The MullederiaWood, 1964 (Acari: Stigmaeidae) is a species-limited genus with a geographic distribution so far restricted to eastern Palaearctic, Indomalaya and Australasia regions. Mullederia sichuanensisWang, 1986 is newly recorded from Japan based on specimens collected from two different evergreen broad-leaved forests at Bōsō Peninsula, Chiba Prefecture (Honshu). Adult females, males and deutonymphs are redescribed and illustrated. Interspecific morphological variations among world species of Mullederia are provided. Also, stigmaeid mite species recorded from Japan are listed.
Introduction
Many species of the family Stigmaeidae Oudemans, 1931 (Acari: Trombidiformes) are important predators, after the phytoseiid mites, against phytophagous mites and insects (Santos & Laing 1985; Gerson et al. 2003; Fan & Flechtmann 2015). This family comprises 33 genera and about 600 described species (Fan & Ueckermann 2016; Fan et al. 2016; Stathakis et al. 2016; Rehman et al. 2018; Khaustov 2019). The genus Mullederia was established by Wood (1964) assigning M. arborea Wood, 1964 as type species. Fan and Ueckermann (2016) redefined the generic status and provided a key to the known species, excluding M. parryorum (Gupta, 1991) due to inadequate original description. Accordingly, the genus includes six species restricted to 3 biogeographic realms: M. sichuanensis Wang, 1986—China (Palaearctic); M. filipina Rimando & Corpuz-Raros, 1996—Philippines, M. parryorum (Gupta, 1991)—India (Indomalaya); and M. arborea Wood, 1964, M. procurrens Fan & Zhang, 2005, M. scutellaris Fan & Zhang, 2005—New Zealand (Australasia).
Although several works have been published about the taxonomy of stigmaeid mites in Japan (Ehara 1962, 1964, 1967, 1980, 1985; Ehara & Ueckermann 2006; Negm et al. 2015; Negm & Gotoh 2019), species richness is still limited (Table 1). Also, Shiba (2015) listed an unidentified species of Mullederia collected from evergreen oak trees (Fagaceae) in Shikoku. The present study aims to redescribe and illustrate females, males and deutonymphs of M. sichuanensis as a new record of Stigmaeidae from Japan.
TABLE 1.
List of stigmaeid mites known from Japan.
Materials and methods
Mites were directly picked up from detached plant leaves under stereomicroscope (SZ40®, Olympus, Japan) and mounted on glass slides using Hoyer's medium. Permanent slides were placed on a hot plate at 50ºC to dry, then sealed with Thorne's cement® (FHK, Fujihira Industry, Japan) applied around the edge of the coverslip using a slide ringer. Mites were examined for their different taxonomic features with the aid of phase contrast (BX43®, Olympus) and differential interference contrast (BX53®, Olympus) compound microscopes and drawn by a camera lucida (U-DA, Olympus) attached to the microscope. Final illustrations were done with Adobe Illustrator (Adobe Systems Incorporated, USA). Measurements were performed using the imaging software Sensiv Measure® ver. 2.6.0 and correspond to the mean followed by minimum and maximum values. Tubercles of dorsal stout setae and leg coxae were not included in measuring setae and legs.
In the present description, the idiosomal and leg setation follow Grandjean (1939, 1944). Voucher materials are deposited in the Laboratory of Applied Entomology and Zoology, Ibaraki University (AEZIU) under the serial voucher specimen numbers.
Systematics
Family Stigmaeidae Oudemans, 1931
Genus Mullederia Wood, 1964
Type species: Mullederia arborea Wood, 1964: 1, by original designation.
Mullederia sichuanensis Wang, 1986
(Figures 1–6)
Redescription
Idiosomal dorsum (Figure 1A): Relatively round 337 (330–344) long, 313 (307–320) wide. Dorsum sclerotized with rounded and polygonal subcuticular reticulations, eye 20 (19–22) in diameter and post-ocular body (pob) 19 (17–21) in diameter. Dorsal setae stout and slightly barbed except dorsal seta d1 and humeral seta c2 simple. Lengths of prodorsal setae: vi 114 (112–116), ve 122 (120–125), sci 102 (98–106), sce 111 (110–113). Distances between their bases: vi–vi 60 (58–63), vi–ve 92 (90–94), ve–ve 214 (207–221), ve–sci 34 (33–36), sci–sci 166 (163–170), sci–sce 74 (72–77), sce–sce 305 (287–324). Lengths of hysterosomal setae: c1 94 (92–97), c2 12 (11–14) in lateral position, d1 9 (7–11), d2 110 (107–113), e1 77 (76–79), e2 107 (106–109). Distances between their bases: c1–c1 66 (62–70), d1–d1 191 (189–194), d2–d2 288 (285–292), c1–d2 116 (112–120), d2–e2 78 (75–81), e2–e2 174 (166–183), e1–e2 68 (64–72), e1–e1 57 (54–60).
Idiosomal venter (Figure 1B): Three pairs of slender setae present between coxae, 1a 29 (27–32) at level of coxa I, 3a 20 (19–22) anterior to coxa III and 4a 18 (17–20) at level between coxae III and IV. Distances between their bases: 1a–1a 45 (43–47), 3a–3a 143 (141–146), 4a–4a 70 (68–73). Anogenital region with two pairs of aggenital setae ag1 11 (10–12), ag2 10 (9–11), ag1–ag2 22 (20–24) laterad genital opening and three pairs of pseudanal setae ps3 7 (6–8), ps2 10 (9–11), ps1 8 (8–9). Suranal shield with two pairs of stout setae h1 40 (39–42), h2 34 (33–35). Distances between their bases: h1–h1 19 (18–21), h2–h2 46 (45–48).
Gnathosoma (Figures 1C & D): Chelicera 60 (57–63), movable digit 36 (34–39). Palp 79 (73–85), palp-coxa with a supracoxal seta (elcp) dorsally. Number of setae on palpal segments: Tr 0, Fe 3 (d, l′, v″), Ge 2 (d, l″), Ti 2 (d, l′), Ts 8 (1) (fused eupathidia sul, eupathidion acm, ba, bp, lp, va, 1 solenidion ω). Subcapitulum 96 (90–103) wide, with two pairs of slender setae proximally, m 20 (18–22), n 22 (21–24) and two pairs of adoral setae distally, ro2 13 (12–14), ro1 16 (15–18). Distances between bases of subcapitular setae: n–n 39 (37–41), m–m 17 (15–19), ro1–ro1 7 (7–8), ro2–ro2 13 (11–16), n–m 20 (19–21), m–ro1 34 (32–37), ro1–ro2 9 (8–10).
Legs (Figure 2): Lengths of legs: leg I 209 (204–215), leg II 210 (202–218), leg III 196 (191–202), leg IV 194 (192–197). Coxa I with setae 1b 20 (19–22) and 1c minute, coxa II with seta 2c minute, coxa III with setae 3b and 3c minute, coxa IV with setae 4b and 4c minute. Measurements of solenidia: φp on Ti I 21 (20–21), ω on Ts I 24 (23–25); φp on Ti II 21 (20–21), ω on Ts II 23 (22–23); φp on Ti III 20 (20–21), ω on Ts III 24 (24–25). Chaetotaxy (I–IV): coxae 2-1-2-2; trochanters 1-1-1-1; femora 5-5-2-1 or 5-5-2-2, in some specimens; genua 2-0-0-0; tibiae 5+(1φρ)-5+(1φρ)-5+(1φρ)-5; tarsi 12+(1ω)-9+(1ω)-7+(1ω)-7.
Idiosomal dorsum (Figure 3A): As in female except posterior margin with median invagination, 251 (247–255) long, 223 (218–228) wide. Eye 16 (15–18) in diameter and pob 16 (14–19) in diameter. Dorsal setae shorter than in female. Lengths of prodorsal setae: vi 78 (75–81), ve 88 (86–90), sci 63 (61–65), sce 68 (66–71). Distances between their bases: vi–vi 44 (43–45), vi–ve 64 (62–67), ve–ve 142 (140–145), ve–sci 31 (29–34), sci–sci 112 (110–114), sci–sce 63 (60–66), sce–sce 214 (211–218). Lengths of hysterosomal setae: c1 54 (52–56), c2 16 (15–17), d1 5 (5–6), d2 61 (59–63), e1 35 (34–37), e2 65 (64–66). Distances between their bases: c1–c1 44 (43–46), d1–d1 115 (112–118), d2–d2 180 (178–182), c1–d2 85 (83–88), d2–e2 58 (56–60), e2–e2 110 (109–111), e1–e2 42 (41–44), e1–e1 36 (35–37).
Idiosomal venter (Figure 3B): Lengths of intercoxal setae: 1a 19 (17–22), 3a 15 (12–19) and 4a 16 (14–18). Distances between their bases: 1a–1a 24 (22–26), 3a–3a 97 (94–100), 4a–4a 39 (38–41). Aggenital setae: ag1 7 (7–8), ag2 10 (9–11), situated as in female. Pseudanal setae: ps3 6 (5–6), ps2 4 (4–5), ps1 3 (3–4). Suranal setae h1 14 (13–15), h2 16 (16–17). Distances between their bases: h1–h1 15 (14–17), h2–h2 39 (38–41).
Gnathosoma (Figures 3C & D): Chelicera 46 (44–49), movable digit 25 (24–27). Palp 67 (66–69), chaetotaxy of palp as in female. Subcapitulum 73 (72–75) wide, with subcapitular setae, m 13 (13–14), n 14 (13–15) and adoral setae, ro2 13 (12–15), ro1 11 (10–13). Distances between bases of subcapitular setae: n–n 31 (30–32), m–m 13 (11–16), ro1–ro1 8 (7–10), ro2–ro2 13 (12–14), n–m 16 (14–18), m–ro1 33 (30–36), ro1–ro2 10 (10–11).
Legs (Figure 4). Lengths of legs: leg I 175 (171–180), leg II 169 (167–172), leg III 165 (162–168), leg IV 167 (164–170). Measurements of solenidia: φp on Ti I 16 (16–17), ω1 on Ts I 17 (16–18), ω2 on Ts I 24(24–25); φp on Ti II 15 (15–16), ω1 on Ts II 17 (17–18), ω2 on Ts II 25 (25–26); φp on Ti III 16 (15–17), ω1 on Ts III 18 (18–19), ω2 on Ts III 24 (23–25); ω1 on Ts IV 19 (19–20), ω2 on Ts IV 26 (25–27). Chaetotaxy (I–IV): coxae 2-1-2-2; trochanters 1-1-1-1; femora 5-5-2-1 or 5-5-2-2, in one specimen; genua 2-0-0-0; tibiae 5+(1φρ)-5+(1φρ)-5+(1φρ)-5; tarsi 12+(2ω)-9+(2ω)-7+(2ω)-7+(2ω).
Idiosomal dorsum (Figure 5A): Shape as in female, 275 (268–282) long, 262 (258–266) wide. Eye 17 (16–18) in diameter and pob 18 (16–20) in diameter. Lengths of prodorsal setae: vi 74 (72–76), ve 87 (85–89), sci 64 (63–65), sce 70 (68–72). Distances between their bases: vi–vi 44 (40–48), vi–ve 72 (70–74), ve–ve 173 (170–176), ve–sci 26 (25–27), sci–sci 142 (140–144), sci–sce 64 (60–68), sce–sce 235 (229–241). Lengths of hysterosomal setae: c1 61 (60–62), c2 8 (7–9), d1 5 (5–6), d2 70 (67–73), e1 45 (43–47), e2 68 (65–71). Distances between their bases: c1–c1 48 (46–50), d1–d1 146 (139–153), d2–d2 215 (211–219), c1–d2 94 (92–96), d2–e2 65 (64–66), e2–e2 137 (132–142), e1–e2 54 (52–56), e1–e1 40 (36–44).
Idiosomal venter (Figure 5B): Lengths of intercoxal setae: 1a 18 (17–19), 3a 14 (13–15) and 4a 15 (13–17). Distances between their bases: 1a–1a 35 (32–37), 3a–3a 108 (102–114), 4a–4a 38 (35–41). Aggenital setae: ag1 7 (7–8), ag2 8 (7–9). Pseudanal setae: ps3 6 (6–7), ps2 7 (7–8), ps1 7 (7–8). Suranal setae h1 20 (18–22), h2 24 (23–25). Distances between their bases: h1–h1 11 (10–12), h2–h2 35 (35–36).
Gnathosoma (Figures 5C & D): Chelicera 54 (52–56), movable digit 23 (20–26). Palp 50 (45–55). Subcapitulum 73 (70–76) wide, with subcapitular setae, m 18 (18–19), n 17 (17–18) and adoral setae, ro2 9 (8–10), ro1 10 (10–11). Distances between bases of subcapitular setae: n–n 30 (28–32), m–m 22 (22–23), ro1–ro1 6 (6–7), ro2–ro2 10 (9–11), n–m 17 (15–19), m–ro1 35 (33–37), ro1–ro2 7 (7–8).
Legs (Figure 6): Lengths of legs: leg I 165 (160–170), leg II 170 (167–173), leg III 162 (160–164), leg IV 155 (151–159). Measurements of solenidia: φp on Ti I 18 (17–19), ω on Ts I 22 (21–22); φp on Ti II 19 (19–20), ω on Ts II 21 (20–22); φp on Ti III 17 (16–18), ω on Ts III 23 (23–24). Chaetotaxy (I–IV): coxae 2-1-2-2; trochanters 1-1-1-0; femora 5-5-2-1; genua 2-0-0-0; tibiae 5+(1φρ)-5+(1φρ)-5+(1φρ)-5; tarsi 12+(1ω)-9+(1ω)-7+(1ω)-7.
FIGURE 5.
Mullederia sichuanensis Wang, 1986. Deutonymph. A—dorsum; B—venter; C—subcapitulum; D—palp.
Material examined
Ten females and 2 males, ex Maesa japonica Merr. (Primulaceae), Bōsō Peninsula, Chiba Prefecture, Japan, 35°10′14″N, 140°10′09″E, 320 m, 23 July 2018, M.W. Negm leg. (voucher specimen no. 890); 2 females, 1 male and 7 deutonymphs, Ilex sp. (Aquifoliaceae), Bōsō Peninsula, Chiba Prefecture, Japan, 35°09′21″N, 140°11′33″E, 80 m, 26 May 2018, M.W. Negm leg. (voucher specimen no. 891).
Remarks
Mullederia sichuanensis Wang, 1986 was originally described from China based on materials collected from different host plants, Holboellia sp. (Lardizabalaceae), Rubus lambertianus Ser. (Rosaceae) and Viburnum brachybotryum Hemsl. (Adoxaceae) (Wang 1986), which are deciduous broad-leaved plants. However, the Japanese specimens were found on another flowering host plants of the families Primulaceae and Aquifoliaceae, which are evergreen broad-leaved plants.
The Japanese specimens of M. sichuanensis can be separated from other species within the genus by the presence of the dorsal seta d1 (= li—in original description) and the absence of seta f1. Conversely, the New Zealand species (arborea Wood; procurrens Fan & Zhang; scutellaris Fan & Zhang) lack seta d1 and bear seta f1. Table 2 lists the interspecific morphological variations among females of Mullederia species of the world.
TABLE 2.
Morphological diagnostic variations among females of Mullederia species of the world.
The examined mites conform to the original description of this species, considering the corrections published by Fan & Ueckermann (2016). However, most of the Japanese specimens have femur IV with one seta, while few individuals with two setae. We consider this alteration in setal counts as an intraspecific variation.
The current species is newly recorded from Japan based on specimens of females, males and deutonymphs. The chaetotaxy of legs between females, males and deutonymphs is relatively similar. However, males differ from females and deutonymphs in the presence of additional solenidia on tarsi I–IV, whereas deutonymphs differ from females and males in having trochanter IV nude.
Discussion
The present work redescribes a new record of stigmaeid mites in Japan, increasing their fauna to 9 genera and 19 species, including three unidentified species, to date. Also, deutonymphal stage of the genus Mullederia is described herein for the first time. Reporting such few numbers of stigmaeid species from Japan, in a rich family with about 600 species described globally, may indicate that this country is expected to contain more species awaiting discovery. The world distribution of Mullederia mites comprises only New Zealand, India, Philippines, China and Japan (Shiba 2015; present study), making this genus quite restricted to eastern Palaearctic, Indomalaya and Australasia biogeographic realms.
Rimando & Corpuz-Raros (1996) provided a key to Mullederia species and stated that M. sichuanensis has coxae I–IV with 2-1-1-1; however, the coxal chaetotaxy was recently corrected to 2-1-2-2 by Fan & Ueckermann (2016). They also re-examined paratype females and corrected the number of tenent hairs on the empodial shaft to 3 rather than 2 in contrast with Wang (1986) and Rimando & Corpuz-Raros (1996), and highlighted that tarsi I–IV with 12+1ω, 9+1ω, 7+1ω, 7 rather than 12+1ω, 8+1ω, 6, 6. Rimando & Corpuz-Raros (1996) mentioned about M. sichuanensis to be the only species that has 3 setae (2+1) on femur IV; however, the present specimens agree with the genus revised diagnosis (Fan & Ueckermann 2016) to have 1 seta (most specimens) or 2 setae (few specimens).
The species M. filipina was described from the Philippines due to the number of coxal setae on legs (I–IV) which were (1-0-0-0). This setal formula is questionable, especially because the coxal setae (1c, 2c, 3b, 3c, 4b, 4c) are minute and rather difficult to be observed. Also, the description of M. parryorum from India is brief and lacks specific information which makes the species difficult to be identified and distinguished from other species in the genus (Gupta 1991; Fan & Ueckermann 2016). Therefore, the genus Mullederia may be in need of updated revision.
Information about the biological traits of Mullederia mites is still unknown. Up to our knowledge, no studies have evaluated the predatory performance of Mullederia mites. This may be due to some difficulties in mite rearing. Despite preliminary trials have failed to rear these mites in laboratory, few individuals were seen attacking the eggs of Tetranychus urticae Koch (unpublished data). Such predation ability may encourage for more ecological studies to figure out the predator-prey interaction between the Mullederia mites and other pestiferous species. Further research should be directed to investigate their efficiency for a better use in biocontrol programs. Hopefully, this work would encourage for setting up new series of biological studies on Mullederia mites.
Acknowledgement
The authors would like to thank the Japan Society for the Promotion of Science for funding the postdoctoral fellowship of MWN. This work was supported by JSPS KAKENHI Grant Number JP17F17397 (MWN, Grant-in-Aid for JSPS Research Fellow). Special thanks to Dr. Yasuki Kitashima for his kind help during the field work and Dr. Qing-Hai Fan for examining the paratype females of M. sichuanensis and providing related information.
