3 October 1991 PROC. ENTOMOL. SOC. WASH. 93(3), 1991, pp. 630-635

HARMONIA AXYRIDrS (PALLAS), THE THIRD SPECIES OF THE GENUS TO BE FOUND IN THE UNITED STATES (COLEOPTERA: COCCINELLIDAE)

J. B. CHAPIN AND V. A. BROU

(JBC) Department of Entomology, Louisiana Agricultural Experiment Station, Loui- siana State University Agricultural Center, Baton Rouge, Louisiana 70803-1710; (VAB) 74320 Jack Loyd Road, Abita Springs, Louisiana 70420.

Abstract.—Harmonia axyridis (Pallas), an Old World Coccinellini, is reported as es- tablished in southeastern Louisiana. A few specimens were also collected in eastern Mis- sissippi. The species is described, illustrated, and compared to //. dimidiala (F.) and II. quadripunctata (Pontopiddian). Key Words: Coleoptera, Coccinellidae, Harmonia

A lady beetle, not previously known to was made in Shreveport, Bossier [sic] Par- be established in the United States, was col- ish, on August 24, 1979, and eight releases lected near Abita Springs, St. Tammany of 3781 specimens were made in Leland and Parish, and in other southeastern Louisiana Stoneville in Washington County, Missis- parishes. A few specimens were also col- sippi, from July 12 to October 23, 1980 (P. lected in eastern Mississippi. Harmonia ax- W. Schaefer, pers. comm.). There were no yridis (Pallas) occurs in southern Siberia, subsequent reports that this species had be- Manchuria, China, Formosa, Korea, Japan, come established. Ryukyu Islands, and the Bonin Islands (Dobzhansky 1933, Timberlake 1943, Chapin 1965, lablokoff-Khnzorian 1982). Harmonia axyridis (Pallas) Specimens of this species were released in Figs. 1-6 California in 1916, 1964, and 1965 (Gordon Diagnosis. —Form oval, convex. Head 1985) and in Nova Scotia, Connecticut, straw-yellow, immaculate, with two longi- District of Columbia, Delaware, Georgia, tudinal rows of faint spots, or with black Louisiana, Maine, Maryland, Mississippi, spot on clypeus sometimes extending onto Ohio, Pennsylvania, and Washington from labrum and head. Antennae and mouth- 1978 to 1982 (Gordon 1985, P. W. Schae- parts yellow-brown, sometimes tinged with fer, pers. comm.). Specimens were also re- black. Pronotum straw-yellow with four leased in Connecticut in 1985 during a study black spots and usually a faint mark above of the potential of H. axyridis to control scutellum, or lateral spots joined to form Matsucoccus resinosae Bean and Godwin two curved lines or an M-shaped mark ex- (McClure 1987). tending to anterior margin, occasionally Japan was the country of origin of the center of pronotum black. Scutellum straw- specimens released in Louisiana and Mis- yellow. Elytra yellow-orange, each elytron sissippi. A single release of 32 specimens in fully maculate individuals with faint mark VOLUME 93, NUMBER 3 631

behind scutellum, two spots at one-fifth, three spots in semicircle at two-fifths, three spots at three-fifths, and one spot at four- fifths, these black spots variously reduced or absent; each elytron usually with trans- verse plica anterior to apex (Fig. 1). Ventral surface yellow-orange to black, hypomeron, epimera, epipleura, and lateral abdominal margins paler. Intercoxal process of pro- sternum with carinae. Legs yellow-brown varying to black with posterior side of mid- \ dle and hind legs and tarsi paler. Length, 4.81-7.47 mm; width, 3.90-5.89 mm. Locality data.—The majority of the more than 1000 specimens were collected by V. A. Brou at his home located 4.2 miles north- east of Abita Springs (Sec. 24, T6, SR12E) using six light traps of varying wattages, ranging from 60-2500 watts per trap. Usu- Fig. 1. Harmonia axyridis, habitus; scale bar = 2 ally a combination of ultraviolet light mm. sources were used on the traps, including fluorescent blacklights and high intensity collected in Mississippi counties: 1, Cal- discharge lamps, e.g. mercury vapor. The houn (5.5 miles north of Vardaman, black- traps operated from dusk to dawn and were light trap in sweetpotato field), August 9, controlled by photoelectric cells. Specimens 1990, James Jarrett; 3, Harrison (T5S, first appeared on July 20, August 8 and 20, R13W, Sec. 1, old field habitat on senescent October 22, and November 17 in 1988. No Erigerori), November 15, 1990, T. C. Lock- specimens were seen previously even though ley; 1, Panola (2 miles south of Crenshaw), the light traps had been operating 365 nights October 6, 1990, S. Jones (student collec- per year since 1982 at this same location. tion) (MSU). In 1989, specimens were taken on January Comments.—The variability of the color 26 and from March 19 to December 27. In pattern has led to the description of more 1990, they were collected on January 13 and than 100 forms (see Korschefsky 1932 for 22 and from February 2 through September synonymy). Twenty-four of these patterns 16 and were present through December. were portrayed by Ayala (1978). Only the Larvae and adults were collected on crab- pale forms are found in Louisiana and Mis- apple trees infested with Aphis spiraecola sissippi, including frigida Mulsant, novem- Patch in May. This species is now the most decimsignata Falderman, andsuccinea Hope common lady beetle at this site. Additional which are more common in the Maritime specimens were collected in July 1990, by Province of Russia, Korea, Manchuria, and the senior author and V. L. Moseley on China. In southwestern Sibera, black forms crapemyrtles infested with Tinocallis kaho- with one to several pale spots predominate waluokalani (Kirkaldy) in the following (Dobzhansky 1933). In Japan, the percent- southeastern parishes: Jefferson (Metaire), age of the pale form, succinca, decreases Orleans (New Orleans), St. Helena (Greens- gradually from northeast to southwest while burg), St. Tammany (Covington, Folsom), one of the dark forms, conspicua, increases Tangipahoa (Hammond), and Washington conversely; two other dark forms do not \ (Franklinton). The following specimens were show such a gradient (Komai 1956). lablo- 632 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON VOI

koff-Khnzorian (1982) Summarized the in- - Apex of each middle and hind tibia with formation known about this species, some 2 sPurs 12 f u- u • • ijj- uji/im-jio 10(9). Postcoxal line on first abdominal segment of which is included in Hodek (1973). . Som. e wit. ,h obliqu,, e dividin,. .,. g .lin. e 11 Of this data, including the host information _ Postcoxal line on first abdominal segment given below, may refer to H. yedoensis (Ta- without oblique dividing line kizawa), a closely related species that occurs Mulsantina Weise in China, Korea, Japan, Ryukyu, and Tai- n<10). Prosternal carinae ending at anterior cox- al margin Neoharmonia Crotch Prosternal carinae extending anterior to Two other species of Harmonia occur in thc anterior coxa, margin or absent the U.S. Harmonia dimidiata (F.) was in- Harmonia Mulsant troduced from China into California and '2(9). Prosternum strongly convex medially, then to Florida in 1926 where it became protuberant at apex (Fig. 614b);mesoster- * ui- v. j ir^ A inoc\ IT • num deeply emarginate for reception of established (Gordon 1985). Harmonia sternai process . 3*M«b»t quadnpunctata (Pontopiddian), which may _ Prosternum normally rounded, not pro- have been accidentally introduced, was re- tuberant at apex; mesosternum truncate ported from New Jersey and New York and or weakly emarginate for reception of has been in the U.S. since 1924 (Vanden- Prosternal process 13 berg 1990). Specimens of//. axyridlS are '3(12)' Postcoxallme on firs, abdominal sternum complete, of the Putins type (Fig. 637a) broadly oval; the pronotal pattern consists Adalia Mulsant of four to five black spots, two Curved lines, - Postcoxal line onfirs t abdominal sternum an M-shaped mark, or the center of the pro- incomplete, of the DiomusorNephusiype notum is black; in addition to the spot be- (Figs. 634b, 682a) 14 i • i .. . ,i i , . , • 14(13). Elytron yellow with black sutural margin hind the scutellum,' eac. h e Jytro n has nine and, 4. blac.. k. spot.s (Fig,c. . 672g),-.- ., spots ofteF. n black spots arranged in a 2,3,3,1 pattern, or somewhat coalesced; pronotal hypome- the spots are variously reduced or absent; ron with shallow fovea; Oriental genus, and a transverse plica, which is lacking in one species possibly established in Florida the other two species, is usually present near Coelophora Mulsant the elytral apex. Harmonia quadnpunctata ~ Elytron w,,h color pattern not resembling J . . . . that of Coelophora; pronotal hypomeron is more elongate in shape with 11 puncti- without shallow fovea. North Arnerican form black spots on the pronotum, one or or European genera 15 two pairs sometimes faint or absent; the el- 15( 14). Tarsai claw with median tooth (Fig. 626a) ytron is immaculate or has a pair of elongate Myzia LeConte SUbqUadrate baSa t0 th black marks at the lateral margin on either SKSj ^ ' ° 16 side of the mid-line (Vandenberg 1990); and ,6( , 5) Pr* ota! surface polished,' shiny,' not aiu- the prosternal carinae, present in the other taceous between punctures .. Cahia Mulsant two species, are absent (lablokoff-Khnzo- - Pronotal surface alutaceous, often dull, not rian 1982). Specimens of H. dimidiata are polished 17 round and very convex with a bilobed black ! 7(16)" Pron°tum black ^ith large, subtrape- . . r . . zoidal or triangular white spot on each spot at the base of the pronotum and Seven anterolateral angle (Fig. 643g) (apical black spots arranged in a 1,3,2,1 pattern on margin of pronotum sometimes narrowly each elytron. pale) Cocdnclla L. With the addition of two more species of - Pronotum not as above 18 Harmonia to our fauna, the key to the gen- '8('7)' Pof °^,al line,on.'lrst abdominal stcrn,um, - _ . „. . ._ ' .X«, ?„,, with oblique dividing line O/w Casey era Of Coccmellim (Gordon 1985, p. 681) _ Postcoxal line on first abdominal sternum ; needs to be modified as follows: without oblique dividing line 19 19(18). Apex of mesosternum notched for recep- 9(6). Apex of each middle and hind tibia with- tion of prosternal process; European ge- F out spurs 10 nus, one species presently established in will \ SpC! VOLUME 93, NUMBER 3 633

Figs. 2-6. Harmonia axyridis, male and female genitalia. Figs. 2, 3, ventral and lateral views of phallobase without and with trabes. Figs. 4, 5, entire sipho and enlarged view of distal end. Fig. 6, spermathecal capsule, sperm duct and infundibulum. 634 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON vo

southeastern Canada, Vermont, and New Toxoptera piricola Matsumura [= Schiza- York' Propylaea Mulsant phispiricola (Matsumura)]. Yasumatsu and lab Apex of mesosternum truncate; occurring Watanabe (1964) listed 13 hosts including over most of North America from south- ern Canada to Mexico .... Cvcloncda Crotch Cinara kochi Inouye, Hyalopterus pinni Matsumura, and Chrysomela vicintipunc- tata Scopoli. Fuyuan and Dongxi (1989) re- Koebele's field notes (Timberlake 1943) ported the control of Nesticoccus sinensis indicated that //. axyridis was common in Tang (Pseudococcidae) and Rhizococcus Ko Japan on various aphid-infested trees, such transversus (Eriococcidae) after coccinel- as maple, walnut, and willow, and also on lids, predominately //. axyridis and //. ob- rose. It fed on Lachnus sp. on Podocarpus scurosignata (Liu-Chung-Lo), were attract- and Kermaphis pini (Koch) [= Pineus pint ed to aphid-infested rape interplanted in the (Koch)] on pine in Japan, on Lachnus sp. \ bamboo forest. on Pinus sinensis at Hongkong, China, and was collected on Lachnus infested pine in ACKNOWLEDGMENTS Formosa. lablokoIT-Khnzorian (1982) also The authors wish to thank R. D. Gordon, stated that it was arboreal, that it was found USDA Systematic Entomology Laboratory, on rosaceous arborescents and also on oak Washington, D.C., for confirming the iden- and other trees, and that it was chiefly an tification of //. axyridis; M. B. Stoetzel, aphid feeder although it fed on Icerya pur- USDA Systematic Entomology Laboratory, chasi Maskell (Margarodidae), Phenaccocus Beltsville, Md., for identifying A. spirae- pergandci Cockcrell (Pseudococcidac) and co/a; Terence Schieier, Mississippi State Anomoneura mori Schwarz (Psyllidae), at University (MSU), Starkville, Miss., for least in the laboratory. Preferred aphid hosts permission to use the label data on the Mis- given by lablokoff-Khnzorian (1982), some sissippi specimens; K. A. Westphal for the of which were listed by Hodek (1973), are illustrations; V. L. Moseley, D. A. Rider, as follows: Acyrthosiphon pisum (Harris), and L. H. Rolston, Louisiana State Uni- Amphorophora oleracea v.d. Goot [= Hy- versity, and P. W. SchaefTer, USDA Bene- peroniyzus carduellinus (Theobald)], Aphis ficial Insects Research Laboratory, for re- pomi De Geer, Cinara laricicola (Borner) viewing earlier drafts of this manuscript. [= C. cuneomaculata (del Guercio)] (?), C. Approved for publication by the Director todocola (Inouye) (?), Cryptosiphum gallar- of the Louisiana Agricultural Experiment um (Kaltenbach) [= C. artemisiaeEuckion], Station as manuscript number 90-17-4432. Eriosoma lanigerum (Hausmann), Hyalop- terus pruni (Geoffrey), Macrosiphum rosae LITERATURE CITED ibarae Matsumura, Megoura viciaejaponica (Matsumura) [= Uroleucon gigantewn Ma- Ayala, F. J. 1978. The mechanisms of evolution. Sci- tsumura], Myzus malisitcta Matsumura [= entific American 239: 56-69. Chapin, E. A. 1965. Coccinellidae. In Insects of Mi- Ovatus malisuctus (Matsumura)], M. pcr- cronesia. Coleoplera. Bernice P. Bishop Museum, sicae (Sulzer), Neophyllaphis podocarpi Honolulu, Hawaii 16: 189-254. Takahashi, Nippolachnus piri Matsumura, Dob/hansky,T. 1933. Geogrphical variation in lady- Periphyllus californiensis (Shinji), Rhopa- beetles. The American Naturalist 67: 97-126. Fuyuan, X. and W. Dongxi. 1989. Control of bamboo losiphum pscudobrassicac Davis [= Lipa- scale insects by intercropping rape in the bamboo phis erysimi (Kaltenbach)], R. pninifoliae forest to attract coccinellid beetles. Chinese Jour- Shinji [= Capitophoruspninifoliae (Shinji)], nal of Biological Control 5: 117-119. Gordon, R. D. 1985. The Coccinellidae (Coleoptera) of America north of Mexico. Journal of the New 1 Dysart, R. J. 1988. J. New York Entomol. Soc. 96: York Entomological Society 93: 1-912. 119-121. Hodek, I. 1973. Biology of Coccinellidae. Academia, VOLUME 93. NUMBER 3 635

Czechoslovak Academy of Sciences, Prague. 260 ed States. Environmental Entomology 16: 224- PP. 230. lablokoll-Khn/orian, S. M. 1982. Lcs Coccinelles Timberlake, P. H. 1943. The Coccinellidae or lady- Coleopteres-Coccincllidae, Trihu Coccinellini dcs beetles of the Koebele collection—Part I. Hawai- Regions Palearctique et Orientale. Socicte Novelle ian Planters' Record 47: 1-67. dcs Editions Boubee, Paris. 568 pp. Vandcnberg, N. J. 1990. First North American re- Komai, T. 1956. Genetics of ladybcctlcs, pp. 155- cords for Harmonia guadripunctata (Pontopid- 188. In Demerec, A., ed., Advances in Genetics. dian) (Coleoptera: Coccinellidae); a lady beetle na- Vol. 8. Academic Press, New York. tive to the Palearctic. Proceedings of the Korschcfsky, R. 1932. Coccinellidae II, pp. 224-659. Entomolological Society of Washington 92: 407- In Junk-Schenkling. Coleopterorum Catalogus, 410. pars 120. Junk, Berlin. Yasumatsu, K. and C. Watanabe. 1964. A Tentative McCIure, M.S. 1987, Potential of the Asian predator, Catalogue of Insect Natural Enemies Of Injurious Harmonia axyridis Pallas (Coleoptera: Coccinel- Insects in Japan. Part 1. Parasite-Predator Host lidae), to control Matsucom/s resinosae Bean and Catalogue. Kyushu University, Fukuoka, Japan. Godwin (Homoptera: Margarodidae) in the Unit- 166 pp.

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