BIOLOGY Leiophron argentinensis Shaw (Hymenoptera: Braconidae): A New Species of Parasitoid from Argentina and Paraguay—Information on Life History and Potential for Controlling Lygus Bugs (: )

LIVY WILLIAMS, III,1, 2 GUILLERMO A. LOGARZO,3 SCOTT R. SHAW,4 LESLIE D. PRICE,1 5 AND VERO´ NICA MANRIQUE

Ann. Entomol. Soc. Am. 96(6): 834Ð846 (2003) ABSTRACT We discovered an undescribed species of Leiophron parasitizing mirid nymphs in Argentina and Paraguay; this euphorine braconid is described as Leiophron argentinensis Shaw n. sp. Wasps were reared from several mirid species collected on numerous host plants, but most parasitoids (Ͼ85%) were reared from Taylorilygus apicalis (Fieber), which was the most abundant mirid. Parasitism rates ranged from 0to 37% and averaged Ϸ7% for the entire study. Excluding samples where parasitism was not observed, parasitism rates averaged Ϸ9%. Parasitism levels were highest in the summer. Host plant species signiÞcantly inßuenced parasitism levels of T. apicalis; nymphs on Conyza spp. suffered Ϸ16% parasitism, signiÞcantly more than nymphs on other host plants. L. argentinensis was collected throughout the study area (Ϸ22Ð35Њ S), although the entire geographic range of this species is not yet known. We observed a transition from a male-biased sex ratio in the summer to a female-biased sex ratio in the fall. L. argentinensis has several generations per year and apparently produces some diapausing individuals in each generation. The incidence of diapause was lowest in the summer (Ϸ40%). In laboratory trials, L. argentinensis readily parasitized Lygus lineolaris (Palisot de Beauvois) and Lygus hesperus Knight, suggesting that L. argentinensis has potential as a biological control agent for these pests in the United States.

KEY WORDS Leiophron argentinensis Shaw n. sp., Taylorilygus apicalis, Lygus lineolaris, Lygus hesperus, parasitoids

THE GENUS Lygus Hahn (Hemiptera: Miridae) occurs densities increase and from which bugs disperse into in the Northern Hemisphere, and throughout this re- crop Þelds after wild hosts senesce. In most crops, gion Lygus species are important pests of many crops L. lineolaris and L. hesperus are controlled by appli- (Wheeler 2001). The two species of primary concern cation of broad-spectrum insecticides. However, an in North America are L. lineolaris (Palisot de Beau- increase in the use of transgenic crops for other pests vois), which occur throughout much of the continent, and the implementation of the boll weevil eradication and L. hesperus Knight, which is limited to western program might reduce the total insecticide load in North America (Schwartz and Foottit 1998). Both some agroecosystems, especially those with histori- species are native to North America, where they infest cally heavy insecticide use, such as cotton (Hardee et many wild host plants and crops (Scott 1977, al. 2001). While a reduction in insecticide use might Snodgrass et al. 1984a, Young 1986). In the springtime, increase Lygus densities, it also will transform agro- Lygus species infest wild host plants, where population ecosystems into more favorable environments for nat- ural enemies, thus creating conditions more condu- cive to biological control (Ruberson and Williams This article reports the results of research only. Mention of a 2000). An effective biological control agent for Lygus proprietary product does not constitute an endorsement or a recom- Ͼ mendation for its use by USDA. spp. could save $1 billion annually as well as sub- 1 United States Department of Agriculture, Agricultural Research stantially reduce the insecticide load in the environ- Service, Southern Management Research Unit, PO Box 346, ment. Stoneville, MS 38776Ð0346. 2 E-mail: [email protected]. Lack of adequate control of Lygus by native natural 3 United States Department of Agriculture, Agricultural Research enemies has led to several attempts at classical bio- Service, South American Biological Control Laboratory, Bolivar 1559 logical control (Van Steenwyk and Stern 1977, Craig (1686), Buenos Aires, Argentina. and Loan 1987, Day 1987, Schuster 1987). The intro- 4 Department of Renewable Natural Resources, Entomology Sec- tion, University of Wyoming, Laramie, WY 82071Ð3354. duction of natural enemies has met with limited suc- 5 Department of Entomology, TexasA&MUniversity, College cess, although recently a European parasitoid, Peri- Station, TX 77843Ð2475. stenus digoneutis Loan (Hymenoptera: Braconidae), November 2003 WILLIAMS ET AL.: NEW SPECIES OF Leiophron 835 was established in the United States (Day et al. 1990), inces) and southeastern Paraguay (six departments). where it has subsequently suppressed L. lineolaris These collections included two growing seasons. populations in alfalfa by as much as 75% (Day 1996). Nymphs were sorted in the Þeld to morphospecies and P. digoneutis has since spread to at least eight north- were placed in rearing chambers similar to those de- eastern states and Que´bec, Canada (Broadbent et al. scribed by Debolt (1981). The rearing chambers con- 1999, Day et al. 2000). Because L. lineolaris and sisted of 0.5-liter cylindrical cardboard cartons with L. hesperus do not occur in Europe, successful establish- the top and bottom removed. The top of the chamber ment of European parasitoids relies on the “new-associ- consisted of mosquito netting held in place by the ring ation” approach (Pimentel 1963, Hokkanen and Pimen- of the lid, and 1.5-mm mesh Þberglass window screen tel 1989, Pimentel 1991), a variant of classical biological was glued to the hole in the bottom of the chamber. control. The new-association strategy involves selection The pupation substrate consisted of black felt cloth of natural enemies from relatives of the target pest with with several 4-cm slits cut in it. The cloth was placed which the natural enemies have not had a previous as- in the inverted lid of a 9.6-cm-diameter plastic petri sociation. This approach has particular merit when na- dish, and the cardboard carton was placed in it. The tive natural enemies are not present or are ineffective. assembled rearing chamber was held together by rub- The success of this approach appears to be increased ber bands. Green bean pods, Phaseolus sp., were pro- when the natural enemy host is taxonomically closely vided as a food source and were changed three times related to the target pest or has a similar life history and per week. The felt cloth was lightly moistened three ecology (Van Driesche and Bellows 1996). For example, times per week. In the Þeld, rearing chambers were a promising situation might be one in which the natural held at Ϸ20Ð30ЊC with ambient light and humidity. In enemy host occurs on plant species that also are infested the laboratory, rearing chambers were held at Ϸ25ЊC by the target pest. with ambient light and humidity, and cocoons were In 1999, we began Þeld exploration in Argentina and removed daily and held individually in gelatin cap- Paraguay for nymphal parasitoids that may help sup- sules until emergence. Wasps were provided with press Lygus in the southern United States. Most of the honey and water for several days, after which they study area is characterized as temperate and subtrop- were either (1) killed and preserved in 70 or 100% ical, with climates, ßora, and geography similar to ethanol for taxonomic study or (2) maintained alive those of the United States. Although Lygus does not for use in host-range studies with Lygus spp. Termi- occur in South America, the region nevertheless has a nology used in the description follows that of Sharkey rich mirid fauna. To our knowledge, Þeld exploration and Wharton (1997) and Day et al. (1999). for nymphal parasitoids of mirids has not been con- Parasitism rates were assessed by rearing, i.e., by ducted previously in South America (Hedlund 1987). dividing the sum of the cocoons and larvae that did not The genera Leiophron Nees and Peristenus Foerster spin cocoons reared from each sample by the number (Hymenoptera: Braconidae) are solitary koinobiont of nymphs in the sample. Gender and stage of dia- endoparasitoids of nymphal and adult pausing individuals were determined by dissecting and Psocoptera (Shaw 1997). Species of Leiophron and cocoons from some Þeld collections in 1999 and 2000. Peristenus that parasitize mirids pupate inside cocoons To facilitate statistical analyses, collection sites in the soil, and on emergence, attack early-instar were grouped into one of four regions: northwest, nymphs. A single wasp larva develops in the host and northeast, central, and Buenos Aires (Fig. 1). Host usually emerges from a late-instar nymph. Parasitism associations between mirids and host plants; abun- rates range from Ͻ5 to nearly 100% (Clancy and Pierce dance of mirids; inßuence of mirid, host plant, and 1966, Norton et al. 1992, Day 1999, Day et al. 1999). Sex collection site on parasitism; and sex ratios of wasps ratio, diapause, and host associations are poorly under- were evaluated by computation of contingency tables stood for some species. Most known species of Leiophron (PROC FREQ) and analysis of variance (ANOVA; and Peristenus have been collected in North America, PROC MIXED) (SAS Institute 2000). western Europe, southcentral Asia, and several countries Host plants from which mirid nymphs were swept in Africa (Hedlund 1987, Shaw 1997). Almost nothing is were collected, pressed, and identiÞed by consultation known about these genera in South America. with specialists. Voucher specimens of plants are de- This paper describes a new species of Leiophron posited in the USDA-ARS South American Biological from Argentina and Paraguay; provides Þeld data on Control Laboratory, Buenos Aires, Argentina. Special- host and host-plant associations, parasitism levels, and ists identiÞed adult mirids reared from nymphs. life history of the wasp; and reports laboratory studies Voucher specimens of mirids are deposited in the of parasitism of L. lineolaris and L. hesperus. Sole au- National Museum of Natural History, Smithsonian In- thorship of the new species is attributed to S.R.S. stitution, Washington, DC, and in the Museo Depart- mento Cientõ´Þco de Entomologõ´a, Facultad de Cien- cias Naturales, Universidad Nacional de La Plata, La Materials and Methods Plata, Argentina. Field Collections Parasitism of Lygus spp. by L. argentinensis From November 1999 to June 2001, sweep-net sam- ples were made periodically in wild and cultivated A preliminary trial was conducted to determine if plants in central and northern Argentina (10prov- L. argentinensis will use Lygus spp. as hosts. First instar 836 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 96, no. 6

Fig. 1. Study area and collection sites in Argentina and Paraguay. Northeast ϭ ●; Northwest ϭ Œ; Central ϭ ; Buenos Aires ϭ ‚.

L. lineolaris and Þrst and second instar L. hesperus Results and Discussion were exposed to L. argentinensis. Two replicates were Species Description set up for Þrst instars of each host species, and four replicates were set up for second instar L. hesperus. Leiophron argentinensis Shaw, new species For each replicate, 10Ð50 nymphs of each instar-host Description of Holotype Female. Body length combination were placed in a ventilated plexiglas cage 2.0mm. Body color black on ocellar triangle, dorsal (26 by 26 by 20cm) with green beans. Honey was margin of eye, entire mesosoma and metasoma; head streaked on the inside of the cage, and distilled water reddish brown dorsally grading to yellowish white was provided on a piece of cotton. One to eight ventrally; compound eye silver; mandible tip dark red- L. argentinensis wasps (3Ð12 d old) were added to each dish brown; antenna light yellowish brown grading cage and allowed to remain for 1Ð3 d. Tests were apically to brown; front leg, middle leg, and hind tarsus conducted with both mated and virgin females. Cages light yellowish brown, hind leg otherwise brown; wing were held at 27 Ϯ 1ЊC, 70Ð85% RH, and 14:10 L:D membrane hyaline; venation pale yellowish brown photoperiod. Cocoons were removed daily and held except apex of vein CϩScϩR, apical 75% of stigma, individually in gelatin capsules under the conditions vein 1M, and base of vein RSϩM dark brown; basal described above until emergence. 25% of stigma and vein RS nearly clear. Head (Figs. 2 Another trial was conducted to better delineate and 3) with frons, vertex, temple, and gena highly parasitism rates of Þrst instar L. lineolaris and L. hes- perus. Four replicates were set up for Þrst instars of each host species. Each replicate consisted of three to Þve subsamples set up in the following manner. For each subsample, 10nymphs of each host were placed in a 600-ml transparent plastic food container (Solo Cup Co., Urbana, IL) with a ventilated lid. Several green beans were added, honey was streaked on the inside of the cage, and distilled water was provided on a piece of cotton. One mated L. argentinensis female wasp (3Ð12 d old) was added to each cage and allowed to remain for 30min. Cages were held at 25 Ϯ 1ЊC, 60Ð85% RH, and 14:10 L:D photoperiod. Cocoons were removed daily and held individually in gelatin capsules under the conditions described above until emergence. Single factor ANOVA (SAS Institute 2000) was used to test for differences in parasitism Fig. 2. Dorsal view of head, occipital carina, pronotum, rates between host species. and mesonotum, 170ϫ. November 2003 WILLIAMS ET AL.: NEW SPECIES OF Leiophron 837

Fig. 3. Dorsal view of head, occipital carina, and sculp- Fig. 5. Apex of ßagellum, 370ϫ. ture of pronotum, 270ϫ.

dially and laterally, punctate posteriorly; mesonotum polished and smooth, but with scattered minute setae smooth and highly polished, mostly devoid of setae, about as long as compound eye facets; face width notauli absent except for slight depressions at antero- equal to face height, shallowly punctate and more lateral corners of mesonotum; scutellum with furrow densely setose than frons, with setae about twice as 4-foveate, median disc smooth and highly polished, long as those of frons; shortest distance between eyes slightly convex; mesopleuron smooth dorsally, punc- equal to distance between tentorial pits; clypeus wide tate ventrally, with foveate sternalus situated antero- and narrow, with ventral margin bilobed, and lined ventrally; metanotum Þnely foveate, posterior margin with setae much longer than elsewhere on head, the smooth; forewing (Fig. 7) with stigma short and very longest of which are about equal to length of Þrst Ϸ ϫ broad, stigma length only two times medial width; Rs ßagellomere; malar space very narrow, 0.7 basal vein very short, strongly curved, and emerging di- width of mandible; antenna (Figs. 4 and 5) with 15 rectly from stigma with no trace of vein r, Rs descle- ßagellomeres, ßagellomere one three times longer rotized apically near wing margin; marginal cell along than wide; following ßagellomeres gradually shorter; wing margin 0.4 times stigma length; veins M, 1cu-a, ßagellomere 14 (penultimate) shortest, just barely and base of RSϩM distinctly sclerotized, but forewing longer than wide; ßagellomere 15 (ultimate) two venation otherwise absent; basal and subbasal cells of times longer than wide; ocellar triangle nearly equi- forewing glabrous, mostly devoid of setae; propodeum lateral, ocelli very small, distance between posterior Þnely reticulate areolate. Metasoma (Figs. 8 and 9) ocelli seven times ocellar width; ocellar-ocular dis- with tergum one coarsely longitudinally rugo-striate, tance also seven times ocellar width; gena at widest remainder of metasoma smooth and highly polished; point equal to widest eye width; occipital carina petiolate tergum one narrowest basally, gradually present laterally, but absent dorsally so occiput grades wider posteriorly, posterior width 1.3 times basal smoothly to vertex. Mesosoma (Fig. 6) with pronotum width, length 2.1 times longer than greatest posterior long and collar-like, pronotum length medially about width; ovipositor very short and thin, slightly curved, one-half head length, pronotum sculpture rugose me- exerted to a length 0.6 times hypopygium length.

Fig. 4. Antennal scape, pedicel, and base of ßagellum, 330ϫ. Fig. 6. Dorsal view of mesosoma, 230ϫ. 838 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 96, no. 6

Fig. 7. Anterior margin of forewing showing stigma and Fig. 9. Dorsal view of petiolate Þrst tergum and dorsal marginal cell, 95ϫ. carinae, 370ϫ.

Essentially as as holotype except coll. 10February; one male, same .(4 ؍ Variation, Paratype Females (n in holotype female except 14Ð15 ßagellomeres; head data as holotype except coll. 10February and em. color dorsally varying from yellowish or reddish 1 March; one male, same data as holotype except coll. brown to nearly black; mesonotum color varying from 10February and em. 24 February; eight males, same yellowish or reddish brown to black; body length vary- data as holotype except coll. 10February and em. ing from 1.5 to 2.2 mm depending on position of meta- 27 February; four females, Misiones Province, near soma at death. Dos de Mayo, ex. Taylorilygus nymph, em. 28 February Other than 2000, coll. sweeping Conyza on 10 February 2000; one .(41 ؍ Variation, Paratype Males (n primary genitalic differences between sexes, similar to male, same data except em. 25 February; two males, females except 15Ð17 ßagellomeres; malar space wider Misiones Province, San Javier on Rio Uruguay, ex. than in female, 0.8Ð0.9 times basal width of mandible; Taylorilygus nymph, em. 28 February 2000, coll. front and middle legs varying from yellow to brown; sweeping Conyza on 9 February 2000; one male, same hind coxa, femur, and tibia varying from brown to data except em. 3 March; seven males, Misiones Prov- nearly black; forewing varying from clear to slightly ince, eight km N. San Pedro by Rte. 20, ex. Taylorilygus dusky medially; tergum one length varying from 2.0to apicalis nymph, em. 17 December 1999, coll. sweeping 2.3 times longer than greatest posterior width. undetermined white composite in clearcut on 19 No- Type Data. HOLOTYPE female: ARGENTINA, vember 1999; one female, Misiones Province, Leandro Misiones Province, 30km N. Obera, Jct. Rte. 5 and 14 N. de Alem, ex. Taylorilygus nymph, em. 28 February (Lat. 27Њ28Ј59Љ S, Long. 55Њ06Ј50Љ W), ex. Taylorilygus 2000, coll. sweeping Conyza on 9 February 2000; one nymph, em. 25 February 2000, coll. sweeping Conyza male, Entre Rios Province, Rte. 14 near El Palmar Park bonariensis on 9 February 2000. L. Williams and and Nature Preserve, ex. Taylorilygus nymph, em. G. Logarzo. Deposited in University of Wyoming In- 1 March 2000, coll. sweeping Conyza on 11 February sect Museum, Laramie. PARATYPES: All specimens 2000; one male, Corrientes Province, Santo Tome near collected in Argentina by L. Williams and G. Logarzo. Rio Uruguay; ex. Taylorilygus apicalis nymph, em. one male, same data as holotype; four males, same data 13 December 1999, died December 1999; coll. sweep- ing “burr” weed (Acicarpha tribuloides) on 23 Novem- ber 1999; three males, Tucuman Province, 10km S. San Miguel de Tucuman by Rte. 38, ex. Taylorilygus api- calis nymph, em. 22 December 1999, coll. sweeping Labiatae (Hyptis lappacea) on 4 and 5 December 1999; one female, two males, Jujuy Province, 5 km S. Lib. Grl. San Martin by Rte. 34, ex. Taylorilygus apicalis nymph, em. 22 December 1999, coll. sweeping Conyza bonariensis and Parthenium sp. on 1 December 1999; one female, Jujuy Province, La Mendieta on Rte. 34, ex. Taylorilygus apicalis nymph, em. 3 January 2000, coll. sweeping Conyza bonariensis on 1 December 1999; one female, Jujuy Province, El Carmen on Rte. 9, ex. Taylorilygus apicalis nymph, em. 30December 1999, coll. sweeping Pterocaulon sp. on 2 December 1999; one male, Jujuy Province, 4 km N. Chalican by Rte. 34, ex. Taylorilygus apicalis nymph, em. 17 De- Fig. 8. Dorsal view of metasoma, 130ϫ. cember 1999, coll. sweeping Conyza bonariensis on November 2003 WILLIAMS ET AL.: NEW SPECIES OF Leiophron 839

Table 1. Host plant associations for mirids collected in four regions of Argentina and Paraguay, 1999–2001

No. mirids collected Host plant Northwest Northeast Buenos Aires Central Total Parthenium hysterophorus L. 10,126 0 0 0 10,126 Baccharis spp. 08071,528 02,335 Solidago chilensis Meyen 04,048 1,382 05,430 Mixed host plants 1,450799 520895 3,664 Conyza spp. 2,364 1,8401,133 05,337 Eupatorium spp. 249 1,495 8001,824 Gomphrena spp. 482 000482 Mikania cordifolia (Lf.) Willd. 405 100 0 0 505 Hyptis spp. 586 000586 Hypericum sp. 0362 0 0362 Gamochaeta spp. 404 217 0 32 653 Acicarpha tribuloides Juss 0150 0 0150 Flaveria bidentis (L.) Kuntze. 0220 0130350 Centratherum camporum Cass. 025 0 025 Sonchus oleraceus L. 065 0 065 Sphaeralcea bonariensis (Cav.) Griseb 500 0 0 0 500 Grindelia sp. 45 00045 Pterocaulon alopecuroides (Lam.) 3100 00310 Ambrosia tenuifolia Sprengel 0 200 0 0 200 Borreria verticillata (L.) G. Mey. 0 200 0 0 200 Labiatae 020 0 020 Stemodia verticillata (Mill.) Hassl. 050 0 050 Wedelia sp. 00 014 14 Physalis pubescens L. 1300 00130 Asteraceae (white ßowers) 0220 0 0220 Asteraceae 0 0 100 0 100 Senecio argentinus Baker 00 03 3 Commelina virginica L. 010 0 010 Total 17,051 10,818 4,743 1,074 33,686

2 December 1999; one male, Salta Province, Tartagal in L. fumipennis), mesopleuron with foveate sternau- on Rte. 34 at Hotel Portico Norte, ex. Taylorilygus lus (sternaulus hardly suggested and not foveate in apicalis nymph, em. 20December 1999, coll. sweeping L. fumipennis), smaller body size (2.9 mm in L. Conyza bonariensis on 2 December 1999; one female, fumipennis), ocellar-ocular distance is seven times Salta Province, San Ramon de La Nueva Oran by Rte. ocellar width (three times in L. fumipennis), and other 50, ex. Taylorilygus apicalis nymph, em. 20December differences. L. fumipennis is known only from Que´bec, 1999, coll. sweeping Parthenium sp. on 1 December Canada. Despite the widely separated distributions of 1999; one male, Salta Province, 23 km N. San Ramon these two species, their similarities in morphology are de La Nueva Oran by Rte. 50, ex. Taylorilygus apicalis remarkable. The wing venation of this new species is nymph, em. 29 December 1999, coll. sweeping Parthe- almost identical to that pictured for L. fumipennis by nium sp. on 1 December 1999. Paratypes deposited at Loan (1974), except that it has an even shorter stub of University of Wyoming Insect Museum (Laramie), the RSϩM vein. U.S. National Museum of Natural History (Washing- Host Plant-Mirid-Region Associations. We col- ton, DC), and Canadian National Collection (Ot- lected mirids from Ͼ30host plant species (Table 1). tawa). Most (Ϸ75%) of the mirids were collected from Þve Etymology. Named for the type locality in Argen- host plants: Parthenium hysterophorus L., Baccharis tina. spp., Solidago chilensis Meyen, Conyza spp., and Remarks. This new species is a typical member of Eupatorium spp. At least 10collections were made the genus Leiophron and can be keyed to genus with- from each of these host plants. Collections from mixed out difÞculty using the key provided by Shaw (1997). populations of hosts accounted for an additional 11% The Neotropical species have not been previously of the mirids collected. The remainder of the mirids studied, but the genus was revised for North America were collected from host plants encountered less fre- by Loan (1974). This new species can be assigned to quently (Table 1). the L. maculipennis species group, as deÞned by Loan More than 23 mirid species were collected during (1974), because of the reduced notauli, glabrous basal, the study (Tables 1 and 2). Taylorilygus apicalis and subbasal cells of the forewing and reduced fore- (Fieber) represented Ͼ80% of the mirids collected wing venation with only a trace of vein RSϩM basally. from all regions (Table 2). Five host plants harbored Of the four species that Loan assigned to that group, the majority (Ͼ77%) of T. apicalis: Parthenium hys- L. argentinensis is most similar to L. fumipennis Loan, terophorus (29%), Conyza spp. (20%), Solidago chil- but can be distinguished by its dorsally effaced occip- ensis (19%), Eupatorium spp. (6%), and Baccharis spp. ital carina (complete in L. fumipennis), light color on (3%). More than one-half of the mirids were collected the lower anterior parts of the head (head all brown in the northwest region. The northeast, Buenos Aires, 840A NNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 96, no. 6

Table 2. Abundance of mirid species collected in Argentina which L. argentinensis has evolved in Argentina and and Paraguay, 1999–2001 Paraguay are also present in the United States. Parasitism Levels. Parasitism rates for all host plant- No. Percent Mirid species collected of total mirid-collection date combinations are presented in Table 3. The majority (Ͼ85%) of L. argentinensis were Taylorilygus apicalis (Fieber) 26,84079.65 Phytocoris aspersus Carvalho and Gomes 8202.43 reared from T. apicalis (Table 3). However, L. argen- Horcias nobilellus (Berg) 362 1.07 tinensis also was reared from Garganus saltensis Berg Polymerus testaceipes (Stal) 200 0.59 and/or Taedia striolata (Bergroth) collected from Taedia striolata (Bergroth) 182 0.54 Gomphrena perennis L. (14 MarchÐ12 April 2000), and Orthotylus sp. 1300.39 Taedia stigmosa (Berg) 500.15 from mixed populations of mirids collected from Tupiocoris cucurbitaceus (Spinola) 31 0.09 Hyptis fasciculata Benth. (30 AprilÐ5 May 2000). Two Hyaliodocoris insignis (Stal) 24 0.07 L. argentinensis were reared from an unidentiÞed Tae- Taedia guttulosa (Reuter) 3 0.01 dia sp. collected on Gomphrena perennis (20Ð30April Taylorilygus apicalis and unidentiÞed 2,552 7.57 mirids 2001), and one L. argentinensis from an unidentiÞed Phytocoris aspersus and Taedia stigmosa 300 0.89 mirid collected on Commelina virginica L. (6Ð9 June (Berg) 2001). Some collections of mixed populations of Taylorilygus apicalis, and Phytocoris 2500.74 T. apicalis and other mirids also yielded L. argentinen- effictus Stal Taylorilygus apicalis, Phytocoris effictus, 2300.68 sis, and while deÞnitive designation of hosts is impos- Polymerus sp., and Dagbertus phaleratus sible in these cases, it is likely that T. apicalis served as (Berg) the host for some of these wasps. A hyperparasitoid, Taedia sp. 215 0.64 Mesochorus sp., also was reared but was not abundant Phytocoris sp. 2100.62 Ͻ Phytocoris subvittatus (Stal), Taedia 100 0.30 (overall parasitism 3%). This is similar to the hyper- signata Carvalho and Gomes, Horcias parasitism rates (1Ð11%) reported for M. curvulus nobilellus. Dagbertus phaleratus, Thomson (Day 2002). Henicocnemus tucumanus (Berg), and More detailed analyses of parasitism rates were Taylorilygus apicalis Garganus saltensis Berg and Taedia 82 0.24 conducted on the Þve host plants from which most striolata T. apicalis were collected. SigniÞcant differences in Phytocoris subvittatus and Taylorilygus 600.18 parasitism rates of T. apicalis were observed among apicalis these host plants (F ϭ 6.28; df ϭ 4, 29.4; P Ͻ 0.0009). Taylorilygus apicalis and Horcias 55 0.16 nobilellus The parasitism rate in Conyza spp. was nearly 16% and Phytocoris subvittatus, Taedia incaica 400.12 was signiÞcantly greater than observed in the other Carvalho and Gomes, Polymerus sp., host plants (Fig. 10). Parasitism rates were relatively and Horcias nobilellus high for some plants that were infrequently collected, Phytocoris sp. and unidentiÞed mirids 4 0.01 UnidentiÞed mirids 956 2.84 e.g., Sonchus oleraceus L., Ambrosia tenuifolia Spren- gel, and Hyptis spp. (Table 3). Parasitism rates of mirids did not differ among the four collection regions (F ϭ 0.87; df ϭ 3, 69.9; P ϭ and central regions had 32, 14, and 3% of the mirids, 0.4626). Percent parasitism in the different regions respectively. These differences reßected differential was: Buenos Aires, 8.63%; northwest, 7.93%; central, collecting efforts. 6.72%, and northeast, 5.21%. However, seasonal dif- The host plant-mirid associations described from ferences in parasitism rates of mirids were observed Argentina and Paraguay are similar to those in the (F ϭ 3.98; df ϭ 11, 36.9; P Ͻ 0.0007). Parasitism rates United States. Many of the plant bug genera collected peaked in the summer, were intermediate in the spring in this study have wide geographic ranges, which in- and fall, and were lowest in the winter (Fig. 11). clude the United States. For example, T. apicalis is Our results indicate that L. argentinensis can para- nearly cosmopolitan; it is known from North and sitize several species of mirids infesting numerous host South America and is widespread in the Old World plants. A strong association was observed between (Wheeler and Henry 1992). T. apicalis infests many of L. argentinensis and T. apicalis. We collected this wasp the same host plants in Argentina and Paraguay as it throughout the study area, from central to northern does in the United States (Knight 1941, Snodgrass et Argentina and southern Paraguay. Additional research al. 1984 a, b, Fontes et al. 1994). The genera Taedia, will be necessary to delineate the geographic range of Polymerus, and Phytocoris also occur in the United L. argentinensis and better understand its interactions States (Knight 1941, Snodgrass et al. 1984 a, b, Henry with host plant-mirid associations. Snodgrass et al. and Wheeler 1988, Rhainds et al. 2002). Many of the (1990) described L. schusteri Loan from specimens host plants that yielded mirids in the current study reared from T. vosserleri (Poppius) and T. virens (Tay- (e.g., P. hysterophorus, Conyza spp., Eupatorium spp., lor) nymphs in Kenya. L. schusteri also developed on Solidago spp., Baccharis spp., and Sonchus spp.) also L. lineolaris, L. hesperus, and T. pallidulus (ϭT. api- occur in the United States (Brako et al. 1997), where calis) in the laboratory. they are infested by T. apicalis, and species of Taedia, Parasitism rates of Þeld-collected nymphs were Polymerus, and Phytocoris (Knight 1941, Snodgrass et highly variable, ranging from 0to 37%, and were sim- al. 1984 a, b, Wheeler 2001, Rhainds et al. 2002). These ilar to parasitism levels reported in other studies results suggest that the host plant-mirid associations in where parasitism was assessed by rearing. Parasitism of November 2003 WILLIAMS ET AL.: NEW SPECIES OF Leiophron 841

Table 3. Seasonal parasitism, assessed by rearing, by L. argentinensis Shaw of mirid nymphs collected on different host plants

No. No. Percent Year Collection dates Host plant Host mirid nymphs cocoons parasitism 1999 19 NovemberÐ4 December Sonchus oleraceus L. Taylorilygus apicalis (Fieber) 65 24 36.9 Hyptis lappacea Benth Taylorilygus apicalis 304 76 25.0 Conyza bonariensis (L.) Cronquist Taylorilygus apicalis 286 28 9.79 Parthenium hysterophorus L. Taylorilygus apicalis 503 6.00 Acicarpha tribuloides Juss Taylorilygus apicalis 1506 4.00 Centratherum camporum (ϭcamporum) Taylorilygus apicalis 25 1 4.00 Cass. Pterocaulon alopecuroides (Lam.) Taylorilygus apicalis 31011 3.55 P. hysterophorus & Chenopodium album L. Taylorilygus apicalis 315 103.17 C. bonariensis & P. hysterophorus Taylorilygus apicalis 259 6 2.32 C. bonariensis, P. hysterophorus & C. album Taylorilygus apicalis 1301 0.77 Sphaeralcea bonariensis (Cav.) Griseb UnidentiÞed mirid 500 0 0 Carthamus tinctorius L. & C. album UnidentiÞed mirid 5000 Grindelia sp. UnidentiÞed mirid 45 00 C. bonariensis & Ambrosia tenuifolia Taylorilygus apicalis 115 00 Sprengel 21Ð22 December Ambrosia tenuifolia Taylorilygus apicalis 200 48 24.0 C. bonariensis Taylorilygus apicalis 101 10.0 Hypericum sp. Horcias nobilellus (Berg) 35000 2000 28 JanuaryÐ11 February Baccharis medulosa DC. Taylorilygus apicalis 102 20.0 C. bonariensis Taylorilygus apicalis 1,848 283 15.3 Solidago chilensis L. Taylorilygus apicalis 35 00 Borreria verticillata (L.) G. Mey. Polymeris testaceipes (Stal) 200 0 0 Labiatae UnidentiÞed mirid 2000 14 MarchÐ12 April Gomphrena perennis L. Garganus saltensis (Berg), 65 12 18.5 Taedia striolata (Bergroth) C. bonariensis Taylorilygus apicalis 1,170179 15.3 Eupatorium oblongifolium (Spreng.) Baker Taylorilygus apicalis 63056 8.88 Solidago chilensis Taylorilygus apicalis 2,593 226 8.72 C. bonariensis and P. hysterophorus Taylorilygus apicalis 1,020 78 7.65 B. medulosa and C. bonariensis Taylorilygus apicalis 26017 6.54 S. chilensis & Eupatorium macrocephalum Taylorilygus apicalis 400 20 5.00 Less. S. chilensis and Ambrosia tenuifolia Taylorilygus apicalis 200 10 5.00 P. hysterophorus Taylorilygus apicalis 4,040 97 2.40 UnidentiÞed composite species 2 Taylorilygus apicalis 801 1.25 Gomphrena perennis Taedia striolata 117 00 Stemodia verticillata (Mill.) Hassl. Taedia stigmosa (Berg) 5000 S. chilensis and Stevia multiaristata Spreng. Taylorilygus apicalis 300 0 0 30AprilÐ5 May Mikania cordifolia (Lf.) Willd. Phytocoris subvittatis (Stal), 100 24 24.0 Taedia signata Carvalho and Gomes, Horcias nobilellus, Dagbertus phaleratus (Berg), Henicocnemus tucumanus (Berg), Taylorilygus apicalis Wedelia sp. Taylorilygus apicalis 14 3 21.4 Hyptis fasciculata Benth. Taylorilygus apicalis, 22017 7.73 Phytocoris effictus Stal, Polymerus sp., Dagbertus phaleratus Mikania cordifolia Taylorilygus apicalis 245 13 5.31 S. chilensis Taylorilygus apicalis 22011 5.00 Hyptis fasciculata Phytocoris subvittatis, Taedia 402 5.00 incaica Carvalho and Gomes, Polymerus sp., Horcias nobilellus P. hysterophorus Taylorilygus apicalis, 25011 4.40 Phytocoris effictus P. hysterophorus Taylorilygus apicalis, 602 3.33 Phytocoris subvitattus P. hysterophorus Taylorilygus apicalis 2,67086 3.22 P. hysterophorus UnidentiÞed mirid 25 00 Flaveria bidentis (L.) Kuntze. Taylorilygus apicalis 35000 Gomphrena pulchella Mart. Taedia guttulosa (Reuter) 3 00 (Continued) 842 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 96, no. 6

Table 3. Continued

No. No. Percent Year Collection dates Host plant Host mirid nymphs cocoons parasitism Gomphrena perennis Garganus saltensis, Taedia 17 00 striolata Gomphrena perennis Taedia striolata 65 00 Physalis pubescens L. Orthotylus sp. 13000 Eupatorium laevigatum Lam. Taylorilygus apicalis 45 00 Eupatorium inuleifolia Kunth Taylorilygus apicalis, 55 00 Horcias nobilellus Baccharis medulosa Taylorilygus apicalis 11000 Eupatorium oblongifolium Taylorilygus apicalis 22000 20JuneÐ6 July Eupatorium inuifolium Taylorilygus apicalis 803 3.75 S. chilensis and B. dracunculifolia DC. Taylorilygus apicalis 601 1.66 S. chilensis, C. bonariensis & Eupatorium sp. Taylorilygus apicalis 6000 UnidentiÞed Asteraceae Phytocoris aspersus Carvalho 100 0 0 and Gomes B. dracunculifolia Phytocoris aspersus, Taedia 300 0 0 stigmosa B. dracunculifolia Phytocoris aspersus 42000 Baccharis sp. Phytocoris aspersus 300 0 0 28 AugustÐ1 September Parthenium hysterophorus Taylorilygus apicalis 38 8 21.1 Conyza sp. & Gamochaeta falcate (Lam.) Taylorilygus apicalis 246 24 9.76 Cabrera Gamochaeta pensylvanica (Willd.) Cabrera Taylorilygus apicalis 621 59 9.50 Eupatorium hecatanthum (DC.) Taylorilygus apicalis 205 1 0.49 Gamochaeta sp. Taylorilygus apicalis 32 1 0.31 Eupatorium hecatanthum Tupiocoris cucurbitaceus 31 00 (Spinola) Senecio argentinus Baker Taylorilygus apicalis 300 2001 6Ð12 January Parthenium hysterophorus Taylorilygus apicalis 1103027.3 Conyza sp. Taylorilygus apicalis 2,078 403 19.4 19Ð25 March Solidago chilensis Taylorilygus apicalis and 11018 16.4 unidentiÞed mirid S. chilensis & Conyza sp. Taylorilygus apicalis 12018 15.0 S. chilensis & Mikania cordifolia Taylorilygus apicalis and 11016 14.5 unidentiÞed mirid Solidago chilensis Taylorilygus apicalis and 23026 11.3 unidentiÞed mirid Solidago chilensis Taylorilygus apicalis 1,345 56 4.16 10April Solidago chilensis Taylorilygus apicalis 341 48 14.1 20Ð30 April Solidago chilensis Taylorilygus apicalis 556 117 21.0 Parthenium hysterophorus Taylorilygus apicalis and 780143 18.3 unidentiÞed mirid Parthenium hysterophorus Taylorilygus apicalis and 75071 9.47 unidentiÞed mirid B. dracunculifolia Taylorilygus apicalis 35026 7.43 Baccharis medulosa and B. coridifolia DC. Taylorilygus apicalis 1309 6.92 Mikania cordifolia Taylorilygus apicalis and 603 5.00 unidentiÞed mirid Parthenium hysterophorus Taylorilygus apicalis and 400 14 3.50 unidentiÞed mirid Parthenium hysterophorus Taylorilygus apicalis 985 13 1.32 Gomphrena perennis Taedia sp. 216 2 0.93 Baccharis medulosa and B. coridifolia UnidentiÞed mirid 1000 Conyza sp. Taylorilygus apicalis 55 00 B. dracunculifolia UnidentiÞed mirid 1000 Baccharis spicata (Lam.) Baill. and Conyza sp. Taylorilygus apicalis 22000 Eupatorium candolleanum Hook. Et Arn. Taylorilygus apicalis 300 0 0 Eupatorium christieanum Baker Taylorilygus apicalis 400 0 0 Mikania cordifolia Taylorilygus apicalis and 100 0 0 unidentiÞed mirid Baccharis medulosa (male) Taylorilygus apicalis 25000 Parthenium hysterophorus UnidentiÞed mirids 33 00 Hyptis fasciculata Taylorilygus apicalis and 12 00 unidentiÞed mirid Eupatorium odoratum L. UnidentiÞed mirid 13 00 6Ð9 June Baccharis punctulata DC. Taylorilygus apicalis 908 8.89 Eupatorium inulifolium Taylorilygus apicalis 65 2 3.08 B. dracunculifolia Taylorilygus apicalis 35 1 0.29 Commelina virginica L. UnidentiÞed mirid 101 0.10 (Continued) November 2003 WILLIAMS ET AL.: NEW SPECIES OF Leiophron 843

Table 3. Continued

No. No. Percent Year Collection dates Host plant Host mirid nymphs cocoons parasitism B. dracunculifolia Phytocoris sp. 205 0 0 Baccharia trimera (Less.) DC. Taylorilygus apicalis 100 0 Baccharia trimera Phytocoris sp. 5 00 B. dracunculifolia and B. medulosa Taylorilygus apicalis 500 B. dracunculifolia and B. medulosa Phytocoris sp. and unidentiÞed 400 mirid Baccharis punctulata UnidentiÞed mirid 2400 0

Lygus spp. by L. uniformis (Gahan) in California some- toids for identiÞcation and host acceptance trials with times reached levels of 25Ð50% in weeds but never Lygus spp., as well as information on sex ratios and exceeded 11% in alfalfa (Clancy and Pierce 1966). Day diapause. In studies that have used both methods con- and Saunders (1990) reported average parasitism rates currently, parasitism levels assessed by dissection are of 4Ð28% for L. uniformis on Halticus bractatus (Say) considerably higher than those determined by rearing infesting alfalfa in the northeastern United States. Par- (Day 1994, 1999, Day et al. 1999, Tilmon et al. 2000). asitism rates of L. lineolaris by Peristenus spp. averaged For example, Day (1994) reported that parasitism of nearly 14% in the northeastern United States (Tilmon plant bug nymphs was 44% higher as assessed by dis- et al. 2000). When parasitism has been assessed by section than by rearing, and Tilmon et al. (2000) found more accurate methods (i.e., by dissection and/or that dissection resulted in 58% higher parasitism than molecular methods), parasitism levels generally ex- did rearing. Therefore, our assessment of parasitism by ceeded those of the current study (Snodgrass and L. argentinensis probably underestimated the true lev- Fayad 1991, Day 1994, 1999, Day et al. 1999, Tilmon et els of parasitism. al. 2000). Sex Ratio of L. argentinensis. Tests for equal sex Studies of host-parasitoid interactions and biologi- ratios of nondiapausing L. argentinensis showed sig- cal control require accurate assessment of host mor- niÞcant differences in each month for which data were tality. The two methods most frequently used, dissec- available. In December 1999, the sex ratio was male- ϭϪ ϭ tion of hosts and rearing of adult parasitoids from biased (0.22:1 female:male; Z0.05(2),22 2.985, P hosts, each have distinct advantages and disadvantages 0.0028). In February 2000, a similar trend was ob- ϭϪ ϭ (Day 1994). Rearing adult parasitoids permits their served (0.35:1 female:male; Z0.05(2),23 2.294, P identiÞcation, provides information on diapause of the 0.0218). In March 2000, however, the sex ratio was host and/or parasitoid, and usually requires less tech- signiÞcantly female-biased (1.75:1 female:male; ϭ ϭ nical expertise than dissection. Dissection, however, Z0.05(2),66 2.216, P 0.0267). These sex ratios dif- avoids most of the confounding mortality inherent in fered signiÞcantly between months (␹2 ϭ 19.65; df ϭ rearing and therefore provides more accurate host 2; P Ͻ 0.0001). SigniÞcant differences were observed mortality data. Dissection also yields a more rapid for comparisons between March 2000 and December measurement of parasitism than does rearing. We used 1999 (␹2 ϭ 14.43; df ϭ 1; P Ͻ 0.0001) and between the rearing method because it provided adult parasi- March 2000 and February 2000 (␹2 ϭ 9.903; df ϭ 1; P ϭ 0.0017). The comparison between December 1999 and

Fig. 10. Percent parasitism of T. apicalis nymphs by L. argentinensis on Þve abundant host plants. Means with the Fig. 11. Seasonal parasitism levels of T. apicalis nymphs same letter are not signiÞcantly different (P Ͻ 0.05). by L. argentinensis, 1999Ð2001. 844 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 96, no. 6

February 2000 was not signiÞcant (␹2 ϭ 0.409; df ϭ 1; P ϭ 0.5224). Sex ratios of diapausing L. argentinensis showed sig- niÞcant differences in each month for which data were available. In December 1999, the sex ratio was male- ϭ Ͻ biased (0.80:1 female:male; Z0.05(2),36 6.00, P 0.0001). In February 2000, a similar trend was ob- ϭ Ͻ served (0.65:1 female:male; Z0.05(2),38 6.1644, P 0.0001). In March 2000, the sex ratio was signiÞcantly ϭ female-biased (1.36:1 female:male; Z0.05(2),229 15.133, P Ͻ 0.0001). In May 2000, a female-biased trend ϭ was also observed (1.83:1 female:male; Z0.05(2),34 5.8310, P Ͻ 0.0001). These sex ratios did not differ signiÞcantly across the 4 mo (␹2 ϭ 7.26; df ϭ 3; P ϭ 0.0640). SigniÞcant differences in the sex ratios of diapausing wasps were observed for comparisons be- tween February 2000 and March 2000 (␹2 ϭ 4.33; df ϭ 1; P ϭ 0.0374) and between February 2000 and March 2000 (␹2 ϭ 4.63; df ϭ 1; P ϭ 0.0315). Other compar- Fig. 12. Seasonal incidence of diapause by L. argentinen- Ͼ sis, 1999Ð2001. Means with the same letter are not signiÞ- isons between months were not signiÞcant (P 0.05). cantly different (P Ͻ 0.05). Lines indicate daylength at 34Њ30Ј For December 2000, sex ratios differed signiÞcantly (●) and 22Њ30Ј (e) south latitude. between diapausing and nondiapausing wasps (␹2 ϭ 4.40; df ϭ 1; P ϭ 0.0359). SigniÞcant differences were not observed for February 2000 or March 2000 (P Ͼ 2to20%forL. lineolaris and from 14 to 32% for 0.05). L. hesperus. Parasitism rates for second-instar L. hes- Sex ratios of L. argentinensis were male-biased in the perus ranged from 8 to 46%. For Þrst instars of L. summer, changing to female-biased in the fall. This lineolaris and L. hesperus combined, the developmen- pattern of seasonal variation in sex ratio might be tal time (mean Ϯ SD) from stinging to formation of attributed to a high proportion of virgin oviposition or cocoon was 14.27 Ϯ 1.79 d (n ϭ 11) and for second- differential sex allocation by mated females. Similar instar L. hesperus was 13.49 Ϯ 1.43 d (n ϭ 41). For Þrst transitions from female-biased sex ratios in the spring instars of L. lineolaris and L. hesperus combined, the to male-biased sex ratios in the fall are known (God- time from formation of cocoon to emergence was fray and Shaw 1987, Allen et al. 1994). Additional 23.5 Ϯ 0.71 d (n ϭ 2) and 22.53 Ϯ 1.68 d (n ϭ 15) for studies are necessary to conÞrm that the observed second-instar L. hesperus. These developmental times seasonal pattern of sex ratio change in L. argentinensis are similar to those reported for P. digoneutis Loan is consistent over several seasons. (Carignan et al. 1995), but are longer than those for Diapause of L. argentinensis. The proportion of dia- P. digoneutis reared under different conditions or for pausing L. argentinensis was monitored throughout the other euphorines (Loan 1965, Lim and Stewart 1976, study, and differed signiÞcantly between months Snodgrass et al. 1990). The observed differences in (␹2 ϭ 204.4; df ϭ 7; P Ͻ 0.0001; Fig. 12). When hosts developmental times between euphorine species were collected during the summer (i.e., November, might reßect different growth rates between species, December, and February), the proportion of diapaus- variable host size, and slight differences in rearing ing wasps was Ϸ40% (Fig. 12). When hosts were col- conditions. lected in the fall and winter (i.e., March through Results of the trial using Þrst instars of L. lineolaris September), the proportion of diapausing wasps av- and L. hesperus indicated that both mirids were eraged Ϸ80% (Fig. 12). equally accepted as hosts (P Ͼ 0.05). For this study, Our results indicate that L. argentinensis is multi- the parasitism rate for L. lineolaris was 21.3% and for voltine and suggest that this wasp undergoes an oblig- L. hesperus was 23.0%. L. argentinensis was successfully atory diapause when photoperiod is short as do several reared through F2 generation on both L. lineolaris and species of Peristenus and L. uniformis (Clancy and L. hesperus before the colony was intentionally ter- Pierce 1966, Day 1987, Day and Saunders 1990, Day minated. 1999, Day et al. 1999). Snodgrass et al. (1990) found no That L. argentinensis accepted L. lineolaris and evidence of diapause in L. schusteri when reared under L. hesperus and successfully developed on these hosts laboratory conditions. Clancy and Pierce (1966) re- through two generations suggests that this parasitoid ported that L. uniformis larvae were found in all has potential for biological control of these pests in the months except December through March and that the United States. Although the entire geographic range of proportion of each generation undergoing adult dia- L. argentinensis is not currently known, this wasp pause in the cocoons increased in the fall. clearly inhabits wide geographic and climatic ranges Parasitization of Lygus spp. by L. argentinensis. Re- in Argentina and Paraguay (from at least Ϸ22Ð35Њ S sults from the preliminary trial indicated that L. ar- latitude), suggesting that much of the United States gentinensis successfully parasitized L. lineolaris and would be suitable habitat for this parasitoid. Multivol- L. hesperus. Parasitism rates of Þrst instars ranged from tinism and the lack of obligate diapause also are at- November 2003 WILLIAMS ET AL.: NEW SPECIES OF Leiophron 845 tributes of L. argentinensis. Moreover, this wasp occurs tance and biological control of Lygus and Adelphocoris in on many of the same host plants that are infested by North America. U.S. Department of Agriculture. L. lineolaris and L. hesperus, which would facilitate Day, W. H. 1994. Estimating mortality caused by parasites early-season suppression of bugs in spring weeds and diseases of : comparisons of the dissection and before dispersal into cotton. However, concerns rearing methods. Environ. Entomol. 23: 543Ð550. about nontarget effects of introduced species (FAO Day, W. H. 1996. Evaluation of biological control of the 1997, Van Driesche and Hoddle 1997), especially in tarnished plant bug (Hemiptera: Miridae) in alfalfa by the introduced parasite Peristenus digoneutis (Hymenoptera: a “new-association” strategy, suggest further re- Braconidae). Environ. Entomol. 25: 512Ð518. search before introduction of L. argentinensis is con- Day, W. H. 1999. Host preferences of introduced and native templated. Investigations of host-range evaluation parasites (Hymenoptera: Braconidae) of phytophagous and parasitoid competition will lead to a better plant bugs (Hemiptera: Miridae) in alfalfa-grass Þelds in understanding of the potential risks to nontarget the northeastern USA. BioControl. 44: 249Ð261. mirids and native euphorines (Kuhlmann et al. 1998; Day, W. H. 2002. Biology, host preferences, and abundance LaChance et al. 2001). These studies are planned, as of Mesochorus curvulus (Hymenoptera: Ichneumonidae), is the development of a polymerase chain reaction a hyperparasite of Peristenus spp. (Hymenoptera: Bra- (PCR)-based approach for early detection and conidae) parasitizing plant bugs (Miridae: Hemiptera) in identiÞcation of L. argentinensis and other eupho- alfalfa-grass forage crops. Ann. Entomol. Soc. Am. 95: rine parasitoids. 218Ð222. Day, W. H., and L. B. Saunders. 1990. Abundance of the garden ßeahopper (Hemiptera: Miridae) on alfalfa and parasitism by Leiophron uniformis (Gahan) (Hymenop- Acknowledgments tera: Braconidae). J. Econ. Entomol. 83: 101Ð106. We thank V. Francisco for technical assistance and J. E. Day, W. H., R. C. Hedlund, L. B. Saunders, and D. Coutinot. Powell and F. M. Williams for coordination of quarantine 1990. Establishment of Peristenus digoneutis (Hymenop- procedures. We also thank the following individuals for tax- tera: Braconidae), a parasite of the tarnished plant bug onomic determinations: D. Carpintero and T. J. Henry (Hemiptera: Miridae), in the United States. Environ. En- (mirids), S. M. Bonaventura and P. Hoc (host plants), and tomol. 19: 1528Ð1533. D. Wahl (Mesochorus). We are grateful to H. Goulet for Day, W. H., C. R. Baird, and S. R. Shaw. 1999. New, native examining the holotype of L. fumipennis and conÞrming the species of Peristenus (Hymenoptera: Braconidae) para- distinctness of L. argentinensis. Lygus nymphs were kindly sitizing Lygus hesperus (Hemiptera: Miridae) in Idaho: provided by A. C. Cohen and G. L. Snodgrass. Constructive biology, importance, and description. Ann. Entomol. Soc. comments on the manuscript were given by W. H. Day, Am. 92: 370Ð375. H. Goulet, T. J. Henry, G. L. Snodgrass, A. G. Wheeler, Jr., and Day, W. H., K. J. Tilmon, R. F. Romig, A. T. Eaton, and K. D. anonymous reviewers. Murray. 2000. Recent range expansions of Peristenus digoneutis (Hymenoptera: Braconidae), a parasite of the tarnished plant bug (Hemiptera: Miridae), and high tem- References Cited peratures limiting its geographic distribution in North America. J. NY Entomol. Soc. 108: 326Ð331. Allen, G. R., D. J. Kazmer, and R. F. Luck. 1994. Postcopu- Debolt, J. W. 1981. Laboratory biology and rearing of Leio- latory male behaviour, sperm precedence and multiple phron uniformis (Gahan) (Hymenoptera: Braconidae), a mating in a solitary parasitoid wasp. Anim. Behav. 48: parasite of Lygus spp. (Hemiptera: Miridae). Ann. Ento- 635Ð644. mol. Soc. Am. 74: 334Ð337. Brako, L., A. Y. Rossman, and D. F. Farr. 1997. ScientiÞc and [FAO] Food and Agriculture Organization. 1997. Code of common names of 7,000 vascular plants in the United conduct for the import and release of exotic biological States. Publication No. 7, Contributions from the U. S. control agents. Biol. News Inform. 18: 119NÐ124N. National Fungus Collections, American Phytopathologi- Fontes, E.M.G., D. H. Habeck, and F. Slansky, Jr. 1994. cal Society Press, St. Paul, MN. Phytophagous insects associated with goldenrods (Soli- Broadbent, A. B., H. Goulet, J. W. Whistlecraft, S. LaChance, dago spp.) in Gainesville, Florida. Fla. Entomol. 77: 209Ð and P. G. Mason. 1999. First Canadian record of three 221. parasitoid species (Hymenoptera: Braconidae: Euphori- nae) of the tarnished plant bug (Hemiptera: Miridae). Godfray, H.J.C., and M. R. Shaw. 1987. Seasonal variation in Proc. Entomol. Soc. Ont. 130: 109Ð111. the reproductive strategy of the parasitic wasp Eulophus Carignan, S., G. Boivin, and R. K. Stewart. 1995. Develop- larvarum (Hymenoptera: Chalcidoidea: Eulophidae). mental biology and morphology of Peristenus digoneutis Ecol. Entomol. 12: 251Ð256. Loan (Hymenoptera: Braconidae: Euphorinae). Biol. Hardee, D. D., J. W. Van Duyn, M. B. Layton, and R. D. Control. 5: 553Ð560. Bagwell. 2001. Bt cotton and management of the to- Clancy, D. W., and H. D. Pierce. 1966. Natural enemies of bacco budworm-bollworm complex. U.S. Department of some Lygus bugs. J. Econ. Entomol. 59: 853Ð858. Agriculture. Craig, C. H., and C. C. Loan. 1987. Biological control efforts Hedlund, R. C. 1987. Foreign exploration for natural ene- on Miridae in Canada, pp. 48Ð53. In R. C. Hedlund and mies of Lygus and Adelphocoris plant bugs, pp. 76Ð81. In H. M. Graham (eds.), Economic importance and biolog- R. C. Hedlund and H. M. Graham (eds.), Economic im- ical control of Lygus and Adelphocoris in North America. portance and biological control of Lygus and Adelphocoris U.S. Department of Agriculture. in North America. U.S. Department of Agriculture. Day, W. H. 1987. Biological control efforts against Lygus Henry, T. J., and A. G. Wheeler, Jr. 1988. Family Miridae and Adelphocoris infesting alfalfa in the United States, Hahn, 1833 (ϭCapsidae Burmeister): the plant bugs, pp. with notes on other associated species, pp. 20Ð39. In R. C. 251Ð507. In T. J. Henry and R. C. Froeschner (eds.), Hedlund and H. M. Graham (eds.), Economic impor- Catalog of the Heteroptera, or true bugs of Canada and 846 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 96, no. 6

the continental United States. Brill, Leiden, The Neth- Scott, D. R. 1977. An annotated listing of host plants of Lygus erlands. hesperus Knight. Bull. Entomol. Soc. Am. 23: 19Ð22. Hokkanen, H.M.T., and D. Pimentel. 1989. New associa- Sharkey, M. J. and R. A. Wharton. 1997. Morphology and tions in biological control: theory and practice. Can. En- terminology, pp. 19Ð38. In R. A. Wharton, P. M. Marsh, tomol. 121: 829Ð840. and M. J. Sharkey (eds.), Manual of the New World Knight, H. K. 1941. The plant bugs, or Miridae, of Illinois. genera of the family Braconidae. Special Publication No. Bull. Illinois Nat. Hist. Surv. 22: 1Ð234. 1. International Society of Hymenopterists, Washington, Kuhlmann, U., P. G. Mason, and D. J. Greathead. 1998. DC. Assessment of potential risks for introducing European Shaw, S. R. 1997. Subfamily Euphorinae, pp. 235Ð256. In Peristenus species as biological control agents of native R. A. Wharton, P. M. Marsh, and M. J. Sharkey (eds.), Lygus species in North America: a cooperative approach. Manual of the New World genera of the family Bra- Biol. News Inform. 19: 83NÐ90N. conidae. Special Publication No. 1. International Society LaChance, S., A. B. Broadbent, and M. K. Sears. 2001. In- of Hymenopterists, Washington, DC. host compatibility and in-host competition of exotic and Snodgrass, G. L., and Y. H. Fayad. 1991. Euphorine (Hyme- native parasitoids of the tarnished plant bug (Heterop- noptera: Braconidae) parasitism of the tarnished plant tera: Miridae). Environ. Entomol. 30: 1158Ð1163. bug (Heteroptera: Miridae) in areas of Washington Lim, K. P., and R. K. Stewart. 1976. Laboratory studies on County, Mississippi disturbed by agricultural production. Peristenus pallipes and P. pseudopallipes (Hymenoptera: J. Entomol. Sci. 26: 350Ð356. Braconidae), parasitoids of the tarnished plant bug, Lygus Snodgrass, G. L., W. P. Scott, and J. W. Smith. 1984a. An lineolaris (Hemiptera: Miridae). Can. Entomol. 108: 815Ð annotated list of the host plants of Lygus lineolaris 821. (Hemiptera: Miridae) in the Arkansas, Louisiana, and Loan, C. C. 1965. Life cycle and development of Leiophron Mississippi delta. J. Ga. Entomol. Soc. 19: 93Ð101. Snodgrass, G. L., W. P. Scott, and J. W. Smith. 1984b. Host pallipes Curtis (Hymenoptera: Braconidae, Euphorinae) plants and seasonal distribution of the tarnished plant bug in Þve mirid hosts in the Belleville district. Proc. Entomol. (Heteroptera: Miridae) in the delta of Arkansas, Louisi- Soc. Ont. 95: 115Ð121. ana, and Mississippi. Environ. Entomol. 13: 110Ð116. Loan, C. C. 1974. The North American species of Leiophron Snodgrass, G. L., C. C. Loan, and H. M. Graham. 1990. New Nees, 1818 and Peristenus Foerster, 1862 (Hymenoptera: species of Leiophron (Hymenoptera: Braconidae, Eu- Braconidae, Euphorinae) including description of 31 new phorinae) from Kenya. Fla. Entomol. 73: 492Ð496. species. Nat. Can. 101: 821Ð860. Tilmon, K. J., B. N. Danforth, W. H. Day, and M. P. Hoffman. Norton, A. P., S. C. Welter, J. L. Flexner, C. G. Jackson, J. W. 2000. Determining parasitoid species composition in a Debolt, and C. Pickel. 1992. Parasitism of Lygus hesperus host population: a molecular approach. Ann. Entomol. (Miridae) by Anaphes iole (Mymaridae) and Leiophron Soc. Am. 93: 640Ð647. uniformis (Braconidae) in California strawberry. Biol. Van Driesche, R. G., and T. S. Bellows, Jr. 1996. Biological Control. 2: 131Ð137. control. Chapman & Hall, New York. Pimentel, D. 1963. Introducing parasites and predators to Van Driesche, R. G., and M. Hoddle. 1997. Should arthro- control native pests. Can. Entomol. 95: 785Ð792. pod parasitoids and predators be subject to host range Pimentel, D. 1991. DiversiÞcation of biological control testing when used as biological control agents? Agric. strategies in agriculture. Crop Prot. 10: 243Ð253. Hum. Val. 14: 211Ð226. Rhainds, M., T. Taft, G. English-Loeb, R. Dunst, and T. Van Steenwyk, R. A., and V. M. Stern. 1977. Propagation, Weigle. 2002. Ecology and economic impact of two release, and evaluation of Peristenus stygicus, a newly plant bugs (Hemiptera: Miridae) in commercial vine- imported parasite of lygus bugs. J. Econ. Entomol. 70: yards. J. Econ. Entomol. 95: 354Ð359. 66Ð69. Ruberson, J. R., and L. H. Williams, III. 2000. Biological Wheeler, A. G., Jr. 2001. Biology of the plant bugs: pests, control of Lygus spp.: a component of areawide manage- predators, opportunists. Cornell University Press, Ithaca, ment. Southwest. Entomol. Suppl. 23: 96Ð110. NY. SAS Institute 2000. SAS/STAT userÕs guide, release 8.01 edi- Wheeler, A. G., Jr., and T. J. Henry. 1992. A synthesis of the tion. Cary, NC. Holarctic Miridae (Heteroptera): distribution, biology, Schuster, M. F. 1987. Biological control of plant bugs in and origin, with emphasis on North America. Thomas Say cotton, pp. 13Ð19. In R. C. Hedlund and H. M. Graham Found. Monogr. vol. 15. Entomological Society of Amer- (eds.), Economic importance and biological control of ica, Lanham, MD. Lygus and Adelphocoris in North America. U.S. Depart- Young, O. P. 1986. Host plants of the tarnished plant bug, ment of Agriculture. Lygus lineolaris (Heteroptera: Miridae). Ann. Entomol. Schwartz M. D., and R. G. Foottit. 1998. Revision of the Soc. Am. 79: 747Ð762. Nearctic species of the genus Lygus Hahn, with a review of the Palaearctic species (Heteroptera: Miridae). Mem- oirs in Entomology, International, vol. 10. Associated Received for publication 26 April 2003; accepted 30 July Publishers, Gainesville, FL. 2003.