F

PROC. ENTOMOL. SOC. WASH. 111(3). 2009. pp. 609--616

ANTHOCORIS CONFUSUS COLLECTED FROM WESTERN WASHINGTON STATE, WITH A SUMMARY OF NORTH AMERICAN RECORDS (: 1-IETEROPTERA: )

DAVID R. HORTON AND TAMERA M. LEWIS

USDA-ARS, 5230 Konnowac Pass Rd., Wapato, WA 98951, U.S.A. (e-mail: [email protected])

Abstract.—The predatory true bug confusus Reuter is native to Europe and Asia. Scattered records for this species in North America date from 1929. In 2007-2008, we collected adults and nymphs of A. con/ilsus from deciduous trees in western Washington State. This is the second North American record for A. conjitsus from west of the Rocky Mountains, and is the first record from the western United States. Specimens were collected from European (Fagus sy/va/ica; Fagaceae) and linden (Ti/ia sp.; Tiliaceae). The linden trees were heavily infested with the Euca/lipterus ti/iae. The presence of adult and immature bugs, and the occurrence of the species at the collecting site in consecutive years, suggests that A. conjusus is established at this location. We summarize North American records for A. con/itsus, briefly discuss host plant records, and list traits used to separate A. conjusus from other Ant/,ocoris spp. Additional predatory Heteroptera collected from linden and European beech included three other Old World species. Anthocoris neinoralis (Anthocoridae), Cainpyloneura virgu/a (Miridae), and Orthot v/us nassatus (Miridae), as well as one native species, Deraeocoris flisciolus (Miridae); the record for 0. nassatus is the first for this species from western North America. Key Words: introduced species, true bugs, Fagus, Ti/ia, Ant/zocoris nemoralis, Cainpyloneura virgula, Orthot v/us nassatus, Deracocoris Jzsciolus

Species of Anthocoridae (Hemiptera: Anthocoris in certain habitats of western Heteroptcra) are important natural ene- Europe (Southwood and Leston 1959; mies in agricultural and natural habitats Anderson 1962; Hill 1965, 1978). This throughout the world (Lattin 1999). predator occurs often on deciduous trees, Anthocoris con,fusus Reuter (Reuter but can be found also on herbaceous 1884) is a widespread species of the plants (Hill 1965). Palearctic Region found throughout There are scattered records for A. western Europe, east into Siberia and conjusus in North America dating back Asia (including China, Mongolia, and to 1929. It is unclear how or when the Japan), and south into Tunisia, Iran, and species was first introduced into North Israel (Hiura 1959; Péricart 1972, 1996; America. The only published record for Elov 1976; Péricart and Halperin 1989). A. conjiisu.v in western North America is It is one of the more common species of for a specimen collected more than 30 years ago in British Columbia (Scudder Accepted by Michael W. Gates 1986). We collected adults and nymphs ha F,

610 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON

Table I. Location of collection, month and year of record, number of specimens, and literature citation for Ani/,oeorjs cantusus collected in North America.

Location Month and Year of Record Number of Specimens Relèrence Ontario, Canada 1929, 1930, 1939, 1943, 1950, multiple Anderson and Kelton 1955, 1958, 1961, 1962 (1963), Kelton (1978) Tannersville, Greene September 1932 1 Scudder and Foottit Co., New York (2006) Bar Harbor, Hancock May 1938 1 Procter (1946) Co., Maine October 1938 multiple Kelton (1978) Isabella County, September 1955 3 Y, 5 Lewis et al. (2005) Michigan Roan Mountain, August 1957 (not stated) Anderson and Kelton Carter Co., (1963), Kelton (1978) Tennessee Grandfather October 1957 1 Is N.C.S.U. museum Mountain, Avery Co., North Carolina Joanna Bald, Graham September 1959 1 N C.S.U. museum Co., North Carolina Mars Hill, Madison July 1995 2 Y, i S N.C.S.U. museum Co., North Carolina Kentville, Nova July 1966 apparently multiple Kelton (1978), Barnes Scotia, Canada et al. (2000) Prince Edward before 1978 (not stated) Kelton (1978) Island, Canada Vancouver, British May 1977 1 y Scudder (1986) Columbia, Canada St. John's, August 2006 19 ?, 12 S Wheeler et al. (2008) Newfoundland, Canada Seattle, King Co., August 2007 1 this study Washington September 2007 (University of 6 Y, 25 July 2008 Washington 9 ?, 3 &18 nymphs campus) August 2008 5 S, 1 nymph

of A. confusus from western Washington Anthocoris confusus Reuter, 1884 State in 2007-2008. Herein, we summa- The first North American record for rize both the historical and new records this Palearctic species is by Anderson for A. confusus in North America. and Kelton (1963) for specimens collect- Characters that can be used to separate ed in the 1920s-1940s from the Great A. confusus from other North American Lakes Region of Ontario, Canada (Ta- species of Anthocoris are discussed. We ble 1). Additional specimens were col- briefly summarize plant records for A. lected by L.A. Kelton from that same confusus in both the Old and New area in the 1950s and 1960s. The earliest World. Finally, we list other species of records for the United States are from predatory Heteroptera that we found in 1932 for a single specimen collected in association with A. con/usus at the eastern New York, followed by speci- collecting site. The samples included mens collected in 1938 at Bar Harbor, three additional Old World species. Maine (Table 1). Other U.S. records p

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include eight specimens collected in 1955 from Isabella County, Michigan (Lewis et al. 2005). Five specimens from western North Carolina are deposited in the museum at North Carolina State Uni- versity. Included are two specimens collected in the late 1950's, and an additional three collected in 1995. The only published record for western North America is for a single specimen collected in 1977 at Vancouver, British Columbia, Canada (Scudder 1986). Henry (1988; with updates in Henry and Froeschner (1992)) listed A. confusus from British Columbia, Nova Fig. I. Clasper of male Ant/weoris conjusus collected from F. s'Ivatica on campus of University Scotia, Ontario, Prince Edward Island, of Washington, Seattle, Washington (September Maine, and Tennessee; the catalog of 2007). Maw et al. (2000) listed the Canadian provinces from which A. conjusus has been collected; Wheeler et al. (2008) partially pruinose, separating this species added Newfoundland to the Canadian from North American species whose records. hemelytra are entirely shiny. The dull New records.—In 2007 and 2008, we or pruinose area of the hemelytra in A. collected adults and nymphs of A. con,fusus encompasses the entire clavus conJiisus from European beech (Fagus and endocorium (except for a narrow sylvatica L.; Fagaceae) and linden (Ti/ia strip adjacent to the membrane), a strip L.; Tiliaceae) on the campus of the along the inner embolium, and the inner University of Washington, Seattle, King angle of the cuneus. The remainder of County, Washington: 26 August 2007 (F. the cuneus and the outer portion of the sy/vatica: 1 ); 13 September 2007 (F. embolium are shiny. Anthocoris nerno- sy/vatica: 6 , 25 ); 2 July 2008 (F. ralis (Fabricius), which may often occu- sy/vatica: 1 S, 18 nymphs; Ti/ia sp.: 8 Y, py the same habitats as A. conjitsus, has a 2 ); 22 July 2008 (F sylvatica: 1 ?); 15 similar appearance. Anthocoris confusus August 2008 (F. sylvatica: 2 ; Ti/ia sp.: can be separated from A. neinora/is by 3 S, 1 nymph). The linden trees were the appearance of the embolium, which heavily infested with the aphid Euca/lip- in A. nemoralis is entirely shiny. The terus ti/iae (L.) (Hemiptera: Homoptera: clasper in the male of A. confusus is Drepanosiphidae); it is unclear what prey distinct in having a sharply defined pre- were available to A. confusus on the apical tooth (Fig. 1). Kelton (1978) beech trees, although a number of cast provided a key to the North American skins from were noted. We species of Anthocoris, which includes A. confirmed identifications of nymphal A. confu.su.c and A. neniora/is. Illustrations conJiisus by rearing them to the adult of claspers are provided by Kelton (1978) stage on a diet of E. ti/iae. and Péricart (1972). Identification.—Characteristics of the Other predatory Heteroptera collect- hemelytra are of particular value in ed.—Predatory Heteroptera found in separating North American species of association with A. confusus on linden Anthocoris (Hill 1957, Kelton 1978). The and European beech at the University of hemelytra of Anthocoris confusus are Washington site included three other 612 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON

non-indigneous species. Adults of A. and Leston 1959, Kelton 1982a). Species nemoralis were collected from both plani in this genus appear to be partially species: F. syliwtica, 13 September 200' predaceous on aphids, mites, or other (2 , 1 ); Ti/ia sp., 2 July 2008 (2 , I soft-bodied (Southwood and (). This species is native to Europe but Leston 1959, Kelton 1982a). Orthoty/us is now well-established in western North nassatus has been found in pear orchards America from British Columbia south infested with pear psylla, Cacopsy/ic, into southern California. Horton et al. pvrico/a (Förster) (Henry 1977, Kelton (2004) provided a chronological summa- 1982a). We obtained feeding by nymphs ry of North American records for this of 0. nassatus on immature pear psylla in species. Both Fagus and Ti/ia are known laboratory assays. Both nymphs and plant sources of A. nemoralis in Europe adults also fed on pear foliage in our (Horton et al. 2004). Anthocorjs nemo- assays. The first North American records rails is an important predator of pear for this Old World species are for three psyllids, C'acopsy//a spp. (Hemiptera: specimens collected in 1973 and 1977 Psyllidae), in pear orchards of both the from three counties in Pennsylvania Old and New World (reviewed in Horton (Henry 1977, Henry and Wheeler 1979). et al. 2004). Henry (1977) also provided a description The second Old World species, cam- of the adult male, drawings of the male pyloneura virgula (Herrich-Schaeffer) genitalia, and a key to Ort/wty/us and (Miridae), was collected from Ti/ia sp.: related genera in eastern North America. 2 July and 22 July 2008 (7 ). This Additional North American records was first recorded in North America were listed in Kelton (1982a), Wheeler from British Columbia, Canada, in 1949 and Henry (1992), and Barnes et al. (Downes 1957), and is now known to (2000): Ontario (1963), Nova Scotia occur in Washington, Oregon, and (1966 and 1976), and Prince Edward northern California (Lattin and Stone- Island (1976), Canada; and Washington, dahl 1984). Both Fagus and Ti/ia are D.C. (1986). Our records are the first for known sources of C. virgiila in the Old this species in western North America. World (Strawiñskj 1964, Lattin and Finall y, a native mind, Deraeocorj.v Stonedahl 1984). The predator feeds on Jiscio1us Knight, was collected from both aphids, psyllids, and other soft-bodied F. s ylvarica and Ti/ia sp. at the Univer- arthropods (Lattin and Stonedahl 1984). sity of Washington site. This predatory The absence of male C virgula in species is widespread throughout Canada samples is typical (Lattin and Stonedahi and the northern United States, and may 1984), as this species is parthenogenic in be collected from a variety of deciduous North America. tree species (Kelton 1982b, Razafimaha The third European species, Orthoty- tratra 1981). his nassatus (Fabricius) (Miridae), was Voucher specimens.—Voucher speci- collected from Ti/ia sp. on 22 July 2008 mens of the two species of Ant/jocorir (1 Y, 2 c, 3 nymphs) and 15 August and the three species of Miridae are 2008 (2 ). Identification was made deposited with the National Museum of using the key in Southwood and Leston Natural History, Smithsonian Institu- (1959) and by examination of claspers tion, Washington, D.C. (Southwood and Leston 1959, Henry 1977, Kelton 1982b). This bug is widely DISCUSSION distributed in Europe on deciduous trees, Faunal lists have shown that the including Ti/ia, Quercus (Fagaceae), Fa- gus, and Anthocoridae in any particular geo- A/ntis (Betulaceae) (Southwood graphic region may include a mix of 613 VOLUME Ill. NUMBER 3 native and introduced species (e.g., Anihocoris conflisus is generally found Scudder and Foottit 2006; Lattin 2007a, on deciduous trees, and in its native b, c). In some regions, the numbers of range appears to have preferences for non-native species of Anthocoridae may beech (Anderson 1962; Hill 1965, 1978; approach or exceed the numbers of native Taksdal 1965; Péricart 1972; Stepanovi- anthocorids, as shown in recent faunal ëová and Lapková 1988; Floren and (Quer- lists for Hawaii and the Galapagos Gogala 2002; GoBner 2006), Islands (Lattin 2007a, Lattin 2007b). ciis) (Southwood and Leston 1959; An- Some introduced species were found to derson 1962; Hill 1965, 1978; Taksdal be quite widespread geographically in the 1965; Péricart 1972; Gof3ner 2006), and region of introduction at the time of linden (Anderson 1962, Taksdal 1965, discovery (e.g., Henry et al. 2008), which Péricart 1972). Other plant records for A. may be evidence of a relatively long confisus in the Palearctic Region include: presence in the new region. Introductions Ulmus (Ulmaceae) (Urban 2003). Plata- of some Anthocoridae are known to have ntis (Platanaceae) and Salix (Salicaceae) been intentional as part of classical (Anderson 1962), Benda (Betulaceae), biological control efforts (Davis and Sorbus (Rosaceae), and (Ro- Krauss 1963, Horton et al. 2004, Lattin saceae) (Hill 1965, 1978), Laurus (Lau- 2007b), although it is not always clear raceae) and (Salicaceae) (Péricart whether establishment of the introduced and Halperin 1989), and Acer (Acera- species in a new geographic region was ceae) (Péricart 1972). Records for A. indeed due to the release or was instead con,fiisus in Canada include most com- the consequence of an accidental intro- monly Fagus (Anderson and Kelton duction either before or after the inten- 1963, Kelton 1978, Wheeler et al. 2008), tional release (Brenner and Lattin 2001, with additional specimens having been (Rosaceae), Horton et al. 2004). collected from Acer, Rosa (Kelton 1978, Wheeler Records for A. confusus in North Ti/ia, and Quercus America are widely distributed, both et al. 2008). Thus, the North American temporally and geographically (Table 1). records include to a large extent plant and This pattern suggests that there have genera (i.e., Fagus, Ti/ia, Acer, been multiple introductions of this spe- Quercus) known to be of importance to cies into North America, although it is A. confusus in Europe. conceivable that the widely dispersed In summary, samples of 1-leteroptera records for this species are in part due collected from European beech and to range expansion associated with hu- linden on the campus of the University man transport (Scudder and Foottit of Washington included the Old World 2006). The sources of the A. conflisus true bug A. confilsus, a species collected introductions are not known, although only very irregularly in North America Kelton (1978) suggested that the species beginning in the late 1920's. Our collec- may have entered the Great Lakes tions from the University of Washington Region of Canada in association with campus in 2007-2008 included both imported nursery stock. Records for A. adults and nymphs, and are the first records for this species in the western conflisus in western North America are limited to the coastal areas (Table 1). United States. The occurrence of nymphs This apparently localized distribution in our samples, combined with the fact suggests that the insect may have entered that the species was present in the same western North America on imported stand of trees in two consecutive years, goods brought in through northwestern suggests that A. conjusus is established at ports. the collecting site on the campus 614 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON

grounds. Wheeler (2008) observed that LITERATURE CITED university campuses in otherwise urban centers may provide islands of habitat Anderson, N. H. 1962. Bionomics of six species of An//zocoris (Heteroptera: Anthocoridae) in for insects and other fauna not found in England. Transactions of the Royal Entomo- the surrounding urban areas, providing logical Society of London 114: 67-95. opportunities for studies of biodiversity Anderson N. H. and L. A. Kelton. 1963. A new not otherwise available in that location. species of Ant/jocoris from Canada, with These studies have often resulted in the distribution records for three other species (Heteroptera: Anthocoridae). Canadian Ento- discovery of immigrant species not pre- mologist 95: 439-442. viously known to be present in the region Barnes, D. I., H. E. L. Maw, and G. G. E. Scudder. (Wheeler 2008), and the occurrence of A. 2000. Early records of alien species of Heter- conflisus and 0. nussc,tus in our samples optera (l-Iemiptera: Prosorrhyncha) in Canada. appear to be additional examples of this Journal of the Entomological Society of British phenomenon. We suggest, however, that Columbia 97: 95 102. Brenner, G. J. and J. D. Lattin. 2001. Notes on these non-native species probably are three species of Anthocoridae (I-Iemiptera: more widespread in the Seattle area than Hetcroptera) from Hawaii, including the first is indicated by our limited sampling record of Buehanunje/fa eon! moo (White). efforts made on the University of Wash- Proceedings of the Entomological Society of ington campus. Both linden and beech Washington 103: 386- 388. have been planted extensively along the Clark, J. and A. L. Jacobson, 2001. Pioneering Seattle's historical trees. h ttp://www.arthurleej . streets of Seattle (Clark and Jacobson (accessed 13 August 2001), and it seems likely that sampling 2008). of these tree-lined areas would lead to Davis. C. J. and N. L. H. Krauss. 1963. Recent additional records for both A. con/usus introductions for biological control in Hawaii and 0. nassatus - VIII. Proceedings of the Hawaiian Entomo- in the Seattle region. logical Society 18: 245-249. ACKNOWLEDGMENTS Downes, W. 1957. Notes on some Hemiptera which have been introduced into British We thank Deb Broers, Merilee Bayer, Columbia. Proceedings of the Entomological Bob Brown, and Keith Kubishta Society of British Columbia 54: 11 13. (USDA-ARS, Wapato) for assistance in Elov, E. S. 1976. Bugs of the Family Anthocoridae collecting and rearing. Frederick Stehr (Heteroptera) in Soviet Central Asia and Kazakhstan. Entomological Review 55: 74-81. and Gary Parsons (Michigan State Uni- Floren, A. and A. Gogala. 2002. Heteroptera from versity) kindly loaned its the eight beech (Fagus sylvatica) and silver fir (A/sies specimens of A. conjitsus found in the a//ia) trees of the primary forest reserve MSU collection. We thank Robert Blinn Rajhenavski Rog, Slovenia. Acta Entomolo- (North Carolina State University) for gica Slovenica 10: 25 -33. GoOner, M. 2006. Phenological activity patterns of examining specimens of A. con/i!sus in the NCSU museum, and providing us imaginal Heteroptera in the canopy of differ- ent tree species in Bavaria, Germany. In with label information. Finally, we are Rabitsch. W., ed. Hug-the-Hug - For the Love grateful to John Lattin (Oregon State of True Bugs. Fetschrift zum 70. Geburtstag University) for confirming our identifi- von Ernst Heiss. Denisia 19: 1055 1094 cations of C virgtila and Henry. T. J. 1977. Orthot v/u.s nassafus, a European D. jàsciolus. plant bug new to North America (Heteroptera: Earlier drafts of the manuscript were Miridae). USDA Cooperative Plant Pest Re- reviewed by Harry Brailovsky (Universi- port, and Plant Health Inspection dad Nacional Autónoma de Mexico), Service 2(31): 605-608. Tom Henry (USDA-ARS, National Mu- 1988. Family Anthocoridae Fieber, 1837. seum of Natural History), John Lattin, The minute pirate bugs, pp. 12-28. In Henry, and Richard Zack (Washington State T. J. and R. C. Froeschner, eds. Catalog of the University). Heteroptera, or True Bugs, of Canada and the Continental United States. E.J. Brill, Leiden. 615 VOLUME Ill. NUMBER 3

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