Morphological variability of Phyllocoptes adalius female ... - BioOne

Systematic & Applied Acarology 21(2): 181–194 (2016) http://doi.org/10.11158/saa.21.2.3 Article

ISSN 1362-1971 (print) ISSN 2056-6069 (online)

http://zoobank.org/Durn:lsid:zoobank.org:pub:CA849132-9120-4A12-BA48-941D16BCFAE9

Morphological variability of Phyllocoptes adalius female forms (Acari: Eriophyoidea), with a supplementary description of the species TOBIASZ DRUCIAREK1, MARCIN KOZAK2, MOSTAFA MAROUFPOOR3 & MARIUSZ LEWANDOWSKI 1,4 1

Department of Applied Entomology, Faculty of Horticulture, Biotechnology and Landscape Architecture, Warsaw University of Life Sciences – SGGW Nowoursynowska 159, 02-776 Warsaw, Poland. 2 Department of Botany, Faculty of Agriculture and Biology, Warsaw University of Life Sciences – SGGW, Nowoursynowska 159, 02-776 Warsaw, Poland. 3 Department of Plant Protection, Agriculture Faculty, University of Kurdistan, Sanandaj, Iran. 4 Corresponding author: Mariusz Lewandowski ([email protected]).

Abstract This paper provides a detailed description of Phyllocoptes adalius, eriophyoid species with a complex life cycle. P. adalius has recently become one of the most important mite pests in greenhouse rose production. We present morphometric data and illustrations that help to distinguish protogyne and deutogyne female forms. Both forms are differentiated by qualitative morphological traits such as ornamentation of the prodorsal shield and shape of microtubercles on the dorsal annuli. Key words: eriophyoid mites, deuterogyny, supplementary description, canonical analysis, rose

Introduction Phyllocoptes adalius Keifer (Acari: Eriophyoidea) is one of the most important pests in rose production. In recent years, P. adalius has emerged as a serious problem in greenhouses in Poland, where mites can rapidly establish populations on rose leaves and petals to densities as high as 340/ cm2. Indications of P. adalius damage range from initial simple mosaic-red discoloration and deformation of leaves, to a severe delayed bud development and stunting of the whole plant. The initial symptoms of leaf discoloration and malformation are especially evident on newly developed leaves that may already harbor hundreds of mites (Labanowski 2009; Druciarek et al. 2014). Although the first published work relevant to eriophyoid mites was made about 270 years ago (Lindquist & Amrine 1996), many aspects of their biology and ecology have not been studied in depth. In the past few decades, we have begun to learn that this most minute of arthropods display frequently variable and complex life cycles that allow them to be extremely resilient and adaptable to their environment (Manson & Oldfield 1996). Today, we know that in the life cycle of some eriophyoids, two different forms of females but usually only one form of male may occur during the year. This phenomenon, called deuterogyny, was first described by Putman (1939) for Aculus fockeui (Nalepa & Trouessart) from plum, and later more clearly explained by Keifer (1942) for Shevtchenkella aesculifoliae (Keifer) from buckeye. The primary form (protogyne) consists of both males and females, and can be morphologically so different from the secondary form (deutogyne) consisting of females only that it has often been mistakenly described as a distinct species (Manson & Oldfield 1996). Deutogynes, usually called ‘winter forms’, differ from female protogynes or

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‘summer forms’ in morphology; this difference is due to evolutionary adaptation for survival in regions with well-defined winters. However, several reports of deuterogyny in species from milder or even tropical regions have been made, albeit infrequently (Britto et al. 2008). In temperate regions, winter generation females, in general, express traits that promote survival in adverse conditions, e.g. modification of microtubercles on the opistosoma for better conservation of body fluids, by rendering the cuticle more resistant to water loss (Krantz & Ehrensing 1990). Such differences, however, may not be readily apparent, even for the trained eye, if the species is deuterogynous. Hence, studies on life cycles of any pest, including eriophyoids, are crucial for correct identification to enable appropriate decisions on plant protection. The aim of this research was to provide an updated description of P. adalius, an eriophyoid species that, in recent years, has been increasingly prevalent in greenhouse rose production systems in Poland. We present morphological differences between protogynes and deutogynes within different populations, together with detailed drawings and scanning electron microscope (SEM) photographs. This study sets out to provide supplementary description and information on one of the most important mite pest species on rose, as a helpful tool of proper identification and control.

Materials and methods Leaf samples of rose cultivars were collected in 2011 from rose city gardens in Warsaw, Poland and in 2014 from Turku, Finland. Specimens of P. adalius were collected from plants by direct examination under a stereomicroscope, mounted on slides in a modified Berlese medium (Amrine & Manson 1996), and studied with a phase-contrast microscope. The morphology nomenclature follows that of Lindquist (1996) and systematic classification follows that of Amrine et al. (2003). All measurements, unless specified otherwise, refer to lengths expressed in micrometers. Measurements of mites were made according to Amrine and Manson (1996) and de Lillo et al. (2010). Length of legs was measured from the posterior margin of trochanter to the tip of the tarsus. Measurements of leg segments and setae (legs and opisthosomal) refer to the lengths of each structure unless specified otherwise. Positions of leg setae were measured from the proximal margin of the seta-bearing segment. Locations of ventral setae c2, d, e, and f on ventral annuli were measured from the first entire annulus after posterior margin of coxae II. Measurements of particular features are given as a range of values. All examined specimens on microscope slides are stored in the collection of the Department of Applied Entomology, Warsaw University of Life Sciences, Warsaw, Poland. For morphometric studies, 30 females of each form (protogyne and deutogyne), mounted on slides in dorso-ventral position were selected from specimens collected from rose cultivars between August 27 and October 8, 2012, in botanical gardens located in Warsaw, Poland: Garden of Museum of King Jan III's Palace at Wilanow, 52°09'52.2"N, 21°05'23.8"E (PL_Wil); Polish Academy of Sciences Botanical Garden in Powsin, 52°06'29.3"N, 21°05'43.6"E (PL_Pow); Saxon Garden, 52°14'29.4"N, 21°00'19.4"E (PL_Sas); specimens collected on October 11, 2014 were from Turku, Finland, 60°27'14.7"N, 22°16'41.0"E (FI_Tur). Twenty-four morphological traits (Fig. 1) of each individual were measured with the Soft Imaging System Cell D. Canonical variate analysis (Krzanowski 2000) was used to explain variability in the morphology of individuals of protogyne and deutogyne females. This method takes into account the grouping structure according to populations, and helps one to find similar/dissimilar individuals. The values of each trait were first standardized to have mean = 0 and variance = 1, so that all traits had the same weight in the analysis. The analysis was carried out using the MASS package (Venables & Ripley 2002) in R (R Core Team 2015). 182

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FIGURE 1. Measurements made on morphological traits of the Phyllocoptes adalius female used in morphometric analysis. Explanation of abbreviations: A—length of opisthosoma, B—prodorsal shield length, C—tubercles sc apart, D—length of setae sc, E—no. of dorsal annuli, F—no. of ventral annuli, G—length of setae c2, H—length of setae d, I—length setae of e, J—length of f, K—length of genitalia, L—width of genitalia, M—length of setae 3a, N—tubercles 3a apart, O—length of setae 1b, P—tubercles 1b apart, Q—length of setae 1a, R—tubercles 1a apart, S—length of setae 2a, T—tubercles 2a apart, U—length of tibia I, W—length of tarsus I , X—length of tibia II, Y—length of tarsus II.

Results Family: Eriophyidae Nalepa Subfamily: Phyllocoptinae Nalepa Tribe: Phyllocoptini Nalepa Genus: Phyllocoptes Nalepa 2016

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Supplementary description of Phyllocoptes adalius Keifer (Figures 2–3) Phyllocoptes adalius Keifer, 1939: Bull. Cal. Dept. Agric., ES VII, 28: 487, pl. 99. Eriophyes rosarum Liro, 1943: Ann. Zool. Soc. Zool.-Bot. Fenn., Vanamo 9(3): 24–25, f. 20. Phyllocoptes rosarum (Liro, 1943): Roivainen 1951, Acta Entomol. Fenn., 8: 1–72.

FIGURE 2. Phyllocoptes adalius female: D—dorsal mite; CG—coxo-genital region; L1, L2—legs; PL— postero-lateral mite; male: GM—genital region. 184


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Diagnosis: Prodorsal shield pattern composed of incomplete median line located on rear part of shield; bifurcated in their anterior part and joined with admedian lines, forming a V-shaped mark; at about 2/3 its length again joined with admedian lines by lines perpendicular or running slightly to the rear end. Admedian lines parallel from anterior margin of the shield to about 1/3 of its length, are joined by transverse line; from that place admedian lines gradually diverging to rear margin. Submedian lines I slightly sinuate and gradually divergent from anterior margin of the shield to its rear margin. Submedian lines II curved, joined with submedian lines I at their 1/3 length. Tubercles of setae sc ahead of rear shield margin; opisthosoma evenly rounded dorsally with 52–62 dorsal and 61–71 ventral annuli; empodium entire 5–6-rayed. Protogyne female (16 specimens): body fusiform, 206–275; width 65–77. Gnathosoma 22–25, curved downward, dorsal pedipalpal genual setae d 8–10, seta ep 3, seta v 2, cheliceral stylets 16– 18. Prodorsal shield subtriangular, 40–44, 48–56 wide, with triangular frontal lobe 4–7 over gnathosomal base. Shield pattern: median line on rear part of shield; at about 2/3 length of shield it is bifurcated and joined with admedian lines, forming a V-shaped mark; at about 2/3 its length there are lines perpendicular or running slightly to the rear and joining with admedian lines. Admedian lines parallel from anterior margin of the shield to about 1/3 of its length, where they are joined by transverse line; from that place admedian lines gradually diverging to rear margin and joined with median lines in 2/3 and in the end of shield length. At rear part of shield median and admedian lines slightly granulated. Submedian lines I slightly sinuate and gradually divergent from anterior margin of the shield to its rear margin. Submedian lines II curved, joined with submedian lines I at their 1/3 length. Tubercles of setae sc ahead of rear shield margin, 21–27 apart, seta sc 17–21. Legs with all usual segments and setae present. Leg I 31–35; femur 10 seta bv 14–17, position of bv 4 genu 5–6, seta l” 22–30, position of l” 3–4; tibia 8–9, seta l’ 8–11, position of l’ 3; tarsus 6–8, setae: ft” 21– 28, ft’ 18–25, u’ 6–9; solenidion ω 8–10, rod-like; empodium 6–8, simple, 5–6-rayed. Leg II 30–33; femur 10–11, seta bv 14–20, position of bv 4–5; genu 4–5, seta l” 10–13, position of l” 2–3; tibia 5– 7; tarsus 7–8, setae: ft” 19–27, ft’ 8–10, u’ 5–8; solenidion ω 9–11, rod-like; empodium 6–7, simple, 5–6-rayed. Coxal plates with lines and dashes. Setae 1b 8–12, 12–15 apart; setae 1a 20–31, 6–10 apart; setae 2a 30–47, 23–29 apart; distance between setae 1b and 1a 7–8, distance between setae 1a and 2a 7–9. External genitalia 11–14, 21–25 wide, genital coverflap with 9–11 longitudinal ridges; setae 3a 41–58, 15–21 apart. Opisthosoma with 55–61 dorsal and 64–73 ventral annuli, 9–13 coxigenital annuli. Dorsal annuli with conical microtubercles, placed on rear margin, ventral annuli with microtubercles oval and pointed, on posterior annuli microtubercles elongated, placed near rear annuli margin. Setae c2 24–35, 52–73 apart, on 10–13th annulus; setae d 47–65, 32–44 apart, on 23– 27th annulus; setae e 35–58, 17–24 apart, on 39–45th annulus; setae f 25–35, 22–28 apart, on 60– 69th annulus, 5–6th annulus from rear. Setae h1 4–6, 5–7 apart; setae h2 70–98, 10–11 apart; distance between h1 and h2 3. Deutogyne female (19 specimens): body fusiform, 174–262; width 59–71. Gnathosoma 25– 29, curved downward, dorsal pedipalpal genual seta d 7–10, seta ep 3–4, seta v 2–3, cheliceral stylets 14–20. Prodorsal shield subtriangular, 38–46, 45–55 wide. Shield pattern: design of clear longitudinal lines. Median line on rear part of shield; at about 2/3 length of shield it is bifurcated and joined with admedian lines, forming V-shaped mark; at about 2/3 its length there are lines perpendicular or running slightly to the rear and joining with admedian lines. Admedian lines parallel from anterior margin of the shield to about 1/3 of its length, from that place admedian lines gradually diverging to rear margin and joined with median lines in 2/3 and in the end of shield length. Submedian lines I slightly sinuate and gradually divergent from anterior margin of the shield to its rear margin. Submedian lines II curved, joined with submedian lines I at their 1/3 length. Tubercles of setae sc ahead of rear shield margin, 20–26 apart, seta sc 15–20. Legs with all usual segments and setae present. Leg I 30–35; femur 9–12, seta bv 10–17, position of bv 4–5; genu 5–6, seta l” 19–33, 2016


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FIGURE 3. Phyllocoptes adalius female: LM—lateral mite; LO—lateral opisthosoma; ADD—antero-dorsal mite (deutogyne); ADP—antero-dorsal mite (protogyne); em—empodium (enlarged); IG—internal genitalia (enlarged); immature: LN—lateral nymph; LL—lateral larva.

position of l” 2–4; tibia 7–9, seta l’ 9–12, position of l’ 2–4; tarsus 6–8, setae: ft” 23–28, ft’ 20–25, u’ 5–9; solenidion ω 8–10, rod-like; empodium 6–8, simple, 6-rayed. Leg II 29–33; femur 9–12, seta bv 15–19, position of bv 3–5; genu 4–6, seta l” 10–13, position of l” 2–3 tibia 5–6; tarsus 7–8, setae:

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ft” 20–27, ft’ 8–10, u’ 6–9; solenidion ω 8–10, rod-like; empodium 6–8, simple, 6-rayed. Coxal plates with granules and dots. Setae 1b 10–14, 13–15 apart; setae 1a 25–33, 7–9 apart; setae 2a 37– 48, 24–28 apart; distance between setae 1b and 1a 7–8, distance between setae 1a and 2a 7–9. External genitalia 10–14, 23–26 wide, genital coverflap with 7–10 longitudinal ridges; setae 3a 48– 69, 15–19 apart. Opisthosoma with 52–58 dorsal annuli with rounded microtubercles; 61–69 ventral annuli with rounded microtubercles, elongated on the posterior annuli, 11–14 coxigenital annuli. Setae c2 29–34, 52–64 apart, on 10–13th annulus; setae d 52–66, 31–38 apart, on 21–28th annulus; setae e 50–59, 15–19 apart, on 36–43rd annulus; setae f 28–35, 20–26 apart, on 56–64th annulus, 5– 6th annulus from rear. Setae h1 5–6, 5–7 apart; setae h2 90–107, 10–12 apart; distance between h1 and h2 2–3. Male (7 specimens): body fusiform, 168–216; width 57–62. Gnathosoma 25–28, curved downward, dorsal pedipalpal genual seta d 6–8, seta ep 3, seta v 2, cheliceral stylets 15–17. Prodorsal shield subtriangular, 38–41, 46–51 wide with pattern similar to that of protogyne female. Tubercles of setae sc ahead of rear shield margin, 20–24 apart, seta sc 12–14. Legs with all usual segments and setae present. Leg I 28–29; femur 8–9, seta bv 12–14, position of bv 4; genu 5, seta l” 18–23, position of l” 2–3; tibia 7–8, seta l’ 7–8, position of l’ 2–3; tarsus 6–7, setae: ft” 21–23, ft’ 17–20, u’ 6–7; solenidion ω 8–9, rod-like; empodium 5–7, simple, 5-rayed. Leg II 26–29; femur 8–9, seta bv 13– 14, position of bv 4; genu 4, seta l” 8–10, position of l” 2–3; tibia 5–6; tarsus 6–7, setae: ft” 18–24, ft’ 7–8, u’ 5–6; solenidion ω 9–10, rod-like; empodium 6, simple, 5-rayed. Coxal plates with granules and dots. Setae 1b 8–9, 11–13 apart; setae 1a 18–25, 6–7 apart; setae 2a 34–39, 22–25 apart; distance between setae 1b and 1a 7–8, distance between setae 1a and 2a 6–8. External genitalia 13– 16, 18–20 wide, surface below the eugenital setae with graniles; setae 3a 45–57, 15–19 apart. Opisthosoma with 50–57 dorsal annuli with pointed microtubercles; 58–65 ventral annuli with rounded microtubercles, elongated on the posterior annuli, 10–11 coxigenital annuli. Setae c2 24– 27, 48–56 apart, on 10–11th annulus; setae d 45–53, 29–36 apart, on 20–21st annulus; setae e 39– 48, 15–20 apart, on 33–38th annulus; setae f 24–29, 18–22 apart, on 54–60th annulus, 5th annulus from rear. Setae h1 4–5, 5–6 apart; setae h2 70–91, 9–10 apart; distance between h1 and h2 2–3. Nymph (7 specimens): body fusiform, 140–180; width 45–57. Gnathosoma 21–25, curved downward, dorsal pedipalpal genual seta d 4–6, seta ep 2–3, seta v 2, cheliceral stylets 13–16. Prodorsal shield subtriangular, 37–40, 40–49 wide, with pattern similar to that of deutogyne female. Tubercles of setae sc ahead of rear shield margin, 18–21 apart, seta sc 11–15. Legs with all usual segments and setae present. Leg I 23–25; femur 7–8, seta bv 8–11, position of bv 3; genu 4, seta l” 14–22, position of l” 2–3; tibia 5, seta l’ 6–7, position of l’ 2–3; tarsus 5–6, setae: ft” 16–20, ft’ 13–18, u’ 4–6; solenidion ω 7–8, rod-like; empodium 5, simple, 5-rayed. Leg II 22–23; femur 7– 8, seta bv 10–11, position of bv 3–4; genu 3–4, seta l” 7–8, position of l” 2–3; tibia 3–4; tarsus 6, setae: ft” 16–20, ft’ 5–6, u’ 4–5; solenidion ω 6–8, rod-like; empodium 4–5, simple, 4–5-rayed. Coxal plates with granules and dots. Setae 1b 6–7, 9–11 apart; setae 1a 14–20, 6–7 apart; setae 2a 22–32, 20–24 apart; distance between setae 1b and 1a 7–8, distance between setae 1a and 2a 5–6. Setae 3a 18–25, 10–12 apart. Opisthosoma with 51–54 dorsal annuli with elongated microtubercles placed on rear margin of annuli; 41–47 ventral annuli with rounded microtubercles, elongated on the posterior annuli. Setae c2 19–22, 40–50 apart, on 7–8th annulus; setae d 25–40, 23–34 apart, on 16– 19th annulus; setae e 21–28, 13–16 apart, on 25–29th annulus; setae f 16–24, 16–19 apart, on 38– 43rd annulus, 4–5th annulus from rear. Setae h1 4, 4–5 apart; setae h2 29–56, 8–9 apart; distance between h1 and h2 2–3. Larva (7 specimens): body fusiform, 94–131; width 39–46. Gnathosoma 12–15, curved downward, dorsal pedipalpal genual seta d 3–4, seta ep 2, seta v 1–2, cheliceral stylets 12–13. Prodorsal shield subtriangular, 27–32, 32–38 wide. Shield pattern: median line absent; admedian lines entire, somewhat sinuate; submedian lines I on the anterior half part of shield only; submedian 2016


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lines II absent. Tubercles of setae sc at rear shield margin, 16–19 apart, seta sc 8–10. Legs with all usual segments and setae present. Leg I 15–18; femur 5–6, seta bv 6–7, position of bv 3; genu 3–4, seta l” 12–16, position of l” 2; tibia 3, seta l’ 4, position of l’ 2; tarsus 3–4, setae: ft” 13–15, ft’ 11– 13, u’ 3–4; solenidion ω 5–6, rod-like; empodium 4, simple, 4–5-rayed. Leg II 16–17; femur 5–6, seta bv 7–9, position of bv 3; genu 3, seta l” 5–6, position of l” 2; tibia 2–3; tarsus 4, setae: ft” 15– 18, ft’ 4–5, u’ 3–4; solenidion ω 5–6, rod-like; empodium 4–5, simple, 4-rayed. Coxal plates with granules and dots. Setae 1b 4–5, 8–10 apart; setae 1a 9–13, 5–7 apart; setae 2a 16–24, 18–21 apart; distance between setae 1b and 1a 5–7, distance between setae 1a and 2a 5–6. Setae 3a 11–15, 8–9 apart. Opisthosoma with 38–42 dorsal annuli with rounded microtubercles; 30–34 ventral annuli with rounded microtubercles, elongated on the posterior annuli. Setae c2 14–17, 31–38 apart, on 5– 6th annulus; setae d 19–29, 18–23 apart, on 11–13th annulus; setae e 15–27, 9–12 apart, on 17–20th annulus; setae f 16–20, 12–15 apart, on 27–30th annulus, 4–5th annulus from rear. Setae h1 3, 3–4 apart; setae h2 29–40, 6–7 apart; distance between h1 and h2 2. Material examined. 10 proto and 9 deutogyne females, 5 males and 10 immature stages were collected from Rosa sp. (cultivars ‘Falstaff [Ausverse]’ and ‘Apricot nectar’) at the Polish Academy of Sciences Botanical Garden in Powsin (52°06'29.3"N, 21°05'43.6"E), leg. T. Druciarek. 6 proto and 10 deutogyne females, 2 males and 4 immature stages were collected from Rosa sp. (a cultivated hybrid rose) in Warsaw (urban park), (52°08'10.6"N, 21°03'51.3"E), leg. T. Druciarek. All specimens were collected in September and October 2011. Other material. Mites collected in Finland: 5 deutogyne females were collected from Rosa sp. in type locality of P. rosarum (Liro, 1943), Merimasku (60°29'45.6"N, 21°52'06.4"E) and Naantali (60°28'05.4"N, 22°00'55.0"E); 30 protogyne and 30 deutogyne females in Turku (60°27'14.7"N, 22°16'41.0"E). All specimens were collected on October 11, 2014. Relation to the host. All stages of P. adalius were found on leaves, mainly on their lower surface, as well as on stems and flowers, causing leaf drop and malformation of flowers. Remarks. Phyllocoptes adalius is very similar to Phyllocoptes fructiphilus Keifer, which also inhabits leaves of rose plants (Keifer 1940). Morphologically, both species have almost the same characteristics and can be distinguished from each other only by the structure of the prodorsal shield: linear patterns on the prodorsal shield of P. fructiphilus are more defined and numerous than those of P. adalius. Key diagnostic features of these two species are the short lines at about 2/3 of median line length which are joining with admedian lines. These lines are directed towards the anterior end of the shield in P. fructiphilus, whereas in P. adalius they are perpendicular or directed towards the rear margin. Also, three additional short lines located on each lateral side of the prodorsal shield are characteristic only for P. fructiphilus. Moreover, an interesting distinction between the two species is their relation to the host. P. fructiphilus primarily inhabits flower buds, petiole bases, and fruits (around seeds), whereas P. adalius is a more likely lower surface leaf vagrant (Baker et al. 1996). At high population densities, however, P. adalius may be found on the upper leaf surface, as well as on flower petals and buds, although not in rose fruits.

Variation in the morphology of protogynes and deutogynes of Phyllocoptes adalius Protogyne and deutogyne females of P. adalius may be differentiated by qualitative morphological traits such as the patterns on the prodorsal shield and the shape of microtubercles on the dorsal annuli. Protogyne females have more distinct lines on the prodorsal shield, as well as slightly granulated median and admedian lines at the rear part of the shield. Microtubercles on dorsal annuli of protogyne females are conical and located at the rear margin of annuli, whereas deutogyne females have no microtubercles or they are very small and rounded (Fig. 3). These two forms of females may 188


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be also identified by quantitative traits. The first canonical variate, which was responsible for the differentiation between protogynes and deutogynes, accounted for 39.7% of the total variation (Fig. 4). Length of genitalia, number of ventral annuli, and length of sc setae have the most distinct discriminative power based on the first canonical function (Table 1). However, this function clearly separates protogynes and deutogynes only in one population (i.e., PL_Sas); in other populations both female forms overlap. The second canonical variate described 24.4% of variability in the populations studied; the most important traits were length of 3a setae, length of sc setae and number of dorsal annuli differ among mites from particular populations (Table 1). This variate discriminated between two female forms in only one population, i.e., PL_Wil (Fig. 4).

FIGURE 4. Canonical variate analysis of 24 traits for protogyne and deutogyne female forms of Phyllocoptes adalius. Explanation of abbreviations: deuto = deutogynes; proto = protogynes; FI_Tur— Turku, Finland; PL_Pow—Powsin garden, Poland; PL_Sas—Saski garden, Poland; PL_Wil—Wilanow garden, Poland. TABLE 1. First (CV1) and second (CV2) canonical variable loadings for Phyllocoptes adalius. Features symbol

Canonical variable loadings

name

CV1

CV2

K

length of genitalia

-0.71

-0.52

F

number of ventral annuli

0.70

-0.47

D

length of setae sc

0.55

0.64

T

tubercle of setae 2a apart

0.53

0.03

M

length of setae 3a

-0.50

0.80

P

tubercle of setae 1b apart

-0.50

0.32

E

number of dorsal annuli

0.03

0.57

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FIGURE 5. SEM photographs of Phyllocoptes adalius Keifer. A—protogyne form; B—deutogyne form; C— prodorsal shield of protogyne form; D—prodorsal shield of deutogyne form.

Discussion To date, six named species assigned to the genus Phyllocoptes have been found on roses all over the world. However, P. rosarum (Liro) was synonymized with P. adalius while P. slinkardensis Keifer with P. fructiphilus, so currently only four species from the genus are known on rose (Amrine & Stasny 1994, 1996). These two synonymized species are also the most economically important rose pests. In the USA, serious damages are caused by P. fructiphilus, which is responsible for rose rosette virus (RRV) transmission on roses growing in natural environments as well as in parks and gardens (Amrine 2014, Di Bello et al. 2015). The second species, P. adalius, causes serious injuries on roses cultivated in greenhouses in Poland (Druciarek et al. 2014). Despite the close similarity between these species, P. adalius is not a rose rosette disease agent (Amrine 2002) and the damage caused is a direct result of mite feeding. P. adalius had originally been reported as the prevalent species inhabiting roses in California (Keifer 1939), but its geographic distribution later expanded to include Finland (Liro 1943, Roivainen 1947, 1951), Sweden (Roivainen 1950), Poland (Boczek 1969, Labanowski 2009, Druciarek et al. 2014), and China (Kuang 1995). The first record of the species in Europe described the new species as Eriophyes rosarum Liro at the basis of specimens collected in Merimasku, Finland, from Rosa caesia Smith (originally listed as Rosa coriifolia Fries). The species was then moved to genus Phyllocoptes by Roivainen (1951). Finally, Amrine & Stasny (1996), taking into account the close morphological similarity between P. rosarum and P. adalius, synonymized both species, so that the first name was accepted as junior synonym of P. adalius. The 190


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results of canonical variate analysis in our study showed that the mites collected in Finland were morphologically similar to the Polish populations. Moreover, the range of values for the morphological characteristics in populations from both countries (including those collected in the type locality of P. rosarum) overlapped and agreed with values measured by Keifer (1939), Liro (1943), and Roivainen (1951) (Table 2). Therefore, our observations validate the synonymization by Amrine and Stasny (1996). TABLE 2. Comparison of morphological traits of Polish and Finnish populations of Phyllocoptes adalius with measurements published in original descriptions of the species. Characteristics of females

P. adalius Poland Protogynes n=16

Length of body

P. adalius Finland

Deutogynes n=19

Protogynes n=30

P. adalius P. rosarum (Keifer (Liro 1939) 1943) Deutogynes n=3 n=unkn. n=30

206.2–274.5 173.5–261.5 199.8–265.8 179.9–272.6

P. rosarum (Roivainen 1951) n=unkn.

150–180

140–175

135–210

Length of chelicerae

16.4–17.9

13.7–19.8

16.4–19.1

16.5–18.8

28 rostrum

21

25–27 rostrum

Length of prod. shield

40.3–43.9

38–45.9

39.7–43.2

36.2–42.7

45

44

37–40

Width of prodorsal shield

47.5–55.8

45–54.6

48.0–51.4

42–52

47

-

-

Length of setae sc

17.1–21.2

15–19.5

17.2–20

14.8–19.4

18

16

9–16

Sc setae tubercle apart

21.3–26.8

20.2–26.4

20.7–23.7

18.2–23.3

17

20

-

No. of dorsal annuli

55–61

51–58

53–59

50–56

55–60

57

50–55

No. of ventral annuli

64–73

61–69

62–69

55–64

65–70

57

55–65

Length of setae c2

24.1–34.7

28.5–34.3

27.7–32.5

25.6–32.3

32

-

17–30

Length of setae d

46.5–65.1

52.3–65.8

48.1–60.8

49.5–61.9

41

-

20–40

Length of setae e

34.6–58.4

49.7–59.3

44.1–53.4

46.3–53.1

26

-

20–30

Length of setae f

24.6–34.6

28–35.2

27.4–31.9

27.2–33.8

26

-

25–32

Length of genitalia

11–14

10.2–13.8

10.4–11.9

9.6–12.8

12

16

11–13

Width of genitalia

20.9–24.7

22.7–26

19.9–23.7

19.7 -25.2

24

24

18–21

Length of setae 3a

41.4–58

47.5–68.9

45.6–57.9

48.3–59.4

26

-

12–20

9–11

7–10

7–8

5–10

6–8

-

10

Length of leg I

30.5–34.8

29.7–34.8

31.1–33.2

30.6–35.3

35

-

27–33

Length of tibia I

7.7–9.1

6.8–9.1

7.7–9

7.3–9.1

9

6.5

6.5–8

Length of tarsus I

6–8.1

6.1–8

6.4–7.5

6.1–7.8

8

6.5

6.5–7

Ribs on genital coverflap

Rays in empodia I

5–6

6

6

6

6

5

5–6

Length of leg II

30.2–32.6

28.6–33.2

27.8–32

28.2–31.2

32

-

-

Length of tibia II

4.8–6.5

5–6.4

5.6–6.7

5–6.6

6.5

-

-

Length of tarsus II

6.8–8.2

7.2–8.4

7.1–8.0

7–7.7

7.5

-

-

Despite the fact that P. adalius has been noted several times in Asia, North America and Europe, literature on the biology of the species is scarce. When Liro (1943) erroneously identified P. rosarum at the genus level, Roivainen (1951) suggested that two female forms may exist, thereby proposing a complex type of species development. This phenomenon was later proved by Baker et al. (1996), and although the authors did not provide a complete description of deutogyne females, they described morphological characteristics that are useful for their identification: weakly developed ornamentation of the prodorsal shield and strongly developed, smooth dorsal annuli, forming a distinct lateral margin with numerous weaker ventral annuli (Baker et al. 1996). Observations made 2016


191

during our studies confirm that such characteristics are the best criteria for distinguishing between protogyne and deutogyne females of P. adalius. Results of our morphological studies indicate that the female forms of the species cannot be simply differentiated using quantitative characteristics. Although deutogynes were longer than protogynes and had fewer ventral annuli and shorter sc setae, these same characteristics determined morphological variability at the population level (Fig. 4). Therefore, deutogyne and protogyne females of P. adalius may be differentiated only by qualitative morphological traits, such as the structure of the prodorsal shield and the shape of microtubercles on the dorsal annuli (Fig. 5). Contrary to our findings, Soika and Kozak (2011, 2013), who also applied canonical variate analysis to distinguish protogynes from deutogynes in four eriophyoid species on Tilia spp., reported that all protogyne and deutogyne females of these species showed noticeable differences in the number of dorsal annuli, location of setae d, length of setae e and 3a, distance between tubercles 3a and the length and pattern of the prodorsal shield. Similar results were also obtained for free-living eriophyoid species by Kozlowski (1998), who reported that the body length and width as well as the number of opisthosomal annuli, are characteristics which distinguish protogyne and deutogyne individuals of Aculus schlechtendali (Nalepa) that inhabited different apple species. Although quantitative traits were useful for the identification of polymorphic forms among genera Aculus, Eriophyes and Phytoptus in the aforementioned studies, they were not applicable in our study of P. adalius. The paucity of similar studies on other Phyllocoptes species makes it difficult to conclude whether such phenomenon is characteristic for all members of this genus or only for particular species. To date, we know that about 150 eriophyoid species with complex life cycles are known (E. de Lillo & J. Amrine, unpubl. databases) and that the degree of differentiation between protogynes and deutogynes is variable and species-dependent. In some species, female polymorphism may be identified based on very few characteristics, such as Trisetacus kirghisorum Shevchenko, in which mainly body size and number of annuli differ between protogynes and deutogynes (de Millo 1967). However, in other species, morphological differences between female forms are more obvious and often cause confusion in morphology-based taxonomy. This results in the classification of two female forms as separate species, e.g. grape rust mites Calepiterimerus vitis (Nalepa), a common pest in vineyards, which deutogynes were identified as Phylocoptes, whereas protogynes were first described as Epitrimerus and later as Calepitrimerus (Duso & de Lillo 1996). Based on our findings, we classify P. adalius with a group of species in which both female forms are similar and may be differentiated only by qualitative characteristics.

Acknowledgments We thank Prof. Jan Boczek (Warsaw University of Life Sciences) and Dr MA Sales (University of Arkansas, USA) for their thoughtful review and suggestions in improving this manuscript. The study was supported by the Faculty of Biotechnology, Horticulture and Landscape Architecture, Warsaw University of Life Sciences—SGGW, Poland.

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