Anthocoris nemoralis ( Fabricius, 1794 )

Yamada, Kazutaka & Yasunaga, Tomohide, 2021, The tribe Anthocorini in Japan (Hemiptera: Anthocoridae): descriptions of new species, review of distribution and bionomics, Acta Entomologica Musei Nationalis Pragae 61 (2), pp. 375-426 : 401-403

Anthocoris nemoralis ( Fabricius, 1794)

( Figs 7I–J , 12D , 13J–L , 15D )

? Cimex silvarum Rossi, 1790: 251 . Syntypes: Italy. Synonymized by Rൾඎඍൾඋ (1888: 317, suspected).

Acanthia nemoralis Fabricius, 1794: 76 . Lectotype (designated by Pඣඋං- ർൺඋඍ 1972: 120): J, Denmark (ZMUC).

Cimex triguttatus Schrank, 1796: 165 . No types verified. Junior primary homonym of C. triguttatus Linnaeus, 1767 and C. triguttatus Fabricius, 1775 ; synonymized by Rൾඎඍൾඋ (1888: 317).

Lygaeus austriacus Fabricius, 1803:239 . Syntypes: Austria (lost) (Zංආඌൾඇ 1964: 331). Synonymized by Fංൾൻൾඋ (1861: 137).

Anthocoris nemoralis var. superbus Westhoff, 1881: 78 . Syntypes: Germany, Westfalia (lost).

Anthocoris dohrni Le Quesne, 1958: 125 . Holotype:J, Spain, Gibraltar (BMNH). Synonymized by Pඣඋංർൺඋඍ (1971: 95).

Anthocoris pemphigi Wagner, 1960: 91 . Holotype: J, Egypt, Mansoura (ZMUH). Synonymized by Pඣඋංർൺඋඍ (1971: 95).

Anthocoris nemoralis (selected references): Fංൾൻൾඋ (1860): 263 (listed); Fංൾൻൾඋ (1861): 137 (in key); GൺඋൻංGඅංൾඍඍං (1869): 122 (listed); Rൾඎඍൾඋ (1871): 316 (listed); Rൾඎඍൾඋ (1879): 13 (in key, taxonomic status); HඈඋඏගඍH (1883): 29 (listed); Rൾඎඍൾඋ (1884): 67, 72 (in key, redescription); Eൽඐൺඋൽඌ (1890): 236 (in key); LൾඍHංൾඋඋඒ & Sൾඏൾඋංඇ (1896): 244 (listed, taxonomic status); Hൺඅൻൾඋඍ (1935): 258 (records, life cycle, habitat); Sൾൺൻඋൺ (1941):22 (listed); Sൺඇൽඌ (1957): 297, 298 (figure, description of immature stages); SඍංർHൾඅ (1958): 22–23 (in key, diagnosis); SඍංർHൾඅ (1960): 357 (listed, distribution); Cൺඋൺඒඈඇ (1961): 546 (prey, remark for record of S.Africa); Lංඇඇൺඏඎඈඋං (1961): 35 (record, habitat, distribution); Aඇൽൾඋඌඈඇ (1962): 75 (bionomics);

Aඇൽൾඋඌඈඇ & Kൾඅඍඈඇ (1963):439 (record); Jඈඌංൿඈඏ (1964):85 (record, habitat); KൾඋඓHඇൾඋ (1964): 698 (in key); EർKൾඋඅൾංඇ & WൺGඇൾඋ (1965): 213 (records); Rංൻൾඌ (1965): 80 (record); Sൾඋඏൺൽൾං (1967): 219 (distribution); EർKൾඋඅൾංඇ & WൺGඇൾඋ (1969): 180 (records); Jඈඌංൿඈඏ (1970): 834, 894 (record, distribution). Pඣඋංർൺඋඍ (1970): 737 (taxonomic history); Cൺඋൺඒඈඇ (1972): 312, 327 (figures, morphology of male reproductive system); Pඣඋංർൺඋඍ (1972): 113, 120–122 (in key, redescription, figures, distribution); Mංඌඃൺ (1973): 139 (record); Cඈඎඅංൺඇඈඌ & Oඌඌංൺඇඇංඅඌඌඈඇ (1976): 150 (listed, distribution); GൾඈඋGHංඈඎ (1977): 114 (record); Hൾංඌඌ (1977): 41–42 (record, distribution, habitat); Hඈൻൾඋඅൺඇൽඍ (1977): 65 (listed); Kൾඅඍඈඇ (1978): 35, 42, 71, 81, 91 (in key, redescription, figures, photo); Fඈඋൽ (1979): 56 (listed,distribution);Aൽඅൻൺඎൾඋ & Hൾංඌඌ (1980):9 (record,distribution); Dඋඈඌඈඉඈඎඅඈඌ (1980): 171 (listed); Öඇൽൾඋ (1982): 14–15, 17, 24, 79, 107 (figures, in key, redescription, prey, habitat, distribution); Rඈ෡ർൺ & Pඈඉඈඏ (1982): 129 (listed); Dංඈඅං (1983): 6 (prey); Hൾඇඋඒ (1988): 14 (catalogue, distribution); Bඈඌආൺඇඌ & Pඣඋංർൺඋඍ (1989): 42 (distribution, records); Pඣඋංർൺඋඍ & Hൺඅඉൾඋංඇ (1989): 92 (listed); HൺGൾඇ & Dඋൾංඌඍൺൽඍ (1990): 323 (record); BൾඋඇHൺඋൽඍ (1992): 305 (listed, habitat); RൾංർHඅංඇG & Gൾඋൾඇൽ (1994): 282 (listed); Dංඈඅං (1995): 10, 23 (listed, distribution);Pඣඋංർൺඋඍ (1996):113 (catalogue,Palaearctic); PඎඍඌHKඈඏ & PඎඍඌHKඈඏ (1996):17 (distribution);DൾඋඓHൺඇඌKඒ (1997): 5 (listed); LඎKൺඌHඎK (1997): 9 (distribution); Cඈඎඅංൺඇඈඌ (1998): 25 (listed, distribution); Pඋඈඍංම (1998):43 (records, distribution, habitat); Kඈඇൽඈඋඈඌඒ (1999): 138 (listed); Hඈඋඍඈඇ et al. (2000): 663 (mating preference,mating propensity,reproductive traits);Lൺඍඍංඇ (2000): 613 (bionomics);Oඌඍඈඏൺඇ & NංൺKൺඇ (2000):6, 9, 11 (record,in key,photo); Hඈඋඍඈඇ et al. (2002): 47 (copulation duration); MඈඋKൾඅ (2002): 108 (record); Hඈൿൿආൺඇඇ & Mൾඅൻൾඋ (2003): 243 (distribution); WඒඇංGൾඋ & BඎඋർKHൺඋൽඍ (2003): 65 (records, distribution, habitat); GඈGൺඅൺ (2004): 248; Hඈඋඍඈඇ et al. (2004): 18 (full summary of N. American records); Cඈඎඅංൺඇඈඌ (2005): 18 (record, distribution); Hඈඋඍඈඇ et al. (2005):331 (ovarian development, lipid reserves); Lൾඐංඌ et al. (2005): 62 (taxonomic history, record); RൺൻංඍඌർH (2005): 36 (listed); Rංൻൾඌ & BඈඋGൾඌ (2005): 191 (record); Aൻൽ- Rൺൻඈඎ & GHൺHൺඋං (2006): 43 (listed as predators of whitefly, associated plant); MඈඋKൾඅ (2006): 228 (record); Öඇൽൾඋ et al. (2006): 28 (listed, distribution); WൺർHආൺඇඇ et al. (2006): 188 (distribution, habitat, photo); Kൾ & Bඎ (2007): 93–94 (figure, description of female genitalia); GHൺHൺඋං et al. (2008): 16 (record,distribution);Hඈඋඍඈඇ (2008):2406,2410 (photo,economic importance); Eඅ- MൾGHඋൺൻං (2009):755 (habitat,distribution);GHൺHൺඋං et al. (2009):47 (catalogue, distribution); HൺඌඌൺඇඓൺൽൾH et al. (2009): 21 (record);HൺඌඌൺඇඓൺൽൾHA ඐൺඅ & MඈൽൺඋඋൾඌA ඐൺඅ (2010):659 (listed,in key, figure); Nൾංආඈඋඈඏൾඍඌ (2010):20 (records); GHൺHൺඋං et al.(2011): 5 (record);HൾർKආൺඇඇ &BඅදർHඅංඇGൾඋ(2011):108 (records);Hඈඋඍඈඇ & Lൾඐංඌ (2011): 1266, 1268–1269, 1271–1274 (description of male and female genitalia, photo, figures); MൺඅൾඇඈඏඌKප et al. (2011): 144 (record, prey, habitat, associated plant); Rංඇඍൺඅൺ & Rංඇඇൾ (2011): 170 (diagnosis, habitat, distribution, photo); Cඎඉඉൾඇ (2012): 159 (listed); Kආൾඇඍ & BൺŃൺෞ (2012): 510 (record, distribution); RൺൻංඍඌർH (2012): 270, 292 (listed); AඎKൾආൺ et al. (2013a): 86 (catalogue, distribution); AඎKൾආൺ et al. (2013b): 462 (record); EඌൾඇൻൾKඈඏൺ (2013): 58 (habitat, prey, distribution); Hඈඋඍඈඇ et al. (2013): 488, 492 (listed); Jൾඋංඇංම- -Pඋඈൽൺඇඈඏංම & Pඋඈඍංම (2013): 175 (record, distribution, prey); KHൺGHൺඇංඇංൺ et al. (2013): 469 (record, distribution); Yංඅൽංඋංආ et al. (2013): 56 (record);AඅൻඋൾർHඍ et al.(2015): 24 (listed); Cൺඋൺඉൾඓඓൺ & Mංൿඌඎൽ (2015): 34 (record); Cൺඋඉංඇඍൾඋඈ (2015): 229 (listed, photo); GHൺHൺඋං et al. (2015): 506 (record, distribution, prey); Bൺඅඅൺඅ & Yൺආൺൽൺ (2016): 186, 198, 200–201 (review of bionomics); Pඋඈඍංම (2016): 367 (listed); FൺඋඌHൻൺൿ Pඈඎඋ- Aൻൺൽ et al. (2017): 337 (record); Oඌඍඈඏൺඇ et al. (2017): 456 (distribution, habitat, prey); MඈඋKൾඅ et al. (2018): 229 (record); Mඈඎඅൾඍ et al. (2018): 136, 140 (listed, distribution, in key); Rඒൺඇ (2018): 26 (listed); GඳඇඍHൾඋ & GඳඇඍHൾඋ (2019): 231 (records); Gඈඎඅൺ et al. (2020): 12 (listed); HൺඌඌൺඇඓൺൽൾH Aඐൺඅ et al. (2020): 1671–1672, 1675 (photo, diagnosis).

Type material examined. Anthocoris dohrni : Hඈඅඈඍඒඉൾ: J, ‘Gibraltar’

[printed], ‘A. minki’ [handwritten],‘Type’ [printed circle with red border],

‘Champion \ Coll. B. M. \ 1927-409.’ [printed], ‘ Anthocoris \ dohrni Le

Q \ TYPE’ [handwritten], ‘ Anthocoris [handwritten] \ nemoralis [hand written] \ J. PERICART,det.1969 [printed + handwritten]’, ‘J’ [printed],

‘BMNH(E) \ 1254856’ [printed] ( BMNH).

Additional material examined. JAPAN: HඈඇඌHඎ: Osaka Pref.: 1 J

( Figs 7I–J ), Osaka-shi,Taishô-ku,Kobayashi-nishi, Rinkôryokuchi Park,

19.v.2020,A.Ichikawa; 1J 1♀ ( Fig. 15D ), same locality, 23.ix.2020,A.

Ichikawa; 1J ( Figs 12D , 13J–L ), Osaka-shi,Taishô-ku, Kobayashi-nishi,

15.vi.2020, on Lantana spp. , A. Ichikawa; Hyogo Pref.: 1 ♀, Kobe-shi,

Higashinada-ku, Kôyô-chô,Naka, 22.ix.2020,A.Ichikawa (all in TKPM).

Differential diagnosis. Recognized by the following combination of characters: head ( Figs 7I–J ) blackish brown to black, sometimes mostly reddish brown; antennal segments I, III, and IV blackish brown, segment II pale brown or yellowish brown and darkened at extreme base and apical half ( Fig. 7I ); labium ( Fig. 7J ) generally reddish brown to blackish brown; pronotum ( Fig. 7I ) blackish brown with light brown or reddish brown on posterior half; scutellum uniformly black, shiny; hemelytra ( Fig. 7I ) blackish brown, but brown or reddish brown on basal half; clavus and endocorium matted or dull, the remainder of corium shiny; embolium and endocorium somewhat semi-transparent mostly at the base; membrane ( Fig. 7I ) smoky black, with large whitish markings on basal portion and area behind apex of cuneus, and whitish area along veins; legs ( Figs 7I–J ) generally reddish brown to blackish brown; ostiolar peritreme straight, almost same width throughout, obtuse at apex; abdominal sternum II ( Fig. 12D ) with a pair of narrow triangle-shaped membranous areas along posterior margin. Most similar in general coloration to A. butleri Le Quesne, 1954 from Europe, but distinguished from it by the shorter antennae and the paramere being shorter and strongly bent at base (in A. butleri , much longer, moderately curved at base). It is also similar in appearance to A. confusus but distinguished from it by the light-brown or reddish-brown posterior half of pronotum, mostly reddish-brown to blackish-brown tibiae, embolium and endocorium being somewhat semi-transparent mostly at the base, and the greater contrast between shiny embolium and dull endocorium.

Redescription. Male genitalia ( Figs 13J–L ): Pygophore ( Fig. 13J ) turbinate, longer than wide, covered with 8–12 long, stout setae intermixed with short, suberect setae along outer margin and on posteroventral surface, of which the longest are approximately half the length of pygophore; mid-dorsal surface very hirsute with suberect setae; paramere ( Figs 13K–L ) slender, curved, gradually becoming acute at apex, sub-basally slightly constricted, with a few short, suberect setae on median portion, angulate at base in posterolateral view; longitudinal groove lacking.

Female genitalia ( Fig. 15D ): Copulatory tube fused on left side of intersegmental membrane between sterna VII and VIII, approximately 1.1 mm in length, thickest at base (cystiform) and gradually narrowing toward apex; trunk of conductive tissue invisible (or possibly dissolved).

Measurements [mm; JJ (n = 3) / ♀♀ (n = 2)]. Body length 3.85–4.25 / 4.00–4.35; head length (excl. neck) 0.46–0.53 / 0.54–0.55; head width across eyes 0.51–0.58 / 0.56–0.58; vertex width 0.29–0.33 / 0.33–0.34; length of antennal segments I – 0.13–0.16 / 0.19, II – 0.50–0.55 / 0.53–0.54, III – 0.29–0.33 / 0.34–0.35, and IV – 0.34–0.39 / 0.38–0.39; length of labial segments II – 0.10–0.14 / 0.13–0.15, III – 0.40–0.45 / 0.45–0.49, and IV – 0.28–0.30 / 0.28; anterior pronotal width 0.43–0.45 / 0.48–0.50; mesal pronotal length 0.56–0.63 / 0.65–0.69; basal pronotal width 1.20–1.36 / 1.45–1.50; length of embolial margin 1.25–1.41 / 1.39–1.44; length of cuneal margin 0.69–0.83 / 0.79–0.85; maximum width across hemelytra 1.29–1.44 / 1.46–1.55.

Bionomics. In Europe, A. nemoralis is common on many trees and shrubs, and is known to prey on psyllids, aphids, thrips, eggs and larvae of moths, and on some mites. This species has been studied extensively in Europe as a major predator of pear psyllids. In North America, this species was accidentally introduced from Europe to the eastern areas before 1958 and was possibly intentionally introduced to pear growing regions of western North America during the 1960s (Hඈඋඍඈඇ et al. 2004).

In Japan, this species was discovered in the harbor areas along Osaka Bay for the first time. Specimens were first collected from several sites in port areas of Osaka Prefecture from May to July 2020, where they were found on various broadleaf trees planted for landscaping (Akihiko Ichikawa, pers. comm.). In September 2020, in addition to the Osaka populations, a few specimens were collected from a port area (landfill) in Kobe, Hyogo Prefecture. It is assumed that this species was accidentally introduced into Japan very recently. This discovery is the first record not only from Japan but also from East Asia; however, the origin of the Japanese populations cannot be determined at present.

Distribution. Japan: Honshu*: Osaka, Hyogo. Anthocoris nemoralis is widespread in the Western Palaearctic (Pඣඋංർൺඋඍ 1996, AඎKൾආൺ et al. 2013a), and has also been introduced to North America (Hඈඋඍඈඇ et al. 2004). Very recently, this species has been found in Japan. This discovery represents the first East Asian record of this species.

Summary of known records: ASIA: Azerbaijan (Pඣඋං- ർൺඋඍ 1996). Armenia (Pඣඋංർൺඋඍ 1996). Turkey: Asian part (HඈඋඏගඍH 1883, Öඇൽൾඋ et al. 2006). Georgia (Pඣඋංർൺඋඍ 1996). Iran (Lංඇඇൺඏඎඈඋං & Hඈඌඌൾංඇං 2000, Oඌඍඈඏൺඇ et al. 2017). Israel (BඈൽൾඇHൾංආൾඋ 1937, Pඣඋංർൺඋඍ & Hൺඅඉൾඋංඇ 1989). Jordan (Pඣඋංർൺඋඍ 1996). Kazakhstan (EඌൾඇൻൾKඈඏൺ 2013). Syria (Rൾඎඍൾඋ 1884, SඍංർHൾඅ 1958). EUROPE: Albania (SඍංർHൾඅ 1958, Mංඌඃൺ 1973). Andorra (Pඣඋංർൺඋඍ 1996). Austria (SඍංർHൾඅ 1958, RൺൻංඍඌർH 2005). Belgium (SඍංർHൾඅ 1958, Bඈඌආൺඇඌ & Pඣඋංർൺඋඍ 1989). Bosnia and Herzegovina (Pඣඋංർൺඋඍ 1996). Bulgaria (SඍංർHൾඅ 1958, Jඈ- ඌංൿඈඏ 1964). Belarus (LඎKൺඌHඎK 1997). Croatia (Pඣඋංർൺඋඍ 1996). Cyprus (GൾඈඋGHංඈඎ 1977). Czech Republic (Hඈൻൾඋ- අൺඇൽඍ 1977, Kආൾඇඍ & BൺŃൺෞ 2012). Denmark (Fൺൻඋංർංඎඌ 1794, SඍංർHൾඅ 1958). Estonia (Cඈඎඅංൺඇඈඌ 2005). Finland (Rൾඎඍൾඋ 1884, AඅൻඋൾർHඍ et al. 2015). France (Rൾඎඍൾඋ 1884, SඍංർHൾඅ 1958). Germany (SඍංർHൾඅ 1958, Hඈൿൿආൺඇඇ & Mൾඅൻൾඋ 2003). Greece (Dඋඈඌඈඉඈඎඅඈඌ 1980, Pඣඋංർൺඋඍ 1996). Hungary (SඍංർHൾඅ 1958, Kඈඇൽඈඋඈඌඒ 1999). Ireland (Hൺඅൻൾඋඍ 1935). Italy (SඍංർHൾඅ 1958, Dංඈඅං 1983). Latvia (SඍංർHൾඅ 1958). Liechtenstein (BൾඋඇHൺඋൽඍ 1992). Luxembourg (Pඣඋංർൺඋඍ 1996). Malta (Pඣඋංർൺඋඍ 1996, Cൺඋൺඉൾඓඓൺ & Mංൿඌඎൽ 2015). Moldavia (Pඣඋංർൺඋඍ 1972, DൾඋඓHൺඇඌKඒ 1997). Montenegro (Pඋඈඍංම 1998, 2016). The Netherlands (SඍංർHൾඅ 1958). North Macedonia (Pඣඋංർൺඋඍ 1996). Norway (SඍංർHൾඅ 1958, Cඈඎඅංൺඇඈඌ 1998). Poland (SඍංർHൾඅ 1958). Portugal (Sൾൺൻඋൺ 1941). Romania (SඍංർHൾඅ 1958, Rඈ෡ർൺ & Pඈඉඈඏ 1982). Russia: Central and South European Territories (SඍංർHൾඅ 1958). Serbia (Pඋඈඍංම 1998). Slovakia (Hඈൻൾඋඅൺඇൽඍ 1977, Pඣඋංർൺඋඍ 1996). Slovenia (GඈGൺඅൺ 2004). Spain (Lൾ Qඎൾඌඇൾ 1958, Gඈඎඅൺ et al. 2020). Sweden (Rൾඎඍൾඋ 1884, SඍංർHൾඅ 1958). Switzerland (SඍංർHൾඅ 1958, HൾർKආൺඇඇ & BඅදർHඅංඇGൾඋ 2011). Ukraine (Pඣඋංർൺඋඍ 1996). United Kingdom (Eൽඐൺඋൽඌ 1890, SඍංർHൾඅ 1958). Turkey: European part (Pඣඋංർൺඋඍ 1996, Öඇൽൾඋ et al. 2006). NORTH AFRICA: Algeria (SඍංർHൾඅ 1958, EർKൾඋඅൾංඇ & WൺGඇൾඋ 1965). Azores (Rංൻൾඌ & BඈඋGൾඌ 2005). Canary Islands (SඍංർHൾඅ 1958, Pඣඋංർൺඋඍ 1972). Egypt (SඍංർHൾඅ 1958, WൺGඇൾඋ 1960). Libya (SඍංർHൾඅ 1958, Eඅ- MൾGHඋൺൻං 2009). Morocco (SඍංർHൾඅ 1958). Tunisia (Rൾඎඍൾඋ 1884, SඍංർHൾඅ 1958). NORTH AMERICA: Canada: Ontario, British Columbia (Aඇൽൾඋඌඈඇ & Kൾඅඍඈඇ 1963, Hඈඋඍඈඇ et al. 2004). USA: Washington, Oregon, California (Hඈඋඍඈඇ et al. 2004).

Figures

Fig. 7. Habitus of Anthocoris spp., dorsal (A, C, E, G, I, K) and lateral (B, D, F, H, J, L) views. A–B – A. chibi Hiura, 1959, male; C–D – A. confusus Reuter, 1884, male; E–F – A. japonicus Poppius, 1909, male; G–H – A. kalopanacis Kerzhner, 1977, female; I–J – A. nemoralis (Fabricius, 1794), male; K–L – A. takahashii Hiura, 1959, male. Scale bars: 1.0 mm.

Fig. 12. Abdominal sterna II–III of Anthocoris spp., male, ventral view (setae omitted). A – A. chibi Hiura, 1959; B – A. confusus Reuter, 1884; C – A. japonicus Poppius, 1909; D – A. nemoralis (Fabricius, 1794); E – A. takahashii Hiura, 1959; F – A. miyamotoi Hiura, 1959; G – A. venustus sp. nov., paratype. Abbreviations: ma ‒ membranous area; st2–3 ‒ abdominal sternum II to III. Scale bars: 0.2 mm.

Fig. 13. Male genitalia of Anthocoris spp. A–C – A. chibi Hiura, 1959; D–F – A. confusus Reuter, 1884; G–I – A. japonicus Poppius, 1909; J–L – A. nemoralis (Fabricius, 1794); M–O – A. takahashii Hiura, 1959. A, D, G, J, M – pygophore with paramere (ejaculatory bulb omitted), dorsal view; B–C, E–F, H–I, K–L, N–O – paramere, two different views. Abbreviations: prm ‒ paramere; pyg ‒ pygophore. Scale bars: 0.1 mm.

Fig. 15. Female genitalia of Anthocoris spp., dorsal view.A – A. chibi Hiura, 1959; B – A. confusus Reuter, 1884; C – A. japonicus Poppius, 1909; D – A. nemoralis (Fabricius,1794); E – A.takahashii Hiura, 1959; F – A. miyamotoi Hiura, 1959; G – A. venustus sp. nov., paratype.Abbreviations: ct ‒ copulatory tube; ism ‒ intersegmental membrane; sp ‒ sperm pouch; t ‒ trunk of conductive tissue (C–D, trunk of conductive tissue dissolved). Scale bars: 0.1 mm.