Phytoptus tetratrichus Nalepa 1890

Soika, Grażyna & Kozak, Marcin, 2011, Problems with the taxonomy of Phytoptus tetratrichus Nalepa 1890 (Acari: Eriophyoidea) inhabiting Tilia spp.: Analysis based on morphological variation among individuals, Zootaxa 2988, pp. 37-52 : 40-48

Phytoptus tetratrichus Nalepa 1890

( Figs. 1 & 2 )

Protogyne female: (n=20). Body worm-like, length 229 (192–285), width 59 (52–70), milky-white. Gnathosoma length 23 (21–24); projecting obliquely downwards, dorsal genual setae (d) 2.4 (2–3), pedipalp coxal setae (ep) 3.8 (3–5), cheliceral stylets 17.7 (16.1–18.9). Prodorsal shield length 26.2 (25–27), width 42.5 (38–45), subtriangular, without lobe over base of chelicerae; median line absent; admedian lines short, on anterior half. Two shallow furrows running forwards from base of prodorsal shield: the first bears tubercles of sc setae, while the second runs almost in parallel to sides and ending close to tubercles ve. Minute granulations present on surface near prodorsal shield. Tubercles bearing external vertical setae (ve) 16.7 (15–18) apart, external vertical setae (ve) 10.7 (9–13), directed anteriorly. Tubercles bearing (sc) ahead of rear shield margin, 18.1 (17–20) apart. Scapular setae (sc) 13.7 (11–17) projecting forwards. Coxigenital area smooth, anterolateral setae on coxisternum I (1b) 10.8 (8–13), proximal setae on coxisternum I (1a) 23.7 (18–29), proximal setae on coxisternum II (2a) 35 (30–44). Prosternal apodeme slightly forked at rear. Leg I 31.4 (30–33); femur 11 (10–12), basiventral femoral setae (bv) 10 (8–12); genu 6 (5–6), antaxial genual setae (l ″) 24 (22–25); tibia 6.0 (5–7), paraxial tibial seta (l ′) 2.4 (2.2–2.9) located 1/3 from proximal tibia margin; tarsus 6.7 (5.8–7.5), tarsal setae (u) 2 (2–3), tarsal empodium 6.3 (5.7–7.2), simple, 3-rayed, tarsal solenidion (ω) 8.1 (7.5–8.8), tapered. Leg II 28.4 (27–30); femur 11 (10–12), basiventral femoral setae (bv) 11 (10–12); genu 6 (5–6), antaxial genual setae (l) 16 (15–18); tibia 5.5 (5–7); tarsus 6.5 (6–7), tarsal setae (u ′) 2 (2–3), tarsal empodium 6.4 (5.7–6.9), simple, 3-rayed, tarsal solenidion (ω) 8.9 (8–10), tapered. Opisthosoma with 70 (65–75) dorsal annuli with elliptical microtubercles except for last five thanosomal annuli being smooth; 64 (59–73) ventral annuli with rounded microtubercles. Setae (c1) 38 (33–42) on dorsal annulus 10–11; setae (c2) 20 (18–20) on ventral annulus 9 (7–11); setae (d) 16 (13–19) on ventral annulus 21 (18–23); setae (e) 12 (9–15) on ventral annulus 35 (33–39); setae (f) 34 (26–43) on 5th ventral annulus from rear. Setae (h1) 3 (2–4), setae (h2) 88 (80–108). Genitalia 11 (10–12) long, 20 (21–23) wide; coverflap without longitudinal ridges, proximal setae on coxisternum III (3a) 9 (7–12).

Diagnosis. The protogyne female of Phytoptus tetratrichus is very similar morphologically to Phytoptus rotundus ( Hall 1967) . Both species have 3-rayed empodia; similar patterns on the prodorsal shield, genital shield and coxae; forked sternal lines and the presence of microtubercles on the ventral annuli between the coxae and the genital shield. The individuals of P. rotundus and P. tetratrichus differ from each other in the length of the scapular setae (sc) and distance between the tubercles of the vertical setae (ve) as well as the lengths of the female genitalia, gnathosoma, chelicerae, tarsus I and II and tibia II.

Deutogyne female: (n = 10). Body wormlike, 229 (193–269), 59 (55–58) wide, amber in colour. Gnathosoma (24–25) projecting obliquely downwards; dorsal pedipalp genual setae (d) 1.9 (2–3), pedipalp coxal setae (ep) 3.8 (3–5), cheliceral stylets 17.1 (16–18). Prodorsal shield 25 (24–25), 43.5 (41–49) wide, subtriangular, without lobe over base of chelicerae, unornamented. Two shallow furrows running forwards from base of prodorsal shield: the first bears tubercles of sc setae, while the second runs almost in parallel to sides and ending close to tubercles ve. Rear margin of prodorsal shield between scapular tubercles almost straight. Tubercles bearing external vertical seta (ve), 15.2 (14–16) apart, external vertical seta (ve) 11 (10–12), directed anteriorly. Tubercles bearing sc ahead of rear margin, 16.7 (16–17) apart. Scapular setae (sc) 12.4 (11–14) projecting forward. Coxigenital area smooth, anterolateral setae on coxisternum I (1b) 10.9 (8–14), proximal setae on coxisternum I (1a) 30.5 (26–35), proximal setae on coxisternum II (2a) 42.1 (36–49). Prosternal apodeme unforked in the rear. Leg I 36.8 (36–38), femur 11.2 (10–12), basiventral femoral setae (bv) 9.8 (10–12), genu 5.8 (5–6), antaxial genual setae (l) 23.6 (22–25), tibia 7.7 (7–8), paraxial tibial setae (l) 2.8 (2–3), tarsus 9.1 (8–10), tarsal setae (u ′) 2 (2–2.6), tarsal empodium 7 (6–8), simple, 3-rayed, tarsal solenidion (ω) 8.8 (8–10), tapered. Leg II 33.7 (32–35), femur 10.7 (10–12), basiventral femoral setae (bv) 10.7 (10–12), genu 5.6 (5–6), antaxial genual setae (l) 16.4 (15–18), tibia; 6.7 (6–8); tarsus 8.4 (7–9), tarsal setae (u ′) 2.2 (2–3), tarsal empodium 7.2 (6–8), simple, 3-rayed, tarsal solenidion (ω) 9 (8–10), tapered. Opisthosoma dorsally with 62 (60–65) annuli with elliptical microtubercles, besides the last 5 thanosomal annuli, which are smooth, ventral with 62 (59–65) annuli with round microtubercles. Setae subdorsales (c1) 31 (29–35) on dorsal annulus 10–11; setae (c2) 18.4 (17–20) on ventral annulus 8–9; setae (d) 14 (12–16) on ventral annulus 21 (19–22); setae (e) 12.5 (11–14) on ventral annulus 35 (33–37); setae (f) 36 (30–41) on 5th ventral annulus from rear. Setae (h1) 4.2 (3–5), setae (h2) 89 (83–96). Genitalia 9.9 (9–11), 19.7 (19–21) wide, coverflap without longitudinal ridges, proximal setae on coxisternum III (3a) 11.2 (10–13).

Diagnosis. The body of the deutogyne female of P. tetratrichus differs from the protogyne female in living colour; the former being amber and the latter being milky-white. Deutogyne females also have reduced microtuberculation on both the dorsal and ventral annuli and on the annuli between the femur and genitalia. In addition, the dorsal shield of the deutogyne female appears to have less ornamentation.

Male: (n=7). Body worm-like, 192.6 (181–220), 56.6 (52–60) wide; milky-white in colour. Gnathosoma 25 (25–26), projecting obliquely down, dorsal pedipalp genual setae (d) 2.4 (2–3), pedipalp coxal setae (ep) 3.5 (3–4). Prodorsal shield 26.4 (25–26), 39 (37–45) wide; subtriangular, without shield lobe over the base of chelicerae; prodorsal shield pattern very similar to protogyne females. Scapular tubercles bearing external vertical setae (ve) in anterior part of shield 17.9 (17–19) apart, external vertical setae (ve) 11.3 (10–13) projecting forward. Scapular tubercles bearing sc ahead of rear shield margin, 18.6 (17–20) apart. Scapular setae (sc) 18 (15–20) projecting forwards. Coxigenital area smooth, anterolateral setae on coxisternum I (1b) 10.6 (10–11), proximal setae on coxisternum I (1a) 20.7 (20–25), proximal setae on coxisternum II (2a) 30 (25–33). Prosternal apodeme slightly forked in the rear. Leg I 29.4 (28–30), femur 10.3 (9–11), basiventral femoral setae (bv) 8.4 (7–10), genu 5, antaxial genual setae (l ″) 20.1 (18–22), tibia 6.0 (5.6–7), paraxial tibial seta (l ′) 2.4 (2.2–2.9) located 1/3 from proximal tibia margin; tarsus 6.1 (5.5–7), tarsal setae (u ′) 2.7 (2.5–3), tarsal empodium 6 (5–6.5), simple, 3-rayed, tarsal solenidion (ω) 8.3 (7.5–9), tapered. Leg II 25.6 (25.0–27.0), femur 9.4 (8–11), basiventral femoral setae (bv) 9.4 (8–11), genu 4.8 (4–5), antaxial genual setae (l ″) 18.6 (17–20), tibia; 5 (4.5–6.0); tarsus 5.5 (5–6), tarsal setae (u ′) 2.3 (2– 3), tarsal empodium 5.6 (5.5–6), simple, 3-rayed, tarsal solenidion (ω) 9.1 (8.0–10.0), tapered. Opisthosoma dorsally with 63 (60–68) annuli with elliptical microtubercles with the exception last five thanosomal annuli, which are smooth, ventral with 56 (51–59) annuli with eliptical microtubercles. Setae subdorsales (c1) 39 (37–40) on dorsal annulus 9–10; setae (c2) 20 (17–22) on ventral annulus 8 (7–9); setae (d) 17.4 (15–20) on ventral annulus 16 (15–18); setae (e) 9.4 (8–11) on ventral annulus 31 (30–33); setae (f) 29.6 (28–35) on 5th ventral annulus from rear. Setae (h1) 3.1 (2.5–4), caudal setae (h2) 69 (65–75). Genitalia 18.9 (17–20) wide, proximal setae on coxisternum III (3a) 7.3 (5–8).

Host plants. Tilia cordata Mill. , Tilia tomentosa Moench , Tilia americana L. and Tilia ×flavescens A. Braun ( Tiliaceae ).

Relation to hosts. Deutogyne females of P. tetratrichus Nalepa were observed to cause various types of damage symptoms on different Tilia species. On T. cordata Mill. and T. × flavescens, the symptoms consisted of upward leaf-roll galls along the edges of leaves ( Fig. 3 ). On T. tomentosa , these resulted in small, round erinea on the lower surface of leaves and small, wart-like galls on the upper surface of leaves ( Figs 4 a & 4b). On T. americana , irregular finger galls were seen on both leaf surfaces ( Fig. 5 ).

Material examined. The counts below are based on a total of 54,566 specimens of P. tetratrichus (mounted on glass microscope slides) collected from Poland as follows: Tilia americana, Kórnik near Poznań, 13 June 2006, 59Ƥd (deutogyne females), 35Ƥp (protogyne females), 73 (males), 134n (nymphs and larvae), Rogów near Łódż, 2 August 2006, 276Ƥd, 4Ƥp, 123, 3n. Tilia cordata, Nowy Dwór near Skierniewice, 26 April 2001, 38Ƥd, Skierniewice, 14 May 2001, 26Ƥd; 3 June 2001 33Ƥp, 3Ƥd, 23; Botanical Garden of the Polish Academy of Sciences, Warsaw, 7 June 2001 ,17Ƥd, 24Ƥp, 3n; 21 June 2001, 8Ƥd, 12 July 2001, 14Ƥd; 29 April 2002, 270Ƥd; 13 May 2002, 12 Ƥd 771 Ƥp 96 3; 27 May 2002, 499Ƥd, 1566 Ƥp, 157 3, 10 June 2002, 3351Ƥd, 429Ƥp, 4873, 23 June 2002, 3121Ƥd, 63Ƥp, 133 3, 8 July 2002, 985Ƥd, 25 July 2002, 750 Ƥd, 26 August 2002, 42 Ƥd; 6 May 2003, 199Ƥd, 12n; 20 May 2003, 107Ƥd, 753Ƥp, 168Ƥp, 463n; 3 June 2003, 682Ƥd; 383Ƥp, 1723, 503n; 18 June 2003. 1275Ƥd, 33Ƥp, 4223, 763n; 1 July 2003, 563Ƥd, 51Ƥp, 923, 117n, 30 July 2003. 158Ƥd, 30Ƥp; 14 May 2004, 31Ƥd; 292Ƥp, 453; 3 June 2004, 201Ƥd, 1603Ƥp, 4753; 22 June 2004, 3475Ƥd, 79Ƥp, 5963; 16 July 2004, 463Ƥd, 51Ƥp, 1923; 4 August 2004, 561Ƥd, 663; 27 August 2004, 401Ƥd; 83; Arboretum in Kórnik near Poznań, 13 June 2006, 12Ƥd, 77Ƥp. T. “ Flavescens” Glenleven Linden, Arboretum in Rogów near Łódż, 2 August 2006, 172Ƥd, 1Ƥp, 113, 2n. Tilia tomentosa , the old campus of the Warsaw University of Life Sciences, Warsaw, 29 April 2002, 47 Ƥd; 13 May 2002, 186 Ƥd, 517 Ƥp, 227 3; 27 May 2002, 424 Ƥd, 1897 Ƥp, 7743; 10 June 2002, 1978 Ƥd, 572 Ƥp, 4563; 23 June 2002, 2741 Ƥd, 9 Ƥp, 1893; 8 July 2002, 118 Ƥd, 3Ƥp, 64 3; 25 July 270 Ƥd; 6 May 2003, 81Ƥd; 20 May 2003, 66Ƥd, 387Ƥp, 1093, 39n 3 June 2003, 2503Ƥd, 95Ƥp, 2313, 206n, 18 June 2003. 2473Ƥd, 8Ƥp, 2423, 199n; 1 July 2003. 452Ƥd, 143, 5n; 30 July 2003, 251Ƥd; 28 August 2003, 79Ƥd; 14 May 2004, 244Ƥd, 361Ƥp, 1073; 3 June 2004, 23Ƥd, 513Ƥp, 2023; 22 June 2004, 3412Ƥd, 193Ƥp, 2023; 16 July 2004, 326Ƥd, 121Ƥp, 5263; 4 August 2004, 148Ƥd, 5Ƥp, 103; 27 August 2004, 190Ƥd; 53; Kórnik near Poznań, 13 June 2006, 245Ƥd, 237Ƥp, 1543, 199n, Rogów near Łódż, 4 July 2006, 54Ƥd, 13Ƥp, 913, 69n.

Morphological comparison of protogyne and deutogyne females. Protogyne and deutogyne females of Phytoptus tetratrichus were differentiated using both qualitative and quantitative traits. In life, the body of the deutogyne female form was amber in colour while that of the protogyne form was milky-white. Deutogyne females, unlike protogyne females, had an obscure pattern on the prodorsal shield. In addition, the anterolateral sides of the prodorsal shield were smooth. The ventral annuli located between the genital shield and coxae were smooth and the prosternal apodeme was un-forked at the rear.

Protogyne and deutogyne females were also clearly differentiated by quantitative traits, as revealed by canonical variate analysis ( Fig. 6 ). This variation was mainly due to the lengths of legs I and II and to a much lesser extent, the length of tarsus I. A possible reason for this is that deutogyne females are a migratory form of P. tetratrichus , so they may need longer legs for the purpose of mobility. Indeed, in the present study, legs I and II and tarsus I were much longer in deutogyne females when compared with protogyne females which spend their entire life in galls. These forms differed substantially; hence, two separate analyses are presented as follows.

Variations in protogyne females. The comparative analysis of morphological traits of females of Phytoptus tetratrichus collected from Tilia cordata , T. tomentosa and T. americana , showed slight differences among protogyne females. These included the distance between tubercles (ve); length of setae d, e, f, 2a and 3a; length of the female genitalia; length of tibia I and the number of dorsal annuli ( Table 2 ).

Concerning the protogyne females inhabiting T. cordata and T. tomentosa that were analysed using canonical variate analysis, these were morphologically different as revealed by the first canonical variate which accounted for 64.7% of the total variation observed within the females ( Fig. 7 ). Of the 47 morphological traits considered, there were eight (8) that mainly accounted for this variation which are listed here in order of decreasing importance: number of dorsal and ventral annuli; position of setae (d) and setae (e); distance between external vertical setae (ve), tubercles of scapular setae (sc) and tubercles setae (d); length of proximal setae 3a on coxisternum III ( Table 3 ).

The second canonical variate analysis represented between-year differences, although this variation was much smaller (15.4%). Especially specific was the year 2004, which for both Tilia species, differed from 2002 and 2003 (these two years were shown to be quite intermingled on the graph in Fig. 7 ). Variations found during the year (as revealed by the second canonical variate), were mainly because of body length, length of proximal setae on coxisternum III (3a) and distance apart, number of dorsal annuli and width of the prodorsal shield.

Variations in deutogyne females. For deutogyne females of Phytoptus tetratrichus collected from T. cordata , T. tomentosa and T. americana , differences were apparent in the length of tarsus I; length of setae f, 1a, sc and 2a and body length ( Table 2 ).

As revealed by canonical variate analysis, deutogyne females collected from different Tilia species and years showed much greater differences than protogyne females ( Fig. 8 ), although both canonical variates are needed to differentiate between the Tilia species. Almost all morphological traits contributed to this very substantial variation, with the number of annuli and length of tibia of leg II, being the most important contributors.

For P. tetratrichus , deutogyne females (individuals from all combinations of Tilia species species × year) were easily differentiated, but the differences between P. tetratrichus on T. cordata and T. tomentosa were not so distinct.

Trait Tilia cordata Tilia tomentosa Tilia americana

Protogyne Deutogyne Protogyne Deutogyne Protogyne Deutogyne

(n=60) (n=30) (n=60) (n=30) (n=10) (n=20)

Figures

FIGURE 1. Phytoptus tetratrichus Nalepa 1890. Protogyne female: D. Dorsal view; AL. Antero-lateral view; CGF. Coxigenital region; em. Empodium. Male: GM. Genital region.

FIGURE 2. Phytoptus tetratrichus Nalepa 1890. Deutogyne female: D. Dorsal view; AL. Antero-lateral view; CGF. Coxigenital region; em. Empodium.

FIGURE 3. Damage caused by Phytoptus tetratrichus Nalepa 1890 as seen on an individual leaf of Tilia cordata.

FIGURE 4. Damage caused by Phytoptus tetratrichus Nalepa 1890 as seen on an individual leaf of Tilia tomentosa: A. Upper surface. B. Lower surface.

FIGURE 5. Leaf damage caused by Phytoptus tetratrichus on Tilia americana.

FIGURE 6. Canonical variate analysis of 47 traits for protogyne and deutogyne females of Phytoptus tetratrichus Nalepa 1890 carried out on pooled data from both Tilia cordata and T. tomentos a over three seasons: gray circles - deutogyne females; dark circles - protogyne females.

FIGURE 7. Canonical variate analysis of 47 traits for protogyne females of Phytoptus tetratrichus Nalepa 1890 on Tilia cordata and Tilia tomentosa in 2002 to 2004: c 2, c 3, c 4 = T. cordata in 2002, 2003 and 2004, respectively; t 2, t 3, t 4 = T. tomentosa in 2002, 2003 and 2004, respectively.

FIGURE 8. Canonical variate analysis of 47 traits for deutogyne females of Phytoptus tetratrichus Nalepa 1890 on Tilia cordata and Tilia tomentosa in 2002 to 2004: c 2, c 3, c 4 = T. cordata in, 2002, 2003 and 2004, respectively; t 2, t 3, t 4 = T. tomentosa in 2002, 2003 and 2004, respectively.