Neoseiulus barkeri (Ueckermann & Loots, 1988)

Beaulieu, Frédéric & Beard, Jennifer J., 2018, Acarine biocontrol agents Neoseiulus californicus sensu Athias-Henriot (1977) and N. barkeri Hughes (Mesostigmata: Phytoseiidae) redescribed, their synonymies assessed, and the identity of N. californicus (McGregor) clarified based on examination of types, Zootaxa 4500 (4), pp. 451-507 : 482-487

Synonyms of N. barkeri —supported, uncertain, not supported.

Several nominal species have been proposed as junior synonyms of N. barkeri , particularly by Ragusa & Athias- Henriot (1983) and Ueckermann & Loots (1988). Here we discuss 12 synonymies (six supported, five uncertain, one rejected), based on direct observation of type specimens or comparisons with the literature:

Neoseiulus picketti ( Specht, 1968) (New Jersey, USA) (synonymy by Ragusa & Athias-Henriot, 1983, based on illustrations)—Synonymy supported. Its synonymy with N. barkeri is strongly supported by similarity in morphometrics (Table 2), spermathecal apparatus, shield ornamentation, adenotaxy and poroidotaxy, based on type material ( Figs 15 , 16f ). The spermathecal calyx varies in shape and length ( Figs 17f–j ), with some calyces showing a slight constriction in the basal quarter to third (g, i); however, in these cases, within a single female, the other spermatheca shows a more typical tapering at the base (g-h, i-j).

Neoseiulus mckenziei ( Schuster & Pritchard, 1963) (California, USA) (synonymy by Ragusa & Athias- Henriot 1983, based on type material) ( Chant & McMurtry, 2003 stated this synonymy was uncertain)—Synonymy supported. Some discrepancies exist between the description of N. mckenziei versus N. barkeri : (1) dorsal seta r3 inserted quite more anteriorly in N. mckenziei , almost to level of z2; (2) ventrianal shield more tapered from level of setae ZV2 to posterior apex; (3) J5 seta 17 µm long (vs. 12–15 in N. barkeri ); and (4) spermathecal apparatus of N. mckenziei shows a strong constriction between the atrium and the calyx, as mentioned by Chant & McMurtry (2003). Having examined the holotype of N. mckenziei , we can state that these are either inaccuracies or are associated with slide mounting. The apparent constriction between the calyx and the atrium is due to the angle at which the left spermatheca is positioned on the slide. The right spermatheca is not markedly constricted between the calyx and the atrium ( Fig. 17c ), and not more so than other specimens identified as N. barkeri (e.g. Figs 17m, t, v, x ). The spermatheca is similar to that of most other specimens identified as N. barkeri , including the lectotype and N. mungeri types ( Figs 11a–c , 17a–b, f, i, m, o, v, w ). Our measurements of the holotype are also compatible with those of N. barkeri specimens, including the lectotype (Table 2), further supporting Ragusa & Athias- Henriot’s synonymy of N. mckenziei with N. barkeri .

Neoseiulus oahuensis ( Prasad, 1968) (Hawaii, USA) (synonymy by Ragusa & Athias-Henriot 1983 based on type material; accepted by de Moraes et al., 2004; listed separately in Chant & McMurtry, 2007)—Synonymy supported. One calyx of one paratype has a constriction in the proximal fifth of its length ( Fig. 17t ), whereas the other calyx, as well as those of the other paratype examined, are typical for N. barkeri ( Figs 17r, s ; note that the calyx in Fig. 17s appears shorter because it is bent in the Z-axis). Similarly, the original illustration shows a calyx more constricted in its proximal third ( Prasad, 1968). This shape is reminiscent of the calyx of N. usitatus (see text below; Fig. 18a–f ), although the constriction is weaker in the N. oahuensis paratype that we examined. Note also that a proximal constriction was seen in the calyx of other specimens that we identified as N. barkeri ( Fig. 17g, x ). Other measurements that we made, including those of the dorsal setae of N. oahuensis essentially match those of the N. barkeri examined, although most setal lengths for the former are near or at the lower extreme of the range for the latter (note that most of the dorsal setae were missing for one of the two N. oahuensis paratypes examined). We therefore agree for now with the synonymy proposed by Ragusa & Athias-Henriot (1983).

Neoseiulus mycophilus ( Karg, 1970) ( Brazil) (synonymy by Ragusa & Athias-Henriot, 1983, based on type material; accepted by de Moraes et al., 2004; listed separately in Chant & McMurtry, 2007)—Synonymy supported. The original description by Karg (1970) is lacking in detail, and does not include the spermathecal apparatus. Although dorsal seta s4 is particularly short on the illustration, we trust Ragusa & Athias-Henriot’s judgement and accept their synonymy. Interestingly, the type material examined by Ragusa & Athias-Henriot (1983) was actually labelled as “ A. mckenziei ”, another synonym of N. barkeri .

Neoseiulus kermanicus Daneshvar, 1987 ( Iran) (synonymy by Faraji et al., 2007)—Synonymy supported. We concur with Faraji et al., that the description of this species, including the lengths of dorsal setae and the shape of spermatheca, is highly similar to that of N. barkeri . However, the male ventrianal shield is illustrated as bearing five pairs of pre-anal setae, including a posterolateral pair, inserted on the shield edge at a level near that of paraanal setae. This probably represents JV5, for two reasons. Firstly, the cuticle flanking the ventrianal shield is often folded, and this can lead to JV5 appearing inserted close to the ventrianal shield margin or on the shield itself, in a position more or less level with para-anal setae ( Figs 3c–d , 6 ; Chant & McMurtry, 2003; Papadoulis et al., 2009). Secondly, JV5 is always present in male phytoseiids ( Chant & Yoshida-Shaul, 1991), and there was no other seta indicated off the ventrianal shield of N. kermanicus that could represent JV5 other than the one apparently on the shield edge. Faraji et al. (2007) had taken these factors into consideration when they suggested the synonymy (F. Faraji, pers. comm. 2017).

Neoseiulus cydnodactylon ( Shehata & Zaher, 1969) ( Egypt) (tentative synonymy by Ragusa & Athias- Henriot, 1983; listed separately in Chant & McMurtry, 2007)—Synonymy supported. The original description is compatible with N. barkeri , including the shape of the spermathecal apparatus and measurements of dorsal setae (their measurement of 25 µm for j6 is out of the range for N. barkeri , but their figure suggests this is an overestimate). Abo-Shnaf & de Moraes (2014) studied N. barkeri from Egypt, including a female specimen that had been identified as A. cydnodactylon by M.A. Zaher, which further supports this putative synonymy.

Neoseiulus masiaka ( Blommers & Chazeau, 1974) ( Madagascar) (synonymy by Ueckermann & Loots, 1988, based on type material) (“= barkeri ?” in Chant & McMurtry, 2003; accepted by de Moraes et al., 2004, Rahmani et al., 2010; listed separately in Ragusa & Athias-Henriot (1983) and Chant & McMurtry (2007) —Synonymy in doubt. Based on original description ( Blommers & Chazeau, 1974) and partial redescription by Ragusa & Athias- Henriot (1983), the following combination of characters suggests that N. masiaka is distinct from N. barkeri :

(1) calyx of masiaka spermatheca longer than that of barkeri , based on measurements in original description (28 vs 17–24)—the calyx of masiaka is more elongate relative to the atrium in both the original illustration of Blommers & Chazeau (1974) (ratio of atrium / calyx lengths = 0.14) and that of Ragusa & Athias-Henriot (1983) (ratio = 0.19–0.20), although the calyx is of similar shape and relative dimensions to those of a few specimens of N. barkeri that we examined ( Fig. 17g, n ; our ratios for N. barkeri (n=20): 0.25 ±0.4; 0.18– 0.33).

(2) Gland pore gd4 of male distinct (see Ragusa & Athias-Henriot, 1983).

(3) Length of most dorsal setae near the lowest extremes of our setal lengths for N. barkeri .

Until further studies are conducted to clarify this potential synonymy, we follow Ragusa & Athias-Henriot (1983) in considering it to be a distinct species. Some of the specimens from Australia identified by Schicha (1987) and Beard (2001) as N. masiaka may actually represent N. usitatus (see notes on N. usitatus below). However, as previously suggested by Beard, the shapes of the calyces of specimens identified as N. masiaka from Australia presented in Beard (2001) indicate that either this character is highly variable in this species, or that there are more than one taxa involved.

Neoseiulus pieteri ( Schultz, 1972) ( South Africa) (synonymy by Ueckermann & Loots, 1988, based on type material)—Synonymy in doubt. The original description by Schultz (1972) shows a dorsal shield with shorter setae (e.g. Z5 is 35 µm) and a distinct spermatheca, including a markedly flaring calyx. Schultz (1972) also mentioned differences between N. pieteri and N. usitatus , such as shorter dorsal setae and distinct ornamentation on the ventrianal shield.

Neoseiulus sugonjaevi ( Wainstein & Abbasova, 1974) ( Azerbaijan) (tentative synonymy by Ragusa & Athias- Henriot, 1983)—Synonymy in doubt. Based on the original description and that in Bregetova et al. (1977: 233), the spermatheca is distinct from that of N. barkeri .

Neoseiulus stolidus ( Chaudhri, 1968) ( Pakistan) —Synonymy in doubt. It was mentioned as similar to N. masiaka by Blommers & Chazeau (1974) and again by Ragusa & Athias-Henriot (1983), implying possible synonymy. Tixier et al. (2016) listed N. stolidus with N. barkeri in their key and stated that the two species could not be distinguished. However, it appears from the literature that no-one has examined the types. The description is indeed similar to N. barkeri (and N. masiaka ), and although some dorsal setae appear shorter on the illustration and the spermathecal calyx appears as long as the most extreme that we have observed for N. barkeri , the measurements provided in the text are compatible with N. barkeri . The gland openings gv3, however, are aligned transversely with setae JV2, and this character state has been highlighted as a potential distinction between N. stolidus and N. barkeri by Ragusa & Athias-Henriot (1983). Neoseiulus barkeri has gv3 at a level 5–8 µm posterior to the level of JV2.

Neoseiulus usitatus ( Van Der Merwe, 1965) ( South Africa) (synonymy by Ueckermann & Loots, 1988, based on type material; “= barkeri ?” in Chant & McMurtry (2003); synonymy accepted by de Moraes et al. (2004); species listed separately in Ragusa & Athias-Henriot (1983) and Chant & McMurtry (2007)) —Synonymy in doubt. The original description of N. usitatus , and the specimens from South Africa (slide lots #50–51, Table 1) and Australia that we examined (lot #52; previously identified as N. masiaka (see comments for N. masiaka above; Schicha, 1987; Beard, 2001)), show the following differences to N. barkeri , which suggest that N. usitatus and N. barkeri represent distinct species:

(1) The spermathecal calyx is generally constricted in its proximal third or fourth, and tends to be shorter than that of N. barkeri ( Figs 18a–f ) (calyx length: 16–17 µm long (lots #50–51), 15–18 µm (lot #52)). However, one female from South Africa and one from Australia did not have both calyces constricted, but instead one calyx was evenly flared from base to apex, simliar to that of N. barkeri ( Figs 18c, f ), while the other calyx was constricted as is normal for N. usitatus ( Figs 18b, e ). Ragusa & Athias-Henriot (1983: 662) illustrates a similarly constricted calyx, whereas that in Van Der Merwe (1965) is only weakly constricted.

(2) Several dorsal setae, in the original description, are slightly shorter or at the lower end of the range in length for N. barkeri . The two female specimens of N. usitatus from South Africa that we examined also exhibit slightly shorter setae, even more so than in description by Van Der Merwe, the following setae in particular (our measurements: N. usitatus from South Africa / from Australia / N. barkeri ): Z4 (31–33 / 34–36 / 35–45), s4 (19–22 / 21–24 / 26–34), S2 (18–19 / 21–23 / 25–37), S4 (18 / 19–22 / 24–36), S5 (14–17 / 17–20 / 20–34), r3 (16–17 /18–21 / 21–28), and R1 (14–15 / 16–19 / 19–27).

(3) The male has a distinct gland pore gd4, hypertrophied, and more complicated than barkeri , according to Ragusa & Athias-Henriot (1983) who examined a non-type male specimen. However, the male from Australia that we examined, associated with females with spermathecae similar to that of N. usitatus , has gd4 similar or identical to that of N. barkeri .

(4) Fixed cheliceral digit with three ( Van Der Merwe 1965) or four to five teeth (our specimens), including two subapical offset teeth. This overlaps with our observations of the variation seen in N. barkeri and hence cannot be used as a species defining character.

Neoseiulus huffakeri ( Schuster & Pritchard, 1963) (possible synonymy suggested as “= N. barkeri ?” by Chant & McMurtry, 2003)—Synonymy not supported. The original description, and the two specimens that we examined, including a paratype (slide lot #48–49, Table 1), show the following differences from N. barkeri , indicating they are distinct species (as is suggested elsewhere, e.g. Ragusa & Athias-Henriot, 1983):

(1) Gland openings gv3 inconspicuous, punctiform, and well separated, more than twice as close to setae JV2 than to each other. The size and position of gv3 makes N. huffakeri more similar to species classified in the N. marinellus group (sensu Ragusa & Athias-Henriot, 1983) than to N. barkeri (note that the marinellus species group was synonymised by Chant & McMurtry, 2003 under the N. barkeri species subgroup).

(2) Dorsal setae shorter, especially Z4 (our measurements: 28–30 for N. huffakeri vs 35–45 for N. barkeri ) and Z5 (34–37 vs 48–66), in addition to ventral seta JV5 (28–32 vs 44–60).

(3) Calyx of spermathecal apparatus tends to be more strongly flared distally ( Fig. 18g, h ; 9–12 µm wide distally; see also Ragusa & Athias-Henriot (1983)). The apparent variation in the shape of the calyx between the holotype, paratypes and other specimens ( Fig. 18g (paratype) vs 18h and Schuster & Pritchard (1963: 272)) should be examined further.

(4) Atrium a truncate cone, and slightly larger: 6–8 µm long x 4–5 µm wide (vs 4–6 x 3–4.5 for N. barkeri ); and longer, relatively to calyx: atrium length / calyx length = 0.37–0.48 (vs 0.18–0.33 for N. barkeri ) (see also Ragusa & Athias-Henriot (1983)).

(5) Shorter macroseta on basitarsus IV (41–46 vs 58–74 for N. barkeri ).

(6) Smaller ventrianal shield (107–110 long, 92–93 wide vs 116–145 long, 99–120 wide for N. barkeri ).

(7) Male apparently with ventrianal shield bearing only three pairs of pre-anal setae, and an L-shaped spermatodactyl ( Schuster & Pritchard, 1963) (vs four pairs, and T-shaped spermatodactyl for N. barkeri ).

Figures

FIGURE 3. Males: (a, c) dorsal shield and ventral idiosoma of Neoseiulus californicus holotype (male); (b, d) and of N. barkeri paralectotype (male).

FIGURE 9. Females: dorsal and ventral idiosoma of (a, b) Neoseiulus mungeri lectotype, and of (c, d) N. barkeri, based on a specimen from California with similar collection data to that of N. mungeri type (slide lot #3, Table 1).

FIGURES 10–11. Females: 10. Dorsal and ventral idiosoma of Neoseiulus barkeri lectotype. 11. Spermathecae of N. mungeri lectotypes (a) and paralectotype (b), and of N. barkeri lectotype (c). [n.b. Several setae on 10b appear shorter than they are because they are bent in the Z-axis; arrow on 11c indicates thickened calyx wall]

FIGURES 12–15. Neoseiulus barkeri. Female: 12–13. Dorsal and ventral idiosoma of specimen from western Canada (slide lot #12, Table 1); opisthogastric region of specimens from (14) California (lot #5) and (15) New Jersey (N. picketti holotype = jun. syn. of N. barkeri; lot #10). [n.b. green arrows indicate gland openings and poroids of particular interest. All figures at the same scale, shown in 12].

FIGURE 16. Neoseiulus barkeri (including jun. syn. of N. barkeri). Female chelicerae: (a) Neoseiulus mungeri lectotype; (b) N. barkeri lectotype; N. barkeri females from (c–e) California (c–d: slide lot #3; e: lot #6, Table 1); (f) New Jersey (N. picketti holotype; lot #10); and (g) South Korea (lot #17). [n.b. (c, d) are from the same individual, (a, b, c, f) are in paraxial view, (d, e) in antiaxial view, (g) in dorsal view. Legend: MDt—movable digit tooth; MD L—movable digit length; pr—proximal (paraxial) teeth of fixed digit; pdb—base of pilus dentilis; su—subapical (antiaxial) teeth of fixed digit].

FIGURE 17. Neoseiulus barkeri (including other nominal species that are jun. syn. of N. barkeri). Variation in the shape of the spermathecae of specimens from: (a) slide lot #5 (Table 1); (b) lot #4; (c) holotype of N. mckenziei, lot #9; (d, e) ‘from type material’ of N. barkeri, lot #8; (f–j) holotype and paratypes of N. picketti, lot #10; (k–m) lot #17; (n, o) lot #16; (p, q) lot #15; (r–t) paratypes of N. oahuensis, lot #11; (u–x) lot #12; (y) lot #14. All figures at the same scale, shown in (y). Abbreviations: CA—California (USA), CAN—Canada, FI—Finland, HA—Hawaii (USA), NJ—New Jersey (USA), SK—South Korea, UK—United Kingdom; calyx L—length of calyx, atrium L—length of atrium, W—width of atrium.

FIGURE 18. Variation in the shape of the spermathecae of N. usitatus (a–f) and N. huffakeri (g–h): (a) slide lot # 51 (Table 1); (b, c) lot # 50; (d–f) lot #52; (g) paratype of N. huffakeri, lot #48; (h) lot # 49. Legend: AU—Australia, CA—California (USA), SA—South Africa.

FIGURES 4–8. Males: 4. Chelicerae and spermatodactyls of (a) Neoseiulus californicus holotype; (b) N. barkeri paralectotype (paraxial view); (c) other N. barkeri from Finland (slide lot #16, Table 1); (d) South Korea (dorsal view; slide lot #17). 5–6. Detail of N. barkeri male idiosoma (5) dorsum and (6) venter, based on a specimen from California with similar collection data to that of N. californicus type (slide lot #3, Table 1). 7. Detail of gland opening gv3 (between JV2 setae) on N. barkeri male ventrianal shield region (from slide lot # 15). 8. Detail of N. barkeri gland openings gd4 of (a) paralectotype; (b–e) Finland specimens (slide lot #16, Table 1); (f) South Korea specimens (slide lot #17). [n.b. 8a, c, e present both left and right gd4 of individual males, at different depths, while 8b, d, f present only left gd4; green arrows indicate the point where the gland duct leads deeper into the body. Poroids id5, id2, idm1–6, and idx shown in 5 are based on observations on male from slide lots #15– 17; poroid idm5 is not shown here in 5, being near the posterior edge of the shield, which is curved on the specimen illustrated; poroids ivo, ivp and sigillae in 6 are mostly based on observations on males from slide lots #16 and 17.]