agriculture and Forestry, West Virginia University (WVU), USA.

Additional material — Mites morphologically very similar to A. benhaiensis n. sp. from Egypt were also found under scaly leaves on T. usneoides in South Africa. In order to test the conscpecificity of the mites from Egypt and South Africa we extracted mite DNA and performed PCR of three marker genes (Cox1, D1D2 28S and ITS1-5.8S-ITS2). Only samples from South Africa provided postitve PCR results. This is most likely because of inappropriate storage of the Egyptian material prior to DNA extraction (the samples spent almost four months in the post office until they were delivered to Russia). Although genetic data on the mites from Egypt were unavailable for comparison, in this paper we consider specimens from Egypt and South Africa conspecific because morphologically they were indistinguishable and assign them to the same species, A. benhaiensis n. sp., until it is disproved by PCR. In South Africa these mites were found in two localities situated about 200 kilometers from each other: (1) near Noorspoort farm, Steytlerville, Eastern Cape, 33.412778°S, 24.565556°E, 22 November 2022, coll. N. Ngubane-Ndhlovu, and (2) near Dwayka River, Western Cape (33.130000°S, 21.778056°E), same date and collector. Additional materials are deposited at The Department of Agriculture, Land Reform and Rural Development at Plant Quarantine Station in Stellenbosch, South Africa and at Zoological Institute of the Russian Academy of Sciences (ZIN RAS), Russia.

Remarks on population of A. benhaiensis from South Africa (Figures 7, 8)

When compared to the Egyptian population, measurements of South African specimens of A. benhaiensis n. sp. were within the ranges of most characters except for the setae that were relatively longer in mites from South Africa. Females from Noorspoort (n=12): 1a 20–38, 2a 28–46; d 34–62, e 33–49, f 30–43, and h2 60–85. Male from Noorspoort (n=5): 1a 21–27, 2a 33–39, bv I 13–20, opithosoma with 47–50 dorsal annuli, d 42–42, and e 36–38, 3a 35–42. Both males and females from Noorspoort had 6-7 empodium rays, the rays were sometimes asymetrical.

GenBank data and Blast search results

Six sequences of three marker genes for three DNA isolates of A. benhaiensis n. sp. from Noorspoort and Dwayka were obtained (Table 3). Two D1D2 28S and two Cox1 sequences from Noorspoort were pairwise identical as well as the ITS sequences from different localities. Blastx search for Cox1 sequences of A. benhaiensis n. sp. against Aceria from GenBank returns the best hit sequence as AIT38252.1 of Aceria sp. from Tamarix sp. from India (this sequence originated from an unpublished study by Menon, Chandrabose and Ramamurthy) with about 90% identity and 56% coverage when sorted by identity. Additionally, blast alignments show that contrary to all other Aceria from GenBank both Cox1 sequences of A. benhaiensis n. sp. have one codon deletion about 500 bp in the 3′ direction from the Cox1 start codon.

Differential diagnosis

Aceria benhaiensis n. sp. is morphologically close to A. aegyptytamaricis n. sp. (described above) in prodorsal shield design, shape of microtubercles, and smooth coxae and genital coverflap. The new species can be differentiated by size of the body, number of dorsal and ventral semiannuli, and lengths of prodorsal shield and setae sc, c2, d, e, f and 3a (Table 4). It is also close to deutogynes of A. tamaricis (Trotter) (described below). The main differences are in the ornamentation of prodorsal shield (median and admedian lines present in the new species but absent in A. tamaricis), shape of microtubercles (linear elongate microtubercles in new species and more rounded microtubercles in A. tamaricis), number of empodial rays and opisthosomal annuli and lengths of prodorsal shield and setae sc, c2, d, e and 3a (Table 4).

Aceria dioicae (Keifer 1979)

(Figures 9–10)

Supplementary description

Female — (n=15). Body vermiform, 200 (155–217) including gnathosoma, 50 (46–51) wide, 49 (49–54) thick; yellowish.

Gnathosoma 26 (23–28), projecting obliquely downwards, ep 3 (2–3), d 7 (6–8), v 1–2, cheliceral stylets 18 (17–20) long.

Prodorsal shield 29 (27–30) long, 33 (33–37) wide. Median line short, present only in posterior ¼ of prodorsal shield. Admedian lines distinct in posterior ⅓, weak in medial ⅓ and absent in anterior 1/3 of prodorsal shield. Submedian I very short, situated near basis of sc tubercle. Posterior ends of median, admedian and submedian I lines connected with sinuous transverse line forming medio-posterior margin of prodorsal shield between tubercles of sc. One or two short curved lines (putative submedian II and III) present in lateral fields of prodorsal shield. Scapular tubercles 22 (21–23) apart, sc 23 (23–35), directed backward. Coxigenital area smooth, with four semiannuli between coxae and genitalia, prosternal apodeme 6 (6–7), forked posteriorly; 1b 10 (9–11), 9 (9–10) apart; 1a 20 (18–20), 7 (6–7) apart; 2a 29 (28–37), 20 (19–21) apart.

Leg I 26 (25–27), femur 8 (8–9), bv 10 (8–11); genu 4 (4–5), l″ 25 (22–25); tibia 4 (4–5), l′ 5 (5–6), located in the middle from dorsal base; tarsus 5 (4–5); empodium simple 7 (7–8), 7-rayed, n. sp. ω tapered, 8 (7–8), ft′ 16 (14–16), ft″ 20 (17–25), u′ 3 (2–3). Leg II 21 (20–21), femur 12 (11–13), bv 13 (12–15); genu 4 (3–4), l″ 10 (8–10); tibia 4 (3 –4); tarsus 4 (4–5); empodium simple 7 (7), 7-rayed, ω tapered 8 (7–8), ft′ 15 (12–15), ft″ 20 (16–23), u′ 2 (2–3).

Opisthosoma dorsally evenly arched, with 56 (54–57) dorsal and 51 (50–55) ventral semiannuli. Dorsal and ventral semiannuli with subcircular microtubercles ahead of rear annuli margin, except the last 10–11^th dorsal annuli bearing pointed microtubercles and the last 5–6^th ventral annuli bearing linear elongate microtubercles. Setae c2 35 (30–48), 44 (44–46) apart, on annulus 7 (7–8) from coxae II; d 40 (38–45), 30 (30–32) apart, on annulus 15 (15–16); e 37 (37–42), 15 (15–16) apart, on annulus 30 (28–30); f 35 (34–40), 30 (30–31) apart, on 8^th annulus from rear, h1 4 (4–5), h2 50 (45–63). External genitalia. Genital coverflap subtriangular, smooth, 13 (13–14), 17 (17–18) wide, 3a 30 (27–44), 11 (11–12) apart.

Male — (n=5). Similar to female, body vermiform, 135–180 including gnathosoma, 45–48 wide and 44–52 thick, whitish.

Gnathosoma 20–25, cheliceral stylets 15–19, ep 2–3, d 6–8. Prodorsal shield pattern similar to that of female, 27–29, 32–37 wide; Scapular tubercles on rear shield margin, 21–25 apart, sc 24–34, directed backward. Coxigenital area smooth, prosternal apodeme 4–6, forked; 1b 6–9, 9–10 apart; 1a 17–19, 6–7 apart; 2a 19–23, 18–19 apart.

Leg I 25–26, femur 7–8, bv 8–10; genu 3–4, l″ 23–24; tibia 3–4, l′ 3–4; tarsus 4–5; empodium simple 6–7, 7-rayed, ω 6–7 tapered, ft′ 13–15, ft″ 19–24, u′ 2–3. Leg II 20–21, femur 7–8, bv 7–9; genu 3–4, l″ 8–10; tibia 3–4; tarsus 4–5; empodium 6–7, 7-rayed, ω 6–7 tapered, ft′ 11–15, ft″ 17–19, u′ 2–3.

Opisthosoma with 52–55 dorso-ventrally semiannuli, microtubercles shape similar to that of female. Setae c2 25–28, 44–46 apart, on annulus 7–8 from coxae II; d 30–35, 27–28 apart, on annulus 15–16; e 25–30, 15–16 apart, on annulus 29–30; f 27–30, 24–27 apart, on 8^th annulus from rear, h1 4–6, h2 40–51. Male genital area 13–15 long, 19–22 wide, eu minute, genital cuticle behind tubercles of eu with granules, 3a 26–40, 15–17 apart.

Nymph — (n=5). Body vermiform, 140–165 including gnathosoma, 48–52 wide, 48–52 thick.

Gnathosoma 15–17, cheliceral stylets 15–17, ep 1–2, d 4–5. Prodorsal shield 21–23, 35–40 wide; with median and admedian lines at ⅔ posterior of prodorsal shield. Scapular tubercles on rear shield margin, 17–20 apart, sc 12–16, directed backward. Coxigenital area smooth; 1b 5–7, 10–11 apart; 1a 9–13, 10–11 apart; 2a 12–15, 21–24 apart; 3a 13–15, 7–8 apart.

Leg I 17–19, femur 3–4, bv 5–6; genu 3, l″ 11–13; tibia 3, l′ 3; tarsus 4; empodium simple 4, 4-rayed, ω 4 tapered, ft′ 10–13, ft″ 15–18, u′ 1–2. Leg II 13–15, femur 3–4, bv 5; genu 2–3, l″ 4–6; tibia 2–3; tarsus 3–4; empodium 4, 4-rayed, ω 4–5 tapered, ft′ 5–7, ft″ 13–15, u′ 1–2. Opisthosoma with 48–52 annuli with pointed microtubercles on rear annuli. Setae c2 13–17, 42–43 apart, on annulus 7 from coxae II; d 17–22, 30–32 apart, on annulus 14–15; e 16–19, 16–18 apart, on annulus 25–26; f 25–28, 30–31 apart, on 6^th annulus from rear, h1 1–2, h2 30–35.

Larva — (n=3). Body vermiform, 105–120 including gnathosoma, 42–46 wide, 47–50 thick.

Gnathosoma 15–17, cheliceral stylets 12–13 long, ep 1–2, d 3–5. Prodorsal shield subtriangular, 20–22 long, 35–37 wide; median line absent, admedian lines at ⅔ posterior of prodorsal shield. Scapular tubercles on rear shield margin, 18–19 apart, sc 11–13, directed backward. Coxigenital area smooth; 1b 4–6, 8–9 apart; 1a 9–11, 6–7 apart; 2a 13–15, 151–17 apart; 3a 12–15, 2–3 apart.

Leg I 17–18, femur 3–4, bv 3–4; genu 2–3, l″ 10–13; tibia 2–3, l′ 2–3; tarsus 3–4; empodium simple 4, 4-rayed, ω 4–5 tapered, ft′ 10–12, ft″ 14–16, u′ 1–2. Leg II 13–14, femur 3, bv 4; genu 2, l″ 3–5; tibia 2–3; tarsus 3–4; empodium 4, 4-rayed, ω 4–5 tapered, ft′ 5–7, ft″ 8–11, u′ 1–2.

Opisthosoma with 38–43 annuli, with pointed microtubercles on rear annuli. Setae c2 12–15, 35–37 apart, on annulus 7–8 from coxae II; d 19–21, 28–29 apart, on annulus 14–15; e 13–16, 16–17 apart, on annulus 22–23; f 18–20, 18–19 apart, on 6^th annulus from rear, h1 1–2, h2 18–22.

Host plant in Egypt

Tamarisk (athel), Tamarix senegalensis DC. (=Tamarix nilotica) and Tamarix spp. (Tamaricaceae).

Relation to the host plant — Mites cause green galls on buds and twigs, about 8–11 mm long and 4–5 mm in diameter (Figure 1 A, B).

Distribution

Egypt; Iran; Pakistan and Turkey

Material examined

Fifteen females, five males, four nymphs and four larvae on five slides (slide no. EGYErio37.1–37.5), from T. senegalensis, deposited in the Plant Protection Research Institute collection, Giza, Egypt, 9 March, 2021, Qalyubia governorate (30°16′14.03» N, 31°14′7.28» E), coll. Ashraf Elhalawany. Four slides (slides no. EgTT01-04) with the same data, deposited at UNIBA, Italy. Four slides with the same data, deposited at Zoological Institute of the Russian Academy of Sciences (ZIN RAS), Russia. Two slides (Acy 13/371), 14 November 2017, deposited at Agriculture Research Council, Plant Health Protection, Biosystematics Division, Pretoria, South Africa ARC-PHP; two slides (NJAUAcariEriEgypt28) 14 November 2017, were deposited in the mite collection of Department of Entomology, College of Plant Protection, Nanjing Agricultural University (NJAU), China; two slides, 19 February 2019, deposited at the College of Agriculture and Forestry, West Virginia University (WVU), USA. Five females on two slides (slide no. EGYErio37.6–37.7), 28 January 2023, deposited at ESAM, Egypt.

Remarks

Aceria dioicae was described from a bud gall of Tamarix dioica Roxb. from the USA (Keifer 1979). The morphometrics of the females from Egypt and those from original description coincide.

Aceria noorspoortiensis Situngu, Ngubane-Ndhlovu et Chetverikov n. sp.

Aceria amrini in Chetverikov et al. 2019:1287

ZOOBANK: F09E50D8-1C3B-4E8B-8DE4-7B1451A66F16

(Figures 11–14)

Description

Female — (n=10). Body vermiform, 211 (157–211) including palps, 47 (38–54) wide; semitransluscent to white.

Gnathosoma 16 (14–19), projecting obliquely downwards, d 6 (4–6), cheliceral stylets 12 (12–16) long, v minute. Prodorsal shield 24 (22–27), 28 (26–34) wide; smooth, almost rounded with an incomplete quadrilateral to pentagonal shaped ditch posteriorly. Scapular tubercles on rear shield margin, 22 (17–22) apart, sc 37 (32–41), directed backward. Coxigenital area smooth, with 3 (2-3) coxigenital annuli before epigynum, prosternal apodeme inversely Ψ-shaped, 1b 7 (4–8), 7 (6–10) apart; 1a 22 (16–28), 6 (5–6) apart; 2a 22 (21–41), 20 (19–22) apart.

Leg I 22 (19–22), femur 7 (–7), bv 11 (9–13); genu 4 (4–5), l″ 14 (14–23); tibia 4 (4–5), l′ 4 (3–4), tarsus 4 (4–5); empodium simple 6 (5–7), 6-rayed, ω tapered, 7 (5–7), ft′ 12 (6–12), ft″ 23 (20–33), u′ 3 (3–4). Leg II 22 (18–22), femur 6 (4–7), bv 13 (10–15); genu 3 (3–4), l″ 4(4–8); tibia 4 (3-4); tarsus 4 (4–5); empodium simple 6 (5–7), 6-rayed, ω tapered 7 (6–7), ft′ 7 (4–7), ft″ 20 (20–23), u′ 4 (3–4).

Opisthosoma dorsally evenly arched, with 59 (54-60) dorsal and 49 (44-50) ventral annuli. All dorsal annuli microtuberculated except for the last 6-7 (telosomal) annuli with rounded microtubercles in most species, and rectangular-like microtubercles on the rear margin of annuli in some specimens. Ventral annuli with smaller round or faint rectangular microtubercles on rear margin of annuli. Telosomal ventral annuli (posterior to f setae) with spiky overlapping microtubercles. Setae c2 63 (36–67), 45 (36–47) apart, on annulus 8 (4–8) from shield; d 53 (35–72), 37 (28–37) apart, on annulus 15 (11–16); e 43 (38–45), 19 (12–19) apart, on annulus 28 (11–13); f 32 (32–38), 28 (27–31) apart, on 7 (6–7^th) annulus from rear, h1 4 (4–5); h2 68 (68–86). External genitalia genital coverflap smooth, subtriangular, 14 (9–14), 18 (12–18) wide, 3a, 48 (34–62), 17 (9–17) apart. Internal genitalia with trapezoidal anterior genital apodeme, relatively short longitudinal bridge; distinct oblique apodeme; short spermathecal tubes directed laterad; and round spermathecae each of them with distinct spermathecal process.

Nymph — (n=1). Body vermiform, transluscent, 137 including palps, 37 wide.

Gnathosoma 16, cheliceral stylets 16 long. Prodorsal shield smooth. Scapular tubercles on rear shield margin, 16 apart, sc 16, directed backwards. Coxigenital area smooth; 1a 5 apart; 2a, 18 apart.

Leg I 16, Leg II 15.

Opisthosoma with 50 smooth dorsal and 42 smooth ventral annuli. Setae c2 27, 34 apart; d 27, 25 apart; e 24, 15 apart; f 17, 24 apart.

Larva — (n=1). Body vermiform, transluscent, 110, 46 wide. Prodorsal shield smooth. Scapular tubercles on rear shield margin, 19 apart, sc 18, directed backwards. Coxigenital area smooth; 1a 5 apart; 2a, 16 apart. Leg I 15, Leg II 14, Opisthosoma with 56 smooth dorsal and 45 smooth ventral annuli. Lateral c2 15, 37 apart; setae d 16, 28 apart; e 17, 15 apart; f 17, 22 apart.

Host plant

Tamarix usneoides E. Mey. ex Bunge.

Relation to the host plant — Mites cause bright pink galls on young shoots (Figure 1G-J).

Etymology

The name ''noorspoortiensis'' refers to the location Noorspoort, Steytlerville, Eastern Cape, South Africa.

Type locality

The mites are found in Noorspoort farm, Steytlerville, Eastern Cape (33.412778°S, 24.565556°E) and near Dwayka River, Western Cape (33.130000°S, 21.778056°E).

Type material

Holotype: female (slide no. X2021-01(#2)), paratypes: Ten females (slides X2021-01 and X2021-04), nymph (slide X2021-10) and larva (slide X2021-12) are deposited at Department of Agriculture, Land Reform and Rural Development at Plant Quarantine Station in Stellenbosch, South Africa. Additionally some paratype material has been deposited at Zoological Institute of the Russian Academy of Sciences (ZIN RAS), Russia.

Additional material — Adult mites on slide #4287, SOUTH AFRICA: Noorspoort, right bank of Grootrivier, 33°18′12.1″S, 24°21′58.6″E; in red-purple callus-like abnormal growth on twigs of Tamarix usneoides Mey. ex Bunge (Tamaricaceae), 5 November 2016, coll. P.E. Chetverikov, C. Craemer, S. Neser

Remarks

This species was first found in Noorspoort (South Africa) in 2016 and identified as Aceria amrini Joshi et al. 2013 (Chetverikov et al. 2019b). In 2021 and 2022 the mites were recollected in Noorspoort by N. Ngubane-Ndhlovu and comprehensively reinvestigated in this study. Morphological comparison of the mites from Noorspoort with specimens of A. amrini from Egypt showed that they belong to different species: Aceria noorspoortiensis n. sp. and A. amrini correspondingly.

GenBank data and Blast search results

Eleven sequences of three marker genes for seven isolates of A. noorspoortiensis n. sp. from Noorspoort and Dwayaka River were obtained. All ITS and D1D2 28S sequences from both localities were pairwise identical as well as all Cox1 sequences from Noorspoort. Similar to Aceria benhaiensis n. sp. (see above) Blastx search for Cox1 sequences OR133635 and OR133636 of A. noorspoortiensis n. sp. against Aceria from GenBank (a) returns the best hit was the sequence AIT38252.1 (Aceria sp. from Tamarix sp. from India, 87% identity, 55% coverage) when sorted by identity and (b) showed one homologous codon deletion in the same region, about 500 bp in the 3′ direction from the Cox1 start codon. Codon-deletion mutations in the middle part of Cox1 gene are rare in Eriophyoidea and currently known in only three eriophyoid species (all from Phytoptidae s.l.): Phytoptus avellanae Nalepa, Retracrus johnstoni Keifer, and Trisetacus indelis Chetverikov et al. (Cvrković et al. 2016, Chetverikov et al. 2021, 2022). The two new species of the genus Aceria described in this study (A. benhaiensis n. sp. and A. noorspoortiensis n. sp.) are the first reported taxa from the large subfamily of gall mites, Eriophyinae, possessing codon deletion in the middle part of Cox1 gene..

Differential diagnosis

Aceria noorspoortiensis n. sp. causes very characteristic pink galls on young shoots of T. usneoides (Fig. 1 G-J) and very often coexists with A. benhaiensis n. sp. that is a common inquiline in the galls caused by A. noorspoortiensis n. sp. Incomplete quadrilateral or pentagonal ditch on the prodorsal shield and the absence of median line unambiguously differentiate A. noorspoortiensis n. sp. from all other Aceria spp. associated with Tamarix.

Aceria tamaricis (Trotter)

(Figure 15)

Supplementary description

Female protogyne — (n=8). Body vermiform, 240 (157–245) including gnathosoma, 57 (46–62) wide, 50 (42–57) thick; yellowish.

Gnathosoma 21 (20–21), projecting obliquely downwards, ep 3 (2–4), d 7 (7–9), cheliceral stylets 18 (16–18) long. Prodorsal shield 28 (25–28), 33 (30–38) wide; semicircular; a small median pit present near rear shield margin. Scapular tubercles on rear shield margin, 25 (25–27) apart, sc 37 (37–48), directed backward. Coxigenital area smooth, with three semiannuli between coxae and genitalia, prosternal apodeme 6 (6–7); 1b 10 (9–10), 9 (9–10) apart; 1a 30 (27–33), 7 (6–7) apart; 2a 35 (33–45), 20 (20–22) apart.

Leg I 26 (24–28), femur 8 (8–9), bv 15 (15–17); genu 4 (4–5), l″ 25 (25–27); tibia 5 (5), l′ 8 (8–10), located at ⅔ from dorsal base; tarsus 5 (4–6); tarsal empodium simple 8 (8–10), 7–8-rayed, tarsal solenidion ω tapered, 9 (9–10), ft′ 23 (23–26), ft″ 25 (25–27), u′ 4 (3–5). Leg II 25 (24–27), femur 8 (8–9), bv 15 (14–15); genu 4 (4–5), l″ 15 (15–16); tibia 4 (3–4); tarsus 5 (5–6); tarsal empodium simple 8 (8–9), 7-rayed, ω tapered 8 (8–9), ft′ 15 (13–15), ft″ 20 (20–27), u′ 4 (3–5).

Opisthosoma dorsally evenly arched, with 60 (58–63) annuli. Dorsal and ventral semiannuli with elliptical microtubercles ahead of rear annuli margin, except the last 4^th dorsal annuli with pointed microtubercles and last 8^th ventral annuli with linear elongate. Setae c2 30 (30–32), 45 (40–50) apart, on annulus 7 (6–7) from coxae II; d 60 (55–70), 41 (41–43) apart, on annulus 15 (15–16); e 41 (41–50), 20 (20–22) apart, on annulus 31 (31–32); f 35 (35–42), 39 (39–40) apart, on 8^th annulus from rear, h1 6 (6–7), h2 75 (70–84). External genitalia. Genital coverflap subtriangular, smooth, 13 (13–14), 20 (20–22) wide, 3a, 45 (45–54), 13 (13–14) apart.

Female deutogyne — (n=7). Body vermiform, 190 (137–190) including gnathosoma, 50 (44–56) wide, 53 (53–55) thick; yellowish.

Gnathosoma 21 (20–22), projecting obliquely downwards, ep 3 (2–3), d 7 (7–8), cheliceral stylets 18 (16–20) long. Prodorsal shield 25 (23–25), 28 (28–32) wide; semicircular with a small medioposterior pit. Scapular tubercles on rear shield margin, 22 (20–22) apart, sc 36 (36–42), directed backward. Coxigenital area smooth, with three semiannuli between coxae and genitalia, prosternal apodeme 6 (6–7); 1b 10 (9–11), 9 (8–10) apart; 1a 25 (22–27), 7 (6–7) apart; 2a 30 (30–35), 20 (20–22) apart.

Leg I 26 (26–28), femur 9 (9–10), bv 15 (13–16); genu 4 (4–5), l″ 24 (22–24); tibia 6 (6–7), l′ 8 (7–10), located at ⅔ from dorsal base; tarsus 5 (5–6); tarsal empodium simple 8 (7–8), 8-rayed, tarsal solenidion ω tapered, 8 (7–8), ft′ 18 (18–22), ft″ 25 (22–27), u′ 4 (3–4). Leg II 25 (25–28), femur 8 (8–9), bv 15 (14–16); genu 4 (4–5), l″ 15 (13–15); tibia 5 (4–6); tarsus 6 (6–7); tarsal empodium simple 8 (7–9), 8-rayed, ω tapered 8 (7–8), ft′ 14 (11–14), ft″ 25 (21–30), u′ 4 (3–5).

Opisthosoma dorsally evenly arched, with 55 (54–57) annuli. Dorsal and ventral semiannuli with elongate microtubercles ahead of rear annuli margin, except the last 4^th dorsal annuli with pointed microtubercles and last 8^th ventral annuli with linear elongate. Setae c2 30 (30–36), 32 (32–50) apart, on annulus 7 (6–7) from coxae II; d 40 (40–58), 40 (30–42) apart, on annulus 15 (15–16); e 40 (40–45), 20 (15–20) apart, on annulus 30 (29–31); f 30 (30–38), 35 (30–38) apart, on 8–9^th annulus from rear, h1 6 (5–6), h2 60 (59–72). External genitalia genital coverflap subtriangular, smooth, 13 (12–13), 20 (20–21) wide, 3a, 40 (40–54), 11 (10–12) apart.

Male — (n=3). Similar to protogyne female. Body vermiform, 150–188 including gnathosoma, 48–57 wide and 48–51 thick; whitish.

Gnathosoma 20–23, cheliceral stylets 17–18, ep 2–3, d 5–7. Prodorsal shield pattern similar to that of female, 20–23, 25–30 wide; scapular tubercles on rear shield margin, 22–24 apart, sc 30–38, directed backward. Coxigenital area smooth, prosternal apodeme 4–5; 1b 6–8, 8–10 apart; 1a 20–25, 6–7 apart; 2a 26–31, 20–23 apart.

Leg I 22–25, femur 7–8, bv 12–13; genu 4–5, l″ 12–14; tibia 4–5, l′ 6–8; tarsus 5; empodium simple 6–7, 7-rayed, ω 6–7 tapered, ft′ 15–21, ft″ 20–24, u′ 3–4. Leg II 21–23, femur 6–7, bv 7–9; genu 4, l″ 8–10; tibia 3–4; tarsus 4–5; empodium 6–7, 7-rayed, ω 6–7 tapered, ft′ 10–12, ft″ 18–23, u′ 3–4.

Opisthosoma with 52–55 annuli, with microtubercles shaped similar to those of protogyne female. Setae c2 20–25, 43–45 apart, on annulus 6–7 from coxae II; d 29–33, 32–34 apart, on annulus 14–15; e 28–30, 20–21 apart, on annulus 28–30; f 25–27, 23–25 apart, on 8^th annulus from rear, h1 5–6, h2 55–60. External genitalia 12–14, 16–17 wide, genital cuticle behind eugenital setae with granules, 3a 28–30, 12–13 apart.

Host plant in Egypt

Tamarisk (athel), Tamarix senegalensis DC. (=Tamarix nilotica) and Tamarix spp. (Tamaricaceae).

Relation to the host plant — Mites cause green galls on buds and twigs, about 5–6.5 mm long and 3–4 mm diameter, elongate (Figure 1 D).

Distribution

China; France; Egypt (first continental record); Greece; Turkey.

Material examined

Ten females and five males on five slides (slide no. EGYErio29.1–29.5), from T. senegalensis, deposited in the Plant Protection Research Institute collection, Giza, Egypt, 9 March, 2021, Qalyubia governorate (30°16′14.03″N, 31°14′7.28″E), coll. Ashraf Elhalawany. Four slides (slides no. EgTT05-08) with the same data, deposited at UNIBA, Italy. Three slides with the same data, deposited at Zoological Institute of the Russian Academy of Sciences (ZIN RAS), Russia. Two slides (Acy 13/370) deposited at Agriculture Research Council, Plant Health Protection, Biosystematics Division, Pretoria, South Africa (ARC-PHP); two slides, 10 January 2019 (NJAUAcariEriEgypt29) were deposited in the mite collection of Department of Entomology, College of Plant Protection, Nanjing Agricultural University (NJAU), China; two slides, 19 February 2019, deposited at the College of Agriculture and Forestry, West Virginia University (WVU), USA. Ten females on two slides (slide no. EGYErio29.6–29.7), Mariotya city (30°01′25.51″N, 31°81′22.94″E), Giza governorate, 28 January 2023, deposited at (ESAM), Egypt.

Remarks

Aceria tamaricis (Trotter) was redescribed by Castagnoli (1992) and later by de Lillo and Sobhian (1994) based on material from Italy from the bud gall on Tamarix gallica.The morphometry of the female appears to match the description by Castagnoli in 1992. The morphometrics of the females from Egypt and those from Italy investigated by Castagnoli (1992) coincide.

Acknowledgements

This research was supported by the National Research Foundation of South Africa (Grant number: 129698) and the Female Academic Leader's Fellowship Grant. The first author wishes to thank Prof James Wesley-Smith from the Microscopy Unit at Sifako Makgatho Heath University as well as Professor Marcus Byrne and Mr Danica Lukac for alerting her of the presence of galls on the Tamarix tree. DIC LM studies, DNA extraction and PCR were supported by the Russian Foundation for Basic Research (Grant; #21-54-46003 CT_a) and the Zoological Institute of RAS (Grant #122031100263-1). Sequencing was performed at The Centre for Molecular and Cell Technologies and The Bio-Bank Resource Center of The Research Park of Saint-Petersburg State University (SPbSU, Russia). A work visit of S.S. and N.N. to Saint-Petersburg was partially supported by SpbSU (project #100352118) and was performed within the framework agreement for cooperation between Saint-Petersburg State University (Russia) and University of the Witwatersrand, Johanesburg, South Africa.

Declaration of Competing Interests

The authors have no conflict of interest.

References

1. Abou-Awad B.A., El-Borolossy M.A. 1995. Two eriophyid mites on tamarisk trees in Egypt (Acari: Eriophyoidea: Eriophyidae). Acarologia, 36(2): 145-148.
2. Amrine J.W.Jr., Manson D.C.M. 1996. Preparation, mounting and descriptive study of eriophyoid mites. In Eriophyoid Mites: Their Biology, Natural Enemies and Control. World Crop Pests; Lindquist, E.E., Sabelis, M.W., Bruin, J., Eds.; Elsevier Science Publishing: Amsterdam, Netherlands; Volume 6, pp. 383-396. https://doi.org/10.1016/S1572-4379(96)80023-6
3. Amrine J.W.Jr., Stasny TA. 1994. Catalog of the Eriophyoidea (Acari: Prostigmata) of the World. Michigan: Indira Publishing House, 798 pp.
4. Amrine J.W. Jr., Stasny T.A., Flechtmann C.H.W. 2003. Revised Keys to the World Genera of the Eriophyoidea (Acari: Prostigmata). Indira Publishing House, West Bloomfield, Michigan. 244pp.
5. Bakr E.M. 2005. A new software for measuring leaf area, and area damaged by Tetranychus urticae Koch. J. Appl. Entomol., 129 (3): 173-175. https://doi.org/10.1111/j.1439-0418.2005.00948.x
6. Baum B.R 1978. The genus Tamarix. Israel Academy of Sciences and Humanities, Jerusalem
7. Bolton S.J., Chetverikov P.E., Ochoa R., Klimov P.B. 2023. Where Eriophyoidea (Acariformes) Belong in the Tree of Life. Insects, 14, 527. doi: 10.3390/insects14060527 https://doi.org/10.3390/insects14060527
8. Boulos L. 1999. Flora of Egypt. Al Hadara Publishing, Cairo, Egypt, 283 pp.
9. Bredenkamp C.L. 2003. Tamaricaceae. In: Germishuizen, G., Meyer, N.L. (Eds.), Plants of the southern Africa. National Botanical Institute, Pretoria.p.927.
10. Byrne M.J., Mayonde S., Venter N., Chidawanyika F., Zachariades C., Martin G. 2021. Three New Biological Control Programmes for South Africa: Brazilian Pepper, Tamarix and Tradescantia. African Entomolo., 29(3): 965-982. https://doi.org/10.4001/003.029.0965
11. Castagnoli M. 1992. Redescription of Aceria tamaricis (Trotter, 1901) (Acari Eriophyidae). Redia, 75(2): 447-45.
12. Chetverikov P.E., Bertone, M. 2022. First rhyncaphytoptine mite (Eriophyoidea, Diptilomiopidae) parasitizing american hazelnut (Corylus americana): molecular identification, confocal microscopy, and phylogenetic position. Exp. Appl. Acarol., 88: 75-95. https://doi.org/10.1007/s10493-022-00740-9
13. Chetverikov P.E., Bolton S.J., Gubin A.I., Letukhova V.Y., Vishnyakov A.E., Zukoff, S. 2019a. The anal secretory apparatus of Eriophyoidea and description of Phyllocoptes bilobospinosus n. sp. (Acariformes: Eriophyidae) from Tamarix (Tamaricaceae) from Ukraine, Crimea and USA. Syst. Appl. Acarol., 24(1): 139-157. https://doi.org/10.11158/saa.24.1.11
14. Chetverikov P.E., Craemer C., Cvrković T., Efimov P.G., Klimov P.B., Petanović R.U., Sukhareva S.I. 2019b. First pentasetacid mite from Australasian Araucariaceae: morphological description and molecular phylogenetic position of Pentasetacus novozelandicus n. sp. (Eriophyoidea, Pentasetacidae) and remarks on anal lobes in eriophyoid mites. Syst. Appl. Acarol., 24(7): 1284-1309. https://doi.org/10.11158/saa.24.7.12
15. Chetverikov P.E., Klimov P.B., He Q. 2022. Vertical transmission and seasonal dimorphism of eriophyoid mites (Acariformes, Eriophyoidea) parasitic on the Norway maple: a case study. Royal Society Open Science, 9(9): 220820. https://doi.org/10.1098/rsos.220820
16. Chetverikov P.E., Craemer C., Gankevich V.D., Vishnyakov A.E., Zhuk A. S. 2023. A New Webbing Aberoptus Speciesspecies from South Africa Provides provides insight in Silk silk production in Gall Mitesgall mites (Eriophyoidea). Diversity, 15(2): 151. https://doi.org/10.3390/d15020151
17. Chetverikov, P.E.; Craemer, C.; Cvrković, T.; Klimov, P.B.; Petanović, R.U.; Romanovich, A.E.; Sukhareva, S.I.; Zukoff, S.N.; Bolton, S.; Amrine, J. 2021. 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. Appl. Acarol., 83, 31-68. https://doi.org/10.1007/s10493-020-00571-6
18. Chetverikov, P. E., Rector, B. G., Tonkel, K., Dimitri, L., Cheglakov, D. S., Romanovich, A. E., & Amrine, J. (2022). Phylogenetic position of a new Trisetacus mite species (Nalepellidae) destroying seeds of North American junipers and new hypotheses on basal divergence of Eriophyoidea. Insects, 13(2), 201. https://doi.org/10.3390/insects13020201
19. Cvrković, T.; Chetverikov, P.; 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. Appl. Acarol., 68, 83-96. https://doi.org/10.1007/s10493-015-9981-5
20. Cotte J. 1924. Les cecides des Alpes Maritimes et leurs producteurs. Mem. Soc. Linneenne de Provence. 3: 1-56.
21. Dçbski B. 1918 Liste des Cécidies signalées en Ègypte jusq′à ce jour. Bull. Soc. Entomol. Egypte, 1(4): 1-37.
22. de Lillo E., Skoracka A. 2010. What's ''cool'' on Eriophyoid mites? Exp. & Appl. Acarol., 51:3-30. https://doi.org/10.1007/s10493-009-9297-4
23. de Lillo E., Sobhian R. 1994. Taxonomy, distribution, and host specificity of a gall-making mite, Aceria tamaricis (Trotter) (Acari Eriophyoidea), associated with Tamarix gallica L. (Parietales: Tamaricaceae) in southern France. Entomologica, 28: 5-16.
24. de Lillo E., Pozzebon A., Valenzano D., Duso C. 2018. An intimate relationship between eriophyoid mites and their host plants - a review. Front Plant Sci., 9:1786. https://doi.org/10.3389/fpls.2018.01786
25. de Lillo, E., Freitas-Astúa, J., Kitajima, E. W., Ramos-Gonzalez, P. L., Simoni, S., Tassi, A. D., Valenzano D. 2021. Phytophagous mites transmitting plant viruses: update and perspectives. Entomologia generalis, 41(5): 439. https://doi.org/10.1127/entomologia/2021/1283
26. Desnitskiy A.G., Chetverikov P.E., Ivanova L.A., Kuzmin I.V., Ozman-Sullivan S.K., Sukhareva S.I. 2023. Molecular Aspectsaspects of Gall Formation Inducedgall formation induced by mites and insects. Life, 13: 1347. https://doi.org/10.3390/life13061347
27. Elhalawany A.S., Ezz ElDein S.A., Ibrahim N.A. 2023. Two new Eriophyes species (Acari: Eriophyidae) on Tamarisk trees from Egypt. Syst. Appl. Acarol., 28 (5): 838-851. https://doi.org/10.11158/saa.28.5.6
28. Harms R.S., Hiebert R.D. 2006. Vegetation response following invasive Tamarisk (Tamarix spp.) removal and implications for riparian restoration. Restoration Ecolo., 14: 461-472. https://doi.org/10.1111/j.1526-100X.2006.00154.x
29. Hosni H.A. 2000. Tamaricaceae in the flora of Egypt. Taeckholmia, 20(1): 17-31. https://doi.org/10.21608/taec.2000.12474
30. Ivanova L.A., Chetverikov P.E., Ivanov L.A., Tumurjav S., Kuzmin I.V., Desnitskiy, A.G., Tolstikov A.V. 2022. The effect of gall mites (Acariformes, Eriophyoidea) on leaf morphology and pigment content of deciduous trees in West Siberia. Acarina, 30: 89-98. https://doi.org/10.21684/0132-8077-2022-30-1-89-98
31. Joshi S., Menon, P., Ramamurthy, V.V. 2013. A new Eriophyid mite (Acari: Prostigmata) from India. The Bioscan, 8(1): 339-342.
32. Keifer H.H. 1940. Eriophyid studies VIII. Bulletin of the Department of Agriculture State of California, XXIX (1): 21-46.
33. Keifer H.H. 1944. Eriophyid studies XIV. Bulletin of the California Department of Agriculture, 33: 18-38.
34. Keifer H.H. 1979. Eriophyid studies C-16. Agricultural research Service, United State Department of Agriculture, 1-24.
35. Keifer H.H., Baker E.W., Kono T., Delfinado M., Styer W.E. 1982. An illustrated guide to plant abnormalities caused by eriophyid mites in North America. Agriculture handbook number 573, United States Dept. of Agriculture, 178pp.
36. Klimov P.B., OConnor B.M., Chetverikov P.E., Bolton S.J., Pepato A.R., Mortazavi A.L., Tolstikov A.V., Bauchan G.R., Ochoa R. 2018. Comprehensive phylogeny of acariform mites (Acariformes) provides insights on the origin of the four-legged mites (Eriophyoidea), a long branch. Molecular Phylogenetics and Evolution. 119: 105-117. https://doi.org/10.1016/j.ympev.2017.10.017
37. Klimov P.B., Chetverikov P.E., Dodueva I.E., Vishnyakov A.E., Bolton S.J. Paponova S.S., Lutova L.A., Tolstikov A.V. 2022. Symbiotic bacteria of the gall-inducing mite Fragariocoptes setiger (Eriophyoidea) and phylogenomic resolution of the eriophyoid position among Acari. Sci Rep-UK, 12: 3811. https://doi.org/10.1038/s41598-022-07535-3
38. Krantz G.W., Walter D.E., 2009. A Manual of Acarology. Third eddition. Texas Tech University Press; Lubbock, Texas, 807 pp.
39. Lindquist E.E. 1996. External Anatomy and Notation of Structures In: Lindquist EE, Sabelis MW, Bruin J, (Eds), Eriophyoid Mites. Their Biology, Natural Enemies and Control. Amsterdam: Elsevier, World Crop Pests, 6, p. 3-31. https://doi.org/10.1016/S1572-4379(96)80003-0
40. Marlin D., Newete S.W., Mayonde S.G. Etienne R.S, Byrne M.J. 2017. Invasive Tamarix (Tamaricaceae) in South Africa: current research and the potential for biological control. Biological Invasions, 19: 2971-2992. https://doi.org/10.1007/s10530-017-1501-6
41. Mayonde S., Cron G.V., Glennon K.L., Byrne M.J. 2019. Genetic diversity assessment of Tamarix in South Africa - Biocontrol and conservation implications. South African Journal of Botany, 121: 54-62. https://doi.org/10.1016/j.sajb.2018.10.030
42. Nalepa A. 1898. Zur Kenntniss der Gattung Trimerus Nal. Zool. Jahrbücher, 11(5): 405-411.
43. Paponova S.S., Chetverikov P.E., Pautov A.A., Yakovleva O.V., Zukoff S.N., Vishnyakov A.E., Sukhareva S.I., Krylova E.G., Dodueva I.E., Lutova L.A. 2018. Gall mite Fragariocoptes setiger (Eriophyoidea) changes leaf developmental program and regulates gene expression in the leaf tissues of Fragaria viridis (Rosaceae). Ann. Appl. Biolo., 172: 33-46. https://doi.org/10.1111/aab.12399
44. Petanović R., Kielkiewicz, M. 2010. Plant-eriophyoid mite interactions: specific and unspecific morphological alterations. Part II. Exp. Appl. Acarol., 51:81-91. https://doi.org/10.1007/978-90-481-9562-6_5
45. The Plant List (2023) Version 1.1. Published on the Internet. http://www.theplantlist.org/ (accessed 2^nd February 2023).
46. Trabut 1917. La galle du Tamarix articulate dite Tak′out au Maroc. Bull. Soc. Hist. Nat. Afrique Nord, Algiers, 3: 29-30.
47. Trotter A. 1901. Di una nuova specie d'acaro (Eriophyes) d'Asia minore produttore di galle su Tamarix. Atti Reale Ist. Ven. Sci. Lett. Arti, 60, II: 953-955.
48. Zhang Z-Q. 2018. Repositories for mite and tick specimens: acronyms and their nomenclature. Syst. Appl. Acarol., 23, 2432-2446. https://doi.org/10.11158/saa.23.12.12

instructions