PROC. ENTOMOL. SOC. WASH. 109(2), 2007, pp. 366-376 THE NON-INDIGENOUS LYCTOCORIDAE AND ANTHOCORIDAE (HEMIPTERA: HETEROPTERA: CIMICOIDEA) OF AMERICA NORTH OF MEXICO John D. Lattin Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR 97331-2902, U.S.A. — Abstract. Eighty-four species of Lasiochilidae, Lyctocoridae and Anthocoridae (Cimicoidea) are known to occur in America north of Mexico. Twenty-six of these are believed to have been introduced (31%). Each non-indigenous species is reviewed and appropriate literature cited. While some species were introduced for possible biological control, others have been introduced accidentally. Key Words: Lasiochilidae, Lyctocoridae, Anthocoridae, Cimicoidea, Canada and United States species, distribution, and biology Insects and other organisms have been lished "Harmful Non-Indigenous Species introduced throughout the world, acci- in the United States" in 1993. This was dentally or deliberately. The late Charles a comprehensive treatment of a variety S. Elton published his pioneer book of introductions and their consequences. "The Ecology of Invasions by Animals The use of the term non-indigenous and Plants" in 1958. Among the insect species follows that publication. Some examples he cited are the winter moth in other books published over the past few northeastern North America, elm bark years on introductions and their con- beetle, Japanese beetle, European gyp—sy sequences include Simberloff et al. moth, sawflies, and even a true bug (1997), Devine (1998), Cox (1999), Stephcmitis rhododendri, in this case in- Mooney and Hobbs (2000), Ruiz and troduced from North America into Carlton (2003), Coombs et al. (2004), Europe, as was the Colorado potato Cox (2004) and Mooney et al. (2005). beetle. Other insects have been intro- The impact of exotic species on our duced into Canada and the United States environments has been enormous. Some more recently, including the Asian gypsy of these species have been with us for moth, cereal leaf beetle, blue alfalfa many years at considerable cost. aphid, Russian wheat aphid, and the Eighty-four species of Lasiochilidae, pine shoot beetle. Lyctocoridae and Anthocoridae (Cimi- Parsons (1983) dealt with the evolu- coidea) are known to occur in America tion of colonizing species. Mooney and north ofMexico. Twenty-six ofthese are Drake (1984) edited a comprehensive considered to be non-indigenous (31%). review of some biological invasions, Some were introduced deliberately and treating the details of invasion and their others accidentally, usually involving the consequences. The Office of Technology activities of human beings. Earlier, Lat- Assessment of the U.S. Congress pub- tin (1993) reported 90 species from VOLUME NUMBER 109, 2 367 America north of Mexico, of which account of L. campestris in the western 12.2% were considered to have been Palearctic, Henry (1988) summarized its introduced, whereas Canada reported occurrence in Canada and the continen- 42 species of which 10 (23.8%) were tal United States, and Lattin (2000) considered introduced. Lattin (1999b, reviewed L. campestris and its economic 2000) provided overviews of the Antho- importance. This species has been in- coridae (sensu lato). This publication troduced into many parts of the world follows the treatment of families and where it has often been associated with tribes of the Lasiochilidae, Lyctocoridae domestic animals, stored-grain, and oth- and Anthocoridae by Schuh and Stys er products. Nesidiocheilus hawaiiensis (1991) and Schuh and Slater (1995). Kirkaldy, 1902 is considered a synonym Scudder and Foottit (2006) included the of L. campestris (Lattin 2006a). Anthocoridae in their extensive review of the introduced true bugs in Canada. Anthocoridae Appropriate references to each species Anthocorini treated here include the date, site of original description, geographic and bi- Acompocoris pygmaeus (Fallen 1807) was described from Europe. Sands ological references. Every species that has been reported as a deliberate in- (1957) illustrated the egg and nymph troduction for biological control pur- and Pericart (1972) published on it in the poses has been cited, including those that western Palearctic. Kelton (1977) first have not become established. It is the rneoprotrhteodf MAe.xipcyogmfareoumsNferwomBrAumnesrwiiccak purpose here to record all such species as a data base of past introductions. Stan- and Nova Scotia and later added On- saewaaycaertgoal.c(o2n0t0a1i)neerxsaimninAeudst3r,al0i0a1.eTmhpetyy t1a9r7i8o).anHdenPrriynce(1E98d8w)aradndIslManadw(Keetltaoln. recovered over 7,400 living and dead (2000) cited these provinces. Scudder and i2n3secstpsecfirmoemns11o7f4 Acnotnhtoaicnoerrisd,aei,ncl1u7dinogf NFoeowttiBtr(u2n0s0w6i)ckr,epNorotvead tShciostisap,eciOenstafrrioom, which were still alive. These sea cargo and Prince Edward Island. The species is containers now being used world wide associated with conifers. have opened yet another pathway of Anthocoris confusus Renter, 1884 was introduction. described from Europe. Procter (1946) first reported this species from North Lyctocoridae America based on specimens from Lyctocoris campestris (Fabricius 1794) Maine. Sands (1957) illustrated the egg was described from Europe and first and nymph and Anderson (1962a) de- reported from America north of Mexico scribed the bionomics of the species in by Dallas (1852) as Xylocorisamericanus. England. Anderson and Kelton (1963) Sands (1957) illustrated the egg and added Ontario and Tennessee. Pericart nymph, and Anderson (1962b) Hsted it (1972) published on the species in the from the Pacific Northwest. Kelton western Palearctic. Kelton (1978) re- (1967) recorded it from Alabama, British ported the species from Maine, Nova Columbia, Colorado, Florida, Georgia, Scotia, Ontario, Prince Edward Island, Idaho, Illinois, Kansas, Manitoba, and Tennessee. Scudder (1986) added Maryland, New York, North Carolina, British Columbia and Henry (1988) Ontario, Oregon, Pennsylvania, Quebec, summarized the above cited localities. South Carolina, Texas, Utah, Wisconsin Barnes et al. (2000) cited Nova Scotia and Mexico. Pericart (1972) pubHshed an and Maw et al. (2000) listed British 368 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON Columbia, Nova Scotia, Ontario. Lattin to Canada from Switzerland and re- (2000) discussed the economic aspects of leased but the species failed to become this species in detail and Scudder and established (L. Humble, Canada, per- Foottit (2006) reported this species from sonal communication). Pericart (1972) British Columbia, Nova Scotia, Ontario, published on this species under the name and Prince Edward Island. Anthocoris sibiricus Renter (1875). Later, Anthocoris ueinoralis (Fabricius 1794) he recognized that two species were was described from Denmark. Sands involved - A. pilosus in the western and (1957) illustrated the egg and nymph A. sibiricus in the eastern Palearctic and Anderson (1962a) published on this (Pericart 1996). species in England. Anderson and Kel- MacrotracheUa nigronitens (Stal 1860) ton (1963) first reported it from North was described from Brazil (Rio Janeiro). America from Ontario. McMullen and It was reported from Panama by Cham- Jong (1967) recorded it from British pion (1900). Davis and Krauss (1966) Columbia and McMullen (1971) re- introduced it into the Hawaiian Islands ported the release of 163 specimens from (as MacrotracheUa thripiformis) as a pos- Switzerland in 1963 into British Colum- sible biological control agent but it failed bia. Pericart (1972) provided a review of to become established (Lattin 2007). A. nenioralis in Europe. Brunner and Lewis et al. (2005) reported finding Burts (1975) raised A. nemoralis in the specimens at Riverside, California on laboratory in Washington. The initial FicLis galls. This was the first record of individuals for this rearing came from M. nigronitens from America north of British Columbia. Henry (1988) reported Mexico. A. nemoralis from British Columbia and Temnostethiis graciUs Horvath, 1907 Ontario. Hagen and Driestadt (1990) was described from Germany and Peri- and Driestadt and Hagen (1994) cited cart (1972) published on it in the western its occurrence in California. Lattin Palearctic. Kelton (1977) first reported it (2000) reviewed the activities of the from North America, based on speci- species and Horton et al. (2004) pub- mens collected in Nova Scotia. No lished a detailed discussion of A. nemor- additional localities have been recorded alis as a biological control agent, partic- (Kelton 1978; Henry 1988; Maw et al. ularly as a predator of the pear psylla. 2000; Scudder and Foottit 2006). Scudder and Foottit (2006) reported this Tetraphleps abdidghani Ghauri, 1964, species from British Columbia and On- was described from Pakistan. It was tario. introduced into America north of Mex- Anthocoris nemorum (Linnaeus 1761) ico as a possible biological control agent was described from Europe. Hill (1957) against the balsam woolly aphid {Adelges studied its biology in Scotland, Sands piceae (Ratz)). Mitchell and Wright (1957) illustrated the egg and nymph, (1967) reported it as Tetraphleps sp. and Anderson (1962a) reported on this and stated that it had been released in species in England. Pericart (1972) pro- Oregon and Washington. Clark et al. vided an account in the western Palearc- (1971) reported that 4622 individuals tic. Two specimens from Switzerland were released in Nova Scotia and New were introduced into British Columbia Brunswick and 1226 in British Columbia in 1963 (McMullen 1971), but it did not from 1962-1965. They indicated that become established. 1436 individuals were released from Anthocorispilosiis (Jakovlev 1877) was cages in New Brunswick from 1962- described from Europe. McMullen 1965. Clausen (1978) cited its introduc- (1971) reported ten specimens brought tion into the Pacific Northwest from VOLUME NUMBER 109, 2 369 Pakistan and India. L.M. Humble, of Buchananiella continua (White 1880) Canada (personal communication 2 was described from the island of Madei- March 1990) stated that no estabhsh- ra. It was first reported from California ment occurred and R.E. Mitchell, retired under the name Cardiastethus cavicoUis from the U.S. Forest Service, indicated Blatchley, 1934, and later synonymized per personal communication on 22 June by Lattin et al. (2001) with Buchananiella 2001 that none of the introductions into continua. Pericart (1972) reviewed this United States were successful. Maw et al. species in the western Palearctic. Brenner (2000) stated that this species was in- and Lattin (2001) reported it for the first troduced into Canada but failed to time from the Hawaiian Islands. Kirby become established. (1999) reported B. continua from Great Tetraphleps raoi Ghauri, 1964, was Britain for the first time and Verdcourt described from Assam. Mitchell and (2005) stated that specimens were found Wright (1967) reported that it had been in sacks ofcompost in the same country. introduced into Oregon and Washing- Whitehead (2005a, b) subsequently re- ton. Clark et al. (1971) cited the open ported the—further spread of this species release of 118 specimens into Nova in Britain invasions still occur! Scotia and 2,457 specimens were released Cardiastethus lurideUus Fieber (1860) from cage and laboratory studies in New was described from Pennsylvania. No Brunswick in 1963 and 1965. Maw et al. further localities were listed until Lattin (2000) stated that the species did not (1999a) reported it from Michigan where become established. it was collected from clusters ofdead oak leaves from fallen trees. Lattin and DUFOURIELLINl LaBonte (2002) documented its recovery from baited traps at a site handling raw Amphiareus constrictus (Stal 1860) was wood at The Dalles, Oregon in 2000. The described from Brazil (Rio Janeiro). same species was recovered at Portland, Blatchley (1926) first recorded the spe- Oregon, from a similar trap in 2004. cies from America north of Mexico Cardiastethus hirideUus is considered —to based on specimens from Dunedin, be a non-indigenous species in Oregon Florida. Henry (1988) reported it from well removed from its natural range. It is Florida and considered it transtropical. not yet known ifthe species is free-living Lattin and Lewis (2001) stated that it in the Portland area or periodically had been intercepted on shipments of reintroduced. orchids at San Francisco, California, and DufourieUus ater (Dufour 1833) was de- clarified previous citations. scribed from Europe. Van Duzee (1916) Brachysteles parvicornis (Costa 1847) first reported it in America north of was described from Italy. Pericart (1972) Mexico ("E."). Blatchley (1928) listed reviewed it in the western Palearctic. California and Kentucky and Anderson Asquith and Lattin (1990) pubhshed the (1962b) added British Columbia and first record from America north of Idaho. Pericart (1972) discussed this spe- Mexico based on specimens from New cies in the western Palearctic. Kelton Jersey and New York. Lattin and As- (1978) added Ontario and Henry (1988) quith (1991) added Massachusetts and reported North Carolina and New York. Maine and Lattin (1993), Nova Scotia, Lattin (2000) discussed D. ater and in- as did Scudder and Foottit (2006). This cluded references to itseconomicrole (e.g., small predatory bug feeds on mites on Arbogast 1984, Awadallah et al. 1984). It conifers in northeastern Canada and the is taken under the bark of trees but also United States. is associated with stored products. 370 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON Physopleurella mundula (White 1877) Cuban laurel thrips. According to Paine was described from the Hawaiian Islands (1992), it did not become established in (as Cardiastethus mimdulus). Blatchley that state. Reimer (1988) reported that (1925) first reported it from America M. moraguesi became a predator on north of Mexico (Florida) (as Physo- a species of thrips introduced into the pleurella Jloridana Blatchley), and later Hawaiian Islands to help control an recorded it from Jamaica (1928). Blatch- introduced weed, and referred to this ley's species was synonymized with condition as biotic interference. Recently, Physopleurella mundulus (White) by Lat- Bennett (1995) reported its accidental tin (2005). Thus far, Florida is the only occurrence in Florida. The bug had been known site in North America. feeding on thrips of an unwanted Ficus. He introduced this bug into Texas as Oriini possible thrips control on ornamental Macrotracheliella nigra Parshley (1917) Ficus in shoppingmalls! Dobbs and Boyd was described from Massachusetts. An- (2006) have provided a detailed study of derson (1962b) recorded it from British the distribution of Montandoniola mora- Columbia. Kelton (1978) reported it guesi, its host thrips and their host plants from British Columbia, Manitoba, On- in the United States (Alabama, Florida, tario, Quebec and Nova Scotia. Henry Louisiana and Mississippi). This work (1988) listed Arkansas, Florida, New establishes an excellent base for future Jersey, New York and Rhode Island, work. and Maw et al. (2000) added New Orius insidiosus (Say) (1832) was de- Brunswick. Lewis et al. (2005) found it scribed from eastern United States. in Montana and Washington. Paine Kelton (1963) reviewed the genus Orius (1992) cited its occurrence in southern for America north of Mexico. Herring California where it was found feeding on (1966b) revised Orius for the Western thrips on Ficus. It is believed to have been Hemisphere, and indicated that O. in- introduced earlier into California as sidiosus occurred over much of eastern a potential biological control agent North America, south through Mexico against the thrips on Ficus (Paine 1992). and Central and South America and The occurrence out of its normal range, onto the West Indies. Henry (1988) coupled with the likely deliberate intro- reported the species from many prov- duction, qualifies the species as non- inces and states. This is a common indigenous in California. species in many agricultural environ- Montandoniola moraguesi (Puton 1896) ments (Lattin 1999b, 2000). Scudder was described from Spain. Carayon and and Foottit (2006) stated that Orius Remade (1962) published an account of insidiosus was introduced from eastern the species in France. Herring (1966a) North America into greenhouses in clarified the name for this predator ofthe British Columbia to control thrips. Cuban laurel thrips. Davis and Krauss While this effort was successful, they (1966) introduced this bug from Manila, reported that some bug individuals have Philippines, into Oahu, the Hawaiian escaped the greenhouses. Thus far, there Islands. It quickly became established as was no evidence that the species had a predator of the thrips on Ficus and become established in the wild. spread to other islands. Pericart (1972) Orius (Heterorius) minutus (Linnaeus reviewed it in the western Palearctic. 1758) was described from Europe. Tonks Clausen (1978) reported on its introduc- (1953) first reported it from America tion into California from Hawaii in north of Mexico, based on specimens 1966-1967 as a potential predator of the from southern British Columbia, as did VOLUME NUMBER 109, 2 371 Downes (1957). Anderson (1962b) re- discussed this species from a world per- corded it from British Columbia, Oregon spective. It is commonly associated with and Washington as did Kelton (1963, food products, likely explaining its wide- 1978), Herring (1966b) and Henry spread distribution. (1988). Pericart (1972) treated this spe- Xylocoris(Proxylocoris)galactinus(Fie- cies in the western Palearctic and Lattin ber 1837) was described from southern et al. (1989) reviewed the species in the Europe. Van Duzee (1905) first recorded Pacific Northwest, including biology and this species from America north of Mex- illustrations of the adult and nymph. ico (New York). Anderson (1962b) re- Barnes et al. (2000) cited British Colum- ported it from Idaho and Oregon. Cara- bia, as did Scudder and Foottit (2006). It yon (1972) included it in his study of has been taken on caneberry vines where Xylocoris, and Pericart (1972) reviewed it feeds on insects and mites (Lattin et al. it in the western Palearctic Region. 1989). Henry (1988) reported it from Alberta, Paratriphleps laeviuscula Champion, British Columbia, California, Florida, 1900, was described from Panama. It is Georgia, Idaho, Illinois, Manitoba, Mis- now known from Honduras (Drake and souri, New Jersey, New York, Ontario, Harris 1926) (see the discussion by Quebec, and Saskatchewan. Dunkel Barber, 1939 on some taxonomic prob- and Ivie (1994) added Montana where lems with Paratriphleps). Bacheler and specimens of X. galactinus were taken Baranowski (1975) described the biology in spilled grain. I have identified this of the species where it appeared to feed species from Oregon. Lattin (2000) in- only on flowers. Hambleton (1944) and cluded this species in his review of Wille (1951) had stated that this was economically important Anthocoridae. a predaceous species in Peru, but Herring This is clearly a non-indigenous species (in Bacheler and Baranowski (1975)) in our area where it is often taken in stated that the Peru specimens were not stored grain. P. laeviuscula. Henry (1988) reported it Xylocoris {Proxylocoris) sordidus (Reu- from Puerto Rico, Mexico and Panama, ter 1871) was described from Brazil besides Florida and Carpentero et al. and Texas. Champion (1900) reported it (1997) added Nicaragua. Lattin (2006b) from Mexico, British Honduras, Guate- deleted records of P. pallida (Reuter mala, Panama, Brazil and the Antilles 1884) from America north of Mexico. (Grenada and St. Vincent). Van Duzee (1903) recorded this species based on Xylocorini specimens from New Mexico. Arbogast Xylocoris (Arrostelus) flavipes (Reuter et al. (1983, 1985) provided biological 1875) was described from Algeria. Bibby information on the species in stored (1961) first reported it from North peanuts in Georgia. Henry (1988) listed America (Arizona). Jay et al. (1968) this species from Arizona, California, published on its biology in Georgia as Florida, Georgia, Kansas, Massachu- did Awadallah and Tawfik (1972) in setts, Maryland, New Jersey, New Mex- Egypt. Pericart (1972) provided an ac- ico, New York, Pennsylvania, South count of the species western Palearctic. Carolina, Tennessee, and Texas besides Arbogast (1975, 1979) wrote on its its natural range in Mexico, Central and biology and Henry (1988) reported X. South America, and the West Indies. It is flavipes from Arizona, District of Co- associated with stored foodstuff in the lumbia, Georgia, Kansas, Maryland and United States. Texas besides Africa, Asia, Australia, Xylocoris {Xylocoris) cursitans (Fallen Europe and South America. Lattin (2000) 1807) was described from Sweden. Van 372 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON Duzee (1916) first recorded this species in and to L. Parks for manuscript prepara- North America from eastern Canada tion. and United States. Sands (1957) figured Literature Cited the egg and a nymph and Anderson (1962b) recorded it from British Colum- Anderson, N. H. 1962a. Bionomics ofsix speciesof bia, Idaho, and Oregon. Carayon (1972) Anthocoris (Heteroptera: Anthocoridae) in England. Transactions of the Royal Entomo- included this species in his review of logical Society ofLondon 114(3): 67-95. Xylocoris and Pericart (1972) provided 1962b. Anthocoridae ofthe Pacific North- . an account of the species in the western west with notes on distributions, Hfe histories, Palearctic. Kelton (1978) reported this and habits (Heteroptera). The Canadian En- species from Alberta, British Columbia, Andetrosmoonl,ogNi.stH9.4:an1d325L-.13A3.4.Kelton. 1963. A new Nova Scotia, Ontario, and Quebec and species of Anthocoris from Canada, with Henry (1988) added Connecticut, Idaho, distribution records for three other species Indiana, Michigan, New Jersey, New (Heteroptera: Anthocoridae). The Canadian York, and Oregon. Lattin and Stanton Entomologist 95: 439^42. Arbogast, R. T. 1975. Population growth of (1992) reported it from Washington. Xylocoris flavipes: influence of temperature Lattin (2000) discussed Xylocoris ciirsi- and humidity. Environmental Entomology 4: taiis and suggested that it may occur 825-831. naturally in the Nearctic but that it also . 1979. The biology and impact of the may have been introduced subsequently predatory bug Xylocoris flavipes (Renter). Proceedings of the Second International in international commerce. It occurs in Working Conference on Stored-Product Ento- both fully winged and brachypterous mology. Ibadan, Nigeria, September 1978. individuals in both regions. It is usually pp. 91-105. found under the bark of dead trees. I 1984. Demography of the predatory bug have taken both forms under the bark of Diifouriellus ater (Hemiptera: Anthocoridae). Environmental Entomology 13: 990-994. old conifer logs in western Oregon. Arbogast, R. T., B. R. Flaherty, and J. W. Press. Xylocoris {Xylocoris) vicarius (Renter) 1983. Demography of the predaceous bug (1884) was described from Colombia. Xylocoris sordidus (Reuter). American Mid- Van Duzee (1916) first reported it in land Naturalist 109: 398^05. North America. Torre-Bueno (1930) in- ArboWga.st,PrRe.ssT..,1B9.85R.. FDlaehveerltoyp,mRe.ntVa.lByrsdta,geasndoJf. dicated that the species was found under Xylocoris sordidus (Hemiptera: Anthocoridae). bark and Anderson (1962b) recorded it Entomological News 96: 53-58. from British Columbia with some hesi- Asquith, A. and J. D. Lattin. 1990. Brachysteles tation, suggesting that his specimen parvicornis (Costa), a species ofAnthocoridae new to North America (Hemiptera: Heterop- might be a macropterous adult of X. tera). Journal ofthe New York Entomological cursitans. Henry (1988) recorded it from Society 98: 352-356. Florida, Massachusetts, New Jersey and Awadallah, K. T. and M. F. S. Tawfik. 1972. The New York besides South America. biology of Xylocoris (= Piezostethus)flavipes (Reut.) (Hemiptera: Anthocoridae). Bulletin de la Societe Entomologique d'Egypte 56: Acknowledgments 177-189. My thanks go to N.H. Anderson, A. Awadallah, K. T., M. F. S. Tawfik, N. Abou-Zeid, Asquith, F.D. Bennett, J. Carayon, T.J. ao^ndDiiMf.ourMi.ellEuls-Hautsesre(iDnuif..)19(8H4e.miTphteerlaif:eAhnistthoor-y Henry, J.L. Herring, D.R. Horton, L.A. coridae). Bulletin de la Societe Entomologique Kelton, J. Pericart, and G.G.E. Scudder d'Egypte 63: 191-197. for their work on these small predators. Bacheler, J. S. and R. M. Baranowski. 1975. 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Nature Pub- quatra et quinta. Napoli. 43 pp. lishing Company, Indianapolis. 1116 pp. Cox, G. W. 1999. Alien Species in North America 1928. Notes on the Heteroptera ofeastern and Hawaii: Impacts on Natural Ecosystems. . North America with descriptions of new Island Press, Washington, D.C. 387 pp. species. 1. Journal ofthe New York Entomo- . 2004. Alien Species and Evolution. Island logical Society 36: 1-23. Press, Washington, D.C. 377 pp. . 1934. Notes on collection of Heteroptera Dallas, W. S. 1851-1852. List ofthe specimens of taken in winter in vicinity of Los Angeles, Hemipterous insects in the collection of the California. Transactions of the American British Museum. Taylor and Frances Incorpo- Entomological Society 60: 1-16. rated, London 1851: 1-368, plates 1-11: 2: Brenner, G. J. and J. D. Lattin. 2001. Notes on 369-592, plates 12-15. three species of Anthocoridae (Hemiptera: Davis, C. J. and N. L. H. Krauss. 1966. 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