Historic, Archive Document

Do not assume content reflects current scientific knowledge, policies, or practices.

UO (jr . ^

United States Department of Economic Importance and Agriculture

Agricultural Research Biological Control of Lygus Service ARS-64 and Adelphocoris in December 1987

Cl North America |2^4A7 , .

ABSTRACT

Hedlund, R.C., and H.M. Graham, editors. 1987. Economic Importance and Biological Control of Lygus and Adelphocoris in North America. U.S. Department of Agriculture, Agricultural Research Service, ARS-64, 95 pp.

This publication contains a series of reports on the status of Lygus spp. and Adelphocoris lineolatus (Goeze) as pests of several crops in North America. Past efforts at controlling these pests by predaceous and parasitic arthropods are reviewed and some new work is documented. In addition, there are sections on the taxonomy of the pests and euphorine braconids that parasitize them. Recommendations are made for future work on the biological control of these pests.

KEYWORDS: Adelphocoris spp., biological control, Braconidae, Diptera, Hemiptera,

Hymenoptera, Ichneumonidae , Lygus spp., Mermithidae, Miridae, Mymaridae, Nematoda, parasitic insects, predaceous insects, Tachinidae.

Copies of this publication may be purchased from the National Technical Information Service, 5285 Port Royal Road, Springfield, VA 22161.

ARS has no additional copies for free distribution United States Department of Economic Importance and Agriculture

Agricultural Biological Control of Lygus Research Service and Adelphocoris in ARS-64 North America

Editors

R.C. Hedlund H.M. Graham

ati0na ' A9riCU" NALBfdg UralLibrary 0301 Baltimore Blvd Beltsville, MD 20705-2351

CONTENTS

Studies on the biological control of plant bugs (Heteroptera: Miridae): An introduction and history, 1961-83 Jack R. Coulson 1

Biological control of plant bugs in cotton M.F. Schuster 13

Biological control efforts against Lygus and Adelphocoris spp. infesting alfalfa in the United States, with notes on other associated mirid species W.H. Day 20

Biological control of lygus bugs on vegetable and fruit crops D.R. Scott 40

Biological control efforts on Miridae in Canada C. Harvey Craig and Conrad C. Loan 48

Taxonomic status, biological attributes, and recommendations for future work on the genus Lygus (Heteroptera: Miridae) Thomas J. Henry and John D. Lattin 54

Euphorine parasites of Lygus and Adelphocoris (Hymenoptera: Braconidae and Heteroptera: Miridae) Conrad C. Loan and Scott R. Shaw 69

Foreign exploration for natural enemies of Lygus and Adelphocoris plant bugs Robert C. Hedlund 76

Augmentation: Rearing, release, and evaluation of plant bug parasites Jack W. Debolt 82

Quarantine procedures for imported parasites of Lygus spp. G.L. Snodgrass and L.R. Ertle 88

Summary and recommendations H.M. Graham 94

STUDIES ON THE BIOLOGICAL CONTROL OF compiled from literature and unpublished

PLANT BUGS (HETEROPTERA: MIRIDAE ) : AN reports and correspondence in the files INTRODUCTION AND HISTORY, 1961-83 of the Beneficial Insects Laboratory, as of 1982, the official Agricultural By Jack R. Coulsonii/ Research Service (ARS) Biological Control Documentation Center. This summary is This brief survey of studies on the not a comprehensive survey of the biological control of plant bugs literature on the subject; Graham et al. (Heteroptera: Miridae) presents an (1984) published a bibliography of the overview of the subject as an worldwide literature on the Lygus introduction to this publication. More complex. Details of the activities detailed accounts of some of the briefly discussed here are in other activities noted here, especially the sections of this publication or can be more recent studies, can be found in obtained from References Cited in this other sections of this publication. article. Except for one early attempt to utilize a fungus to control a miriu pest Tne targets of these biological control (Dustan, 1923), all studies on the activities have been primarily species of biological control of plant bugs in North the Lygus complex (Mirinae, tribe Mirini) America began in the 1960's. These in the United States and Canada, activities are discussed in 5-year including several destructive pests of segments in the following account. such crops as cotton, alfalfa, many Summaries of the Canadian studies were vegetables, and deciduous fruits. Within published by Craig and Loan (1984). the complex are the tarnished plant bug,

Lygus lineolaris (Palisot), the most 1961-65 . Studies were undertaken by ARS serious of tne mirict pests throughout at Riverside, Calif., in 1961 with field North America, and L. nesperus Knight and surveys in southern California and otner L. elisus Van Duzee, major pests in the Western States to determine the complex Western United States. Two other species of natural enemies of Lygus hesperus and of the subfamily Mirinae, the meadow L. elisus in alfalfa. In 1962-64, plant bug, Leptopterna dolabrata (L.) similar surveys of natural enemies of

(tribe Stenodemini) , and the alfalfa L. lineolaris in alfalfa were conducted plant bug, Adelphocoris lineolatus by ARS at Moorestown, N.J., in New Jersey (Goeze) (tribe Mirini), have been more and Pennsylvania. In 1963-65, several recent targets of biological control shipments of the native hymenopterous studies. Of these target pests, only parasites Peristenus pallipes (Curtis) A. lineolatus is clearly an introduced and P. pseudopallipes (Loan) (Braconidae) species in North America, being first were shipped from Nev* Jersey collections recorded in 1917 in Nova Scotia (Knight, for study and release (1964 only) in 1922). It is unclear whether California, where the species did not L. dolabrata is native or introduced; occur. During this period, specimens of whether it is truly Holarctic is open to a dipterous parasite, Alopnorella sp. conjecture (Slater, 1974). (Tachinidae) , were also sent from New Jersey but not released. Parasitism of This summary is mainly concerned with lygus bugs in all areas surveyed was "classical" biological control found to be low. activities, that is, the importation of foreign natural enemies. It has been Limited surveys of natural enemies of mirids were also conducted in France by the ArS European Parasite Laboratory (EPL) from 1962 to 1965. One shipment of "Euphorus pallipes " cocoons from Lygus rugulipennis Poppius was sent from France i/Benef icial Insects Laboratory, to California in 1963, but no adult Agricultural Research Service, U.S. parasites emerged. During tnis same Department of Agriculture, Bldg. 47o, period, Canadian workers also conducted BARC-East, Beltsville, MD 20705. research on mirid pests and their natural

1 . ,

enemies. Results of tne studies in the Stoneville, Miss. Shipments of a Polish

Eastern and Western United States, Peristenus sp. ( rubricollis (Thomson) Europe, and Canada were published by according to W.H. Day, ARS, Newark, Del., Craig (1963), Adlung (1964), Loan (1965), in litt., Sept. 26, 1983) were made to Clancy and Pierce (1966), and Streams et Arizona in 1970 through ARS quarantine al. (1968). Late in this period, the facilities at Moorestown, N.J., and were Commonwealth Institute of biological released at four locations in Arizona. Control (CIBC) station in Switzerland This was the first exotic mirid parasite conducted a literature survey of European to be released in North America. Also, mirids and their natural enemies and studies of the indigenous parasites of produced an unpublished, undated report Lygus spp. were begun in Arizona (for (Carl, 1964 (?)). This report concluded example, see Stoner and Surber, 1969). tnat little was known of European natural Because of the increased interest in enemies of mirids. exotic parasites, work on lygus bugs was reinitiated in 1970 at the ARS European

1906-7U . Studies of L. lineolaris in the Parasite Laboratory (EPL) in France. Eastern United States continued in

1966-68 in Connecticut under an ARS- 1971-75 . The Polish project was supported research grant (University of terminated in March 1971 and resulted in Connecticut, Storrs) (Streams et al., an unpublished final report by 1968; Shahjahan and Streams, 1973). Bilewicz-Pawinska [1971] and several Studies also continued in Canada, publications on the field studies and on including the initiation of critically the biologies and culture of the needed taxonomic studies of the braconid parasites (for example, Bilewicz- parasites of mirids (Loan, 1970). Pawinska, 1974a; Bilewicz-Pawinska and Pankanin, 1974). Taxonomic studies in In March 1966, a 5-year Special Foreign Canada clarified the identity of the Currency (PL-480) Project (E21-ENT-11) braconid parasites of mirids in North was undertaken with the Institute of America and in Europe (Loan and Ecology of the Polish Academy of Bilewicz-Pawinska, 1973; Loan 1974a,

Sciences, Warsaw. The purposes of this 1974b) . In March 1973, a new 4-year project were to study tne role of PL-480 project (PL-ARS-18) was undertaken braconid parasites in the regulation of with the Polish Institute of Ecology to populations of L. rugulipennis and other further study the role of the Peristenus Lygus species, primarily in rye and spp., now known as ]?. digoneutis Loan, potato crops, to develop techniques for .P. rubricollis (Thomson), ]?. stygicus rearing the parasites, and to define the Loan, and j>. stenodemae Loan, in reducing parasites taxonomically. A complex of populations of the plant bugs Lygus three Peristenus species was found that rugulipennis , Adelphocoris lineolatus , required later taxonomic clarification. and Stenodema virens (L.) in crop In 1968-70, several shipments of these environments. Results of these studies braconid parasites were made to the are in an unpublished final report by United States for study and propagation. Bilewicz-Pawinska [1977d] and in several Bilewicz-Pawinska (1969) published a publications that appeared near or after report of these early studies. the conclusion of the project (see

below) . Small numbers of Peristenus A "Lygus Bug Research Workshop," cocoons were shipped to the United States sponsored by the University of in 1974 and 1975 and a larger number in California, Davis, was held at Davis in 1976 (see below) March 1969. Unfortunately the proceedings of this workshop were never In 1971, the new braconid, described as published. During the workshop, progress Peristenus stygicus (Loan and Bilewicz- of the Polish studies was reported by Pawinska, 19 73) , was recovered from the

ARS . This resulted in interest in mirine plant bug Polymerus unif asciatus importing Polish parasites for release (F.) during EPL surveys in Turkey. EPL against Lygus spp. in cotton at ARS later found this species and the other stations in Tucson, Ariz. , and two previously found in Poland,

2 , ,

EL rubricollis and EL digoneutis , from California during this period. No Lygus spp. nymphs in France (Drea et al. parasites were recovered at any Arizona 1973). EPL began shipments of these release site in 1972 surveys. species to the United States in 1971 to the ARS quarantine facility of the In 1971, Turkish _P. stygicus was sent to Beneficial Insects Research Laboratory Texas A&M University by BIRL and released (BIRL) (Moorestown, N.J., 1971-73; against Lygus spp. in Texas alfalfa.

Newark, Del., 1973+) . Two of the species, EL digoneutis and P. stygicus, And in 1975, adults of EL stygicus from were cultured on L. rugulipennis at EPL. the California culture were received, cultured, and released by Mississippi During this period, work at BIRL State University personnel at several consisted primarily of receiving locations in Mississippi against Lygus Peristenus cocoons from overseas in lineolaris in wild host plants. Recovery quarantine, overwintering the diapausing attempts in 1976 were unsuccessful. cocoons, and shipping emerged adult Adults of the French EL digoneutis were parasites to Arizona, California, also sent to Mississippi State University Mississippi, Texas, and Canada for by BIRL in 1975, but attempts to culture culture, study, and release. However, a the species were unsuccessful. During few specimens of EL stygicus from France this period, the ARS Stoneville, Miss., and Turkey and of FL digoneutis from laboratory completed surveys of lygus bug France were released against Lygus spp. natural enemies in Mississippi (Scales, in alfalfa in New Jersey in 1972 and 1973). 1973, respectively. Improvements in Lygus culture techniques In 1971-72 and 1974, shipments of were made in both Mississippi and Arizona EL stygicus from both Turkey and France (Parrott et al., 1975; Bryan et al. were sent from BIRL to the Department of 1976). Entomology, University of California, Riverside, where the species was MacDonald College in Quebec, Canada, also cultured. In 1972-73, over 20,000 received P. stygicus from the University EL stygicus specimens from this culture of California culture during this period were released against Lygus hesperus in for culture and study, but no releases alfalfa in the San Joaquin Valley of were made. Broadbent (1976) expressed California. Although populations of the the need for parasite biotypes that might parasites were small (Van Steenwyk and be better adapted to the climatic Stern, 1976, 1977), the species was conditions of Quebec. A few recovered in the release fields at least P. digoneutis specimens also were through 1978. Small numbers of French received at MacDonald in 1973, 1976, and EL digoneutis were also sent to 1977 and EL stygicus in 1976-77 from the California for culture from 1971 to ARS quarantine facility in Delaware. 1974, and this species was released in the field there in 1972. Attempts to In 1974, the CIBC station in Pakistan culture the French EL rubricollis sent to issued an unpublished memorandum on the California in 1975 were unsuccessful. possibilities of biological control of

Lygus spp. (Khan et al. , 1974). Though In 1971-72, EL stygicus from Turkey and not as detailed as the later (1979) CIBC France was also sent to the ARS Tucson, report (see below), this memorandum ARS of a Ariz. , laboratory, where it was cultured resulted in negotiation by (Butler and Wardecker, 1974) and released 3-year PL-480 project with the CIBC against Lygus spp. in cotton. Adults of Pakistan Station for a survey of natural EL rubricollis from Poland also were enemies of mirid plant bugs in Pakistan, released in Arizona in 1971. That same Afghanistan, Iran, Turkey, and China. year a shipment of French EL digoneutis This project was undertaken in December specimens was sent to Arizona from BIRL 19 75. for culture. The Arizona laboratory also received _P. stygicus from the culture in

3 .

In 1975, an important taxonomic report alfalfa. Parasites from EPL collections clarifying the status of Lygus spp. in from the same hosts in Spain were North America was published (Kelton, directed to the revived importation 1975). program at the ARS laboratory at Tucson, Ariz., for releases against Lygus pests

1976-80 . The PL-480 project in Poland of cotton. was terminated in March 1977. A final shipment of 200 Polish parasite cocoons At BIRL, laboratory rearing methods for was sent to the 8IRL quarantine the parasites were studied in 1976-77, facilities in Delaware in 1976. and the three Lygus parasites were Publications from the project include released in Delaware alfalfa fields Bilewicz-Pawinska, 1973, 1974b, 1976a, during 1976-78. In 1977, releases of the 1976b, 1977a, 1977b, 1977c, and parasites were begun in New Jersey Bilewicz-Pawinska and Kamionek, 1973. alfalfa fields; these releases continued See also the unpublished final report by in 1978-80, targeted against Lygus

19 7 7d ] Bilewicz-Pawinska [ lineolaris , A. lineolatus , and Leptopterna dolabrata in alfalfa at two In 1976, a second lygus bug workshop, northern New Jersey study sites. Though organized by members of the Department of a few recoveries of Peristenus stygicus Entomology, University of Idaho, was held and .P. rubricollis were made in Delaware at the XV International Congress of and New Jersey, apparently none of the Entomology in Washington, D.C. parasites were established. In 1980, a Proceedings of this workshop on host tachinid parasite of lygus bugs, Alophora plant-lygus bug interactions were obesa (F.), from EPL collections in published (Scott and O’Keeffe, 1976). Austria, was released in Delaware.

EPL collections in Europe in 1976-77 were European parasites also were shipped by expanded to France, Germany, Hungary, BIRL to Mississippi State University in Austria, and Denmark, but they were 1976-78 for study, culture, and release confined to France and Austria in 1978 (.P. stygicus and P.. digoneutis ; attempts and only to France in 1979. Collections to culture the latter and .P. rubricollis were made of Lygus rugulipennis , failed; see Hormchan, 1977). The same

L. pratensis (L. ) , and Adelphocoris species were sent to MacDonald College in lineolatus . Shipments of the three Quebec for culture and study in 1976-77 Peristenus spp., primarily from France (see above). The need for determining and Austria, were made from 1976 to 1979, the host ranges of the mirid parasites and a fourth species of Peristenus , later was discussed by researchers in 1977-78, described as P_. adelphocoridis Loan partially as a result of the 1976 (Loan, 1979), was recovered from workshop. Consequently, shipments were

A. lineolatus ; .P. rubricollis and made to the ARS laboratory in Yakima, P. digoneutis were also found on this Wash., in 1978 and to Texas A&M host, the latter species only rarely. A University, College Station, in 1976-79 nematode parasite was found in Lygus spp. for such studies. The culture in in 1977; a nematode had also been found Washington was unsuccessful, but testing earlier in the Polish studies of 1?. stygicus in Texas was completed by

(Bilewicz-Pawinska and Kamionek, 1973). Porter (1979) , and some adults of this Cultures at EPL were discontinued during species were released in the State in 1978 in favor of direct shipment to U.S. 1979. In 1979, European Peristenus quarantine (BIRL) of large numbers of cocoons were sent to the ARS laboratory parasite cocoons directly from field at Stoneville, Miss., and ]?. digoneutis collections. In 1980, efforts were and ]?. stygicus were released in that renewed at EPL to obtain parasites from State against L. lineolaris in wild collections of Lygus and Adelphocoris in mustard. The P. stygicus specimens from France and Austria. They were destined the 1980 EPL collections in Spain were for the BIRL program in New Jersey for sent to the ARS laboratory in Tucson, releases against plant bug pests of Ariz. A healthy culture was initiated,

4 . , :

and as a result mass releases of this mymarids parasitized 55 percent of the species against Lygus spp. in alfalfa eggs of Lygus spp. in Indonesia. No were begun in Arizona in 1980. parasites were recovered from the nymphal or adult mirids collected during these During this period, scientists of studies. Predators of Lygus spp. were Agriculture Canada's Research Station at also recorded, the most important of Saskatoon, Saskatchewan, obtained which was Nabis f erus L. (Heteroptera European parasites for release against Nabidae) (CIBC, 1981). Lygus and Adelphocoris in alfalfa seed crops of Canada's Western Provinces. In 1979, CIBC published another report on Research at Saskatoon had begun in 1975 the possibilities for biological control with a survey of nymphal parasites of of lygus bugs (CIBC, 1979), noting, among Lygus in the area. The CIBC station in others, studies of parasites of lygus Switzerland began surveys and collections bugs in East Africa conducted by in 1977 in Switzerland, France, Germany, scientists in the 1940' s. As a partial and Austria. Cocoons of Peristenus were result of this report, a 3-year shipped to Canada in 1977-79, primarily cooperative agreement was negotiated in

. from JL. rugulipennis Adelphocoris 1980 by ARS at Tucson, Ariz. , with lineolatus was rare during the CIBC scientists of Texas A&M University, surveys. In 1980, collections were Dallas, for a survey and collection of concentrated on Adelphocoris in Austria plant bug parasites in Africa that might and Germany; about 500 cocoons from this be useful introductions against Lygus host were sent to Canada in 1980. spp. in cotton in the Southern United Between 1978 and 1980, a total of 1,720 States. _P. digoneutis and 64 _P. stygicus adults from the CIBC collections were released Other activities during this period into Lygus populations in alfalfa seed included the initiation in June 1978 of a fields in Saskatchewan and Alberta; in 4-year (later extended to 5-year) PL-480 1980, 49 _P. rubricollis and 76 project, EG-ARS-83, at the University of ]?. adelphocoridis were released against Assiut in Egypt to search for natural

A. lineolatus (Craig and Loan, 1984) . enemies of Lygus spp. and related mirids All recovery attempts were negative. in that country for possible introduction into the United States. Progress during The CIBC Pakistan Station carried out the first year of the project included a studies, explorations, and collections of survey of mirids and their predators, a mirids and their natural enemies from seasonal and host plant study of December 1975 through November 1978 under Taylorilygus pallidulus (Blanchard) the PL-480 project PK-ARS-91. These recovery of an egg parasitoid from T.

studies were conducted in Pakistan, pallidulus , and initiation of a India, Iran, Turkey, and Indonesia, the bibliography of lygus bug literature last in lieu of China, in which travel (Graham et al., 1984). A bibliography of approval was never obtained. Several the genus Lygus was published in 1980 in mirid species previously unknown in Idaho (Scott, 1980, 1981). Pakistan were found. Parasites were extremely rare in Pakistan; only egg In 1980, a survey of mirids and their parasites were found on Lygus gemellatus natural enemies in cotton and wild host (Herrich-Schaef f er) and Adelphocoris plants in the Transcaucasian area of the

lineolatus . No Lygus spp. were found in Soviet Union was proposed under the

the areas surveyed in India; 12 species U . S .-U . S . S .R. Environmental Agreement. of other mirids were collected. About However, because of political 25,000 adults and nymphs of 19 mirid developments, the proposal was not species were collected in Iran, and implemented 14,500 specimens of 35 species were collected in Turkey. No parasites were In view of the many exploration and recovered from any of the collections in importation activities for lygus bug India, Iran, and Turkey. Two species of biological control, and the large number

5 of U.S. locations and scientists specimens from these field studies for interested in studying and releasing taxonomic study at the ARS Systematic exotic parasites, a Coordinating Subgroup Entomology Laboratory at Washington, D.C. on Biological Control of Lygus and Other Mirids, under the ARS Working Group on The objectives at BIRL during 1981-83 Natural Enemies, was established by ARS concerned the quarantine clearance and for a 3-year period in June 1980. The shipment of P. stygicus from southern objectives of this subgroup were to (1) Europe to the ARS laboratory in Arizona assist in planning for foreign for culture and release, and the release exploration and collections and for of European parasites to attempt quarantine receipt of natural enemies in establishment on and reduce the abundance

the United States; (2) help expedite of plant bugs ( Lygus lineolaris ,

research on testing and propagation of Adelphocoris lineolatus , and Leptopterna

introduced natural enemies and their dolabrata ) in alfalfa in the Middle dissemination to interested Federal and Atlantic States. State scientists for study and release; (3) promote adequate exchange of Spanish and Greek P. stygicus specimens information; and (4) coordinate the were forwarded by BIRL to the Arizona evaluation of field releases and laboratory in 1982 and 1983. Also, some reporting of the results. The first specimens of the native Leiophron meeting of the subgroup was held in July unif ormis (Gahan) ( Hymenoptera :

1980 at Texas A&M University facilities Braconidae ) from Lygus lineolaris in at Dallas. Delaware were sent by BIRL to Tucson in 1981 for study of their effectiveness

1981-83 . During this period, overseas against Lygus hesperus nymphs in Arizona. explorations and studies were conducted

in Europe and in Africa. The EPL About 1,450 digoneutis , 100 .P. concentrated on obtaining nymphal rubricollis , and 28 P_. stygicus parasites of Lygus spp. from southern females were released against Europe for release against Lygus spp. in L. lineolaris during these 3 years at cotton by the ARS laboratory in Arizona, BIRL's New Jersey release sites, and 48 and of Lygus and Adelphocoris from more .P. adelphocoridis females were released northern Europe for release against these against A. lineolatus in 1983. No bugs in alfalfa by the ARS in Delaware. recoveries were made of any of the species in 1981-82; one male The parasites emerging at BIRL in 1981 £. digoneutis was recovered in 1983. A from cocoons collected in 1980 by EPL study of field parasitism of included Peristenus digoneutis and a L. lineolaris , A. lineolatus , and small number of P_. rubricollis from Leptopterna dolabrata by native parasites France and Austria, but no in New Jersey yielded only Peristenus

£. adelphocoridis . There was no parasite pallipes . Host acceptance tests with the emergence in 1981 from the host material European parasites and the three target collected in Spain in 1980. plant bug species were also conducted in the laboratory at BIRL during 1981-83. Collections of Lygus and Adelphocoris spp. were made in 1981-83 by EPL in The objectives of the studies conducted Austria, France, Spain, Italy, Greece, at the ARS Biological Control of Insects and Hungary. Some of the Peristenus Laboratory at Tucson during these years cocoons from these collections were sent continued to be to reduce populations of immediately to BIRL for overwintering. Lygus hesperus and other Lygus pests of Others were held at EPL for cotton in the Southwest by introducing overwintering, and the adult parasites and augmenting releases of promising that emerged were shipped the year parasites. Successful laboratory following collection. All four European cultures of Peristenus stygicus from species of Peristenus were included in Spain and Greece were established in 1980 the shipments to BIRL. EPL personnel and 1983, respectively; more parasites also prepared a large number of mirid from Spain were received in 1982 and

6 , ,

1983. Mass releases from these cultures Canada were expected to be possible in were conducted in alfalfa test plots near the late summer of 1984. Tucson in 1981-83. There were no recoveries of the parasite in 1981, but Canadian studies continued at the peak field parasitism in 1982 and 1983 research station at Saskatoon, was 16.7 and 10.2 percent, respectively, Saskatchewan, with the objective of during peak Lygus nymph populations in reducing populations of Lygus spp. and the season of release. When releases A. lineolatus in alfalfa seed crops in ceased in late summer, no further the Prairie Provinces. The fields in parasites were found, and there was no Saskatchewan and Alberta where Peristenus evidence of overwintering of P^. stygicus parasites were released during 1978-80 in Arizona. were monitored during 1981-82, but no introduced parasites were recovered. A In 1982, stygicus specimens from the total of 51 1?. adelphocoridis adults from Arizona culture were sent to researchers CIBC Austrian shipments were received at Texas A&M University at Dallas for in 1981 from the Ottawa quarantine release. No recoveries of the parasite station. They were released in alfalfa, were made at Texas release sites in 1982 but synchronization with the target or 1983. Adelphocoris host was poor and no recoveries were expected. Adults of

Studies of the effectiveness of native ]?. digoneutis were also received in 1981 parasites and predators of Lygus were and released against Lygus spp. In 1982, also continued at the Arizona laboratory, some of the cocoons of _P. adelphocoridis including studies on the native nymphal from the CIBC Austrian collections were parasite Leiophron unif ormis and egg sent by the Ottawa quarantine station to parasite Anaphes ovi jentatus (Crosby and BIRL for host acceptance tests.

Leonard) (Hymenoptera : Mymaridae) (Graham et al., 1986). Also in 1983, the Studies and explorations in Africa in cooperative worldwide bibliography of 1981-83 were conducted in Egypt and literature concerning the Lygus complex, several areas of subsaharan Africa. begun under the Egyptian PL-480 project in 1978, was completed (Graham et al. Work at the University of Assiut in Egypt

1984) . continued under the PL-480 project initiated in 1978. The objectives of Studies in Europe were also conducted by this work continued to be to study the the CIBC station in Switzerland in distribution, faunistic composition, 1981-83, with the objective of obtaining seasonal abundance, and host ranges of parasites of the alfalfa plant bug, Egyptian Heteroptera, particularly the

Adelphocoris lineolatus , for release and Lygus complex, and to discover and study establishment in alfalfa seed crops in predators and egg and nymphal parasites midwestern Canada. Collections in of mirids in Egypt. The biological Austria in 1981 resulted in shipment to control related activities conducted Canada Agriculture quarantine facilities during 1981-83 are summarized as follows: in Ottawa of 820 Peristenus cocoons from No nymphal parasites were recovered from

A. lineolatus . These cocoons yielded 103 Taylorilygus pallidulus or any other

£. digoneutis , 64 _P. adelphocoridis , 13 mirid in Egypt. An egg parasite, ]?. rubricollis , and 3 £. stygicus adults Telenomus sp. (Hymenoptera: Scelionidae) and 9 of the hyperparasite Mesochorus sp. was found parasitizing up to 95 percent

(Hymenoptera: Ichneumonidae) . Efforts by of T. pallidulus eggs in the Fayoum area, CIBC in 1982-83 were concentrated on particularly on Matricaria chamomilla L. studies of the population dynamics of the favored host plant of T. pallidulus A. lineolatus and on developing improved in that area. Studies were reported to collection and cocooning techniques to be underway to determine whether other obtain greater quantities of mirids also served as hosts of this egg

]?. adelphocoridis . Mass collections of parasite. Also, a worldwide bibliography this parasite in Austria for shipment to of the Lygus complex started in 1978 was

completed in 1983 (Graham et al. , 1984).

7 .

Under the ARS-funded cooperative In October 1983, explorations took place agreement with the Texas A&M University, in Kenya, where collections were mainly Dallas, begun in 1980, three exploration of mirids from grain sorghum and lantana; trips to subsaharan Africa were conducted collections in cotton were poor. in 1981, 1982, and 1983. The several shipments of mirid parasites collected Parasite cocoons were obtained from during those explorations were sent to Taylorilygus spp., and a shipment of the ARS Stoneville Research Quarantine parasitized nymphs and parasite cocoons Facility at Stoneville, Miss. The was made to Mississippi. objectives of this agreement were to discover, evaluate, and introduce Activities at the ARS Stoneville, Miss., parasites of African mirids, particularly location included quarantine receipt, nymphal parasites, some of which were clearance, and initial culture of the reported from earlier studies (Taylor, parasites received from Africa. The two 1945; Nixon, 1946), that would attack 1981 shipments of nymphal parasites from Lygus pests of cotton in the Southwestern South Africa were delayed in reaching United States, and to determine if hosts Stoneville, and only three braconid of these parasites included predaceous parasites were received alive. No mating mirids, particularly of the genus was observed and no parasitization of the

Deraeocoris . Lygus lineolaris or L. hesperus offered as hosts was obtained. A total of 17

In May 1981, nymphs of the brown wattle adult Peristenus praetor , 140 P. mirid, Lygidolon laevigatum Reuter, were nigricarpus , and 10 Mesochorus collected from wattle, Acacia mearnsii De hyperparasites emerged from the 3 Wild., in Natal Province of the Republic shipments received from Africa in 1982. of South Africa. Also, mirids of the The remaining uneraerged African cocoons were placed in cold storage, but no genera Orthotylus , Taylorilygus , and Deraeocoris were collected from further emergence occurred when they were surrounding vegetation. Two removed in 1983. The adult parasites hymenopterous egg and two nymphal obtained in 1982 were exposed to Lygus parasites of Lygidolon were found and lineolaris nymphs (2-4 instar) resulting identified by the collector (M.F. in 17 F^ and 3 F 2 _P. praetor progeny Schuster) as, respectively, Chaetostricha and 24 F]_ but no F 2 _P. nigricarpus and Telenomus spp. (Trichogrammatidae and progeny. Unfortunately both colonies nigricarpus expired. ]?. Scelionidae ) , and Peristenus Eight nigricarpus adults and (Szepligeti) and .P. praetor (Nixon) an undescribed Leiophron sp. were

(Braconidae) . Two shipments of the recovered in quarantine from the 1983 nymphal parasites were sent to the African shipment. A small F^ (10 Mississippi quarantine facility (see adults) of IP. nigricarpus was produced on L. below) lineolaris and a smaller F 2 (5 adults) on L. hesperus No F 3 In 1982, an exploratory collection trip generation was produced. was made from January to March through Egypt, Sudan, Kenya, and the Republic of Scientists at Stoneville also conducted a South Africa. Information collected survey of mirids and their host plants during this trip indicated that both and natural enemies in the Delta area of

.P Peristenus nigricarpus and . praetor Mississippi and associated areas, and were parasites of Taylorilygus and they sent a large number of mirid species Lygidolon spp. from Sudan to South Africa and specimens to the AR.S Systematic and west to the Cape Verde Islands, and Entomology Laboratory (SEL) in that there was another Peristenus Washington, D.C., for taxonomic study and parasite of the predaceous mirid deposit in the U.S. National Collection

Deraeocoris spp. that should be excluded of Insects (Snodgrass et al. , 1984a, from any shipments to the United States. 1984b) . Some taxonomic studies were Three shipments of parasites collected conducted in collaboration between during the trip were sent to the scientists at SEL and the Department of quarantine facility in Mississippi. Entomology, Oregon State University (see

8 . . . ] , )

the report in this publication by T.J. REFERENCES CITED Henry and J.D. Lattin) Adlung, K. 1964. Beobachtungen liber During 1981-83, efforts to establish das Auftreten von Lucerne-schadlingen cooperative arrangements for collections und ihrer Parasiten. Gesunde Pflanz. of mirids and their natural enemies in 16:135-140. Morocco, Israel, and the People’s Republic of China were unsuccessful. Bilewicz-Pawinska, T. 1969. Natural limitation of Lygus rugulipennis Popp, In October 1983, a meeting of the ARS by a group of Leiophron pallipes Curtis Coordinating Subgroup on Biological on the rye crop fields. Ekol. Pol., Control of Lygus and Other Mirids, Ser. A, 17:811-825. established in 1980, was held at Beltsville, Md. At, and subsequent to, Bilewicz-Pawinska, T. [1971.] Role of that meeting, plans for this publication parasitic Hymenoptera in reduction size were finalized. Summary information and of two species of the genus Lygus . several recommendations were prepared and [Final rpt. of PL-480 proj. E21-ENT-11], submitted for consideration by the ARS Inst. Ecol. , Pol. Acad. Sci., Warsaw, 54

National Program Staff, including further pp . [Unpub. research on the taxonomy, biology, and rearing of mirids and their parasites; Bilewicz-Pawinska, T. 1973. (Remarks foreign exploration for and quarantine on three species of Peristenus Foerster procedures for these parasites; and (Hym.: Braconidae) and their parasites studies on their release, recovery, and Mesochorus spp. (Hym.: Ichneumonidae) . evaluation Pol. Pisrao Entomol. 43:841-845. [In Polish]

Bilewicz-Pawinska, T. 1974a. Emergence This completes this summary of studies on and longevity of two species of the biological control of mirid plant Peristenus Foerster (Braconidae) under bugs in North America. Despite over 13 laboratory conditions. Ekol. Pol. years of efforts to establish exotic 22:213-222. parasites of plant bug pests in North America, there is no evidence at this Bilewicz-Pawinska, T. 1974b. date that any have been established. Observations of introduction of However, much information on mirids and Peristenus rubricollis Thomson under their natural enemies has been laboratory conditions. Bui. Acad. Pol. accumulated. Many research approaches Sci. 22:681-684. remain to be explored, as discussed at the 1983 subgroup meeting noted here and Bilewicz-Pawinska, T. 1976a. (Natural in the last article of this publication. enemies of some plant bugs (Miridae) in

This summary and publication may Poland.) Rocz. Nauk Roln. , Ser. E, therefore be considered only an interim 6:125-135. [In Polish; English summary] report on the biological control of plant bug pests. Bilewicz-Pawinska, T. 1976b. Distribution of the insect parasites As noted in the introduction, this Peristenus Foerster (Braconidae) and summary was prepared from several Mesochorus Gravenhorst (Ichneumonidae) published references and many unpublished in Poland. Bui. Acad. Pol. Sci. reports and correspondence on file at the 23:823-827. Beneficial Insects Laboratory. Many of these documents have been prepared and Bilewicz-Pawinska, T. 1977a. provided by the authors of the reports in (Occurrence and role of the parasitic this publication, and the reader is genus Peristenus Foerster (Hym. referred to these reports for additional Braconidae) on the rye crop fields.) details Pol. Pismo Entomol. 47:123-135. [In Polish; English summary]

9 ]

Bilewicz-Pawinska , T. 1977b. Time CIBC (Commonwealth Institute of reduction of diapause of parasitic Biological Control). 1979. Peristenus Foerster (Hymenoptera) under Possibilities for biological control of laboratory conditions. Bui. Acad. Pol. lygus bugs (Hemiptera: Miridae). Sci. 25:301-305. Commonw. Inst. Biol. Control, Status Paper 15, 7 pp. Bilewicz-Pawinska, T. 1977c. Parasitism of Adelphocoris lineolatus CIBC. 1981. Investigations on the Goeze and Lygus regulipennis [sic] Popp. natural enemies of Lygus spp. and other (Heteroptera) by braconids and their plant bugs (Miridae). Final rpt. [of occurrence on alfalfa. Ekol. Pol. PL-480 proj. PK-ARS-91], Commonw. Inst. 25:539-550. Biol. Control, Pakistan Station, 39 pp., with appendixes and plates. [Unpub.]

Bilewicz-Pawinska, T. [ 197 7d . ] Role of Peristenus spp. in reducing plant bug Clancy, D.W., and H.D. Pierce. 1966. populations in crop environment. Final Natural enemies of some lygus bugs.

rpt . 1973-1977 PL-ARS-18, Inst. Ecol., Jour. Econ. Entomol. 59:853-858. Pol. Acad. Sci., Warsaw, 41 pp. [Unpub.] Craig, C.H. 1963. The alfalfa plant

Bilewicz-Pawinska, T. , and M. Kamionek. bug, Adelphocoris lineolatus (Goeze), in

1973. ( Lygus rugulipennis Popp. (Het.: northern Saskatchewan. Can. Entomol. Miridae) as a host of a nematode 95:6-13.

(Mermithidae) . ) Pol. Pismo Entomol. 43:847-849. Craig, C.H., and C.C. Loan. 1984.

Adelphocoris lineolatus (Goeze) , alfalfa plant bug (Heteroptera: Miridae) [and] Bilewicz-Pawinska, T. , and M. Pankanin. 1974. (Larvae of Peristenus Foerster Lygus spp., plant bugs (Heteroptera: Miridae), pp. 9-10 [and] 45-47. In. (Hym., Braconidae) , parasites of Lygus Kelleher, rugulipennis Popp. (Heteroptera, J.S., and M.A. Hulme, eds. , Miridae).) Pol. Pismo Entomol. Biological Control Programmes Against 44:759-764. [In Polish; English summary] Insects and Weeds in Canada, 1969-1980, 410 pp. Commonw. Agr. Bur., Page Bros. Broadbent, A.B. 1976. Laboratory Ltd., Norwich, U.K. studies on the biology of Peristenus stygicus Loan (Hymenoptera: Braconidae), Drea, J.J., Jr., L. Dureseau, and a parasite of Lygus lineolaris (P. de E. Rivet. 1973. Biology of Peristenus B.) (Hemiptera: Miridae). Thesis, stygicus from Turkey, a potential natural enemy of lygus bugs in North McGill Univ. , Quebec, Montreal. America. Environ. Entomol. 2:278-280. Bryan, D.E., C.G. Jackson, R.L. Carranza, and E.G. Neeman. 1976. Lygus Dustan, A.G. 1923. The natural control hesperus: Production and development in of the green apple bug ( Lygus communis the laboratory. Jour. Econ. Entomol. var. novascotiensis Knight) by a new 69:127-129. species of Empusa . Quebec Soc. Prot. Plants, Ann. Rpt. 15:61-66. Butler, G.D., and A.L. Wardecker. 1974. Development of Peristenus Graham, H.M., C.G. Jackson, and J.W. Debolt. 1986. Lygus spp. stygicus , a parasite of Lygus hesperus , in relation to temperature. Jour. Econ. (Hemiptera: Miridae) and their parasites Entomol. 67:132-133. in agricultural areas of southern Arizona. Environ. Entomol. 15:132-142. Carl, K. [1964?]. Miridae on Graham, H.M. cultivated plants in Europe and their , A. A. Negm, and L.R. Ertle, natural enemies: A literature review. compilers. 1984. Worldwide literature Commonw. Inst. Biol. Control Rpt., 16 of the Lygus complex (Hemiptera: Miridae), 1900-1980. U.S. Dept. Agr., pp . [Unpub.

Agr. Res. Serv. , Bibliogr. and Lit. Agr. No. 30, 205 pp.

10 ] .

Hormchan, P. 1977. Biology of three Loan, C.C., and T. Bilewicz-Pawinska exotic species, and role of native 1973. Systematics and biology of four species of the genus Peristenus - Polish species of Peristenus Foerster parasites of tarnished plant bug, Lygus (Hymenoptera: Braconidae, Euphorinae). lineolaris , in Mississippi. Ph.D. Environ. Entomol. 2:271-278.

Dissertation, Miss. State Univ. , 74 pp. Nixon, G.E.J. 1946. Euphorine Kelton, L.A. 1975. The lygus bugs parasites of capsid and lygaeid bugs in (genus Lygus Hahn) of North America Uganda (Hymenoptera, Braconidae). Bui.

(He teroptera : Miridae) . Entomol. Soc. Entomol. Res. 37:113-129. Canada Mem. 95:1-101. Parrott, W.L., J.N. Jenkins, Khan, A.G., M. Mushtaque, and F.G. Maxwell, and M.L. Bostick. 1975. Sana-Ullah. 1974. Memorandum on the Improved techniques for rearing the possibilities of biological control of tarnished plant bug, Lygus lineolaris

Lygus spp. Commonw. Inst. Biol. (Palisot de Beauvois) . Miss. Agr. and Control, Pakistan Station, 15 pp. Forestry Expt. Sta. Tech. Bui. 72, 8 pp [Unpub. Porter, B.J. 1979. Host selection in Knight, H.H. 1922. Nearctic records Peristenus stygicus Loan (Hymenoptera: for species of Miridae known heretofore Braconidae); an approach to the only from the Palearctic Region evaluation of host range for

(Heteroptera) . Can. Entomol. 53:280-288. parasitoids. M.S. Thesis, Tex. A&M

Univ. , 55 pp. Loan, C.C. 1965. Life cycle and development of Leiophron pallipes Curtis Scales, A.L. 1973. Parasites of the (Hymenoptera: Braconidae, Euphorinae) in tarnished plant bug in the Mississippi five mirid hosts in the Belleville Delta. Environ. Entomol. 2:304-306. district. Proc. Entomol. Soc. Ontario 95:115-121. Scott, D.R. 1980. A bibliography of Lygus Hahn (Hemiptera: Miridae). Idaho Loan, C.C. 1970. Two new parasites of Agr. Expt. Sta., Misc. Ser. 58, 71 pp. the tarnished plant bug in Ontario: Leiophron pseudopallipes and Euphoriana Scott, D.R. 1981. Supplement to the lygivora (Hymenoptera: Braconidae, bibliography of Lygus Hahn. Bui. Euphorinae). Proc. Entomol. Soc. Entomol. Soc. Amer. 27:275-279. Ontario 100:188-195. Scott, D.R., and L.E. O'Keeffe, eds. Loan, C.C. 1974a. The North American 1976. Lygus bug: Host plant species of Leiophron Nees, 1818, and interactions. Proc. workshop XV Peristenus Foerster, 1862 (Hymenoptera: Internatl. Cong. Entomol. Aug. 19-28, Braconidae, Euphorinae), including the 1976, Washington, D.C. 38 pp. Univ. description of 31 new species. Idaho Press, Moscow. Naturaliste Can. 101:821-860. Shahjahan, M., and F.A. Streams. 1973. Loan, C.C. 1974b. The European species Plant effects on host finding by of Leiophron Nees and Peristenus Leiophron pseudopallipes (Hymenoptera:

Foerster (Hymenoptera: Braconidae, Braconidae) , a parasitoid of tarnished Euphorinae). Trans. Roy. Entomol. Soc. plant bug. Environ. Entomol. 2:921-925 Lond. 126:207-238. Slater, J.A. 1974. A preliminary Loan, C.C. 1979. Three new species of analysis of the derivation of the Peristenus Foerster from Canada and Heteroptera fauna of the northeastern western Europe (Hymenoptera: Braconidae, United States with special reference to Euphorinae). Naturaliste Can. ttie fauna of Connecticut. Conn. 106:387-391. Entomol. Soc. Mem. 1974:145-213. ,

Snodgrass, G.L., T.J. Henry, and W.P. Scott. 1984a. An annotated list of the Miridae (He teroptera) found in the Yazoo-Mississippi Delta and associated areas in Arkansas and

Louisiana. Proc . Entomol. Soc. Wash. 86:845-860.

Snodgrass, G.L., W.P. Scott, and J.W. Smith. 1984b. An annotated list of the host plants of Lygus lineolaris (Hemiptera: Miridae) in the Arkansas, Louisiana, and Mississippi Delta. Jour. Ga. Entomol. Soc. 19:93-101.

Stoner, A., and D.E. Surber. 1969. Notes on the biology and rearing of

Anaphes ovi jentatus , a new parasite of Lygus hesperus in Arizona. Jour. Econ. Entomol. 62:501-502.

Streams, F.A., M. Shahjahan, and H.G. LeMasurier. 1968. Influence of plants on the parasitization of the tarnished plant bug by Leiophron pallipes. Jour. Econ. Entomol. 61:996-999.

Taylor, T.H.C. 1945. Lygus simonyi as a cotton pest in Uganda. Bui. Entomol. Res. 36:121-148.

Van Steenwyk, R.A. and V.M. Stern. 1976. The biology of Peristenus stygicus (Hymenoptera : Braconidae) , a newly imported parasite of lygus bugs. Environ. Entomol. 5:931-934.

Van Steenwyk, R.A., and V.M. Stern. 1977. Propagation, release and

evaluation of Peristenus stygicus , a newly imported parasite of lygus bugs. Jour. Econ. Entomol. 70:66-69.

12 BIOLOGICAL CONTROL OF PLANT BUGS IN deformed plants with reduced rates of COTTON squaring for 2 to 4 weeks. Yield losses occurred when conditions were not By M.F. Schusteri^ favorable for late season recovery of the cotton in Arizona. Blank squares resulted when L. hesperus fed on DEFINITION AND HISTORY OF THE PROBLEM meristematic tissue of presquaring cotton. This was also true for Damage to cotton caused by the tarnished L. lineolaris (Scales and Furr, 1968; plant bug, Lygus lineolaris (Palisot), Tugwell et al., 1976; Hanney et al., was first investigated shortly after 1977). damage caused by the cotton fleahopper, Pseudatomoscelis seriatus (Reuter), was Both yield potential of cotton and time demonstrated by Reinhard (1926). Ewing of infestation by L. lineolaris were (1929) reported that feeding of shown by Tugwell et al. (1976) to L. lineolaris caused swelling of determine the type and severity of internodes and petioles and abnormal damage. Plants with extremely low yield branching. Subsequent studies by Ewing potential sustained large numbers of and McGarr (1933) showed that feeding of L. lineolaris without loss in yield. L. lineolaris and other rnirids reduced Infestations at or just before onset of retention of fruits by plants, whereas squaring caused significant terminal feeding of several leafhoppers had no abortion, and yield was reduced 40 effect on fruiting. percent. These studies used larger bug populations than normal. The Mechanically debudding cotton to infestation period resulting in the simulate plant bug damage increased the greatest yield loss was the 3 weeks total number of buds produced by a plant following the fourth week of squaring, (Hamner, 1941; Dunnam et al., 1943). when pinhead squares, small squares, and Complete debudding until tne third week bolls were subject to injury. Nerech of July in Mississippi did not (1976) found the economic injury level significantly reduce yields of cotton to be a single third-instar nymph per when plots were protected in late season foot of row (13,560 per acre) during the from boll weevils, Anthonomus grandis first 3 weeks of squaring, with greatest Boheman, and bollworms, Heliothis zea damage the first week. Abortion of (Boddie) (Hamner, 1941). Late season terminals caused by feeding occurred at protection of bolls, however, required this time. Lygus lineolaris removed extensive control measures for boll more than three squares per insect weevils and bollworms. Bolls produced per day, with results agreeing closely late in the season were more often with those of Mauney and Henneberry subject to early frosts, had increased (1979) in studies with L. hesperus . incidence of boll rot, had reduced boll Neresh (1976), Pack and Tugwell (1976), size, and produced less fiber of lower and Mauney and Henneberry (1979) quality and value than earlier bolls. indicated that Lygus spp. preferred to feed on young squares; this meristematic Damage to cotton caused by Lygus feeding resulted in abnormal growth, hesperus Knight was dramatically shown blank squares, and reduced yield. Yield by Wene and Sheets (1964). They reductions were greatest when plants reported that L. hesperus could kill were infested at first squaring (Scales seedling cotton, and that feeding damage and Furr, 1968; Neresh, 1976). Maximum to presquaring cotton resulted in damage occurred when dispersion of insects coincided with susceptible plant stages.

.L^Texas A&M University, Research and Extension Center, 17360 Coit Road, Dallas, TX 75252.

13 ROLE OF HOST PLANTS Hormchan, 1977), but the literature contains numerous references to casual The wild host plants of Lygus spp. on observations of predation by both which they feed and reproduce, and the insects and spiders. Quantitative work key hosts that furnish individuals that is lacking, but Lygus spp. appear to disperse to cotton, have only recently have an important role in the food chain been investigated. The relative of cotton ecosystems; the genus is a importance of these wild host plants is facultative predator as well as a determined by their abundance, effects phytophagous pest. on populations and reproductive

potential of Lygus , and effects on Parasites are more specific to nymphs of predators and parasites of Lygus spp. plant bugs. Leiophron unif ormis (Gahan) Cleveland (1982) and Anderson and in the Western and Peristenus pallipes Schuster (1983) found a succession of (Curtis) in the Eastern United States weed hosts from early spring until frost give varying degrees of nymph control at

for L. lineolaris . The hosts that less than economic reductions. In furnished individuals dispersing to addition, the egg parasite Anaphes cotton when it was most susceptible to ovi jentatus (Crosby and Leonard) occurs damage did not necessarily support the across the Cotton Belt. In Mississippi, greatest Lygus populations. There the tachinid Alophorella spp., prob.

appeared to be ecologically equivalent aeneoventris (Williston) , and mermithid weed species in Texas and Mississippi. nematodes also exert a low degree of control. In the Western United States, a complex of Lygus spp. is closely associated with Parasitization of Lygus hesperus by safflower or alfalfa production (Stern, Leiophron unif ormis never exceeded 11

1976; Graham et al. , 1982), with percent in California according to L. hesperus the predominant species. Clancy and Pierce (1966). In Arizona, Maturation of safflower or harvest of the egg parasite A. ovi jentatus alfalfa causes dispersal of bugs to parasitized 34 percent of Lygus spp. cotton, a less preferred host. eggs in London rocket but only 9 percent in alfalfa (Graham and Jackson, 1982). NEED FOR BIOLOGICAL CONTROL Parasitization by _P. pallipes occurred Additional biological control is clearly at 4-24 percent during the single needed for Lygus spp. that invade parasite generation in eastern cotton. The literature indicates a Mississippi (Hormchan, 1977). Limited succession of hosts is necessary for samples were also taken in the Lygus to increase sufficiently to damage Mississippi River Delta, but parasite cotton when insects disperse from plants effectiveness was no better than in lost through maturity or harvesting. A eastern Mississippi. biological control organism effective in noncrop host plants could reduce EXOTIC INTRODUCTIONS dispersing populations to below economic levels. A noncrop host plant could also Parasites of mirids were identified from a be source of parasites for dispersion Turkey in 1971 (Drea et al. , 1973) and in with Lygus spp. into cotton. Europe during 1966-71 (Bilewicz-Pawinska, 1973). In 1971-72 and 1974, specimens of NATIVE PARASITES AND PREDATORS Peristenus stygicus Loan from Turkey and France were shipped to the United States, Native parasites and predators of Lygus and cultures were established in spp. in cotton-growing regions of the California. The University of California United States are shown in tables 1 and initially maintained separate colonies of 2. Predators of Lygus spp. have not Turkish and French strains but eventually been extensively evaluated (Clancy and combined them (Van Steenwyk and Stern, Pierce, 1966; Perkins and Watson, 1972; 1976). During 1972-73, over 20,000

14 Table 1 Native parasites of Lygus lineolaris (Palisot) in Southeastern United States

Parasite species Location Source

Braconidae Peristenus pallipes (Curtis) Mississippi Delta Scales, 1973 Eastern Mississippi Hormchan, 1977

Tachinidae

Alophorella sp. , prob. Mississippi Delta Scales, 1973 aeneoventris (Williston)

Mymaridae Anaphes ovijentatus Mississippi Delta Scales, 1973 (Crosby and Leonard)

Nematoda, Mermithidae Mississippi Delta Scales, 1973

Table 2 Native parasites and predators of western Lygus spp. in Western United States

Parasite species Location Source

Braconidae Leiophron uniformis (Gahan) California Clancy and Pierce, 1966

Mymaridae Anaphes ovijentatus Arizona Graham and Jackson, (Crosby and Leonard) 1982

Nabidae Nabis alternatus Parshley Arizona Clancy and Pierce, 1966; Perkins and Watson, 1972

Lygaeidae Geocoris spp. California Clancy and Pierce, 1966

parasites were released in the San Mississippi Delta near Scott. A total of Joaquin Valley on alfalfa (Van Steenwyk 800 females were released at 4 sites. and Stern, 1977). Subsequent studies Monthly sweep net samples were taken at showed that the parasite was ineffective. the four sites during 1976 and 1977; nymphs were held for parasite emergence, of but Initial releases J?. stygicus from no parasites were recovered. imported material were made in the

Mississippi Delta on cotton during 1974 A second strain of .P. stygicus was (Coulson, pers. commun.). In 1975, a maintained and increased for release in colony of JP. stygicus was obtained from Mississippi using shipments of the the University of California at Riverside parasite from the European Parasite by the Department of Entomology, Laboratory during 1977. Small numbers of Mississippi State University. The females were released in Clay, Lee, California strain was increased during Bolivar, and Oktibbeha Counties. Sweep 1975 for biological studies with Lygus net samples were taken 7 days after lineolaris and for release during the release, and nymphs were examined for late summer in eastern Mississippi. Some parasites in three of the locations. An releases were also made in the average of 13 percent of the nymphs were

15 parasitized, but subsequent samples P. digoneutus were insufficient to indicated failure of the parasites to conclude that these two species cannot establish reproducing populations. Adult become established on Lygus in the parasites were effective when released Southern United States. but did not successfully complete a generation. The author searched for parasites in South and East Africa during 1981-83. A third strain of _P. stygicus from Spain Peristenus nigricarpus (Szepligeti) and was introduced and increased at the P. praetor (Nixon) were collected from Biological Control of Insects Laboratory, Lygidolon laevigatum Reuter in Natal, Tucson, Ariz. (H.M. Graham, pers. Republic of South Africa. The mirid commun.). Weekly releases of 1,500 to L. laevigatum is a serious pest of 1,900 parasites for control of Lygus seedling black wattle, Acacia mearnsii De hesperus were made on alfalfa during Wild., in Natal and southeastern periods of bug infestation. In addition, Transvaal as well as in Kenya. Natural distributed 152,000 parasite cocoons were parasites include J?. praetor , in alfalfa during 1983. Percent P^. nigricarpus , Chaetostricha miridiphaga parasitism in the field was low, and most Viggiani, and Telenomus spp. The two parasitized nymphs were found immediately Peristenus species parasitized 60-70 following releases of laboratory-reared percent of mirid nymphs during the second adult parasites. The results were less year of wattle growth and soon reduced than satisfactory. infestations to below economic levels (Connell, 1970). Collections made at These four efforts to establish Pietermaritzburg, Richmond, and Wart burg .P. stygicus for control of Lygus spp. on during the fall (May) of 1981 and summer cotton indicate that the parasite is (February) of 1982 were sent to the poorly adapted to cotton-growing regions Stoneville, Miss., quarantine facility. of the United States. The cause of this An F]_ generation of both parasite species' failure to establish has not species was obtained using nymphs of been determined. Lygus lineolaris as the host. An F 2

generation was obtained for £. praetor , Two other species of Peristenus have been but efforts to obtain the F 3 generation introduced into southeastern were unsuccessful. cotton-growing regions through the European Parasite Laboratory (Hormchan, During 1983, an exploration trip was made 1977). A total of 29 females and 54 to Kenya near Kisumu, Nyanza Province. males of £. rubricollis (Thomson) During October, parasites of mirids were collected in France were sent to the collected in the highlands north of Lake Department of Entomology, Mississippi Victoria to the Ugandan border. State University, in 1977. Females Parasites were found in Taylorilygus oviposited in L. lineolaris nymphs in indecorus (Taylor) , T. vosseleri laboratory studies and a few cocoons were (Poppius) , and T. virens (Taylor) . Only produced, but no adults emerged. cocoons from the last two species survived shipment to quarantine at Specimens of French Peristenus digoneutus Stoneville. Parasites collected were Loan were received at Mississippi State Pe ristenus nigricarpus and an undescribed

University during 1975-76. A total of 75 Leiophron . The latter oviposited readily females and 91 males were utilized to in both Lygus lineolaris and Taylorilygus begin a colony, although a laboratory pallidulus (Blanchard) but failed to F 2 generation was not obtained. emerge from cocoons (G.L. Snodgrass, Twenty-five individuals were released in pers. commun.). each of 2 sites in Oktibbeha and Bolivar Counties in 1977. Monthly sweep net The Commonwealth Institute of Biological collections during 1978-79 did not Control laboratory in Kenya undertook recover .P. digoneutus from either site. additional searches for parasites of The limited releases of P. stygicus and Taylorilygus spp. in 1984 and 1985 with

16 . . .

the support of the ARS Biological Control Case histories from Europe and Africa of Insects Laboratory, Tucson, Ariz. No indicate that successful biological parasites were collected until the last control of Lygus spp. could be possible part of 1985. At that time, a shipment with successfully adapted parasites. of the undescribed Leiophron was sent to the Stoneville quarantine facility, and REFERENCES CITED colonies were established in Lygus

lineolaris and L. hesperus . This Anderson, R.A. , and M.F. Schuster. parasite has been tested against nymphs 1983. Phenology of the tarnished plant of the predators Orius insidiosus (Say) bug on natural host plants in relation to

(Anthocoridae) , Geocoris punctipes (Say) populations in cotton. Southwest.

(Lygaeidae) , Nabis roseipennis Reuter Entomol. 8:131-136.

(Nabidae) , and Deraeocoris nebulosus

(Uhler) (Miridae), with no parasitization Bilewicz-Pawinska , T. 1973. Remarks on of any of the species (Snodgrass, pers. three species of Peristenus Foerster commun. ) (Hym.: Braconidae) and their parasite Mesochorus spp. (Hym.: Ichneumonidae) FUTURE DIRECTION - PROBABILITY OF SUCCESS Pol. Pismo Entomol. 43:841-845. [In Polish] Parasites from the Ethiopian and Palaearctic regions utilized thus far for Clancy, D.W., and H.D. Pierce. 1966. biological control of Lygus have not Natural enemies of some lygus bugs. adapted to cotton-growing regions in the Jour. Econ. Entomol. 59:853-858. Nearctic region. However, a large number of species from the Ethiopian region have Cleveland, T.C. 1982. Hibernation and yet to be evaluated (Nixon, 1946). The host plant sequence studies of tarnished

successful culturing of the undescribed plant bugs, Lygus lineolaris , in the Leiophron from Kenya in Lygus lineolaris Mississippi Delta. Environ. Entomol. and L. hesperus suggests some promise. 11:1049-1052. The diversity of mirid parasites in the Ethiopian region indicates that Connell, A.D. 1970. Aspects of the additional research on the East and West morphology and bionomics of African fauna might yet yield other Batrachomorphus cedaranus (Naude) and promising parasite species. Lygidolon laevigatum Reut. on black wattle. Ph.D. Thesis, Univ. Natal, It is not known whether it will be Pietermaritzburg feasible to use parasites for biological control of plant bugs in native host Drea, J.J., Jr., L. Dureseau, and plants or in crops that sustain little E. Rivet. 1973. Biology of Peristenus damage in order to prevent large numbers s tygicus from Turkey, a potential natural of emigrants into very sensitive crops enemy of lygus bugs in North America. such as cotton in the United States. Environ. Entomol. 2:278-280. However, Taylor (1945) found similar ecosystem interactions in Uganda with Dunnam, E.W., J.C. Clark, and respect to cotton. In Uganda, the brown S.L. Calhoun. 1943. Effects of the removal of squares on yield of upland lygus bug, Taylorilygus vosseleri , is a pest of cotton that moves into cotton cotton. Jour. Econ. Entomol. 36:896-900. from maturing wild host plants found in the elephant grass zone. Parasitization Ewing, K.P. 1929. Effects on the cotton of T_. vosseleri by Peristenus on these plant of the feeding of certain Hemiptera wild hosts is continuous, and when it of the family Miridae. Jour. Econ. disperses to cotton, the parasites Entomol. 22:761-765. disperse with it. Biological control was rather effective in the small cotton Ewing, K.P., and R.L. McGarr. 1933. The fields characteristic of that area. effect of certain homopterous insects as

17 : , 1 ,

compared with three common mirids upon Pack, T.M., and P. Tugvell . 1976. the growth and fruiting of cotton Clouded and tarnished plant bugs on plants. Jour. Econ. Entomol. 26:943-955. cotton: a comparison of injury symptoms and damage on fruit parts. Ark. Agr. Graham, H.M., and C.G. Jackson. 1982. Expt. Sta. Rpt. 226, 17 pp. Distribution of eggs and parasites of

Lygus spp. (Hemiptera: Miridae) , Nabis Perkins, P.V., and T.F. Watson. 1972. spp. (Hemiptera: Nabidae) , and Nabis alternatus as a predator of Lygus

Spissistilus festinus (Say) (Homoptera he s perns . Ann. Entomol. Soc. Amer. Membracidae) on plant stems. Ann. 65:625-629.

Entomol. Soc. Amer . 75:56-60. Reinhard, H.J. 1926. The cotton flea Graham, H.M., C.G. Jackson, and hopper. Tex. Agr. Expt. Sta. Bui. 339, G.D. Butler, Jr. 1982. Composition of 39 pp. the Lygus complex in some crop and weed habitats of Arizona. Southwest. Entomol. Scales, A.L. 1973. Parasites of the

7 : 10 5-110. tarnished plant bug in the Mississippi Delta. Environ. Entomol. 2:304-305. Hamner, A.L. 1941. Fruiting of cotton in relation to cotton fleahopper and Scales, A.L., and R.E. Furr. 1968. other insects which do similar damage to Relationship between the tarnished plant squares. Miss. Agr. Expt. Sta. Bui. 360, bug and deformed cotton plants. Jour. 11 pp. Econ. Entomol. 61:114-118.

Hanny, B.W., T.C. Cleveland, and Stern, V.M. 1976. Ecological studies of W.R. Meredith, Jr. 1977. Effects of lygus bugs In developing a pest tarnished plant bug, ( Lygus llneolaris ) management program for cotton pests in infestation on presquaring cotton, the San Joaquin Valley, California. In

(Gossypium hirsutum) . Environ. Entomol. Scott, D.R., and L.E. O’Keeffe, eds. 6:460-462. Lygus Bug: Host Plant Interactions. 38 pp. Univ. Idaho Press, Moscow. Hormchan, P. 1977. Biology of three exotic species, and role of native Taylor, T.H.C. 1945. Lygus simony - species of the genus Peristenus Reut . as a cotton pest in Uganda. Bui. parasites of tarnished plant bug, Lygus Entomol. Res . 36:121-148. lineolaris , in Mississippi. Ph.D. Dissertation, Miss. State Univ. , 74 pp. Tugwell, P . , S.C. Young, Jr., B.A. Dumas, and J.R. Phillips. 1976. Plant bugs in Mauney, J.R., and T.J. Henneberry. cotton. Importance of infestation time, 1979. Identification of damage symptoms types of cotton injury and significance and patterns of feeding of plant bugs in of wild hosts near cotton. Ark. Agr. cotton. Jour. Econ. Entomol. 72:496-501. Expt. Sta. Rpt. 227, 24 pp.

Nerech, J.S. 1976. Interactions of the Van Steenwyk, R.A., and V.M. Stern. tarnished plant bug, Lygus lineolaris (P. 1976. The biology of Peristenus stygicus de B.) (Hemiptera: Miridae), and frego (Hymenoptera: Braconidae), a newly bract gene in different cotton variety imported parasite of lygus bugs. backgrounds. Ph.D. Dissertation, Miss. Environ. Entomol. 5:931-934. State Univ. Van Steenwyk, R.A., and V.M. Stern. Nixon, G.E.J. 1946. Euphorine parasites 1977. Propagation, release and of capsid and lygaeid bugs In Uganda evaluation of Peristenus stygicus , a

(Hymenoptera , Braconidae) . Bui. Entomol. newly imported parasite of lygus bugs. Res. 37:113-129. Jour. Econ. Entomol. 70:66-69.

18 Wene, G.P., and L.W. Sheets. 1964. Lygus bug Injury to presquaring cotton. Ariz. Agr. Expt. Sta. Tech. Bui. 166, 28 pp. . ,

BIOLOGICAL CONTROL EFFORTS AGAINST LYGUS established alfalfa stands is now AND ADELPHOCORIS SPP. INFESTING ALFALFA treated with insecticides, with a IN THE UNITED STATES, WITH NOTES ON savings to agriculture of millions of OTHER ASSOCIATED MIRID SPECIES dollars each year (Day, 1981). Most of the insecticides still applied to By W.H. Dayi/ alfalfa in this region are used against the potato leafhopper, Bmpoasca fabae

(Harris) . Since economic populations of Alfalfa is an important crop in the this insect are produced by migrants United States. Nearly 27 million acres arriving from the Gulf States in late are grown each year, an area exceeded spring, injurious populations usually do only by wheat, corn, and soybeans not develop until midsummer to late (Johnson, 1982 ). It is the principal summer. Damage to alfalfa, is most protein source for dairy and beef cattle severe if young, spring-seeded fields and for most other farm animals. are heavily infested. Occasionally moderate injury occurs in older, Many insect species feed on alfalfa. established fields, especially during However, only a few (number varies among summers with inadequate rainfall. locations and years) significantly Overall, however, I estimate that only affect the costs of producing alfalfa by about 5-20 percent of alfalfa fields, reducing stand or yield or by requiring depending on the State, are treated for chemical or other control measures. leafhopper control. The absence of Because alfalfa Is not native to the severe damage to most alfalfa acreage Western Hemisphere, it is not surprising has directed attention to other insects that most of its major insect pests have that feed on alfalfa in the Northeast, been accidentally introduced into North like the plant bugs (Miridae: America, and for this reason many of Adelphocoris , Lygus , and others) these pests have been the target of Research on this plant bug complex is applied biological control research by warranted because— the U.S. Department of Agriculture. As a result of these parasite (1) Several species of mirids feed on introductions, the alfalfa weevil, alfalfa, and others attack timothy and (Gyllenhal) once the Hypera postlca , other grasses that are planted with most important insect pest of alfalfa alfalfa. nationwide, now is at such low levels that it causes little or no damage in (2) Damage by these sucking insects is most of the eastern third of the United much less obvious than injury by chewing States north of latitude 36° N. (Day, insects, so either it is unnoticed or it 1981). Similar results have been is confused with damage caused by obtained against two other introduced nutrient deficiencies, leaf hoppers- .pests, the pea aphid, Acyrthosiphon aphids, or plant diseases (Day, unpub.; pi sum (Harris) (Angalet and Fuester, Osborn, 1939; Radcliffe and Barnes, 1977) and the alfalfa blotch leafminer, 1970). Agromyza f rontella (Rondani) (Hendrickson and Plummer, 1983). (3) The plant bugs apparently have become more abundant because of greatly As a consequence of these successful reduced insecticide use or reduced research projects in the Northeastern competition by the alfalfa weevil. States, only a small proportion of (4) Alfalfa, being a perennial, serves as a reservoir for the tarnished plant

bug, Lygus lineolaris (Palisot) , and the 3:/ Beneficial Insects Research legume bug, L. hesperus Knight, which Laboratory, Agricultural Research have been serious pests of numerous Service, U.S. Department of fruit and vegetable crops for many years Agriculture, 501 South Chapel Street, (Crosby and Leonard, 1914). Newark, DE 19713.

20 , )

Chemical control of the introduction from Europe (Knight, 1922). alfalfa-infesting plant bugs is no It is generally regarded as a significant longer a desirable solution in the pest only of alfalfa that is used for Northeastern United States, because seed and forage production (Craig, 1963; parasite mortality and, consequently, Newton and Hill, 1970). The related reduced biological control of these rapid plant bug, A. rapidus, is also three pests would result. For this included in table 1 because occasionally reason in the early 1970's, it is abundant and has been regarded as a entomologists at the ARS Beneficial pest of alfalfa. However, it probably Insects Research Laboratory at Newark, feeds mainly on Rumex weeds in alfalfa Del., became interested in the fields (Slater and Baranowski, 1978). possibility of reducing plant bug numbers in alfalfa with introduced The meadow plant bug, Leptopterna

parasites. This work dovetailed with dolabrata , an early immigrant from Europe

exploration studies that had been (Osborn, 1918) , is usually the most underway for several years at the ARS numerous mirid in the spring in European Parasite Laboratory in France northeastern alfalfa fields that have (an extension of the pioneering work by been planted in a mixture of alfalfa and Bilewicz-Pawinski in Poland, sponsored by timothy or other grasses (Day, unpub.). the USDA PL-480 program) and related I am not aware of an economic impact research in the Southwestern States. In study of this insect on forage grasses, the Southwest, Federal and State but its sheer numbers suggest that it has entomologists were interested in the a deleterious effect on at least the biological control of Lygus spp. in grass component of the yield (Day, forage alfalfa, primarily to reduce the unpub.; Osborn, 1918). number of plant bugs emigrating to cotton, and in alfalfa grown for seed. Two native species of Lygus ( hesperus and

lineolaris ) are important pests of This report is an attempt to integrate alfalfa in North America (table 1). and summarize the large amount of Their coloration varies with age (Day, available information from the unpub.), temperature (Kelton, 1975) literature and my ongoing research on (darker shades occurring in cooler locations and seasons) and possibly also the mirids that are important pests of , alfalfa and alfalfa-grass crops. among different host plants. These color Additional information may be found in differences have caused considerable other reports in this publication. confusion as to the identity and the number of species actually present (Kelton, 1975). THE MIRID COMPLEX IN ALFALFA

Species and Host Plants Lygus bugs are not without some beneficial habits. Apparently all Lygus The common plant bugs found in alfalfa spp. are able to feed on other insects, and alfalfa-grass mixtures in North especially when short of food (Kelton, America are listed in table 1. Keys and 1975; Wheeler, 1976), and for optimum drawings of these species to aid in their development this predation may even be required (Bryan et al. 1976). However, identification are in Knight (1941) and , Slater and Baranowski (1978). Two since in most field situations the mirids ecological homologs, Lygus pratensis (L. greatly outnumber aphids and other and L. rugulipennis Poppius, which occur potential prey, their phytophagous more in Europe, have been included in table 1 activities are likely to be much for comparison. Mirid species that feed important than their predatory indicates primarily on weeds present in most older tendencies. Other evidence alfalfa fields are not listed. that aphid honeydew may be essential for survival if alfalfa is not yet in bloom The alfalfa plant bug, Adelphocoris or does not contain flowering weeds (Butler, 1968). Because Lygus spp. feed lineolatus is a comparatively recent on weed flowers and seeds, some reduction

21 ) ) ,

Table 1 Common mirid species found in alfalfa and alfalfa-timothy fields in North America^

Genera- tions/ Over- Distri- Species year winter bution// Hosts Origin//

Adelphocoris lineolatus 2-3 Egg N, Eur Alfalfa, sweetclover, Introduced (Goeze) vegetables, fruits;

alfalfa plant bug buds , seeds

A. rapidus (Say) 1-2 Egg NE Dock, clovers, cotton Native rapid plant bug

Leptopterna dolabrata (L. ) 1 Egg N, Eur Timothy, orchardgrass Introduced meadow plant bug

Lygus hesperus Knight 2-5 Adult W Alfalfa, cotton, Native legume bug insects, weeds, beans; western 1/3 U.S.

L. lineolaris (Palisot) 2-4 Adult NA Legumes, insects, Native tarnished plant bug vegetables, fruits, weeds (Erigeron, milkweed, etc.)

L. pratensis (L. 2-3 Adult Eur Similar to L. ruguli- (resembles L. rugulipennis pennis as far as is Poppius and confused in known literature until 1951)

L. rugulipennis Poppius 2-3 Adult Eur Alfalfa, potato, rye, — European tarnished plant weeds, flowers bug

Megaloceroea recticornis 1 Egg NE, Eur Bluegrass, fescues, Introduced (Geof froy other grasses

Stenotus binotatus (F.) 1 Egg N, Eur Orchardgrass Introduced timothy grass bug timothy

Trigonotylus coelestialium 1-2 Egg N Timothy, oats, Native (Kirkaldy grasses green grass bug

l^Data from Bilewicz-Pawinska (1970), Crosby and Leonard (1914), W.H. Day (unpub.), Graham (1982), Hardee et al. (1963), T.J. Henry (pers. commun.), Kelton (1975), Knight (1922, 1923), J.D. Lattin (pers. commun.), Osborn (1918), Slater and Baranowski (1978), Southwood (1956), Stephens (1982), Watson (1928), and Wheeler (1974).

//Eur = Europe; N = northern 1/2 of North America; NA = North America; NE = northeastern 1/4 of NA; W = western NA.

^/introduced = introduced into North America; native = native to NA; = not present.

22 of weeds likely occurs, as suggested by unpub.). Significant damage to alfalfa Snodgrass et al. (1984). However, any has been documented by Newton and Hill benefit would be offset if the increased (1970). The movement of both adults and plant bug numbers resulting later moved nymphs (Kelton, 1975; Khattat and into nearby crops. Finally, Scott (1983) Stewart, 1980) from one plant host to has found that lygus bugs may increase another suggests that alfalfa serves as yields of certain crops by pollinating an important source of L. lineolaris flowers and, surprisingly, also by a infestations in fruit and vegetable delayed stimulation effect on the seed crops. Consequently, reduction of this that they have consumed. insect by parasites, even if the latter are restricted to alfalfa, could be of In the Western States, L. hesperus is broad economic importance. much more numerous on alfalfa than L. lineolaris (table 1). The former In Europe, there are apparently also two species could be called the western similar Lygus species (table 1), which tarnished plant bug, because it occupies were confused until comparatively approximately the same ecological niche recently (Southwood, 1956), that have as L. lineolaris does in the East, broad host ranges. The "European attacking cotton and many other crops in tarnished plant bug," _L. rugulipennis addition to alfalfa. A closely related (Southwood, 1956) is by far the most species, L. elisus Van Duzee, is seldom important species. abundant in southwestern alfalfa (Graham et al. , 1982, 1986). What was long The remaining species in table 1 feed thought to be a third species on alfalfa, only on grasses in alfalfa fields as far L. desertinus Knight, will probably be as is known. Megaloceroea recticornis eventually declared a synonym or has been reported as a pest of lawn and subspecies of L. elisus , because two-way pasture grasses (Kamm, 1979) and other crosses yielded progeny readily in grasses (Slater, 1956) in the United laboratory tests, and the offspring of States, but I have not discovered any single females from the field included reference indicating that this introduced individuals of both "species" (Sluss et species reduces yields of the timothy or al., 1982; Graham, 1982). The western orchardgrass frequently planted with Lygus complex is especially important, alfalfa. It is listed in table 1 because because most of our alfalfa seed is it is often common in mirid samples from produced there, and large reductions in northeastern alfalfa fields. seed yield (Carlson, 1946) are more likely to result from mirid feeding than The timothy grass bug, Stenotus are reduced foliage yields. However, binotatus , is another grass-feeding, forage yield losses have also been introduced plant bug (table 1). In my documented (Stitt, 1943; Newton and Hill, field observations, it has been second or

1970) . In addition, forage alfalfa is third in abundance in alfalfa-grass often an important reservoir for mixtures, and it is also abundant in New

L. hesperus , which emigrates to cotton York (Hardee et al., 1963), so it may and other nearby crops when the alfalfa well have an economic impact. This is mowed. species feeds on timothy and orchardgrass

(Watson, 1928) , both commonly planted Lygus lineolaris is often very numerous with alfalfa (Knapp and Seaney, 1979). in alfalfa fields in the Eastern and Since the nymphs closely resemble Central States. As previously mentioned, Adelphocoris lineolatus nymphs, it feeds on a wide range of crops (Scott, especially the early instars, skilled see p. 40) and weeds (Snodgrass et al., identification is necessary to make 1984) (table 1). Many overwinter in accurate field counts of these two alfalfa, because it offers considerable species. Adults are easily identified. cover since it is not plowed or cultivated annually like most crops, and, The green grass bug, Trigonotylus in addition, large numbers are produced coelestialium , is a small, slender mirid in alfalfa during the summer (Day, that is usually less numerous than the

23 other grass-feeding species (table 1). Presumably the mirids that overwinter as It is probably of little economic adults would also have an advantage, importance in alfalfa-grass plantings. because the mobile adults can relocate in the spring, colonizing fields with low or Biology of Common Mirids zero infestations. However, of the listed species, only members of the genus Lygus overwinter in the adult stage. Table 1 also includes additional biological information that can be useful of occurrence and in devising sampling or control methods. An approximate time Obviously, species with more than one sequence of the common mirid nymphs in the Northeastern States is in figure 1. generation each year will generally be Adult mirids have not been included, more difficult to control by biological because they are generally long lived or other means, because an additional generation allows the population to (the resulting overlap prevents compensate by reproduction or emigration separation of generations) and because in the same year for earlier mortality. only the nymphs are parasitized

Adelphocorls lineolatus

Host: Alfalfa -

Lygus lineolaris

Leptopterna dolabrata

Tr igonoty lus coelestialium

Host: Grasses

Megaloceroea recticornis

Stenotus binotatus

Figure 1 Approximate time of occurrence, relative

abundance (ellipse height) , and number of generations of common mirid nymphs in northeastern alfalfa-grass fields, 1978-82. Dotted lines indicate occasional fourth generations of A. lineolatus and L. lineolaris.

24 significantly. The "height" of each endoparasites of braconid larvae. The ellipse represents the relative abundance Mesochorus egg is injected into the of each species and generation. Since braconid when it is inside the live mirid most of these mirid species feed on host. Braconid cocoons are believed to grasses, they will be scarce or absent in largely escape additional hyperparasitism young, pure plantings of alfalfa, which because they are concealed and dispersed contain few weed grasses. In such in the soil, but I am not aware of this situations, Adelphocoris and Lygus are actually having been investigated. The usually the only genera abundant enough data, along with data of Lim and Stewart to be of possible economic importance. (1976) and Dasch (1971), are not In irrigated fields in the Southwest, sufficient to indicate whether all only Lygus is regarded as a significant Mesochorus spp. in North America are the pest. Whether or not grasses are present same species as in Europe, but with the alfalfa, it is important to note R. W. Carlson (pers. commun.) has that there is a complex of species, recently determined that my specimens are generations (fig. 1), and stages of the all morphologically identical to the mirids that combine to provide continuous European M. curvulus Thomson. feeding "pressure" on the crop throughout the growing season. This probably Measurement of the effectiveness of the increases the importance of what might native primary parasites is difficult. A otherwise be minor feeding damage. two-step process is necessary: The parasites must be identified and the PARASITES AND PREDATORS amount of parasitism must be accurately measured. For identification of the Parasitism by Native Species parasites of nymphs and adults, the hosts must be collected, identified, separated Once the species of the target pest have by species and stage, and fed adequately been identified and their relative until the parasites exit; suitable importance is estimated, it is necessary pupation media must be provided for the to determine the species of parasites braconids; and diapausing parasites in that are already present. Very little cocoons must be kept alive for many was known in North America prior to the months until the adult parasites emerge, comparatively recent work by Loan (1965) as adults are required for identi- and Clancy and Pierce (1966). However, fication. In most instances, since this since then considerably more information long rearing process results in has been obtained, and this has been substantial mortality of both hosts and summarized in table 2. Several points parasites, accurate data on the degree of that are not self-explanatory are parasitism are not obtained by this discussed here. method. Clancy and Pierce (1966) pointed this out and indicated that dissection No species of nematodes are listed by was the only accurate method for Poinar (1975) as parasites of the measuring parasitism. My data (Day, American species of mirids listed in unpub.) for 1982 corroborate this. table 1 —a reflection of the difficulty Parasitism by dissection was 48 percent in rearing nematodes to the adult stage higher than by rearing, showing that the as required for identification, their low rearing method seriously underestimates incidence, and the small number of parasitism, probably because the survival intensive investigations on parasites of of parasitized mirids is markedly lower mirids. Welch (1965) has stated that low than unparasitized individuals. Samples levels of nematode parasitism are likely, too large to dissect in 1 day can be except in wet or very humid environments, frozen at -15°C (Day, 1971), so the work and my observations agree (table 3). can be done over an extended period.

Little work has been done on secondary Most of the data available, including parasites. All common species are in the references cited here and my data genus Mesochorus and are solitary referred to later, indicate that

25 . , , , ,), ,

Table 2 Common parasites in North America of mirids associated with alfalfa^/

Genera- Plant Parasites Family/./ Hosts tions/yr!/ association

Anaphes ovijentatus My Lygus lineolaris, 2-4 Alfalfa weeds (Crosby and Leonard) L. hesperus

Leiophron uniformis Br L. hesperus. 2-4 Alfalfa weeds (Gahan) L. elisus, L. lineolaris

L. trigonotylidis Br Trigonotylus (?) Grasses (Loan) coelestialium

Peristenus pallipes Br L. lineolaris, 1-E Alfalfa weeds (Curtis)!/ Adelphocoris lineolatus, grasses Leptopterna dolabrata

P. pseudopallipes Br L. lineolaris 1-L Erigeron (not (Loan) alfalfa

Alophorella aeneoventris Ta L. lineolaris, (?) Alfalfa weeds (Williston) (plus L. elisus, occasionally A. fumosa L. hesperus, and possibly A. pulverea L. dolabrata, and A. opaca) Stenotus binotatus, Pentatomidae Cercopidae

Undetermined nematode Me A. lineolatus, (?) Alfalfa L. lineolaris grasses S. binotatus

Mesochorus curvulus Ic Leiophron 2-3 Alfalfa Thomson!./ Peristenus grasses (also M. acuminatus weeds (Thomson) and M. punctifrons Dasch)

i/Data from Loan (1970, 1980), Shahjahan and Streams (1973), and Day (unpub.) except as indicated in footnotes.

^Br = Braconidae; some generic and specific names are different in references published prior to revisions by Loan (1974a). Ic = Ichneumonidae ; secondary parasites; for further information, = see Dasch (1971). Me Mermithidae; possibly Hexamermis ; must be reared to adult stage for identification (Poinar, 1975). My = Mymaridae (Crosby and Leonard, 1914; Clancy and Pierce, 1966; Jackson and Graham, 1983). Ta = Tachinidae (Arnaud, 1978); some of these species may be synonyms and some host records may be erroneous.

^/Number of generations of polyvoltine species varies with length of growing season. E = spring-early summer; L = late summer-fall

1/This species is rare in Southwestern United States (Clancy and Pierce, 1 56).

5/The Mesochorus species that emerge from mirids are secondary parasites and attack the braconid primary parasites.

26 . . . . .

Table 3 Parasitism of mirids in New Jersey alfalfa, by dissection

Number Parasitism!/ of nymphs (%) Number Parasitism!/ of adults (%) Hosts sampled Brae Tach. Nema Fung Total sampled Brae Tach. Nema Fung. Total

Adelphocoris 339 11.2 0 0 0.3 11.5 418 0 0 0.2 1.7 1.9 lineolatusA /

Leptopterna 3/203 36.9 0 0 0 36.9 3/l62 2.5 0 0 0 2.5 dolabrata//

Lygus 357 10.1 0 1.4 0 11.5 626 4.5 .8 .8 0 6.1 lineolaris

Megaloceroea 3/l03 6.8 0 0 1.0 7.8 3/86 0 0 0 0 0 recticornis//

Stenotus 3/73 0 0 1.4 0 1.4 3/ll4 0 0 0 0 0 binotatus!/

Trigonotylus 3/25 A/32 .O 0 0 0 A/32.0 111 2.7 0 0 0 2.7 coelestialium

% mortality — 95 0 3 1 100 — 66 9 11 13 100 i^Brac. = Braconidae; Tach. = Tachinidae; Nema. = nematode; Fung. = fungus disease.

^/Accidentally introduced into North America.

3/Most of these samples were from Warren County, N.J. (1982-83). All other samples were from this location and

Burlington County, N.J. , in 1983. Mirids were collected by sweeping 3 fields per county at weekly (May- June) and biweekly (July-Oct.) intervals. d/ Unreliable data due to small sample size.

parasitism of the nymphal stage of most Peristenus pallipes may have also been common alfalfa-grass mirids in the United introduced along with L. dolabrata rather than be a Holarctic species, because (1) States is 0 to 20 percent. This is not parasite is apparently also present surprising, because four (57 percent) of this in Europe (Loan, 1974b), and (2) although the seven common U.S. mirids (table 1, the major parasite of the native Lygus species 1, 3-5, 8-10) affecting alfalfa and associated grasses are known to be lineolaris in the United States is also .P. pallipes the degree of parasitism is introduced species, and they usually , establish with few or none of their much less, which suggests a recent natural enemies. In addition, alfalfa is host-parasite association. not native to North America, which may explain why native parasites of For all species except L. lineolaris (table 3) it is also noteworthy that the Lygus lineolaris attack this pest in , affected by certain weeds but not in alfalfa, as adult stage is much less instances, reported by Shahjahan and Streams (1973). natural enemies. In most these are parasites that failed to the An example of the type of data needed to complete their development and kill molt. evaluate parasitism is in table 3. All host prior to the final nymphal was the principal generations of the multivoltine species Lygus lineolaris also have been combined in this table to allow mirid parasitized by tachinids which apparently space for both stages and the minor ( Alophorella spp.), been mortality factors. These data show that oviposit only in adults; none have of nymphs that overall only one species, Leptopterna found in the large numbers dissected (Day and Saunders, dolabrata is parasitized to even a have been , may be due moderate degree. This also suggests that unpub.). These two exceptions 27 .

to long coevolution, because Generally less attention has been given L. lineolaris is a native species, to parasites of the egg stage. Probably whereas all but one of the other species this is because mirid eggs are very are immigrants. difficult to sample in adequate numbers since they are small and embedded in Only a small proportion of any mirid plant stems. Graham et al. (1986) in stage and species was parasitized by Arizona have found parasitism of Lygus nematodes, fungi, and tachinid flies eggs up to 75 percent, but usually the (table 3). The braconids were of much high percentages occurred only in low greater importance, affecting 95 percent mirid populations, when mowing of the of all parasitized nymphs and 66 percent alfalfa had been delayed 2-4 weeks, or in of the parasitized adults (table 3). certain weeds. Evidently only one species, Anaphes ovi jentatus (Crosby and The need for additional parasite species Leonard), commonly attacks mirid eggs, is also obvious in table 4. Parasitism and it parasitizes a variety of host of the second and third generations of species (Jackson and Graham, 1983) the alfalfa-feeding mirids (A. lineolatus Clancy and Pierce (1966) found nearly 50 and L. lineolaris ) is especially low and percent of second- and third-generation would require establishment of a Lygus eggs to be parasitized, and bivoltine parasite like Peristenus Sillings and Broersma (1974) found 64 to digoneutis Loan or a polyvoltine species 85 percent of the same generations to like Peristenus stygicus Loan. have been attacked. I have not seen egg Parasitism of the introduced grass- parasitism data in the literature for

feeding mirids M. recticornis and genera other than Lygus . S^. binotatus is also insignificant. As

noted earlier, S_. binotatus is very Considerably more information has been abundant and may thus warrant a search published on parasitism of mirid nymphs. for parasites in Europe. However, the picture is still

Table 4 Parasitism!/ of mirid nymphs in New Jersey alfalfa, by generation

Generation 1 Generation 2 Generation 3

Hosts Number sampled Parasitism (%) Number sampled Parasitism (%) Number sampled Parasitism (%)

Adelphocoris 171 20 91 0 77 4 lineolatus//

Leptopterna 202 37 (3/) — (3/) dolabratai/

Lygus 81 27 116 6 160 4 lineolaris

Megaloceroea 103 7 on — on recticornis//

Stenotus 73 0 on — on binotatus/./

Trigonotylus 21 d/38 2 4/ 0 on coelestialium

i/By dissection. Sampling methods same as in table 3. Only major parasites (Braconidae) included in this table.

2/ Accidentally introduced into North America.

3/no generation.

A 7 Unreliable data due to small sample size.

28 .

incomplete. Some reports cover only part No literature data have been found for of the generations or species of the Megaloceroea recticornis to compare with mirid complex, whereas others have used the low rates in New Jersey (table 4). rearing, which considerably under- rather estimates the degree of parasitism, Stenotus binotatus , which is evidently than the dissection method. regarded as a pest of timothy in Europe (Watson, 1928), has not yet been

For Adelphocoris lineolatus , Loan (1965) recognized as an important pest in North observed 40-60 percent parasitism of the America. Thus, no parasitism data have first generation in Ontario, considerably been previously published to my knowledge higher than I have observed in New Jersey for comparison with the zero rates I have (table 4). Wheeler (1972) noted 0-5 observed (table 4). percent mortality by a fungus disease in a 4-year study in New York. Additional Parasitism of the native Trigonotylus and information for Canada is in Craig coelestialium , one of the green grass Loan ( see p. 48) bugs, was surprisingly high (table 4) in its first generation and then Parasitism levels of Lygus lineolaris insignificant in the second generation in that are similar to our results have been New Jersey. Loan (1980) reported a reported by Loan (1965), with rates of 30 slightly higher (43 percent) rate for the percent in the first generation and 12 first generation in Ontario. percent in the second generation in Ontario. Lim and Stewart (1976) found Predation by Native Species only 5 percent parasitism in the first generation in alfalfa, but 8 percent in Several species of Nabis (Nabidae) the second generation in weeds. (Perkins and Watson, 1972; Wheeler, Shahjahan and Streams (1973) reported 1977), Chrysopa (Chrysopidae) (Wheeler, average parasitism rates of 20-30 percent 1977), and spiders (Oxyopidae,

(apparently first and second generations, Tetragnathidae , Thomisidae) (Wheeler, but not stated) on weed hosts, although 1971) have been observed feeding on Lygus the rates varied considerably among the and Adelphocoris in alfalfa fields. species of weeds. Although several species of Geocoris Only low nymphal parasitism rates for (Lygaeidae) are regarded as important of Lygus hesperus , the western homolog predators of Lygus in California cotton recorded. Gonzalez, other L. lineolaris , have been (Leigh and 1976), Clancy and Pierce (1966) reported about 1 investigators in Arizona concluded that percent parasitization of the first they were not effective in reducing mirid several generations, and 5-7 percent for populations (Wene and Sheets, 1962). the last two to three generations during Crocker and Whitcomb (1980) did not 2 years. Graham et al. (1986) observed a observe Geocoris feeding on mirids in 1-5 percent parasitization of the third alfalfa, although they did record this and fourth generations on forage alfalfa predator eating mirids on other host in Arizona; higher rates were plants. They also observed Geocoris occasionally observed where mowing had feeding on dead insects, beneficial been delayed and in fields grown for seed. species, and plants, and they noted that this omnivorousness will confound Parasitism data in the literature on the estimates of control value. Gupta et al. remaining mirid species are limited. The (1980) studied prey consumption by only reference to Leptopterna dolabrata Geocoris bullatus (Say) in the that I have found (Loan, 1980) listed a laboratory, observing that Acyrthosiphon 42 percent parasitization in Ontario pisum was preferred over mirids and that collections, slightly higher tnan my late-instar Lygus nymphs and adults were results in New Jersey (table 4). too large to be captured. Nevertheless,

29 . .

they concluded that Geocoris is the major It is important to note that since natural enemy of Lygus in Washington collection efforts have been mostly concentrated on Lygus rugulipennis the State alfalfa. , ecological equivalent of our L. Wheeler (1977) found several additional lineolaris and L. hesperus , larger numbers of parasites have been obtained predator taxa in alfalfa ( Orius , Podisus , from this host. Fewer Adelphocoris coccinellids , sphecids, and vespids) but did not observe them attacking Lygus or lineolatus specimens have been collected

Adelphocoris . However, sphecids were because this species was not a target reported by Kurczewski and Peckam (1970) pest in the early years, and later to provision their nests with Lygus in because even moderate field populations New York State of this species are rare under the short European harvesting schedules (Hedlund, At present, the effectiveness of pers. commun.). Collections in Europe predators in preventing outbreaks or were concentrated on alfalfa to avoid reducing damaging populations of parasite species or subspecies that were alfalfa-feeding mirids in the field not adapted to this crop. remains largely unknown. This is primarily because predation is much more As in the United States, the dominant difficult to quantify than parasitism in parasites were all braconids. Moreover, nature. The percentage of the mirid because three of the four braconid population that has been parasitized at species attacked both Lygus and any one time is relatively easily and Adelphocoris (table 5), they were accurately determined, as outlined potentially more useful parasites. In earlier. On the other hand, the direct most samples, parasitism rates were measurement of predation in the field is considerably higher than in the United prevented for the following reasons: States (K. Carl, J.J. Drea, R.W. Fuester, Mirids that have previously been consumed R.C. Hedlund, pers. commun.). This is an by predators usually cannot be counted; important additional indicator of their each predator feeds on many prey in its biological control potential. lifetime; the prey consumption rate varies considerably among the numerous Tachinids and nematodes were, in stages and instars of botir the predator contrast, rarely found to be significant and the prey; and the wide range of parasites in Europe (CIBC, 1979). species accepted as prey by most predators leaves much uncertainty Parasite Shipments From BIRL Quarantine regarding the number of mirids that have been consumed. Extrapolation of Until 1982, all imported parasites of laboratory feeding tests to field mirids were processed through quarantine conditions adds further biases, and large at the ARS Beneficial Insects Research errors are likely (Crocker and Whitcomb, Laboratory ( BIRL) at Newark, Del. The 1980) . primary parasites that emerged were then sent to various State and Federal Species in Europe Parasite cooperators. Table 6 gives the number of parasites released in the field in each As mentioned earlier, the ARS European State or Province and the percentage Parasite Laboratory in France has been released (number released divided by exploring for exotic parasites of mirids number received) for several years. Prior to this, ARS had a cooperative agreement with Teresa At several locations, one species of Bilewicz-Pawinska in Poland. I have parasite, Peristenus stygicus , was summarized pertinent results of the successfully reared in the laboratory, so collections and rearings in Europe by more were released than had been these two groups in table 5. Further received. This may increase the odds for details are in Hedlund (see p. 76).

30 establishment, especially if the The principal target pests for the individuals released are or F 2 , so they parasites listed in table 6 have been have not undergone prolonged selection to Adelphocoris lineolatus and Lygus artificial conditions in the laboratory. lineolaris in the Northeast, L. lineolaris in the South Central, and In other instances, field releases were L. hesperus in the Southwest. few or nonexistent because laboratory culture was attempted with all or most of Locations where significant numbers of the parasites received, and the species parasites have been released have been could not be successfully reared. systematically checked for parasite Peristenus digoneutis and, especially, establishment. Places with positive P. rubricollis have a diapause that has recoveries are listed in table 7. impeded their rearing. Similar Although a few locations have produced difficulties are likely with parasites, the results have not been ]?• adelphocoridis . Diapause and the encouraging. Parasite release and small numbers received so far have not recovery efforts are continuing only in made laboratory rearing a practical Warren County, N.J., and in Pima and alternative. In a few other instances, Cochise Counties, Ariz. , where it is only laboratory studies were planned at hoped that successful establishment will the outset. result in the next several years.

Table 5 Common parasites in Europe of mirids associated with alfalfa

Generations/ Plant Parasites!/ Family!/ Hosts!./ yrl/ association

Peristenus Br Adelphocoris 1-E Alfalfa adelphocoridis Loan lineolatus (F)

P. digoneutis Loan Br Lygus rugulipennis (F), 2-3 Alfalfa, potatoes, A. lineolatus (F) rye

P. rubricollis Br L. rugulipennis (F), 1-E Alfalfa, rye "(Thomson) A. lineolatus (F)

P. stygicus Loan Br L. rugulipennis (F), 2-4 Alfalfa, weeds, L. lineolaris (L), potatoes, and L. hesperus (L), other vegetables Polymerus unifasciatus (F.) (F), A. lineolatus (L)

Alophora obesa (F.) Ta Lygus sp. (F) (?) Alfalfa, clover

!/ In addition, the same nominal species of Mesochorus (table 2) is known from Europe and also an unidentified mermithid nematode based Bilewicz- (Bilewicz-Pawinska and Kamionek , 1973). Data on Pawinska (1970), Drea et al. (1973), and Fuester (pers. commun.).

2/ Br = Braconidae. Most generic and specific names are different in references published prior to revisions by Loan (1974b, 1979) and Loan and Bilewicz-Pawinska (1973). Ta = Tachinidae.

2/ Verified by laboratory (L) or field (F) (more accurate) observations by W.H. Day, J.W. Debolt, L.R. Ertle, R.W. Fuester, and R.C. Hedlund (unpub.). L. rugulipennis may have included some

L. pratensis .

!/This varies for polyvoltine species with length of growing season; E = spring-early summer.

31 : . . . .. -

Table 6 Disposition of European parasites of mirids shipped from ARS Beneficial Insects Research Laboratory, 1963-83i/

State or Peristenus sod. released Agamermis Region Province adelphocoridis digoneutis rubr icollis styglcus Alophora decaudatai/

NE Del. 1/ — 1,182 428 Z/6,702 15 — 5 /92 % 80% 780 % 100%

Md. "" 0 0%

N.J.3/ 48 7,232 155 1/2,103 — — 76% 100% 100% 74%

Quebec — 0 — 0 0% 0% — —

SC Miss — 173 0 216 — — 18% 0% 23% — —

Tex — 0 0 511 — - 0% 0% 45% —

NW Wash — 0 — 0% — —

sw Ariz.Z/ 0 51 i/l35,884 ___ 0% 15% 20,800% —

Calif. — 100 0 i/l6,263 ___ — 66% 0% 12,050% ““

Totals ShippedZ/ 63 9,772 1,176 7,349 15 31 Released 48 8,687 634 161,679 15 0 76% 89% 54% 2,200% 100% 0%

l^Based on information provided by recipients of shipments. Proportion of males in each release varied, usually between 45-55 percent.

2/Nematode - A. decaudata Cobb, Steiner, Christie.

^/Releases by ARS-BIRL, Newark, Del.

i/ Including a significant proportion of laboratory- reared parasites and (Arizona only) parasitized hosts (J.W. Debolt, pers. commun., 1983). Number of parasitized hosts has been discounted to allow for parasite mortality and unparasitized individuals.

^/Proportion released (92% of 1,285 shipped in this case)

6/ln addition, there were 92 undetermined Peristenus specimens received here in 1971-72; 52 of them were released

— / If cocoon stage shipped (a few cases), actual number emerged was significantly less.

32 . . . ,

Table 7 Recoveries of European parasites of mirids in the United States, 1964-84

Year Recovered parasites Tentati ve State County Collected p-ri^ Species.?/ Amount Sex establishment Remarks

Ar iz Pima 1982 0 Ps Many (?) Parasites recovered same year as released only; most fields later plowed under

Calif Kern 1974-75 1-2 Ps (?) (?) (- -) Parasitism less than 1%; field converted to housing by 1979—^

Del. New Castle 1978 1 Pr 10 Male Dissected ex cocoons

1979 2 Pr 1 Male (- - ) Male only;

Ps 1, 1 Male see 1980 remarks female

1980 3 — 0 — Previous tentative establishment not confirmed

N.J. Burlington 1972 0 Ps 2 Male Parasites recovered same year as released

Warren 1983, 1 Pd 2, 1 Male, (!') 1984 female

t/p-r = post release.

2/ pd = Peristenus dlgoneutis , Pr = £. rubricollis , Ps = P. stygicus. All parasites were reared from hosts, unless otherwise stated in remarks.

3/Recovery of at least 1 female of released species was made a year after last release, constituting a tentative establishment ftf Establishment not substantiated later.

5/ For other details, see Van Steenwyk and Stern (1977). .

EVALUATION PROCEDURES accurate parasitism percentages and rearing for identification of parasite It is becoming increasingly clear that species. Collection of both types of biological control projects should parasite data must be continued during include plans for evaluating the degree the postestablishment period. Ideally, of control obtained. Not only are cost- parasite reproduction and in some benefit data from previous programs instances the addition of new parasite often essential for approval of new species will gradually increase the project proposals, but it is frequently proportion of the target mirid necessary to prove that biocontrol population that is parasitized, and agents have actually been the control concurrently the mirid will become much factor responsible for the reduced less abundant. importance of a former pest insect. This task is neither simple nor easy, AN ASSESSMENT OF THE PROJECT because it is not practical in most instances to provide valid "control" Progress has been uneven. At least (natural enemy-free) plots side by side satisfactory numbers of three of the with "treatment" plots in the field, as four braconid parasites have been is commonly done in chemical or cultural received from Europe, and new methods comparisons. are being used there to obtain larger quantities of the fourth species, Fortunately, long-term studies and an Peristenus adelphocoridis . Adequate indirect approach will usually provide numbers of two parasite species have adequate data. "Baseline" data on pest been released in two or more different abundance should be collected for a locations or environments and of the third minimum of 3 years prior to the species in one location. Although establishment of an introduced natural diapause problems have allowed only one enemy. Crop damage and yield data are species to be multiplied in the also desirable if not already laboratory, large numbers have not available. Several years' data are generally been essential for establish- required to allow for fluctuations in ment of other parasite species in the pest density, weather effects, and other past variables beyond the experimenter's control. Initial difficulties in obtaining reasonable survival of the three The same data should be collected for parasites and a native species that several years after the natural enemy diapause for extended periods have been has become firmly established. overcome, enabling the rearing of much Continued observations are very larger numbers for establishment important because usually 3 to 5 years determinations. are required for the biotic agents to become abundant and, in turn, for the There has been some concern that pest population to fall to a new, lower introduced parasites of phytophagous equilibrium level. Establishment of mirids might also attack predatory additional natural enemy species later, mirids in North America. Careful work which is desirable if the first species in the laboratory by Porter (1979) has fails to provide sufficient control, shown that a much wider host range would prolong this evaluation period. occurs in the laboratory for Peristenus stygicus compared to available field To determine whether there are native data. However, the actual host range in parasites, as there were for most of the nature is considerably more restricted, mirids discussed here, parasitism data as indicated by the failure of this or must also be collected prior to any of the other exotic parasites so far establishment of the exotic species. As to establish even on the same plant- outlined earlier, these data must be feeding genus or species that they were obtained by two methods —dissections for originally obtained from in Europe, much

34 less on predatory species in other genera parasites are available. As far as I am or families and in different (arboreal) aware, only Alophora (table 6) has been habitats. released in this manner.

This specificity could be the major FUTURE DIRECTIONS reason that none of the European parasites of Lygus has yet become Several more years will be required for established in North America on our two two aspects of the work. Both Peristenus

(different) species of Lygus . Because adelphocoridis and rubricollis should three of these parasites attack at least be released in larger numbers in the

two different genera ( Lygus and Northeast. Monitoring of release sites

Adelphocoris ) in the field in Europe must continue for all species for at

(table 5) , this was not assumed to be a least 3 years after the last release to potential problem. However, detect species that have established but host-acceptance laboratory tests by the are initially present at very low levels. author (still in progress) suggest that neither Lygus lineolaris nor Several parasite releases in the Adelphocoris lineolatus is an adequate Northeast may have failed because of This has occurred host for Pe ristenus adelphocoridis , poor synchronization. always been digoneutis , or £. rubricollis , and because host nymphs have not that Leptopterna dolabrata is not an numerous on the target release dates, adequate host for _P. adelphocoridis . which must be planned in advance to schedule parasite emergence from Different environments and climates have overwintering cocoons. In addition, the been used to improve the chances for exact date of emergence of exotic establishment of released parasites (see parasites from their cocoons is usually table 6). Sites have varied within a impossible to predict. It is expected State (for example, in Arizona, two that additional Peristenus digoneutis different elevations were selected) or and P. stygicus specimens will be even between adjacent States (for obtained from collections intended for _P. example, Delaware locations are coastal _P. adelphocoridis or rubricollis , and plain, New Jersey sites are piedmont and they can be used for supplemental appalachian) . However, the summer releases to obtain better timing. photoperiod is shorter because all release sites in the United States have Possibly some of the failures to been considerably farther south than the establish exotic parasites have been original collection sites of the caused by a low incidence of their parasites in Europe. The importance of mating prior to release. The day length on the establishment success recovery of only males in several of Pe ristenus is not known, but it has instances (table 7; overall 89 percent not prevented establishment in North males) suggests this but could also have America of other exotic euphorine resulted from low parasite density in the field, because or later females braconids ( Microctonus spp.) that have obligatory diapause (Day et al., 1971). were too dispersed to be located by males. Day (unpub. ) found that females Loan, a It is important to note that adequate of Microctonus aethiopoides parasite release and recovery attempts parasite in the same subfamily as Peristenus usually mate only during the have been made only in the Northeast and , the Southwest, and the results may be day of emergence; if unmated, all different in another region of the progeny will be males. Accordingly, United States. mating success should be tested for each large lot of field-collected parasites Parasite releases inside a field cage released in the future. are occasionally used to reduce dispersion of the parasites and hosts, especially when only small numbers of

35 ACKNOWLEDGMENTS^./ REFERENCES CITED

I thank the following individuals for Angalet, G.W., and R.W. Fuester. 1977. their assistance: R.J. Dysart, L.R. The Aphidius parasites of the pea aphid Ertle, and K.S. Swan (BIRL) for Acyrthosiphum pi sum in the eastern half shipment, release, and recovery data; of the United States. Ann. Entomol. Soc. L.B. Saunders (BIRL) for technical Amer. 70:87-96. assistance; R.W. Fuester (BIRL) for

advice on parasite identification, Arnaud , P.H., Jr. 1978. A host-parasite rearing, and biology; R.C. Hedlund, catalog of North American Tachinidae. D. Coutinot, and H. Hoyer (EPL) for U.S. Dept. Agr. Misc. Pub. 1316, 86 pp. European parasites; C.C. Loan (CDA) for parasite identifications and biological Bilewicz-Pawinska, T. 1970. Studies on information; J.S. Kelleher (CDA) for natural limitations of some lygus bugs in European parasites and biological and ecosystems of cultivated fields. Rocz.

shipment data; H.M. Graham ( BCIL) for Nauk Roln. , Ser. E, 1:193-204. parasitism information; J.W. Debolt

(BCIL) for parasites and shipment and Bilewicz-Pawinska, T. , and M. Kamionek. release data; J.J. Drea, Jr. (BID for 1973. Lygus rugulipennis Popp.

biological information; K.P. Carl (Heteroptera : Miridae) as a host of a

(CIBC-Delemont) for parasite nematode (Merraithidae) . Pol. Pismo information; N.E. Woodley (SEL) for Entomol. 43:847-849. identification of tachinid parasites; and T.J. Henry (SEL) and J.D. Lattin (Oreg. Bryan, D.E., C.G. Jackson, R.L. Caranza,

State Univ. ) for identification, and E.G. Neeman. 1976. Lygus hesperus: references, and biological information Production and development in the on the mirid hosts. laboratory. Jour. Econ. Entomol. 69:127-129.

Butler, G.D., Jr. 1968. Sugar for the survival of Lygus hesperus on alfalfa. Jour. Econ. Entomol. 61:854-855.

Carlson, J.W. 1946. Pollination, lygus infestation, genotypes, and size of plants as affecting seed setting and seed production in alfalfa. Jour, Amer. Soc. Agron. 38:502-514. !/ BCIL = ARS Biological Control of Insects Laboratory, Tucson, Ariz.; CIBC. 1979. Possibilities for = BIL ARS Beneficial Insects biological control of lygus bugs = Laboratory, Beltsville, Md.; BIRL ARS (Hemiptera: Miridae). Commonw. Inst. Beneficial Insects Research Laboratory, Biol. Control, Status Paper 15, 7 pp. Newark, Del.; CDA = Canada Department = of Agriculture, Ottawa; CIBC Clancy, D.W., and H.D. Pierce. 1966. Commonwealth Institute of Biological Natural enemies of some lygus bugs. = Control, Delemont, Switzerland; EPL Jour. Econ. Entomol. 59:853-858. ARS European Parasite Laboratory, Sevres (now Orgerus-Behoust) France; , Craig, C.H. 1963. The alfalfa plant = SEL ARS Systematic Entomology bug, Adelphocoris lineolatus (Goeze) , in Laboratory, Washington, D.C. northern Saskatchewan. Can. Entomol. 95:6-13.

36 5

Crocker, R.L. , and W.H. Whitcomb. 1980. Graham, H.M., C.G. Jackson, and Feeding niches of the big-eyed bugs J.W. Debolt. 1986. Lygus spp. Geocoris bullatus G. , punctipes , and G. (Hemiptera: Miridae) and their parasites uliginosus (Hemiptera: Lygaeidae: in agricultural areas of southern Geocorinae) . Environ. Entomol. 9:508-513. Arizona. Environ. Entomol. 15:132-142.

Crosby, C.R., and M.D . Leonard. 1914. Gupta, R.K., G. Tamaki, and The tarnished plant bug. Cornell Agr. C.A. Johansen. 1980. Lygus bug damage, Expt . Sta. Bui. 346:461-526. predator-prey interaction, and pest management implications on alfalfa grown Dasch, C.E. 1971. Subfamily for seed. Wash. State Univ. Tech. Bui. Mesochorinae . No. 6. Ichneumon-flies of 92, 18 pp. America north of Mexico. Mem. Amer. Entomol. Inst. 16, 376 pp. Hardee, D.D., H.Y. Forsythe, Jr., and G.G. Gyrisco. 1963. A survey of the Day, W.H. 1971. Reproductive status and Hemiptera and Homoptera infesting grasses survival of alfalfa weevil adults: (Graminae) in New York. Jour. Econ. Effects of certain foods and Entomol. 56:555-559. temperatures. Ann. Entomol. Soc. Amer. 64:208-212. Hendrickson, R.M., Jr., and J.A. Plummer. 1983. Biological control Day, W.H. 1981. Biological control of of alfalfa blotch leafminer (Diptera: the alfalfa weevil in the northeastern Agromyzidae) in Delaware. Jour. Econ. United States. In Papavizas, G.C., ed., Entomol. 76:757-761. Biological Control in Crop Production, pp. 361-374. Beltsville Symp. Agr. Res. Jackson, C.G., and H.M. Graham. 1983. No. 5, 461 pp. Allenheld, Osraun Co., Parasitism of four species of Lygus Totowa, N.J. (Hemiptera: Miridae) by Anaphes

ovi jentatus (Hymenoptera : Mymaridae) and Day, W.H., L.W. Coles, J.A. Stewart, and an evaluation of other possible hosts. R.W. Fuester. 1971. Distribution of Ann. Entomol. Soc. Amer. 76:772-775.

Micr oc tonus aethiops and M. colesi , parasites of the alfalfa weevil, in the Johnson, E., ed. 1982. Hay, alfalfa, eastern United States. Jour. Econ. and alfalfa mixtures. Ln Agr. Statistics Entomol. 64:190-193. 1982. 566 pp. U.S. Dept. Agr., Washington, D.C. Drea, J.J., Jr., L. Dureseau, and E. Rivet. 1973. Biology of Peristenus Kamm, J.A. 1979. Plant bugs: Effects of stygicus from Turkey, a potential natural feeding on grass seed development; and enemy of lygus bugs in North America. cultural control. Environ. Entomol. Environ. Entomol. 2:278-280. 8:73-76.

Graham, H.M. 1982. Interbreeding of Kelton, L.A. 1975. The lygus bugs Lygus elisus Van Duzee and L,. desertinus (genus Lygus Hahn) of North America

Knight in the field. Southwest. Entomol. (Heteroptera : Miridae). Entomol. Soc. 7:60-64. Canada Mem. 95, 101 pp.

Graham, H.M., C.G. Jackson, and Khattat, A.R. , and R.K. Stewart. 1980. G.D. Butler. 1982. Composition of the Population fluctuations and interplant lygus complex in some crop and weed movements of Lygus lineolaris . Ann. habitats of Arizona. Southwest. Entomol. Entomol. Soc. Amer. 73:282-287. - 7 : 10 1 10 . Knapp, W.R., and R.R. Seaney, eds. 1979. Cornell field crops handbook. N.Y. State Col. Agr. Bui. 5516-A, 160 pp.

37 : .

Knight, H.H. 1922. Nearctic records for Loan, C.C. 1974b. The European species species of Miridae known heretofore only of Leiophron Nees and Peristenus Foerster from the Palearctic region. Can. (Hymenoptera: Braconidae, Euphorinae). Entomol. 53:280-288. Trans. Roy. Entomol. Soc. Lond. 126:207-238. Knight, H.H. 1923. Miridae. In Loan, C.C. 1979. Three new species of Britton, W.E., ed. , Hemiptera or Sucking Insects of Connecticut. State Geol. and Peristenus Foerster from Canada and Nat. Hist. Bui. 34, 807 pp. Western Europe (Hymenoptera: Braconidae, Euphorinae). Naturaliste Can. Knight, H.H. 1941. The plant bugs, or 106:387-391. Miridae, of Illinois. Nat. Hist. Div. Bui. 22, 234 pp. Loan, C.C. 1980. Plant bug hosts

(Heteroptera : Miridae) of some euphorine Kurczewski, F.E., and D.J. Peckham. parasites (Hymenoptera: Braconidae) near 1970. Nesting behavior of Anacrabro Belleville, Ontario, Canada. Naturaliste ocellatus ocellatus (Hymenoptera Can. 107:87-93.

Sphecidae) . Ann. Entomol. Soc. Arner. 63:1419-1424. Loan, C.C., and T. Bilewicz-Pawinska. 1973. Systematics and biology of four Leigh, T.F., and D. Gonzalez. 1976. Polish species of Peristenus Foerster Field cage evaluation of predators for (Hymenoptera: Braconidae, Euphorinae). control of Lygus hesperus Knight on Environ. Entomol. 2:271-278. cotton. Environ. Entomol. 5:948-952. Newton, R.C., and R.R. Hill, Jr. 1970. Lim, K.P., and R.K. Stewart. 1976. Use of 1970 caged adult forage insects to Parasitism of the tarnished plant bug, determine their comparative roles in

Lygus lineolaris (Hemiptera: Miridae) , by delaying the regrowth of alfalfa. Jour. Peristenus pallipes and .P. pseudopallipes Econ. Entomol. 63:1542-1543.

(Hymenoptera: Braconidae) . Can. Entomol. 108:601-608. Osborn, H. 1918. The meadow plant bug, Miris dolobratus [sic]. Jour. Agr. Res. Loan, C.C. 1965. Life cycle and 15:175-200. development of Leiophron pallipes Curtis (Hymenoptera: Braconidae, Euphorinae) in Osborn, H. 1939. Meadow and pasture five mirid hosts in the Belleville insects. 288 pp. Educator's Press, district. Proc. Entomol. Soc. Ontario Columbus, Ohio. 95:115-121. Perkins, P.V., and T.F. Watson. 1972. Loan, C.C. 1970. Two new parasites of Nabis alternatus as a predator of Lygus the tarnished plant bug in Ontario: hesperus. Ann. Entomol. Soc. Amer. Leiophron pseudopallipes and Euphoriana 65:625-629. lygivora (Hymenoptera: Braconidae, Euphorinae). Proc. Entomol. Soc. Ontario Poinar, G.O., Jr. 1975. Entoraogenous 100:188-195. nematodes. A manual and host list of insect-nematode associations. 317 pp. Loan, C.C. 1974a. The North American Brill, Leiden. species of Leiophron Nees, 1818, and Peristenus Foerster, 1862 (Hymenoptera: Porter, B.J. 1979. Host selection in Braconidae, Euphorinae), including the Peristenus stygicus Loan (Hymenoptera: descriptions of 31 new species. Braconidae); an approach to the Naturaliste Can. 101:821-860. evaluation of host range for parasitoids. M.S. Thesis, Tex. A&M

Univ. , 55 pp

38 :

Radcliffe, E.B., and D.K. Barnes. 1970. Stephens, G.M. 1982. Plant bug fauna Alfalfa plant bug Injury and evidence of (Heteroptera: Miridae) of grasses plant resistance in alfalfa. Jour. Econ. (Poaceae) of Medicine Bow Mountains and Entomol. 63:1995-1996. Pole Mountain range district, Wyoming. Wyo. Agr. Expt. Sta., Sci. Monog. 43, Scott, D.R. 1983. Lygus hesperus Knight 175 pp. (Hemiptera: Miridae) and Daucus carota L.

(Umbellif lorae : Umbellif lerae) : An Stitt, L.L. 1948. Reduction of example of relationships between a vegetative growth of alfalfa by insects. phytophagous insect and one of its plant Jour. Econ. Entomol. 41:739-741. hosts. Environ. Entomol. 12:6-9. Van Steenwyk, R.A., and V.M. Stern. Shahjahan, M., and F.A. Streams. 1973. 1977. Propagation, release, and Plant effects on host-finding by evaluation of Peristenus stygicus , a Leiophron pseudopallipes (Hymenoptera newly imported parasite of lygus bugs. Braconidae) a parasitoid of the , Jour. Econ. Entomol. 70:66-69. tarnished plant bug. Environ. Entomol. 2:921-925. Watson, S.A. 1928. Miridae of Ohio. Ohio Biol. Survey Bui. 16:1-44. Sillings, J.O., and D.B. Broersma. 1974. The parasites of the tarnished Welch, H.E. 1965. Entomophilic plant bug Lygus lineolaris in Indiana. nematodes. Ann. Rev. Entomol. 10:275-302. Proc . North Cent. Branch, Entomol. Soc. Amer. 29:120-125. Wene, G.P., and L.W. Sheets. 1962. Relationship of predatory and injurious Slater, J.A. 1956. Megaloceroea insects in cotton fields in the Salt recticornis (Geoffr.), a mirid new to the River Valley of Arizona. Jour. Econ. eastern United States, with the Entomol. 55:395-398. description of a new genus of Stenodemini (Hemiptera: Miridae). Proc. Entomol. Wheeler, A.G., Jr. 1971. Studies on the Soc. Wash. 58:116-120. arthropod fauna of alfalfa. V. Spiders

(Araneida) . Can. Entomol. 105:425-432. Slater, J.A., and R.M. Baranowski. 1978. How to know the true bugs Wheeler, A.G., Jr. 1972. Studies on the (Hemiptera: Heteroptera) . 256 pp. Brown arthropod fauna of alfalfa. III. Pub. Iowa. , Dubuque, Infection of the alfalfa plant bug,

Adelphocoris lineolatus , by the fungus Sluss, T.P., H.M. Graham, and E.S. Entomophthora erupta. Can. Entomol. Sluss. 1982. Morphometric, allozyme, 104:1763-1766. and hybridization comparisons of four Lygus species (Hemiptera: Miridae). Ann. Wheeler, A.G., Jr. 1974. Studies on the Entomol. Soc. Amer. 75:448-456. arthropod fauna of alfalfa. VI. Plant bugs (Miridae). Can. Entomol. and Snodgrass, G.L. , W.P. Scott, 106:1267-1275. J.W. Smith. 1984. An annotated list of the host plants of Lygus lineolaris Wheeler, A.G. , Jr. 1976. Lygus bugs as (Hemiptera: Miridae) in the Arkansas, facultative predators. In Scott, D.R., Louisiana, and Mississippi Delta. Jour. and L.E. O'Keeffe, eds. , Lygus Bug: Host Ga. Entomol. Soc. 19:93-101. Plant Interactions, pp. 28-35. Univ. Idaho Press, Moscow. Southwood, T.R.E. 1956. The nomenclature and life cycles of the Wheeler, A.G., Jr. 1977. Studies of the European tarnished plant bug, Lygus arthropod fauna of alfalfa. VII. rugulipennis Poppius (Hemiptera: Predaceous insects. Can. Entomol. Miridae). Bui. Entomol. Res. 46:845-848. 109:423-427.

39 ,

BIOLOGICAL CONTROL OF LYGUS BUGS ON possibly to 500 m, by as much as 99 VEGETABLE AND FRUIT CROPS percent (Fye, 1980, 1982; Domek, 1982). As the altitude increases, this dominance By D.R. Scotti^ decreases. At 762 m, L. atrif lavus is the dominant species in alfalfa (Fisher and Shull, 1942). Above 1,200 m, the four Only plant bugs of the genus Lygus Hahn, major species are almost absent, with the as described and restricted by Kelton other five--L. robustus , L. atrif lavus ,

(1975), are considered here. Other L. nigrosignatus , L. ravus , and species of closely related genera, for L. shulli—becoming dominant (Domek, example, Adelphocoris lineolatus (Goeze) 1982). Since most of the U.S. vegetables or species of Lygus indigenous to the and fruits are grown below 1,200 m, few other continents, such as Lygus reports of damage by these five species rugulipennis Poppius, will cause the same are in U.S. crop protection literature. type of damage and affect many of the Higher latitudes have much the same same crops. In North America, 34 of the effect on flora and fauna as higher 43 recognized species of this genus altitudes; therefore, more reports of occur. Of these 34, Lygus lineolaris damage to all crops by Lygus species

(Palisot) , L. hesperus Knight, L. elisus other than the four dominant ones are Van Duzee, and L. desertinus Knight are present in Canadian literature. the most important economically. Lygus bugs are among the most insidious Some of the vegetables and fruits that pests of vegetables and fruits. These are plant hosts of lygus bugs are listed insects are especially troublesome in in the appendix. Based on information that much of their damage may go about hosts of these plant pests, two unnoticed, especially in the seed crops. hypotheses can be made. First, probably The effect of lygus bugs on fruit was most plants used as vegetables and fruits noticed for many years before the by humans may be damaged by these insects magnitude of their damage to seed crops if the circumstances are right. Second, was known. although the four economic species of Lygus mentioned here are responsible for "Catfacing" of peach and "apical most of the damage reported, other seediness" of strawberries are species can and will inflict the same deformities that are apparent when the type of damage under different fruit matures, if not earlier. Reduction conditions. These species include, but of seed yields is not so readily are not limited to, Lygus robustus apparent, especially if no "uninfested

(Uhler) , L. atrif lavus Knight, control" yields are available for L. nigrosignatus Knight, L. ravus comparison. The research of Sorenson Stanger, and L. shulli Knight. According (1932) on alfalfa and Shull (1933) on to some authors (Fisher and Shull, 1942; beans paved the way for elucidating the

Frick, 1972) , these species can inflict effects of Lygus on seed yields. Flemion the same type and degree of damage as any et al. (1949) pioneered the of the four economic species. Also, they investigations of the effects of lygus share many of the same hosts (Domek and bugs on seed germination and the reasons Scott, 1985). Whether they inflict for those effects. Following these early damage on any vegetable or fruit crop is reports, many investigators have reported probably an accident of proximity. on the effects of feeding on vegetable and fruit crops. The four major species dominate lygus bug populations at the lower altitudes, Lygus bugs, as well as some other mirids, are especially devastating to seed crops because they tend to concentrate their Professor emeritus, Department of feeding on developing flowers and Entomology, College of Agriculture, seeds. When feeding, they inject a University of Idaho, Moscow, ID toxic substance, which tends to liquefy 83843-4196.

40 . .

plant cell contents so that they can be other Lygus species and plant hosts may

Ingested by the insect (Hori, 1976). have the same limitation. ) Spraying the Some of this toxic substance undoubtedly plant with a sugar solution apparently remains in the plant and results In a satisfies the insects needs, and they small necrotic spot at the site of will then reproduce. Butler suggested stylet insertion. However, the salivary that aphid honeydew could serve the same secretion also contains a growth- purpose. On carrot, L. hesperus and promoting factor. This factor L. elisus only oviposited in flowering causes increased growth around the umbels. No nymphs hatched in umbels original necrotic spot of stylet collected at the petal fall stage or insertion (Hori, 1976). later (Scott et al., 1966). This indicates that lygus bugs will only When the embryo of the seed is not utilize plants as oviposition sites affected by the initial effects of lygus during a short time in the plant bug feeding, the growth-promoting development. In the laboratory, these substance apparently stays in the seed. pests will oviposit in bean or lentil Plants grown from such seeds, for pods or other plant parts. Possibly example, beans and carrot, are more they may do so in the field in the vigorous and produce more than plants absence of preferred sites. grown from seeds not fed on (Scott,

1970) . The growth-promoting substance In an intensive study of lygus bugs and apparently has some effect on the their host plants, few were found on concentration of indole acetic acid. At plants that were not in the reproductive least carrot seed developed on lygus stage (Domek, unpub.). Of those records bug-infested umbels may have as much as of hosts that were not in this stage, a ninefold increase of the acetic acid most lygus bugs were on mullein, compared with seeds not exposed to Verbascum thapsus L. , in the late fall feeding during development (Scott, and early spring (Domek, 1982)

1983) . Also a proteinase inhibitor Apparently this plant is an important inducing factor (PIIF) apparently may be overwintering host. Since it is a increased following feeding by Lygus biannual with succulent foliage in late hesperus (Scott, 1983). This PIIF may fall, it can provide sustenance when also cause increased indole acetic acid most host plants are dead (McAtee, 1924). content. PIIF could inhibit a factor that destroys or "ties up" the acetic Much has been reported concerning the acid and thus results in higher levels role of "weed" hosts in Lygus population in the seed. buildup, especially in the spring (Stitt, 1949; Malcolm, 1953; Fye, 1980, PLANT HOST REQUIREMENTS 1982). However, few articles mention the role of these hosts as primary Apparently lygus bugs will attack many attractants for parasites and predators species of plants. However, a (Taksdal, 1961). This attractiveness succession of plants in the reproductive could be both good and bad for Lygus stage through the spring and summer is control on crops. A buildup of natural required to develop damaging populations enemies may reduce or "brake" lygus bug (Domek, 1982). Alternatively, host population buildup and thus leave fewer sources such as alfalfa or carrot, which to migrate to the food crops. flower continuously once bloom is Conversely, if these "weed" hosts were initiated, serve as a substitute for the close to the food crop, most of the host sequencing (Domek, 1982) parasites would be searching these plant hosts for their prey. Strip-cutting

According to Butler (1968) , L. hesperus alfalfa (Stern, 1976) did impinge on the cannot reproduce on alfalfa while it is idea of keeping natural enemies of Lygus in the vegetative phase. (Presumably in the desired crop.

41 )

PROSPECTS FOR BIOLOGICAL CONTROL mutations occurred in all three groups — the natural enemies, the Lygus The classical definition of biological species, and their plant hosts. Many of control is that method that uses such these mutations had no effect on the natural enemies as parasites, predators, natural enemy-lygus bug symbiosis. and diseases to achieve a measure of However, a few probably occurred that pest control. That is the context in had some effect on that relationship, which it is discussed here. However, a either detrimental to or favorable for gray area exists, which could include the survival of the natural enemy. One the use of sprays or dusts to keep of those that favored the natural natural enemies on, or attract them to, enemies apparently was involved in their crops to be protected. Somewhat allied, searching capability. Apparently, but even further removed from survival of the natural enemies was biocontrol, is genetic control, higher when they could identify the especially biogenetic engineering. possible host plants of Lygus bugs and then search those plants. A thorough discussion of the native and introduced parasites of lygus bugs has With human introduction of many plants, been presented elsewhere in this accidental (such as Ant'hemis cotula L., publication. Since little can be added Hypericum perforatum L.) or purposeful as far as the natural enemies of Lygus (most of the vegetables and fruits), the pests of vegetable crops are concerned, original "search mechanism" of the this discussion is mainly confined to natural enemies would not lead them to some of the philosophical and other the introduced plant species. The

aspects of possible biocontrol of Lygus . parasites mostly flew over the introduced species and concentrated on Schuster (p. 14) wrote that the native plant hosts (Taksdal, 1961).

".. .predators. . .have not been On the other hand, the lygus bugs, being extensively evaluated. . .but the "fast food connoisseurs" (Domek, 1982), literature contains numerous references made the switch and utilized many of

to. . .predation by both insects and these new plant species as hosts. In spiders...." In the intensive study by one study of Lygus species and their Domek and Scott (1985), Domek observed plant hosts (Domek and Scott, 1985), aphid-tending ants, crab spiders, and about half of the 70 plant hosts asilid flies with Lygus prey. utilized for food or oviposition were Furthermore, he observed that lygus bugs introduced. were not present on plant hosts when the aphid-tending ants were, although the When European settlers introduced their lygus bugs were on nearby plants free of food plants and did not utilize native ants. Also, Tamaki (pers. commun. plants, the stage was set for the high reported that big-eyed bugs, Geocoris pest status of Lygus species. Taksdal sp., were effective predators of early (1961) reported that Lygus lineolaris nymphal stages of lygus bugs, but not of was parasitized less than 5 percent on more mature stages. Damsel bugs, Nabis an introduced crop, whereas in adjacent spp., were effective against all stages, native "weeds," the same species of but males were less so than females. Lygus had a 30 percent parasite The spined assassin bug, Sinea diadema infestation. A consistent 30 percent (F.), was an effective predator, but it reduction of lygus bugs in our food, also preyed on many beneficial insects. fiber, and forage crops would eliminate or drastically reduce the Lygus problem. Native Species of Natural Enemies Introduced Species These species have evolved with the native Lygus species and their plant Several exotic parasites of Lygus bugs hosts on this continent for millions of and related species have been introduced years. During those years, many genetic into the United States. This program

42 has not met with great success. Again, problem could be undertaken. First, the the millions of years of coevolution of genes in the exotic parasites that are the parasite with its host and its host involved in searching for plant hosts of plant provide the answer. The their prey could be identified and introduced parasites are well equipped transferred into the most efficient of to search the vegetable and fruit crops the native parasites. Second, the genes for their prey. They may do well with in native parasites that are responsible the Lygus species in their native lands, for successful parasite development in as Lygus rugulipennis , but their native species of Lygus could be phytogenetic development has not identified and transferred into exotic equipped them to deal with, to them, parasite species. Thus biogenetic exotic hosts, apparently. Possibly the engineering could proceed along two mechanisms developed for successful paths that would require intensive study attack on the Lygus spp. in their of the genes in both native and exotic geographic area do not work on these parasites. "exotic" hosts. One must wonder at the damage that L. lineolaris might inflict REFERENCES CITED on the crops in Europe. Butler, G.D., Jr. 1968. Sugar for the ATTRACTANTS survival of Lygus hesperus on alfalfa. Jour. Econ. Entomol. 61:854-855. Techniques to attract and keep natural enemies can be called the use of Domek, J.M. 1982. Plant hosts of attractants to control pests. When species of Lygus Hahn (Hemiptera: these attractants come from host plants Miridae) in the Lewiston-Moscow area of or host insects, this practice verges on Idaho. M.S. Thesis, Univ. Idaho, Moscow. biological control. Hagen and Hale (1974) reported on the use of food Domek, J.M., and D.R. Scott. 1985. sprays to attract and keep populations Species of the genus Lygus Hahn and of predators when the populations of their host plants in the Lewiston-Moscow

their natural prey were low. Their area of Idaho (Hemiptera: Miridae) . technique has not been very successful. Entomography 3:75-105.

A technique that might have value would Fisher, R.A. , and W.E. Shull. 1942. be to protect crops with a spray of Insecticidal control of legume bugs in ground, or synthesized, material from a seed alfalfa. Jour. Econ. Entomol. preferred native host of lygus bug. If 35:503-507. successful, the attractive ingredients

could be synthesized on a large scale. Flemion, F. , H. Poole, and J. Olson. The complex relationships between host 1949. Relation of lygus bugs to plants, phytophagous insects, and insect embryoless seeds in dill. Contrib. parasites are detailed by Price (1975). Boyce Thompson Inst. Plant Res. 15:299-310. BIOGENETIC ENGINEERING

Frick, K.E . 1972. Third list of This topic would normally be under insects that feed upon tansy ragwart, the United genetic control. However, when Senecio jacobaea , in the Western objective is to engineer a more States. Ann. Entomol. Soc. Amer. efficient parasite, then it is also 65:629-631. biocontrol. The dilemma facing biocontrol of lygus bugs—that of native Fye R.E. 1980. Weed sources of lygus , parasites searching noncrop hosts or bugs in the Yakima Valley and Columbia that of exotic parasites not able to Basin in Washington. Jour. Econ. complete development on native species Entomol. 73:469-473. of Lygus—may be solved by genetic engineering. Two approaches to the

43 :

Fye, R.E. 1982. Weed hosts of the Scott, D.R., A.J. Walz, and H.C. Manis. lygus (Heteroptera : Miridae) complex in 1966. The effect of Lygus spp. on central Washington. Jour. Econ. carrot seed production in Idaho Entomol. 75:724-727. (Hemiptera: Miridae). Idaho Agr. Expt. Sta. Res. Bui. 69, 12 pp. Hagen, K.S., and R. Hale. 1974. Increasing natural enemies through use Shull, W.E. 1933. An investigation of of supplementary feeding and non-target the Lygus species which are pests of prey. In Maxwell, F.G., and F.A. beans (Hemiptera: Miridae) . Idaho Agr. Expt. Sta. Res. Bui. 11, 42 Harris, eds. , Proc. Summer Inst. Biol. pp. Control Plant Insects and Dis. Univ. Miss. Press, Jackson. Sorenson, C.J. 1932. The tarnished plant bug Lygus pratensis (Linn.) and Hori, K. 1976. Physiological changes the superb plant bug Adelphocorus in host and insect. In Scott, D.R., and superbus (Uhler) in relation to flower L.E. O'Keeffe, eds., Lygus bug: Host drop in alfalfa. Utah Acad. Sci. Proc. Plant Interactions. Proc. workshop XV 9:67-70. Internatl. Cong. Entomol., Aug. 19-28, Washington, D.C., pp. 19-25. Univ. Stern, V.M. 1976. Ecological studies Idaho Press, Moscow. of lygus bugs in developing a pest management program for cotton pests in lygus bugs the San Joaquin Valley, California. In Kelton , L. A. 1975. The (genus Lygus Hahn) of North America Scott, D.R., and L.E. O'Keeffe, eds., (Heteroptera: Miridae). Entomol. Soc. Lygus Bug: Host Plant Interactions. Canada Mem. 95:1-101. Proc. workshop XV Internatl. Cong. Entomol., Aug. 19-28, Washington, D.C., McAtee, W.L. 1924. Mullen rosettes as pp. 8-13. Univ. Idaho Press, Moscow. winter shelters for insects. Jour. Econ. Entomol. 17:414-415. Stitt, L.L. 1949. Host plant sources of Lygus species infesting the alfalfa Malcolm, D.R. 1953. Host relationship seed crop in southern Arizona and studies of Lygus in south-central southwestern California. Jour. Econ. Washington. Jour. Econ. Entomol. Entomol. 42:93-99. 46:435-488. Taksdal, F. 1961. Ecology of plant Price, P.W. 1975. Insect ecology. 514 resistance to the tarnished plant bug, pp. John Wiley and Sons, New York. Lygus lineolaris (P. de B.). M.S. Thesis, Cornell Univ., Ithaca, N.Y. Scott, D.R. 1970. Feeding of Lygus bugs (Hemiptera: Miridae) on developing carrot and bean seed: Increased growth and yields of plants grown from that seed. Ann. Entomol. Soc. Amer. 63:1604-1608.

Scott, D.R. 1983. Lygus hesperus Knight (Hemiptera: Miridae) and Daucus carota L. (Umbellif lorae

Umbellif lerae) : An example of relationships between a polyphagous insect and one of its plant hosts. Environ. Entomol. 12:6-9.

44 . ) ) )

APPENDIX

This is an annotated listing of vegetables and fruits used as hosts by Lygus spp. The numbers in parentheses refer to citations at the end.

Lygus spp.

Apple: Malus sylvestris Mill. elisus (1), hesperus (20), lineolaris (26) Apricot: Prunus armeniaca L. hesperus (30) Artichoke: Cynara scolymus L. hesperus (30) Asparagus: As paragus officinalis L. hesperus (30), lineolaris (8) Bean, broad: Vicia faba L. hesperus (30) Bean, garden: Phaseolus vulgaris L. desertinus (21), elisus (32), hesperus (30), lineolaris (11), (17) Bean, lima: P. lunatus L. hesperus (30), lineolaris (23) Beet: Beta vulgaris L. desertinus (21), elisus (32), hesperus (30), lineolaris (26 Broccoli: Brassica oleracea L. lineolaris (26 Cabbage: _B. oleracea L. hesperus (30), lineolaris (26) Carrot: Daucus carota L. elisus (32), hesperus (30), lineolaris (7) Celery: Apium graveolens L. atriflavus (15), hesperus (30), lineolaris (18) Cherry: Prunus sp. lineolaris (19 Chicory: Cichorium intybus L. atriflavus (14), elisus (14), hesperus (14), ravus (14), robustus (14), shulli (14) Chokecherry: Prunus virginiana L. lineolaris (26) Corn, sweet: Zea mays L. hesperus (30), lineolaris (24) Cucumber: Cucumis sativus L. hesperus (30), lineolaris (8) Currant, black: Ribes nigrum L. lineolaris (26) Dill: Anethum graveolens L. elisus (29), hesperus (30) Eggplant: Solanum melongena L. hesperus (30) Endive: Cichorium endivia L. lineolaris (6) Escarole: C. endivia L. lineolaris (6) Fig: Ficus carica L. hesperus (30) Horseradish: Armoracia rusticana lineolaris (26) Gaertn., Mey., & Scherb. Lentil: Lens culinaris Medik. elisus (25), hesperus (25), robustus (25) Lettuce: Lactuca sativa L. hesperus (30), lineolaris (26) Mustard: Brassica juncea (L. borealis (Keltonl (20), lineolaris (22), Czern. & Coss. nigrosignatus (20) Onion: Allium cepa L. lineolaris (31~X Parsnip: Pastinaca sativa L. hesperus (30) Pea, black-eyed: Vigna hesperus (30)

unguiculata (L. ) Walp Pea, garden: Pisum sativum L. hesperus (30), lineolaris (9) Peach: Prunus persica (L.) Batsch elisus (3), hesperus (30), lineolaris (13), nigrosignatus (20) Pear: Pyrus communis (L.) elisus (1), hesperus (30), lineolaris (4) Pecan: Carya illinoensis (Wangenh.) lineolaris (12) K. Koch Pepper: Capsicum annuum L. hesperus (30), lineolaris (23) Peppermint: Mentha piperita L. elisus (21), hesperus (30), nigrosignatus (21) Plum: Prunus spp. lineolaris (27) Potato: Solanum tuberosum L. elisus (21), hesperus (30), lineolaris (18) Prune: Prunus domestica L. lineolaris (2dl Radish: Raphanus sativus L. hesperus (30) Raspberry, red: Rubus idaeus L. lineolaris (5)

45 . . ) . . )

Sesame: Sesamum indicum L. hesperus ( 30 Spinach: Spinacia oleracea L. elisus (33), hesperus (30) lineolaris (10) Squash: Cucurbita spp. lineolaris (11), (16) Strawberry: Fragaria spp. hesperus (30), lineolaris (26), shulli (32) Sunflower: Helianthus annuus L. desertinus (14), elisus (14), hesperus (14) Sweetpotato: Ipomea batatas (L. hesperus (30 Lam. Swiss chard: Beta vulgaris L. lineolaris (26) Tomato: Lycopersicon esculentum elisus (2), hesperus (30), lineolaris (26) Mill. Turnip: Brassica rapa L. hesperus (30), lineolaris (26) Watermelon: Citrullus lanatus hesperus (30) (Thunb.) Matsum & Nakai

( 1 ) Anon . 1952. Coop. Econ Insect Rpt 2: 359.

( 2 ) Anon 1954. Coop. Econ Insect Rpt 4: 1050. (3) Anon 1958. Coop. Econ Insect Rpt 8: 585. (4) Anon 1959. Coop. Econ Insect Rpt 9: 353.

(5) Anon 1961. Coop. Econ. Insect Rpt . 11 : 721 .

( 6 ) Anon . 1964. Coop. Econ. Insect Rpt . 14 : 943.

. ;. . (7) Burbutis, P.P . , and M.S. Conrad 1958 Coop Econ. Insect Rpt 8:930.

i # ( 8 ) Burbutis, P.P . , and M.S. Conrad 1959 Coop Econ. Insect Rpt. 9:572,

604 . (9) Burbutis, P.P., and L.P. Kelsey. 1964. Coop. Econ. Insect Rpt. 14:577.

( 10 ) Burbutis, P.P., and A.H. Mason. 1959. Coop. Econ. Insect Rpt. 9:995. (ID Burbutis, P.P., and A.H. Mason. 1961. Coop. Econ. Insect Rpt. 11:778.

( 12 ) Butram, J.R. 1962. Coop. Econ. Insect Rpt. 12:436. (13) Chandler, S.C. 1952. Coop. Econ. Insect Rpt. 2:7. (14) Domek, J.M., and D.R. Scott. 1985. Species of the genus Lygus Hahn and their host plants in the Lewiston-Moscow area of Idaho (Hemiptera: Miridae). Entomography 3:75-105. (15) Frick, K.E. 1972. Third list of insects that feed upon tansy ragwort, Senecio jacobaea, in the Western United States. Ann. Soc. Entomol. Amer. 65:629-631. (16) Grimes, W.H. 1958. Coop. Econ. Insect Rpt. 8:367. (17) Hagel, G.T. 1978. Lygus spp.: Damage to beans by reducing yields, seed pitting, and control by varietal resistance and chemical sprays. Jour. Econ. Entomol. 71:613-615. (18) Hutson, R. 1952. Coop. Econ. Insect Rpt. 2:179. (19) Hutson, R. 1953. Coop. Econ. Insect Rpt. 3:348.

( 20 ) Kelton, L.A. 1955. Species of Lygus , Liocoris , and their allies in the Prairie Provinces of Canada (Hemiptera: Miridae). Can. Entomol. 87:531-556.

( 21 ) Malcolm, D.R. 1953. Host relationship studies of Lygus in south-central Washington. Jour. Econ. Entomol. 46:485-488.

( 22 ) Meredith, W.R., and M.L. Laster. 1975. Agronomic and genetic analysis of tarnished plant bug tolerance in cotton. Crop Sci. 15:535-538.

46 (23) Milliron, H.E. 1955. Coop. Econ. Insect Rpt. 5:796. (24) Nettles, W.C., and M.D. Farrar. 1953. Coop. Econ. Insect Rpt. 3:192. (25) O'Keeffe, L.E. Unpublished data. (26) Painter, R.H. 1927. Some notes on the oviposition habits of the tarnished plant bug, Lygus pratensis Linn., with a list of host plants.

Ann. Rpt. Entomol. Soc . Ontario 57:44-46. (27) Rings, R.W. 1957. Coop. Econ. Insect Rpt. 7:339. (28) Rings, R.W. 1958. Coop. Econ. Insect Rpt. 8:384. (29) Scott, D.R. 1961. Coop. Econ. Insect Rpt. 11:721. (30) Scott, D.R. 1977. An annotated listing of host plants of Lygus hesperus Knight. Bui. Entomol. Soc. Amer. 23:19-22. (31) Severin, H.H.P., and H.C. Severin. 1915. Life history, natural enemies and the poisoned bait spray as a method of control of the imported onion

fly ( Phorbia cepetorum Mead) with notes on other onion pests. Jour. Econ. Entomol. 8:342. (32) Shull, W.E. 1933. An investigation of the Lygus species which are pests of beans (Hemiptera: Miridae). Idaho Agr. Expt. Sta. Res. Bui. 11, 42 pp. (33) Woodward, R.F. 1958. Coop. Econ. Insect Rpt. 8:297. . . .

BIOLOGICAL CONTROL EFFORTS ON MIRIDAE IN Canada are Peristenus (formerly Leiophron CANADA ) pallipes (Curtis) and _P. pseudopallipes (Loan) . In Ontario, _P pallipes attacks first-generation By C. Harvey Craig and Conrad C. Loani:^ . nymphs feeding on forage legumes, and Although many species of the family .P. pseudopallipes attacks Miridae (Heteroptera) are economically second-generation nymphs feeding mainly important pests of field, fruit, and on several weed species. The incidence vegetable crops, they have only recently of parasitism was 45 to 60 percent by received attention in Canada as targets P_. pallipes in the first generation and 8 for biological control. Research was to 12 percent by _P. pseudopallipes in the undertaken to integrate a biological second generation, with good component into ongoing control programs host-parasite synchrony (Loan, 1965, for rairid pests of alfalfa grown for seed 1970, 1980). In southwestern Quebec, the in western Canada and of vegetables in incidence of parasitism in L. lineolaris Quebec. To date, emphasis has been on by combined £. pallipes and P_. certain species of Lygus Hahn and the pseudopallipes was 7 percent in a weedy alfalfa plant bug, Adelphocoris habitat and 4.7 percent in an alfalfa habitat; host and parasites were not well lineolatus (Goeze) , and their associated euphorine parasites, Peristenus Foerster. synchronized in that area (Lim and Stewart, 1976a). BIOCONTROL AGAINST LYGUS In the prairie area of western Canada, In western Canada, the species of Lygus parasitism of first-generation Lygus spp. most abundant on alfalfa include by j?. pallipes averaged 22 percent (Loan and Craig, 1976) and 34 percent (Moline, L. borealis (Kelton) , L. lineolaris

1983) . Euphorine parasitism has also (Palisot) , L. desertinus been confirmed in the second generation, Knight, L. unctuosus (Kelton) , and L elisus Van Duzee (Kelton, 1975). South but the parasite species is not known of about latitude 50° N. these species (Moline, 1983; Craig, unpub.). Maximum are partially bivoltine; about 70 percent parasitism in both generations is of the summer adults become reproductive coincident with peak host nymphal and produce a second generation. population, an indication of good Progressively northward a smaller synchrony (Moline, 1983). In Lygus proportion of summer adults becomes populations from 43 southern Alberta reproductive, until north of latitude alfalfa seed fields, in which parasitism 53°30' N. no summer adults become ranged from 2 to 83 percent, no reproductive in the same year and the correlation was found between the maximum species are entirely univoltine (Craig, level of parasitism in the first host

1983) . generation and the numerical size of the second host generation (Moline, 1983). In the agricultural regions of eastern Canada, the dominant species on alfalfa Loan (1965) briefly described the development of _P. pallipes on several is L. lineolaris , which is largely bivoltine, with about 88 percent of mirid hosts and outlined its life history summer adults becoming reproductive in Leptopterna dolabrata (L. ) The (Guppy, 1958; Loan, 1965). parasite oviposits in second-, third-, and occasionally in fourth-instar nymphs, Euphorine (Braconidae) parasites and development time is 5 to 6 weeks in indigenous in the Lygus population in the field. The mature larva emerges from either the fifth-instar nymph or the adult. The larva spins a cocoon in the

^/Respectively , Agriculture Canada soil and development proceeds to the late Research Station, 107 Science pupal stage. The pharate adult diapauses Crescent, Saskatoon, SK S7N 0X2, in the cocoon and emerges the following and Agriculture Canada Research spring Station, Ottawa, ON K1A 0C6.

48 Lim and Stewart (1976a, b) , working at production management practices, except MacDonald College, Quebec, reported insecticide treatment. seasonal similarities and differences in parasitism of L. lineolaris by both The following three methods were used to

_P. pallipes and JP. pseudopallipes in detect the presence of euphorine weedy and alfalfa habitats. They parasites: (1) Alfalfa and nearby host reported further on laboratory plant vegetation at the liberation sites development of these two species, with were sampled by sweep net to recover particular attention to a description of parasite adults. In three seasons' the immature stages of P. pseudo- sampling, 1980-82, only 70 adults were

pallipes. Broadbent (1976) , also captured and all were the native species

. of MacDonald College, conducted P . pallipes laboratory studies on the biology of an imported parasite, Peristenus stygicus (2) Late-instar Lygus nymphs were mass Loan. He concluded that this species collected from the sites and reared in possesses many desirable qualities for cages in a controlled environment to Lygus control, such as facultative obtain parasite cocoons. A technique diapause, relatively short developmental similar to that of Van Steenwyk and time, long adult lifespan, high level of Stern (1976) was used, with about equal parasitization, and ease of mass rearing. success in utilizing either a felt strip maze or peat moss as the A program to augment the native cocooning medium. Adult emergence from parasitism in Lygus populations in the cocoons has been very inconsistent western Canada by introducing euphorine from year to year and even from lot to parasites of European origin was started lot. Several combinations of duration in 1977-78. A contract was made with the and temperature of cold treatment to Commonwealth Institute of Biological break diapause and various incubation Control, European Station, Delemont, temperatures and humidities have been Switzerland, to supply the parasites. tested to improve emergence. Inconsist-

Peristenus spp. were reared to the cocoon encies still exist , but up to 85 stage at Delemont from the host Lygus percent emergence has been achieved with rugulipennis Poppius collected from a cold treatment of 210 days at 2°C alfalfa and red clover near the Tullner followed by an incubation period of 25 to Feld, Austria. Cocoons were shipped, 50 days at 22°. Also, from nonemerged usually in the fall, to the Biocontrol cocoons the pharate adult can be excised Unit of Agriculture Canada, Ottawa, for and identified. This method of rearing quarantine and overwintering, and in the and excision has yielded about 1,300 spring for rearing to adults under adults in the 3 seasons. All specimens controlled conditions. Because of obtained to date are the native parasite

limited resources at Saskatoon and other .P. pallipes . considerations, the direct release method of introduction was adopted. The (3) At least once each season, and synchrony of adult parasite emergence and always just prior to each release of release with optimum first-generation imports, samples of not less than 200 host development was of prime importance, Lygus specimens from the sites have been and in most instances this was achieved. dissected for parasite presence. From The sites selected for parasite release 1979 through 1983, during and since the were established alfalfa seed production introductions, the incidence of fields in several ecologically different parasitism has not changed, averaging locations in Saskatchewan and Alberta. 20 percent overall within a range of 1.6 During 1978-81, 1,960 P. digoneutis Loan to 50 percent and with no obvious and 64 stygicus specimens were increase at any individual release released (table 1). Their lifespan at site. After 4 years' introductions the liberation sites for monitoring (1978-81), followed by 3 years' purposes was about 5 years. During that monitoring (1980-82), there is no time they were subject to normal seed evidence that the introduced parasites have become established.

49 , , ) ;; ; ;;

Table 1 Liberations of Peristenus spp. in alfalfa against Lygus spp. and Adelphocoris lineolatus (Goeze) in western Canada

Date of Location of liberation liberation site Species Number

Lygus spp.

1978

June 7 Moose Jaw, SK; 50° N.; P. digoneutis 197 shortgrass prairie; dry

June 9 13, 21 Saskatoon, SK; 50° N. P. digoneutis 177 mixed prairie; dry

1979

21 AB; 50°30’ P. digoneutis 541 June 14 , Tilley, N.; shortgrass prairie; P. stygicus 41 irrigated

53° June 29 Shellbrook , SK; N. P, digoneutis 159 parkland-mixed forest; P. stygicus 23 dry

1980

May 30 Ardath, SK; 51°30' N.; P. digoneutis 167 mixed prairie; dry

Saskatoon, SK; mixed P. digoneutis 80 prairie; irrigated

June 3 Shellbrook, SK; P. digoneutis 261 (supplement to 1979 release)

June 10 Saskatoon, SK; P. digoneutis 138 (supplement to 1978 release)

1981

June 12 Yellow Creek, SK; 53° N. P. digoneutis 125 parkland; dry

Saskatoon, SK; P. digoneutis 115 (supplement to 1980 release)

Adelphocoris lineolatus (Goeze)

1980

July 2 Clavet, SK; 52° N.; P. adelphocoridis 47 mixed prairie; dry

Lygus spp.

July 8 Shellbrook SK; 53° N. P. adelphocoridis 29 parkland-forest; dry P. rubricollis 49

1981

June 5 Saskatoon, SK; 52° N. P. adelphocoridis 23 mixed prairie; dry

June 12 Yellow Creek, SK; 53° N. P. adelphocoridis 16 parkland; dry

June 26 Shellbrook, SK; P. adelphocoridis 12 (supplement to 1980 liberations

50 The work on parasitism in Lygus and bud. Damage is most severe to the other Peristenus biological studies flower buds (bud blast) and to the early under R.K. Stewart at MacDonald College blossoms. A population of 12-15 was largely discontinued in the late late-instar nymphs per 180° sweep of a 1970's. At the Saskatoon Research 38-cm net can prevent an alfalfa crop Station, no further introductions of from blooming. This insect reproduces Lygus parasites are planned at this on other forage legumes such as sainfoin time. Site and vicinity monitoring will and trefoil, but its injury to these continue on a modest scale to detect any crops has not been evaluated. indication of parasite establishment. In the early 1960 's at Belleville, One of the major constraints to research Ontario, and in northern Saskatchewan,

on Lygus , particularly in areas and on first-generation nymphs of A. lineolatus host plants where a complex of species were found to be parasitized by

occurs, is the lack of nymphal taxonomy Peristenus pallipes . The incidence, for the genus. The major problem in determined by dissection of nymphs, rearing Peristenus parasites is spotty ranged from 40 to 60 percent in Ontario and inconsistent adult emergence from to 3 percent in Saskatchewan (Craig, the cocoon. The key factors that 1963; Loan, 1965). From 1976 to 1980, initiate emergence in the pharate adult the incidence of euphorine parasitism are still unknown for diapausing averaged 0.3 percent, with a range of 0 Peristenus species. to 4 percent in midwestern populations. Only nymphs of the first generation were BIOCONTROL AGAINST ADELPHOCORIS parasitized; those of the second LINEOLATUS (GOEZE) generation, where parasitism occurs, were entirely parasite-free, as were the The alfalfa plant bug, Adelphocoris adults. No other nymphal parasites have

lineolatus , a native insect of Europe been found. and western Asia, was introduced into

North America at Cape Breton, Nova Scotia, Adelphocoris lineolatus , because of its Canada, about 1917. In the succeeding recent introduction to North America 50 years, it spread westward through from Europe without its specific agricultural areas of eastern and parasite, Peristenus adelphocoridis Loan central Canada to the foothills of the (Loan, 1979) or other parasite species, Rocky Mountains in western Alberta is considered to be an excellent (Craig, 1971). Throughout its range of candidate host for imported biocontrol distribution south of about latitude 50° agents. Consequently, the Delemont N., the species is largely bivoltine, Station of the Commonwealth Institute of with two complete generations a year in Biological Control has been requested to southern Ontario (Guppy, 1958; Loan, supply parasites in sufficient quantity for direct release into A. lineolatus 1965) , whereas in western Canada some individuals of the second generation do populations in western Canada. not reach maturity (Craig, unpub.). North of about latitude 53° N., the In the summers of 1979 and 1980, species is largely univoltine; only A. lineolatus nymphs were collected in about 5 percent of the eggs hatch the eastern Austria and reared at the year they are laid and no Delemont Station. Parasite cocoons from second-generation individuals reach these rearings were sent to the maturity (Craig, 1963). Biocontrol Unit of Agriculture Canada, Ottawa, for quarantine, overwintering, Adelphocoris lineolatus is an important and subsequent completion of rearing. pest of alfalfa seed production. In the spring of 1980, two species, Because it overwinters in the egg stage, Peristenus adelphocoridis and peak nymphal populations occur earlier P. rubricollis (Thomson), emerged from these cocoons. In the 1981 rearings, in the season than Lygus , at about the time that alfalfa is coming into flower only P. adelphocoridis was present. The

51 . ; . . : ,

adult parasites were shipped to the REFERENCES CITED Saskatoon Research Station for release in western Canada. A total of 127 Broadbent, A.B. 1976. Laboratory P. adelphocoridis and 49 ]?. rubricollis studies on the biology of Peristenus specimens were released directly into styglcus Loan (Hymenoptera: Braconldae) A. lineolatus populations in alfalfa a parasltoid of Lygus lineolaris (P. de

seed fields (table 1) . B.) (Hemiptera: Miridae) . M.S. Thesis,

Dept. Ent . , McGill Univ. , Montreal, Because of erratic emergence of parasite Quebec adults, the 1980 releases were not well synchronized with A. lineolatus Carl, K.P., and W. Bittermann. 1983.

development. This, and the few Alfalfa plant bug ( Adelphocoris

individuals released in the 2 years, lineolatus ) work in Europe In 1983. greatly reduced the likelihood of Commonw. Inst. Biol. Control, European establishment. From about 3,000 Sta. , Delemont, Switzerland, Rpt . , 11 pp. first-generation A. lineolatus specimens the sites in collected at release Craig , C.H. 1963. The alfalfa plant bug

1981-82, only 17 parasite cocoons were ( Adelphocoris lineolatus (Goeze) ) in obtained. No adults emerged, and 14 northern Saskatchewan. Can. Entomol. pharate adults excised from these 95:6-13.

.P . cocoons were all . pallipes Craig, C.H. 1971. Distribution of Constraints to this parasite Adelphocoris lineolatus (Heteroptera: introduction program have been the lack Miridae) in western Canada. Can. of a technique for continuous rearing of Entomol. 103:280-281. A. lineolatus and the difficulty of obtaining the large quantities of Craig, C.H. 1983. Seasonal occurrence parasites in Europe that are required of Lygus spp. (Heteroptera: Miridae) on for the direct release method of alfalfa in Saskatchewan. Can. Entomol. introduction. Consequently, the 155:329-331. research emphasis, under K.P. Carl at

Delemont , has latterly shifted to Guppy, J.C. 1958. Insect surveys of biological parameters in the European clovers, alfalfa, and birdsfoot trefoil Adelphocoris-Peristenus association in In eastern Ontario. Can. Entomol. both the laboratory and the field, with 90:523-531. the objective of developing techniques to obtain parasites in sufficient Kelton, L. 1975. The lygus bugs (genus quantity for direct release in western Lygus Hahn) of North America Canada. Considerable progress has been (Heteroptera: Miridae). Entomol. Soc made, and parasites may be available for Canada Mem. 95, 101 pp. 1985 introductions (Carl, 1983). Lim, K.P., and R.K. Stewart. 1976a. ACKNOWLEDGMENTS Parasitism of the tarnished plant bug,

Lygus lineolaris (Hemiptera: Miridae) , by the The authors acknowledge with thanks Peristenus pallipes and JP, pseudopallipes

contributions to content and manuscript (Hymenoptera : Braconidae) . Can. Entomol. review by A.P. Arthur and L. Burgess, 108:601-608. Agriculture Canada, Saskatoon, Saskatch- Coulson, ARS Beltsville Md ewan; J.R. , , . Lim, K.P., and R.K. Stewart . 1976b. Agriculture J.C. Guppy and J.S. Kelleher , Laboratory studies on Peristenus pallipes Canada, Ottawa, Ontario; D.K. Moline, and jP. pseudopallipes (Hymenoptera: Creston, British Columbia; and R.K. Braconidae) parasitoids of the tarnished Stewart, McGill University, Montreal, plant bug, Lygus lineolaris (Hemiptera Quebec Miridae). Can. Entomol. 108:815-822,

52 Loan, C.C. 19b5. Life cycle and development of Leiophron pallipes Curtis (Hymenoptera: Braconidae, Euphorinae) in five mirid hosts in the Belleville district. Proc. Entomol. Soc. Ontario 95:115-121.

Loan, C.C. 1970. Two new parasites of the tarnished plant bug in Ontario: Leiophron pseudopallipes and Euphoriana lygivora. Proc. Entomol. Soc. Ontario 100:188-195.

Loan, C.C. 1979. Three new species of Pe ristenus Foerster from Canada and western Europe (Hymenoptera: Braconidae,

Euphorinae) . Naturaliste Can. 106:387-391.

Loan, C.C. 1980. Plant bug hosts

(Heteroptera : Miridae) of some parasites (Hymenoptera: Braconidae) near Belleville, Ontario, Canada. Naturaliste Can. 107:87-93.

Loan, C.C., and C.H. Craig. 1976. Euphorine parasitism of Lygus spp. in alfalfa in western Canada. Naturaliste Can. 103:497-500.

Moline, D.K. 1983. Parasitism by Peristenus pallipes and the subsequent development of Lygus populations in alfalfa grown for seed (Hym.: Braconidae;

Heteroptera: Miridae) . Report to Alberta Crops Research and Development Program.

(Unpub. ; contact author, Box 2176, Creston, BC, Canada, VOB 1G0.)

Van Steenwyk, R.A., and V.M. Stern. 1976. The biology of Peristenus stygicus

(Hymenoptera: Braconidae) , a newly imported parasite of lygus bugs. Environ. Entomol. 5:931-934. , ,

TAXONOMIC STATUS, BIOLOGICAL ATTRIBUTES, species, contribute to the difficulty in AND RECOMMENDATIONS FOR FUTURE WORK ON accurately assessing important economic THE GENUS LYGUS (HETEROPTERA: MIRIDAE) problems.

By Thomas J. Henry and John D. Lattiai^ ORIGIN OF PEST SPECIES

Pest status varies with the organism and Species of Lygus , frequently called lygus bugs, are the most important agricultural resource being evaluated. Acceptable pests in the plant bug family Miridae population levels may be low when dealing with disease vectors (Burgess (Heteroptera) . The tarnished plant bug, et al. Lygus lineolaris (Palisot) 1983) or much higher when considering occurring over most of North America, is certain defoliators. The pest problem a pest of cotton in the Southern United then is a relative state dependent on the States. In the Western United States, circumstances. Norton and Conway (1977, several species attack alfalfa and p. 205) provided a useful definition: "A cotton. Because of the severe damage pest problem is, therefore, characterized these plant bugs inflict, an extensive not only by the state of the pest search has been implemented by the U.S. population itself but, more importantly, Department of Agriculture and cooperating as the damage or illness it causes and agencies for natural enemies, especially the value placed on these consequences by nymphal parasites in the wasp family human society." Several Lygus spp. are Braconidae. This report is an overview considered pests because their feeding of the taxonomic status of the genus damage on certain crops is unacceptable Lygus to help biological control to those involved in crop production

researchers better understand the (Graham et al. , 1984). This damage often taxonomy of Lygus and the taxonomic is enhanced because lygus bugs frequently problems related to controlling this pest feed on reproductive parts of the plant group. and thus are frequently pests of seed

crops (Burgess et al. , 1983). The plant bug genus Lygus in North America contains several economically Some Lygus spp. have become pests because important species. They feed on a they are usually highly mobile, variety of crops and native plants. Some multivoltine , and oligophagous and species are widely distributed (r-selected) , feeding on new growth and broadly overlap the ranges of others. reproductive parts. In contrast to many Great morphological variation in adults other insect pests in North America, often makes positive identification these species are native insects difficult. At least some species of attacking a large array of introduced Lygus are parasitized regularly by crops, except in a few instances, such as Braconidae, chiefly in the nymphal an Oregon species that feeds on native stages. Positive identification of Lygus Limnanthes (meadowfoam) (J.D. Lattin, nymphs except in rare instances is not pers. observ. ) and a California species now possible. The variations caused by that attacks guayule (Romney, 1946; seasonal factors, the variety of host Bolton et al. , 1972; Lattin and Oman, plants, and genetic factors, coupled with 1983). Price (1976), Southwood (1977), the problem of identifying nymphs to and others have pointed out that many pest herbivores are r-selected species, and in the disturbed environments typical of most agroecosystems, such species can ^/Respectively Systematic Entomology , often colonize faster than their Laboratory, Agricultural Research predators and parasites. Southwood Service, U.S. Department of (1977) stated that polyphagous predators Agriculture, c/o National Museum of are likely to be important in such Natural History, Washington DC 20560, habitats. The neteropteran family and Systematic Entomology Laboratory, Nabidae contains several very common, Department of Entomology, Oregon polyphagous predators found frequently in State University, Corvallis, OR 97331. such disturbed habitats in North

54 . , , ,

America, for example, Nabis alternatus 1975; Scott, 1977; Fye, 1980; Snodgrass Parshley and N. americoferus Caravon et al., 1984). Since not all such plant (Graham and Jackson, 1982) records represent hosts on which eggs are laid, care should be taken to distinguish Lygus bugs, highly mobile as adults, between hosts, where nymphs occur, and often move from disturbed habitats into resting or feeding hosts, where only crop fields (Fye, 1980). Some species adults are found. Often host plant migrate from wild to cultivated plants records in the literature cannot be and have been collected at elevations as associated positively with species of high as 5,000 ft (Glick, 1939; Johnson Lygus because of the difficulty in making and Southwood, 1949). Although most accurate specific identifications and the Lygus spp. are normally multivoltine lack of voucher specimens, particularly single generations may occur in the in western North America. If voucher northern part of their ranges (Kelton, specimens have been retained from the 1975; Craig, 1983). At least one numerous economic studies (see Graham et species, Lygus unctuosus (Kelton) , may al., 1984), some associations can be have only a single generation (Kelton, verified or corrected. Fortunately the 1975; Craig, 1983). Other univoltine widespread Lygus lineolaris is more species of Lygus , for example, L. easily recognized throughout much of its vanduzeei Knight, normally are not range than is the complex group of economically important (Reid et al. western taxa. 1976). Care should be taken in determining the actual number of Because legumes frequently are utilized generations (Shull, 1933; Salt, 1945; as hosts by North American species of Craig, 1983). Lygus , it is curious that L. lineolaris , with a large array of hosts (Snodgrass et Feeding occurs most often on growing tips al. , 1984) , is not a pest on soybeans, or reproductive parts of the plant, areas even though this species occurs of high nutrients. This is particularly throughout much of the crop's range and damaging to plants grown for seed 453 insect species have been recorded (Jeppson and MacLeod, 1946; Craig, 1983; from this crop in North America (Kogan,

Rice et al. , 1985). According to Scott 1981) . The establishment and subsequent (1970, 1983), such feeding might reduce spread of alfalfa in western North seed yield and germination in carrots, America likely affected significantly the but the plants grown from damaged seed movement and colonization of western fed on by Lygus spp. may show accelerated species of Lygus bugs (Bolton et al. growth and larger plants and roots. 1972). The effect of such a crop on the Conversely, some evidence indicates that widely scattered, naturally occurring such feeding might stimulate increased populations of Lygus remains to be productivity in some crop species (Scott, studied. When positive species In the plant 1970). some instances, host identifications can be combined with may and fertility affect adult longevity accurate host associations, it will be in Lygus bugs (Al-Munshi et al., 1982). possible to examine the status and distribution of some western Lygus Lygus bugs also feed as scavengers and species. This may be an example of facultative predators of arthropods. "reverse" island biogeography, where a Predation on living insects probably crop plant provides a corridor for involves moribund individuals or those dispersal between naturally separated undergoing ecdysis (Wheeler, 1976). The populations. laboratory rearing of Lygus spp. may be enhanced by adding animal food to the DEFINITION AND PLACEMENT OF LYGUS IN THE diet (e.g., Bryan et al., 1976). FAMILY MIRIDAE

Several pest species of Lygus are known The group of bugs commonly referred to as to occur on a wide variety of plants, lygus bugs belongs in the genus Lygus both introduced and native (Stitt, 1949; Hahn and to the plant bug family Miridae, Malcolm, 1953; Parker and Hauschild,

55 . ,

the largest family in the true bug order the subgenus Exolygus to accommodate it Heteroptera (superorder Hemiptera) and allies. Leston (1952), in the first About one-third to one-half of all attempt to evaluate internal Heteroptera are mirids. Although fewer relationships of the genus on a worldwide than 7,000 species were listed in the basis, recognized six subgenera,

Carvalho world Miridae catalog (1957-60), including his new subgenus Taylorilygus , many have been described since the 1950's, which contained Lygus pallidulus probably bringing the total to 10,000 or (Blanchard) (as Lygus apicalis Fieber, a more. Most mirid workers predict that junior synonym) and the African "lygus the species inventory for the world will bugs." reach 20,000. Within the Miridae, Lygus is included in the largest subfamily, the Leston' s work served as the basis for an Mirinae. According to Carvalho (1957-60), important revision by Kelton (1955a), more than 250 mirine genera were who, by utilizing male and female described by 1955. Of these, Lygus genitalia and external morphology, gave (sensu lato) contained the greatest strong evidence that most of the number of species, about 300. subgenera previously placed in Lygus deserved generic status. He recognized Currently, however, only 34 species are as valid genera Agnocoris Reuter (type- placed in Lygus in North America and species Lygaeus rubicundus Fallen) about 8 are known from the Old World Liocoris Fieber (type-species Cimex (Kelton, 1975). The reduced tripustulatus Fabricius) (with Exolygus number of species recognized in Lygus Wagner as a junior synonym (type-species deserves some explanation. Historically, Cimex pratensis Linnaeus) ) , Lygus Hahn the broad definition of the Lygus was (type-species Cimex pabulinus Linnaeus), based largely on the overall similarity Ort hops Fieber (type-species Cimex kalmii of many species, which were Linnaeus), and Taylorilygus Leston inconsistently broken into several (type-species Lygus simonyi Reuter) similar appearing subgenera. Even so, (appendix). This revision produced the the economic literature on Lygus was result Slater (1950) had predicted should basically stable, and few entomologists several subgenera in Lygus be raised to were concerned that the pestiferous lygus genus, viz, that the economically bugs did not belong in the nominate important lygus bugs would be placed in a

. subgenus Lygus , that is, until more genus other than Lygus Because the recently, when the type of Lygus became North American lygus bugs are congeneric more than an academic problem. with Cimex pratensis (the type-species of Exolygus), Kelton' s revision required

The current classification of Lygus is that they be transferred to Exolygus . built primarily on the work of several Kelton (1955a, 1955b) considered Exolygus

key workers (appendix). Knight (1917) a junior synonym of Liocoris , meaning, provided the first comprehensive review that if this interpretation was followed, of the North American species. He the lygus bugs would take the generic

. recognized six species groups of Lygus , name Liocoris Wagner (1957), however, including his new subgenus Neolygus. maintained that Exolygus and Liocoris China (1941), on discovering that Distant were not congeneric, leaving the (1904) had designated Cimex pabulinus status of Exolygus problematic. Linnaeus as the type-species of Lygus, described the subgenus Apolygus To prevent such an upheaval in the (type-species Lygaeus limbatus Fallen) to economic literature, Carvalho, Knight, accommodate what he thought would include and Usinger (1961) , with the agreement of Lygus pratensis (L.) and other British most of the mirid-worker community, "lygus bugs" (China, 1943). Wagner including Kelton, petitioned the (1949), in a revision of the Palaearctic International Commission of Zoological Lygus , noted that the European L. Nomenclature (I.C.Z.N.) to reject Cimex pratensis was not consubgeneric with pabulinus as the type of the subgenus species in other subgenera and described

56 .. .

Lygus and to designate Cimex pratensis as to genera of North American Miridae. the type-species. The I.C.Z.N. (Opinion Its simple terminology with numerous 667, 1963) thus ruled to preserve the illustrations makes it a good generic well-known concept of Lygus with the reference following decisions: At the species level, Kelton's (1975) (1) Lygus Hahn, 1833 (fix Cimex revision of North American Lygus is the pratensis Linneaus, 1738, as the best reference to consult. It contains type-species) a key and descriptions of all recognized Exolygus Wagner, 1949 (type-species species, notes on their distribution and hosts, and clarification of earlier

Cimex pratensis Linneaus) , an misidentif ications of Palaearctic objective junior synonym of Lygus species. Although he reevaluated the to be placed on the list of Nearctic fauna and recognized several officially rejected names. synonyms, determination of species remains difficult, even for the (2) Lygocoris Reuter, 1875 (fix Cimex specialist with correctly identified pabulinus Linneaus, 1761, as the specimens for comparison. Most species type-species) of Lygus are multivoltine and have numerous seasonal or color forms, which These changes have insured that the compound the degree of difficulty in economic lygus bugs will remain in the species recognition. In table 1 is a genus Lygus and that Exolygus will summary of overwintering stages, always be a junior synonym because they voltinism, and host plant groups of have the same type-species. Presently, Lygus and associated genera. Current Liocoris is considered distinct from difficulties in associating certain Lygus, but if Kelton's conclusions are populations of Lygus with specific names followed, it becomes a junior synonym of indicate that some of the 34 Nearctic Lygus . species may be conspecific.

AND SPECIES RECOGNITION GENERIC Palaearctic Taxa Taxa Nearctic For the Palaearctic region, several good references can be used to identify identify species Anyone who has tried to genera and species. Southwood and of Lygus will agree that the genus is Leston (1959) provided a key to the difficult to define. particularly species and genera of the tribe Mirini in a monumental effort Carvalho (1955) found in the British Isles. Stichel’s illustrates it best. Of 154 probably (1958) publication is one of the best to the Genera mirine genera in his "Keys for the European species of Miridae. of the World," Lygus of the Miridae Kiritshenko's (1951) keys to the bugs of clear falls out at couplet 153, a the European U.S.S.R., although having most easily indication that the genus is an outdated generic scheme, can be used the other more diagnosed by eliminating for species identifications. Kerzhner's study, "distinct" genera. Carvalho's (1964) key is good for the genera and (1955a) and however, predated Kelton the species found in the European others who published their U.S.S.R.; Vinokurov's (1979) key is complex. interpretations of the Lygus available for the more eastern region of of the Kelton's (1955a) key to genera Yakut. Wagner's (1970-71) key to the if used in conjunction Lygus complex, Miridae of the Mediterranean region, keys of with the more comprehensive although still using the name Exolygus Blatchley (1926), Knight (1941, 1968), instead of Lygus , is the most recent and and Kelton (1980) to reach the Lygus comprehensive European reference. As in complex, will allow relatively easy North America, the species are variable recognition of the North American and often difficult to recognize with genera. Slater and Baranowski's (1978) certainty. publication contains the only recent key

57 .

Table 1 General life history and host information of Lygus and other genera previously included in the Lygus complex

Overwintering Number of Genus stage generations Hosts

Agnocoris Adult Multiple (?) Host specific on Salix spp.

Dagbertus Adult and egg (?) Multiple Polyphagous

Lygocoris

Subg. Apolygus Egg Single Polyphagous (?) weeds and trees

Subg. Lygocoris Egg Multiple Polyphagous

Subg. Neolygus Egg Single Host specific on trees and shrubs

Lygus 1/ Adult Multiple Polyphagous

Egg Single Host specific

Orthops Adult Multiple (?) Host specific on Umbelliferae

Pinalitus Egg Single Host specific on Picea and Pinus spp.

Tayiorilygus Adult and egg Multiple Polyphagous

i^Appears to have 2 distinct species groups.

IDENTIFICATION OF NYMPHS of classification, similar to that presented by Wagner (1949), is given. Late-instar nymphs of North American Users of these references need to update Miridae may be recognized using several the generic placement of the species nymphal keys, including DeCoursey treated

(1971) , Herring and Ashlock (1971) , and Slater and Baranowski (1978). Southwood Akingbohungbe et al. (1973) published (1956) developed a key for determining the only text containing nymphal keys to the instar of cimicomorphan nymphs. the genera of Miridae in North America. Leston and Scudder (1956) gave Their "Keys to the Nymphs of the descriptions and family keys to the Wisconsin Miridae" show that it is nymphs of the British Heteroptera. possible to recognize genera and even Butler's (1923) "Biology of the British species of Miridae in the immature Hemiptera-Heteroptera" contains stages. descriptions, life histories, and hosts of many species, including those in the RELATIONSHIPS OF GENERA PREVIOUSLY Lygus complex found in the British PLACED IN LYGUS Isles. Bech (1969) should be consulted for information on the life history, Agnocoris Reuter. The Holarctic willow- ecology, and nymphs and particularly for feeding genus Agnocoris externally is the long host list of the Palaearctic similar to Lygus , but the genital species of Lygus and related genera. In structures, silky pubescence, and short both of the last texts, an older scheme second antennal segment define a

58 , ,

distinct genus (Kelton, 1955a). cervinus (Herrich-Schaef f er) , atomarius Although Slater (1950) believed the (Meyer-Dur) , and rubricatus (Fallen) female genitalia of Agnocoris were indicated that they were not congeneric rather distinct from those of other with kalmii Linnaeus, the type-species

Lygus groups (subgenera), Kelton (1955a) of Orthops . Later, the spruce-feeding suggested that Agnocoris along with , rubricatus was transferred to Pinalitus the Palaearctic genus Cyphodema Fieber, Kelton with the pine-feeding was one of the few genera previously approximatus StSl (Kelton, 1977) and three placed in the Lygus complex that showed other Nearctic species. Kelton (1955a) close relationship to Lygus . considered the umbelliferous-feeding species of the genus Orthops remotely Knightomiris Kelton. The parameres of related to Lygus . Orthops is considered Knightomiris distinctus (Knight) are closely related to the Afro-tropical similar to those of Lygus but , genus Lygidolon Reuter, which has been K. distinctus has a prominent tubercle reviewed by Odhiambo (1960) , Ghauri on the margin of the pygophore above the (1971), and Linnavuori (1974). left paramere and the vesica differs in Linnavuori (1975) noted that the having two distinct spiculi (Kelton, African species of Lygidolon , Orthops , 1974) . Kelton erected Knightomiris to and Taylorilygus need to be revised and accommodate this single species. should be studied along with the genera Gutrida Kirkaldy, Oreolygus Linnavuori, Lygocoris Reuter. This genus, now and Yngveella Poppius. divided into four subgenera, probably has little relationship to Lygus . Pinalitus Kelton. The genus Pinalitus , Slater (1950) indicated that the erected to accommodate the species subgenus Neolygus does not appear even approximatus Stlil, apparently is related closely related to Lygus . Kelton to the Neotropical genus Alda, but it female (1955a) confirmed that male and differs in having a much shorter first genitalia and many external characters antennal segment (Kelton, 1955a). Alda linked the subgenera Apolygus , resembles certain members of the widely Lygocoris Neolygus and Stechus . Based , , distributed genus Phytocoris Fallen and, on this information, Kelton considered like Pinalitus , is not closely related Lygocoris distinct from Lygus [as to Lygus .

Liocoris ] . Clayton (1982) further distinctiveness of supported the P r oba Distant. The species Lygus sallei Lygocoris and suggested that the St&l, included in Knight's (1917) subgenera Apolygus Lygocoris and , , catchall group I, now is placed in the Neolygus might best be considered as Neotropical genus Proba . Carvalho separate genera. Zheng and Wang (1982, (1952) previously considered Paralygus 1983) and Wang and Zheng (1982) Reuter a junior synonym of Proba . although apparently correctly placing 20 new species from China in Apolygus , Kelton (1955a) noted a superficial incorrectly placed them in the genus resemblance of Proba to Horcias Distant Lygus . As members of the subgenus (the latter is now in part subdivided, Apolygus, they must be placed in the with the North American species genus Lygocoris . Kelton (1971) reviewed transferred to the genus the Nearctic species of Lygocoris , Metriorrhynchomiris Distant (Carvalho redescribed the adults, furnished host and Jurberg, 1974)), but he stated that plant information, and provided a key to the absence of a transverse carina help distinguish species found in Canada between the eyes and the form of the and Alaska. genital structures on Horcias easily

separated it from Proba . Orthops Fieber. Wagner's (1949) vague definition of Orthops includes a group Sabactus Distant. Another monotypic of heterogeneous species (Kelton, genus known from Sri Lanka, it contains 1955a). Kelton' s study of the only the species institutus (Distant). Palaearctic species visicola (Puton)

59 Previously this genus was placed in microscope (SEM), are called for and, in Lygus, but Kelton showed that the two fact, have produced some promising genera are not closely related. results on a limited basis (J.D. Lattin

and V. Razaf imahatratra , unpub.). Salignus Kelton. This Nearctic, monotypic genus (Kelton, 1955a) Contemporary biochemical techniques possesses unique characters making it should be used, such as those of Sluss distinct from Lygus . Salignus et al. (1982), together with distinguendus (Knight) , a willow-feeding crossbreeding investigations (Graham, species, differs in structure from any 1982). The development of an artificial taxon studied by Kelton (1955a). diet for Lygus makes easier the main- tenance of laboratory cultures for Taylorilygus Leston. Kelton (1955a) study (Debolt, 1982). Sex pheromones considered Leston' s subgenus have been detected in several species of

Taylorilygus a distinct genus, noting Miridae, including Lygus , and should be that the male and female genitalia investigated further (Boivin and indicated it was not closely related to Stewart, 1982). Adequate samples, well

Lygus . All species of Taylorilygus are documented and appropriately preserved, confined to the Afro-tropical region, should be collected over a wide area. except T. pallidulus (Blanchard) , a Such samples would also assist in polyphagous "cosmopolitan" species. studies involving geographic variation. Taylor (1947) described most of the Because considerable seasonal variation species, indicated host plants, and in the adults is known to occur (Kelton, provided an identification key. Kelton 1975), samples should be taken during (1955a) considered Taylorilygus most more than one season. closely related to the Neotropical genus Dagbertus Distant. These two genera are It is not now possible to identify similar externally, but the genital nymphs to species accurately. structures and the very short third Well-preserved nymphs associated with antennal segment of Dagbertus will adults should be collected for study. distinguish them (Kelton, 1955a; Slater Some mirid nymphs can be identified to and Baranowski, 1978). Carvalho (1983) species in other genera, but comparatively little work has been done reviewed Dagbertus , providing descriptions of 12 new species, a on nymphal taxonomy (see previous checklist of the species, and a key to section on nymphs). It also is possible help separate them. that useful taxonomic characters might

be found on the eggs of Lygus . The SEM PROBLEMS INVOLVING THE TAXONOMY OF NORTH would be an essential investigative tool AMERICAN LYGUS for such work. All the available information should be assembled and Despite efforts to clarify the species analyzed utilizing contemporary level taxonomy of Lygus and related systematic methods. genera, it is difficult to positively identify many commonly encountered Once a more solid systematic base has specimens. This hinders the development been established, it may be possible to of species-specific programs involving, clarify other puzzling questions, for for example, biological control agents. example, the broad geographical ranges The taxonomic difficulty stems chiefly of many species that often overlap those from the inability to determine species of several others. Is this the case, or in Lygus accurately and from their are we unable to recognize other taxa variability throughout their ranges. adequately, or are they the same Macromorphological systematic techniques species? It is clear that there is may have been used to their limit. seasonal variation and, most likely, Micromorphological studies, including geographical variation. We are not yet the use of the scanning electron able to cope fully with these

60 variables. Carefully conducted life RECOMMENDATIONS FOR FUTURE WORK history studies, with voucher specimens, are to clarify needed these problems. (A) Short term (1) Adults The available host plant data present a Micromorphological studies bewildering array of plant taxa with few Biochemical studies, including indications of any ordered associations. allozymes and pheromones Clear distinction should be made between Hybridization studies resting, feeding, and hosts supporting Adequately vouchered and nymphs such as was done by Fye (1980) or preserved samples from broad Snodgrass et al. (1984), who indicate geographical areas when adults or nymphs or both were (2) Nymphs and eggs collected. Damage can occur on crops Procurement of associated where Lygus bugs do not breed and samples oviposit, especially because adults Micromorphological studies readily migrate to and feed on plants (3) General where nymphs do not occur. Accurate, vouchered host data over broad geographical area Careful attention should be given to the Thorough life history studies, phenology of the host plant and the including hosts, phenology, occurrence of Lygus on the plant. and population dynamics Almost certainly some of the apparent Studies of associated confusion over host association is due predators and parasites to host plant shifts in different parts (B) Long term of the bug's range. Fox and Morrow Analysis and synthesis of short- (1981) pointed out that a species may be term information a generalist throughout its range but a Systematic revision of the specialist locally. Species of the genus Lygus genus Lygus would seem to be excellent Phylogenetic studies of Lygus subjects for such an analysis once the spp. and near relatives taxonomy is better known. A species Host plant resistance studies such as Lygus lineolaris , already well defined but very widespread and SOME FINAL QUESTIONS apparently rather polyphagous, would be a fine candidate for such a study. A review of this kind frequently raises more questions than it answers. Our And finally, if a rational approach is knowledge is so rudimentary in some to be taken in seeking possible areas as to make progress difficult. biological control agents, particularly Nevertheless, some intriguing questions in other parts of the world, it is may be raised, the answers to some of essential to know just where the genus which may eventually come from work on Lygus fits in the overall phylogeny of Lygus . the Miridae. A more indepth comparison of the mirine genera is needed using —What makes the native species of contemporary phylogenetic analysis. Lygus move so readily to introduced When we know more about the near plants, including crop plants? relatives of Lygus and where they occur, —Although some Lygus feed on various searches for more effective biological legumes, why have they not control agents are likely to be more transferred to soybeans, even successful. Although there is no though a large number of other guarantee that seeking such agents from insects have done so, including near relatives will produce successful Lygocoris ( Apolygus ) lucorum results, it does put such efforts on a (Meyer-Diir) (Lattin and Hall, 1983)? more ordered basis (Condit and Cate, —How is it possible to explain the 1982). apparent great range of acceptable

61 . ,

host plants for some Lygus ACKNOWLEDGMENTS species? There are species

Included in the genus that appear We thank V.D. Razaf imahatratra , National to be host-plant specific and may University, Malagasy Republic, be typical k-selected species. Madagascar, for sharing his views on some

of the problems in the genus Lygus . Many —What adaptive features of Lygus useful suggestions have been made by R.C. spp. enable them to occupy Froeschner, Department of Entomology, (apparently) such a wide geographic National Museum of Natural History range? Can these attributes be (NMNH) , Washington, D.C.; R.W. Hodges, identified and included in Systematic Entomology Laboratory, predictive models on pest potential? Agricultural Research Service, USDA, c/o —Some species of Lygus are sometimes NMNH; and A.G. Wheeler, Jr., Bureau of found together on crops. What are Plant Industry, Pennsylvania Department of apparent the consequences this of Agriculture, Harrisburg, Pa. interspecific competition? —Are there special attributes of the pest species of Lygus that allow REFERENCES CITED them to adjust to unstable,

disturbed environments and thereby Akingbohungbe , A.E., J.L. Libby, and enable them to become pests in the R.D. Shenefelt. 1973. Nymphs of first place? Are they less of a Wisconsin Miridae. Hemiptera: problem in no-tillage systems? Heteroptera. Univ. Wis. Expt. Sta. Bui. —What can be learned by analyzing R2561, 24 pp. the nature of the predator-parasite complex associated with each Al-Munshi, D.M., D.R. Scott, and H.W.

species of Lygus , including those Smith. 1982. Some plant host effects on that are not pests? Lygus hesperus (Hemiptera: Miridae). —Why haven't some Lygus species been Jour. Econ. Entomol. 75:813-815. introduced into other countries accidentally? Bech, R. 1969. Untersuchungen zur —Although many European insects have Systematik. Biologie und Okologie been introduced into North America, wirtschaf tlich wichtiger Lygus-Arten. including a large number of (Hemiptera: Miridae). Beitr. Ent Miridae, where are the common 19:63-103. European species of Lygus ? Several European species of Lygus are Blatchley, W.S. 1926. Heteroptera or regularly intercepted at U.S. ports true bugs of eastern North America. 1116 by APHIS Plant Pest Quarantine pp. Nature Pub. Co., Indianapolis, Ind.

personnel (pers. observ. , T.J.

Henry) . All earlier reports of Boivin, G., and R.K. Stewart. 1982. European species of Lygus in North Attraction of male green apple bugs, America apparently are based on Lygocoris communis (Hemiptera: Miridae), misidentif ications. It is possible to caged females. Can. Entomol. that some of these species are 114:765-766. present in our fauna but have gone

undetected. If not, why haven't Bolton, J.L. , B.P. Goplen, and these species become established? H. Baenziger. 1972. World distribution and historical developments. In Hanson, Quite clearly, although much is known C.H., ed., Alfalfa Science and about Lygus bugs and many authors have Technology, pp. 1-34. Amer. Soc. Agron. contributed to this knowledge, there is Inc., Madison, Wis. much to learn. Bryan, D.E., C.G. Jackson, R.L. Carranza,

and E.G. Neeman. 1976. Lygus hesperus : Production and development in the laboratory. Jour. Econ. Entomol. 69:127-129.

62 .

Burgess, L. , J. Dueck, and Clayton, R.A. 1982. A phylogenetic D.L. McKenzie. 1983. Insect vectors of analysis of Lygocoris Reuter

the yeast Nematospora coryli in mustard, (Heteroptera : Miridae) with notes on life

Brassica juncea , crops in southern histories and zoogeography. M.S. Thesis,

Saskatchewan. Can. Entomol. 115:25-30. Univ. Conn. , Storrs, 78 pp.

Butler, E.A. 1923. A biology of the Condit, B.P., and J.R. Cate. 1982. British Hemiptera-Heteroptera. 682 pp. Determination of host range in relation H.F. & G. Witherby, London. to systematics for Peristenus stygicus

(Hym.: Braconidae) , a parasite of Carvalho, J.C.M. 1952. On the major Miridae. Entomophaga 27:203-210. classification of the Miridae

(Hemiptera) . (With keys to subfamilies Craig, C.H. 1983. Seasonal occurrence and tribes and a catalogue of the world of Lygus spp. (Heteroptera: Miridae) on genera.) Acad. Brasil. Cien. 25:31-110. alfalfa in Saskatchewan. Can. Entomol. 115:329-331. Carvalho, J.C.M. 1955. Keys to the genera of Miridae of the world Debolt, J.W. 1982. Meridic diet for (Hemiptera). Bol. Mus. Goeldi. 11:1-151. rearing successive generations of Lygus hesperus. Ann. Entomol. Soc. Amer. Carvalho, J.C.M. 1957-60. Catalog of 75:119-122. the Miridae of the world. Pt. I DeCoursey, R.M. 1971. Keys to the (44(1) : 1-158 (1957)), pt. II (45(2):1-216 (1958)), pt. Ill (47 (3) :1-161 (1958)), families and subfamilies of the nymphs of pt. IV (48(4) :l-384 (1959)), pt. V North American Hemiptera-Heteroptera. (51(5):1-194 (I960)). Arq. Mus. Nac., Proc. Entomol. Soc. Wash. 73:413-428. Rio de Janeiro 48:1-384. Distant, W.L. 1904. The fauna of British India including Ceylon and J.C.M. 1983. Mirideos Carvalho, Burma. Rhynchota. Vol. II. neotropicais CCXXXIII: Genero Dagbertus (Heteroptera). 503 pp. Taylor and especies e revisao Distant—Descrigoes de Francis Printers, London. das que ocorrem na regiao (Hemiptera) Rev. Brasil. Biol. 43:157-176. Fox, L.R., and P.A. Morrow. 1981. Specialization: Species property or local Carvalho, J.C.M., and J. Jurberg. 1974. phenomenon? Science 211:887-893. Neotropical Miridae, CLXXX: On the Horcias complex (Hemiptera) . Rev. Fye, R.E. 1980. Weed sources of Lygus Brasil. Biol. 34:49-65. bugs in the Yakima Valley and Columbia Basin in Washington. Jour. Econ. Carvalho, J.C.M., H.H. Knight, and R.L. Entomol. 73:469-473. Usinger. 1961. Lygus Hahn, 1833 (Insecta, Hemiptera); proposed Ghauri, M.S.K. 1971. New species of designation under the plenary powers of Lygldolon Reuter (Hemiptera-Heteroptera: the type-species in harmony with Miridae) infesting wattle in South and accustomed usage. ZH.(S.) 1062. Bui. East Africa. Jour. Entomol. 40:133-138. Zool. Nomencl. 18:281-284. Glick, P.A. 1939. The distribution of China, W.E. 1941. A new subgeneric name insects, spiders and mites in the air. for Lygus Reuter 1875 nec Hahn 1833 U.S. Dept. Agr. Tech. Bui. 673:1-150.

(Hemipt .-Heteropt . ) . Proc. Roy. Entomol. Soc. Lond. 10:60. Graham, H.M. 1982. Interbreeding of Lygus elisus Van Duzee and L. desertinus China, W.E. 1943. The generic names of Knight in the field. Southwest. Entomol. British Hemiptera-Heteroptera, with a 7:60-64. check list of the British species. 316 pp. Roy. Entomol. Soc. Lond.

63 , , . . ,

Graham, H.M., and C.G. Jackson. 1982. Kelton, L.A. 1975. The lygus bugs Distribution of eggs and parasites of (genus Lygus Hahn) of North America

Lygus spp. (Heraiptera: Miridae) , Nabis (Heteroptera: Miridae). Entomol. Soc. spp. (Hemiptera: Nabidae) , and Canada Mem. 95:1-101. Spissistilus f estinus (Say) (Horaoptera: Membracidae) on plant stems. Ann. Kelton, L.A. 1977. Species of the genus Entomol. Soc. Amer. 75:56-60. Pinalitus Kelton found in North America (Heteroptera: Miridae). Can. Entomol.

L.R . Ertle 109:1549-1554. Graham, H.M. , A. A. Negm, and 1984. Worldwide literature of the Lygus complex (Heraiptera: Miridae), 1900-1980. Kelton, L.A. 1980. The plant bugs of

U.S. Dept. Agr. , Agr. Res. Serv. the Prairie Provinces. Heteroptera: Bibliogr. Lit. Agr. No. 30, 205 pp. Miridae. Agr. Can. Pub. 1703, 408 pp. Ottawa. Herring, J.L., and P.D. Ashlock. 1971. A key to the nymphs of the families of Kerzhner, I.M. 1964. Order Hemiptera

Hemiptera (Heteroptera) of America north (Heteroptera) . Family Miridae

Entomol. 54:207-212. . of Mexico. Fla. (Capsidae) In Bei-Bienko, G.Y., ed . Keys to the Insects of the European International Commission of Zoological U.S.S.R., vol. I, pp. 911-1003, Nomenclature. 1963. Opinion 667. Bui. Apterygota, Paleoptera, Hemimetabola Zool. Nomencl. 20:270-271. Zool. Inst. Acad. Sci. U.S.S.R., Leningrad. [English transl., 1967; Jeppson, L.R., and G.F. MacLeod. 1946. Russian edition, 1964] Lygus bug injury and its effect on the growth of alfalfa. Hilgardia. 17:165-188. Kiritshenko, A.N. 1951. True bugs of the European U.S.S.R. (Heraiptera). Key Johnson, C.G., and T.R.E. Southwood. and bibliography. 423 pp. Acad. Sci.

1949. Seasonal records in 1947 and 1948 U.S.S.R., Moscow-Leningrad . [In Russian] of flying Hemiptera-Heteroptera particularly Lygus pratensis L., caught Knight, H.H. 1917. A revision of the in nets 50 ft to 3,000 ft above ground. genus Lygus as it occurs in America north Proc. Roy. Entomol. Soc. Lond. (A) of Mexico, with biological data on the 24:128-130. species from New York. Cornell Univ.

Agr. Expt . Sta. Bui. 391:555-645. Kelton, L.A. 1955a. Genera and subgenera of the Lygus complex Knight, H.H. 1941. The plant bugs, or (Hemiptera: Miridae). Can. Entomol. Miridae,. of Illinois. 111. Nat. Hist. 87:277-301. Surv. Bui. 22:1-234.

Kelton, L.A. 1955b. Species of Lygus , Knight, H.H. 1968. Taxonomic review:

Liocoris , and their allies in the Prairie Miridae of the Nevada Test Site and the Provinces of Canada. Can. Entomol. Western United States. Brigham Young 87:531-556. Univ. Sci. Bui. 9(3):l-282.

Kelton, L.A. 1971. Review of Lygocoris Kogan, M. 1981. Dynamics of insect species found in Canada and Alaska adaptations to soybeans: Impact of (Heteroptera: Miridae). Entomol. Soc. integrated pest management. Environ. Canada Mem. 83:1-87. Entomol. 10:363-371.

Kelton, L.A. 1974. Knightomiris new Lattin, J.D., and B.B. Hall. 1983. genus, for Lygus distinctus (Heteroptera: Lygocoris ( Apolygus ) lucorum (Meyer-Dur) Miridae). Can. Entomol. 105:1417-1420. 1843 (Hemiptera: Miridae). Potential host of parasites for biological control

of Lygus . Oreg. State Univ., Syst. Entomol. Lab. Inform. Sheet, 2 pp.

64 , .

Lattin, J.D., and P. Oman. 1983. Where Reid, D.G., C.C. Loan, and R. Harmsen. are the exotic insect threats? In 1976. The mirid (Hemiptera) fauna of Wilson, C.L., and C.L. Graham, eds. Solidago canadensis (Asteraceae) in Exotic Plant Pests and North American south-eastern Ontario. Can. Entomol. Agriculture, pp. 93-137. Academic Press, 108:561-567. New York. Rice, R.E., J.K. Uyemota, J.M. Ogawa, and Leston, D. 1952. On certain subgenera W.M. Pemberton. 1985. New findings on of Lygus Hahn 1833 (Hem. , Miridae) , with pistachio problems. Calif. Agr. a review of the British species. 39(1-2) :15-18. Entomol. Gaz. 3:213-230. Romney, Van E. 1946. Control of Lygus Scudder. 1956. A Leston, D. , and G.G.E. bugs with DDT as related to guayule seed key to the larvae of the families of production. Jour. Econ. Entomol. British Hemiptera-Heteroptera. 39:664-665. Entomologist 85:223-231. Salt, R.W. 1945. Number of generations Linnavuori, R. 1974. Studies on African of Lygus hesperus Knt. and L. elisus Van

Miridae (Heteroptera) . Occas. Pub. D. in Alberta. Sci. Agr. 25:573-576. Entomol. Soc. Nigeria 12:1-67. Scott, D.R. 1970. Feeding of Lygus bugs Linnavuori, R. 1975. Hemiptera of (Hemiptera: Miridae) on developing carrot Sudan, with remarks on some species of and bean seed: Increased growth and the adjacent countries. 4. Miridae and yields of plants grown from that seed.

Isometopidae . Ann. Zool. Fenn. 12:1-118. Ann. Entomol. Soc. Amer. 63:1604-1608.

Malcolm, D.R. 1953. Host relationship Scott, D.R. 1977. An annotated listing studies of Lygus in south-central of host plants of Lygus hesperus Knight. Washington. Jour. Econ. Entomol. Bui. Entomol. Soc. Amer. 23:19-22. 46:485-488. Scott, D.R. 1983. Lygus hesperus Knight

Norton, G.A. , and G.R. Conway. 1977. The (Hemiptera: Miridae) and Daucus carota L. economic and social context of pest, (Umbellif lorae : Umbellif lerae) : An disease and weed problems. _In Cherrett, example of relationships between a J.M., and G.R. Sagar, eds., Origins of polyphagous insect and one of its plant Pest, Parasite, Disease and Weed hosts. Environ. Entomol. 12:6-9. Problems, pp. 205-226. 18th Symp. Brit. Ecol. Soc., Bangor, 12-14 Apr. 1976. Shull, W.E. 1933. An investigation of Blackwell Sci. Pub., Oxford. the Lygus species which are pests of beans (Hemiptera, Miridae). Univ. Idaho Odhiarabo, T.R. 1960. Taxonomic notes on Agr. Expt. Sta. Res. Bui. 11:1-42. three species of Mirinae (Hemiptera: Miridae) including the descriptions of Slater, J.A. 1950. An investigation of two new species. Proc . Roy. Entomol. the female genitalia as taxonomic Soc. Lond. 29:120-126. characters in the Miridae (Hemiptera) Iowa State Jour. Sci. 25:1-87. Parker, B.L., and K.I. Hauschild. 1975. Baranowski. 1978. A bibliography of the tarnished plant Slater, J.A. , and R.M. bug, Lygus lineolaris (Hemiptera: How to know the true bugs (Hemiptera- Miridae), on apple. Bui. Entomol. Soc. Heteroptera). 256 pp. W.C. Brown Co. Amer. 21:119-121. Pub., Dubuque, Iowa.

Price, P.W. 1976. Colonization of crops by arthropods: Non-equilibrium communities in soybean fields. Environ. Entomol. 5:605-611.

65 . . . .

Sluss, T.P., H.M. Graham, and Wagner, E. 1949. Zur Systematik der E.S. Sluss. 1982. Morphometric, Gattung Lygus Hhn. (Hem. Het. Miridae) allozyrae, and hybridization comparisons Verh. Ver. Naturw. Heimatf., Hamburg. of four Lygus species (Hemiptera: 30:26-40.

Miridae) . Ann. Entomol. Soc. Amer. 75:448-456. Wagner, E. 1957. Das Lygus-Liocoris Problem (Hem. Het. Miridae). Deut. Entomol. 4:91-94. Snodgrass, G.L. , W.P. Scott, and Ztschr. J.W. Smith. 1984. An annotated list of the host plants of Lygus lineolaris Wagner, E. 1970-71. Die Miridae Hahn, (Hemiptera: Miridae) in the Arkansas, 1831, des Mittelmeerraumes und der Louisiana, and Mississippi Delta. Jour. Makaronesischen Inseln (Hemiptera,

Ga. Entomol. Soc. 19:93-101. Heteroptera) . Tell 1. Entomol. Abh. Mus. Tierk. Dresden, Sup. 37:1-484.

Southwood , T.R.E. 1956. A key to [1970:1-273; 1971:274-484] determine the instar of an heteropterous

larva. Entomologist 89:220-222. Wang, X. , and L. Zheng. 1982. Three new species of Lygus of the subgenus Apolygus Southwood, T.R.E. 1977. The relevance from Fujian, China (Hemiptera: Miridae).

of population dynamic theory to pest Wuyi Sci . Jour. 2:118-123.

status. In Cherrett , J.M. , and G.R.

Sagar, eds. , Origins of Pest, Parasite, Wheeler, A.G., Jr. 1976. Lygus bugs as Disease and Weed Problems, pp. 35-54. facultative predators, in Scott, D.R., 18th Symp. Brit. Ecol. Soc., Bangor, and L.E. O'Keeffe, eds., Lygus Bugs: Host 12-14 Apr. 1976. Blackwell Sci. Pub., Plant Interactions, pp. 28-35. Univ. Oxford Idaho Press, Moscow.

Zheng L. and X. Wang. 1982. Southwood, T.R.E., and D. Leston. 1959. , , New Land and water bugs of the British species of Lygus bugs from China. 5:47-59. Isles. 436 pp. Frederick Warne & Co. Entomotaxonomia Ltd., London.

Zheng, L . , and X . Wang. 1983. New species and records of Lygus (subg. Stichel , W. 1958. Illustrierte Bestimmungstbellen der Wanzen. II. Apolygus ) from China. Acta Zootaxonom. Europa (Hemiptera-Heteroptera Europae) Sinica. 8:422-433. Vol. 2, 24 Heft, pp. 737-768. Martin-Luther, Berlin-Hermsdorf

Stitt, L.L. 1949. Host-plant sources of Lygus spp. infesting the alfalfa seed crop In southern Arizona and southeastern California. Jour. Econ. Entomol. 42:93-99.

Taylor, T.J.C. 1947. Some East African

species of Lygus , with notes on their host plants. Bui. Entomol. Res. 38:233-258.

Vinokurov, N.N. 1979. Keys to the fauna of the U.S.S.R. Heteropterous Insects of Yakutia. 231 pp. Zool. Inst., Acad.

Sci. U.S.S.R. , Leningrad. [In Russian]

66 :

APPENDIX Subgenus Apolygus

(type-species limbatus ) The following classifications of Lygus Subgenus Exolygus Wagner are from Knight (1917) to the present: (type-species pratensis ) Subgenus Lygus

(1) Knight (1917) treated only North (type-species pabulinus ) American taxa: Subgenus Qrthops

Genus Lygus Hahn (type-species kalmii )

Group I ( pratensis group; considered Lygus lineolaris (4) Leston (1952) gave a world review of (Palisot) a junior synonym of Lygus and subgenera: Lygus pratensis (Linneaus)) Genus Lygus

Group II ( campestris group) Subgenus Agnocoris

campestris Linneaus (subg. (type-species rubicundus ) Qrthops Fieber) Subgenus Exolygus

distinctus Knight (now in (type-species pratensis ) Knightomiris Kelton) Subgenus Lygus

rubicundus Fallen (subg. (type-species pabulinus ) Agnocoris Reuter) Subgenus Neolygus sallei Still (now in Proba (type-species communis Knight) Distant) Subgenus Apolygus , a junior

Group III approximatus Stal (now synonym (type-species limbatus ) in Pinalitus Kelton) Subgenus Qrthops

Group IV (type-species kalmii ) f asciatus Reuter (now in Subgenus Taylorilygus Leston Dagbertus Distant) (type-species simonyi Reuter) olivaceus Reuter (now in

Dagbertus ) (5) Kelton (1955a) treated Lygus and Group V associated genera: apicalis Fieber (now in Genus Agnocoris

Taylorilygus Leston) (type-species rubicundus )

Group VI ( communis group; subg. Genus Cyphodema Fieber Heolygus Knight) (type-species instabilis Lucas) contains 39 species in North Genus Dagbertus America (type-species darwini Butler) Genus Liocoris (2) China (1943) treated British genera: (type-species tripustulatus ) synonym Genus Liocoris Fieber Genus Exolygus , a junior

(type-species tripustulatus (type-species pratensis )

( Fabricius) ) Genus Lygus

Genus Lygus (type-species pabulinus ) Subgenus Agnocoris Subgenus Apolygus

(type-species rubicundus ) (type-species limbatus ) Subgenus Apolygus China Subgenus Lygus

(type-species limbatus Fallen) (type-species pabulinus ) Subgenus Lygus Subgenus Neolygus

(type-species pabulinus (type-species communis ) Linnaeus) Subgenus Stechus Distant Subgenus Qrthops (type-species libertus Distant) (type-species kalmii Linnaeus) Genus Qrthops Fieber

(type-species kalmii ) (3) Wagner (1949) treated Palaearctic Genus Pinalitus genera (type-species approximatus ) Genus Lygus (group III of Knight (1917)) Subgenus Agnocoris Genus Proba

(type-species rubicundus )

67 :

(type-species gracilis Distant)

( saliei group of Knight (1917)) Genus Sabactus Distant (type-species institutes Distant) Genus Salignus (type-species distinguendus

Reuter ) (in group I of Knight (1917)) Genus Jaylorilygus (type-species simonyi)

(6) Current scheme, ruling of International Commission of Zoological Nomenclature (1963); other generic concepts (not listed) follow Kelton (1955a, 1974) Genus Liocoris (a subjective junior synonym of

Lygus ; currently considered a distinct genus) Genus Lygocoris

(type-species pabulinus ) Subgenus Apolygus

(type-species limbatus ) Subgenus Lygocoris

(type-species pabulinus ) Subgenus Neolygus

(type-species communis ) Subgenus Stechus

(type-species libertus ) Genus Lygus

(type-species pratensie ) Genus Exo lygus (same type-species; an objective junior synonym of

Lygus )

68 . . .

EUPHORINE PARASITES OF LYGUS AND cocoon. Spring emergence is nearly ADELPHOCORIS (HYMENOPTERA: BRACONIDAE AND synchronous with the hatching of host HETEROPTERA: MIRIDAE) nymphs from overwintered eggs (Waloff, 1967; Bilewicz-Pawinska, 1978). Nondia- By Conrad C. Loan and Scott R. Shawi/ pausing species occur in Kenya (Taylor, 1945) and bivoltine ones in Poland Lygus Hahn is a genus with 34 North (Bilewicz-Pawinska, 1977). American and 7 European species. Adelphocoris Reuter is a European genus The relatively few host-associated with three species, of which two are species have a restricted host range. introduced economic pests in North Some are monophagous, but others attack a America. Insects in both genera are small number of species on the same plant attacked in their nymphal stages by or type of plant growth (Loan, 1980). It parasites in the tribe Euphorini, family is clear that diapause of plant bug Braconidae parasites is an important component of specificity, because it prevents temporal Peristenus Foerster and Leiophron Nees separation from the host after are allied to four other genera in the overwintering

Euphorini (Loan, 1983) , which are each host specific for a family of Heteroptera Peristenus and Leiophron are most easily or Psocoptera. Reared material is rare detected by dissection of nymphs and and the parasites are not well known, adults, because the parasite cocoon is although their plant bug hosts are the hard to find in the soil and parasite commonest of the Heteroptera. For adults are difficult to collect; they fly example, in the British Isles, six for only a short time. Rearing species of Peristenus and two of field-collected material in the Leiophron have been associated with hosts laboratory is more successful if one (Brindley, 1939; Richards, 1967; Waloff, obtains late-instar nymphs to minimize 1967; Loan and Bilewicz-Pawinska, 1973). the duration of host feeding and parasite These hosts are from a plant bug fauna of development 193 species, of which 26 percent are recorded as hosts of euphorine larvae TAXONOMY (Southwood and Leston, 1959). In North America, hosts are known for 14 species Taxonomic reviews of Peristenus and

of Peristenus and 4 of Leiophron , and Leiophron are available for species from unidentified euphorine larvae occur in 24 North America (Muesebeck, 1936; Loan, additional host species (Loan, 1980) . 1974b) and from Europe (Richards, 1967; Loan and Bilewicz-Pawinska, 1973; Loan, BIOLOGY 1974a). Nixon (1946) reviewed the

African species reared by Taylor (1945) . The euphorines attacking plant bugs New name combinations were provided emerge from overwintered cocoons, and, (Loan, 1974b) because of the separation having ripe oocytes, they immediately of Peristenus from Leiophron (Loan and attack early-instar nymphs. A single Bilewicz-Pawinska, 1973). parasite larva develops in the host and usually emerges from the fifth-instar Larvae have specific characters of setae nymph. Infrequently, development of the and head sclerites (Waloff, 1967; first instar is arrested until the host Bilewicz-Pawinska, 1974), but their is an adult (Leston, 1961; Loan, 1965, taxonomy has not progressed enough to 1966). For most reported associations, permit identifications to either genus or the adult parasite diapauses in its species.

Species of Leiophron have diverse .^Respectively, Agriculture Canada structural characters and thus are easier

Research Station, Ottawa, ON K1A 0C6, to recognize than species of Peristenus , and Museum of Comparative Zoology, which are very similar and identified Harvard University, Cambridge, MA 02138. chiefly by host association or seasonal

69 . . , , .

3. occurrence. Among current taxonomic Mesonotum smooth and polished problems is the species complex of anteriorly, not punctate

_P. pallipes (Curtis), £. pseudopallipes (fig. 2, E) . Radial cell on

(Loan) , and adelphocoridis Loan. wing margin about 0.3 times as Studies should assess the validity of P. long as stigma (fig. 2, D) adelphocoridis and also the status of the Antennal segments 18-20 (?), North American _P. pallipes (Loan, 19-21 (rf)

1974b) . Although j?. pseudopallipes is Peristenus stygicus Loan nearly inseparable morphologically from .P. pallipes its temporal separation is , 4. Mesonotum punctate anteriorly evidence of species isolation (Loan, (figs. 1, D; 2, F) . Radial 1970) cell at least 0.5 times as long as stigma. Antennal KEY TO EUROPEAN AND NORTH AMERICAN segments 19-25 (?), 22-28 EUPHORINE PARASITES OF LYGUS AND OO 4 ADELPHOCORIS 5. Bicolored, or black with face 1. Ventral margins of abdominal distinctly paler than genae, tergite 1 widely separated from frons, and vertex 5 each other (fig. 1, A). Mesonotum with notauli absent Black without pale face or red- or at least effaced posteriorly dish head or thorax - pallipes (fig. 1, C) . Forewing veins species group!/ 6 effaced apically (fig. 1, E) first intercubitus and Bicolored, head behind eye recurrent vein absent (?) and face, genae, vertex, and Genus Leiophron Nees 2 mesonotum (<*) light reddish. Antennal segments 22-25 Ventral margins of abdominal (?), 22-24 (d 1 ) tergite 1 meeting basally (fig. — Peristenus rubricollis (Thomson) 1, .B) . Mesonotum with notauli foveate and always distinct Black, dorsal eye orbit black or posteriorly (figs. 1, D; 2, narrowly reddish (?), face E-F) . Forewing veins complete paler than genae or vertex. apically (figs. 1, F; 2, D) Antennal segments 18-20 first intercubitus and (?), 18-21 (o') recurrent vein present — Peristenus digoneutis Loan Genus Peristenus Foerster 3

2. Occipital carina effaced dorsally (fig. 2, A). Eye not as wide

as temple (fig. 2, B) . Dis- tance between eye and base of mandible (malar space) approxi- mately as long as basal width

of mandible (fig. 2 , C) Propodeum usually yellow, not notably darker than thorax Leiophron unif ormis (Gahan)

Occipital carina weakly present dorsally. Eye as wide or wider than temple. Malar space 2.0 1/ A complex group of sibling species, times as long as basal width of which needs further taxonomic work. The mandible. Propodeum brown, species are morphologically similar and notably darker than thorax most easily identified if host and date Leiophron lygivora Loan of emergence are known.

70 Figure 1 Petiole, ventral view: A, Leiophron unif ormis (Gahan); I), Peristenus digoneutis Loan. Mesonotum, dorsal view: C^, uniforrais; _P. pallipes J_,. D,

(Curtis). Wings: E, L. "unif ormis ; F, P. stygicus Loan.

71 Figure 2

Head, Leiophron unif ormis (Gahan) : A, ratio. Forewing: D, Peristenus Dorsal view showing effaced occipital stygicus Loan. Mesonotum, dorsal carina; B, lateral view showing view: E, P. stygicus ; F, P. digoneutis eye/temple ratio; lateral view Loan. showing malar space/mandible width

72 Figure 3 Petiole, dorsal view: A, Peristenus adelphocoridis Loan; B,

ti . pseudopallipes (Loan) ; C and _D, nl If . pallipes (Curtis).

6. Spiracles of abdominal tergite 1 7. Antennal segments (?), 21-25, distinctly behind middle of usually 22-23. In North tergite (fig. 3, A), tergite America, adults occurring in before spiracle 1.6 times as spring and early summer (prior

long as tergite behind to mid-July) . Abdominal spiracle. Parasites of tergite 1 with distinct costae Adelphocoris — (figs. 3, C-D) Peristenus adelphocoridis Loan Peristenus pallipes (Curtis)

Spiracles of abdominal tergite 1 Antennal segments (?), 19-24, closer to middle of tergite usually 21-22. In North America, (figs. 3, _B-D) , tergite before adults occurring in spiracle 1. 1-1.3 times as long late summer to fall (after mid-

as tergite behind spiracle. July) . Abdominal tergite 1 Parasites of Lygus or mostly without distinct Adelphocoris 7 costae (fig. 3, .B) - Peristenus pseudopallipes (Loan)

73 : .

ACKNOWLEDGMENTS Loan, C.C. 1970. Two new parasites of the tarnished plant bug in Ontario: We thank W.R.M. Mason, Biosysteraatics Leiophron pseudopallipes and Research Centre, Agriculture Canada, Euphoriana lygivora (Hymenoptera: Ottawa, and P.M. Marsh, Systematic Braconidae, Euphorinae). Proc. Entomology Laboratory, U.S. Department of Entomol. Soc. Ontario 100:188-195. Agriculture, Washington, D.C., for their helpful suggestions. Loan, C.C. 1974a. The European species of Leiophron Nees and REFERENCES CITED Peristenus Foerster (Hymenoptera: Braconidae, Euphorinae). Trans. Roy. Entomol. Soc. Lond. 126:207-238. Bilewicz-Pawinska , T. 1974. Larvae of Peristenus (Hymenoptera Braconidae) parasites of Lygus Loan, C.C. 1974b. The North American rugulipennis (Heteroptera: Miridae) species of Leiophron Nees, 1818, and Pol. Pismo Entomol. 44:759-764. Peristenus Foerster, 1862 (Hymenoptera: Braconidae, Euphorinae) Bilewicz-Pawinska, T. 1977. including the description of 31 new Occurrence and role of the parasitic species. Naturaliste Can. 101:821-860. genus Peristenus Foerster (Hymenoptera: Braconidae) in fields of Loan, C.C. 1980. Plant bug hosts rye. Pol. Pismo Entomol. 47:123-125. (Heteroptera: Miridae) of some euphorine parasites (Hymenoptera: Bilewicz-Pawinska, T. 1978. Braconidae) near Belleville, Ontario, Ecological properties of Peristenus Canada. Naturaliste Can. 107:87-93. digoneutis and Peristenus stygicus (Hymenoptera: Braconidae) parasitoids Loan, C.C. 1983. Host and generic of Lygus bugs (Heteroptera: Miridae). relations of the Euphorini Bui. Acad. Sci. 26:441-446. (Hymenoptera: Braconidae). Amer. Entomol. Inst. 20:388-397. Brindley, M.D.A. 1939. Observations S on the life history of Leiophron Loan, C.C. and T. Bilewicz- pawinska. pallipes (Curtis) (Hymenoptera: 1973. Systematics and biology of four

Braconidae) , a parasite of Polish species of Peristenus Foerster Hemiptera-Heteroptera. Proc. Roy. (Hymenoptera: Braconidae,

Entomol. Soc. Lond. (A) 14:51-56. Euphorinae) . Environ. Entomol. 2:271-278. Leston, D. 1961. Observations on the mirid (Hem.) hosts of Braconidae Muesebeck, C.F.W. 1936. The genera (Hym.) in Britain. Entomol. Monthly of parasitic wasps of the braconid Mag. 95:97-100. subfamily Euphorinae with a review of the Nearctic species. U.S. Dept. Agr. Loan, C.C. 1965. Life cycle and Misc. Pub. 241, 36 pp. development of Leiophron pallipes (Curtis) (Hymenoptera: Braconidae, Nixon, G.E.J. 1946. Euphorine Euphorinae) in five mirid hosts in the parasites of capsid and lygaeid bugs Belleville district. Proc. Entomol. in Uganda. Bui. Entomol. Res. Soc. Ontario 95:115-121. 37:113-129.

Loan, C.C. 1966. A new species of Richards, O.W.R. 1967. Some British Leiophron Nees (Hymenoptera: species of Leiophron Nees Braconidae, Euphorinae) with (Hymenoptera: Braconidae, observations of its biology and that Euphorinae). Trans. Roy. Entomol. of its host Plagiognathus sp. Soc. Lond. 119:171-186. (Heteroptera: Miridae). Ohio Jour. Sci. 66:89-94.

74 :

Southwood, T.R.E., and D. Leston. 1959. Land and water bugs of the British Isles. 436 pp. Frederick Warne & Co. Ltd., London and New York.

Taylor, T.H.C. 1945. Lygus simonyi Reut. as a cotton pest in Uganda. Bui. Entoraol. Res. 36:121-148.

Waloff, N. 1967. Biology of three species of Leiophron (Hymenoptera Braconidae, Euphorinae) parasitic on Miridae on broom. Trans. Roy. Entomol. Soc. Lond. 119:187-213. FOREIGN EXPLORATION FOR NATURAL ENEMIES DISCUSSION OF LYGUS AND ADELPHOCORIS PLANT BUGS Poland Project By Robert C. Hedlundi' The work in Poland has been well Exploration for natural enemies of Lygus documented by the chief investigator, and Adelphocoris (Hemiptera: Miridae) Teresa Bilewicz-Pawinska, in several plant bugs has been undertaken in Europe, publications (1969, 1974a, 1974b, 1975, Africa, and Asia since the 1960's. 1977). In alfalfa she found three Earlier studies (Taylor, 1945; Nixon, species of Peristenus Foerster 1946) were completed in Uganda. Most (Braconidae, Euphorinae) attacking Lygus exploration work outside of North America nymphs. They were _P. rubricollis has been funded by United States and (Thomson) , ?. digoneutis Loan, and Canada. The major efforts have been P_. stygicus Loan; PL digoneutis was the undertaken by Bilewicz-Pawinska (1969, most common. Parasitism ranged from 1 to 1974a, 1974b, 1975, 1977) in Poland; the 25 percent and peaked at about the same Commonwealth Institute of Biological time as the host population. Control (CIBC, 1981) in Pakistan, India, Iran, Turkey, and Indonesia; the European Adelphocoris lineolatus (Goeze) was

Parasite Laboratory (EPL), USDA reported to be attacked by _P . rubricollis P_. (Drea et al., 1973; Hedlund and Coutinot, and pallipes (Curtis) , and parasitism 1984) in France, Austria, Germany, did not exceed 10 percent. Parasitism of Switzerland, Turkey, Spain, Italy, adult A. lineolatus by Peristenus was Greece, and Hungary; the CIBC, Delemont extremely rare, whereas parasitism of Station (CIBC, annual reports, Delemont adult Lygus rugulipennis Poppius was Station) in Austria, Switzerland, common. For both host species, the Germany, and France; and A. A. Negm and percent parasitism was calculated for the M.F. Abou Ghadir (annual reports, PL-480 total sample, which included both nymphs project FG-EG-193) in Egypt. Survey and adults. trips to the Republic of South Africa and Kenya have recently been completed by In an earlier study (1969) in rye, she M.F. Schuster (see p. 13). separated the parasitism of nymphs and adults. As would be expected, the Evaluating the results of these studies percentage of parasitized nymphs was is difficult because much of the generally much higher than that of literature is in annual reports rather parasitized adults. This is because the than in scientific publications, and only euphorine parasites found in adults adequate details of the methods are were those that did not complete their sometimes lacking. Also, the development in the nymphs as is usual. nomenclature of both the hosts and their In studies by EPL (Hedlund, unpub.), natural enemies is changing or is emergence of euphorine parasites from imprecise (Henry and Lattin, see p. 54; adults, although recorded, has been Loan and Shaw, see p. 69). extremely rare.

A list of natural enemies of some rairid Several shipments of these four bugs around the world has been published Peristenus species from Poland were sent by Clancy and Pierce (1966) and was later to the United States. Unfortunately no updated by CIBC (1979). establishments resulted, but a great deal of knowledge about the ecology and biology of both the hosts and their parasites was acquired.

Pakistan Project -^-International Research Division, Office of International Cooperation and This summary is based on the annual and Development, U.S. Department of final reports of a PL-480 project Agriculture, Washington, DC 20250. (PK-ARS-91) (CIBC, 1981). This study by

76 . , .

the Pakistan Station of CIBC was done what the investigators presumed were eggs from 1975 to 1978. The original proposal of Lygus . One of the parasites was called for work in Afghanistan and China, identified as Ery thmelus helopeltidis as well as Pakistan, Iran, and Turkey, Gahan, and it attacked up to 55 percent but the first two countries were later of the eggs deposited in Amaranthus omitted and the work was done in India dubius Mart, ex Thell. , a weed. Nymphs and Indonesia. of a probable Lygus species are mentioned as being more abundant in one field than In Pakistan, parasites were extremely in another, but the report does not rare. Some mymarid egg parasites were indicate how many were collected,

found on both Lygus and Adelphocoris . No examined, or reared to detect the parasites were recorded from the rearing presence of parasites. Hundreds of or dissection of over 160,000 nymphs and Nesidiocoris tenuis (Reuter) specimens adults during the 3-year study, despite from tomato were reared, but they collections in more than 30 localities, produced no parasites. in 8 different climatic zones, and throughout the year. It is interesting Iran and Turkey were surveyed in a to note that Lygus spp. were not found in 3-month tour during May- July 1977. In the cotton-growing areas of Pakistan. Iran, over 25,000 adults and nymphs of 19 Twenty-seven species of mirids were species of mirids were collected. A recorded for the first time from total of 1,541 nymphs and 10,151 adults Pakistan. The collections included more of Lygus gemellatus , L. rugulipennis , and than 42,000 nymphs of Lygus gemellatus L. pratensis (L.) were collected from

(Herrich-Schaef f er) , 5,000 nymphs of about a dozen sites and several different Taylorilygus pallidulus (Blanchard) host plants. Also, 242 nymphs of nearly 13,000 nymphs of Calocoris spp., Adelphocoris lineolatus were collected. and 5,000 nymphs of Adelphocoris No egg or nymphal parasites were lineolatus . These numbers seem adequate recovered in Iran. to have detected the presence of nymphal parasites if they occurred. Six species In Turkey, over 14,500 adults and nymphs of predators were found in association of 35 species of mirids were collected. with Lygus. The most common were Nabis Although no parasites were recorded, the predator Nabis ferus was fairly abundant, f erus L. a well-known predator of Lygus , , and Geocoris and Chrysopa species were and a Chrysopa sp. (Chrysopidae) . The nymphs other four were Tropiconabis capsif ormis seen occasionally. Nearly 2,000 (Germar) (Nabidae) Geocoris tricolor F., of the same 3 species of Lygus as , reported from Iran were recovered along Piocoris sp. (Lygaeidae) , and Orlus sp (Anthocoridae) with almost 2,000 nymphs of A. lineolatus

Egypt Project One collecting trip of 3 to 4 months was made to Bangalore, India. Although 12 The study in Egypt included cataloging species of mirids were recorded, only 376 the mirid fauna and its parasites as nymphs from 19 locations were collected. No Lygus or Adelphocoris species were completely as possible. Although Lygus species had previously been reported from found. Of the nymphs, 146 were Egypt (Hoberlandt, Priesner and Taylorilygus pallidulus collected on 1953; Alfieri, 1953; Linnavuori, 1964), none Erigeron bonariensis L. in 5 localities. have been recovered in the current This sample is not adequate to draw any survey, which began in 1978 and is now in conclusions about the presence of mirid its eighth year. No parasites of any parasites in India. nymphal mirids have been recovered. During 1978-79, 128 specimens of The survey in Indonesia was carried out Taylorilygus pallidulus were recovered around Bogor, West Java, between August and held for parasite emergence. In and December 1976. Two species of 1980, 151 T. pallidulus specimens were mymarid egg parasites were recovered from

77 . . ,

collected. The annual reports on which EPL Project this summary is based do not indicate what percentage were nymphs. Predators Exploration for natural enemies of mirids in the genera Orius Chrysopa , , began in August 1962 at EPL. Collections Coccinella Scymnus Geocoris, Nabis, and , , were made throughout France, in the Ura Coranus were recovered in association region of Switzerland, and in West with the mirids. In the combined report Germany. Few nymphs were collected, but for 1981 and nymphs were collected 1982, parasitism ranged up to 50 percent in from March to June 1981, and no nymphal some Lygus collections. These parasites parasites have yet been recovered. A were later identified as Euphorus scelionid egg parasite, Telenomus sp., pallipes (Curtis). No parasites were was collected. In the 1983-84 report, no recovered from any stage of Adelphocoris , nymphal parasites were recovered by although this pest was far more abundant rearing or by dissecting nymphs. than Lygus . In a second survey in April and May 1963, 9,000 nymphs were collected in West Germany and 3,000 in France. These produced 56 cocoons. Laboratory In the remainder of Africa, this subject culture increased this number to 110 was studied in Uganda in the 1940's progeny, which were sent to California, (Taylor, 1945) and in Kenya and South where there was no adult emergence. In Africa at the present time. Taylor found 1964, surveys were made in the Paris area Peristenus praetor (Nixon) and during August and September, but only 40 EL nigricarpus (Szepligeti) attacking up parasite cocoons were formed, although to 98 percent of Taylorilygus vosseleri 140 parasite larvae emerged from 3,243 (Poppius) on cotton. nymphs. Work on this project then ceased until 1970, when a September survey near Explorations in the Republic of South Chartres, France, resulted in 27 cocoons Africa during May 1981 resulted in the ( Leiophron spp.) from 600 Lygus nymphs. collection and shipment of 900 nymphs, of which 40-50 parasitized percent were In 1971, 300 nymphs of Polymerus (Schuster, see p. 16). Unfortunately unifasciatus (F.) collected on asparagus the delayed shipment resulted in near near Izmir, Turkey, produced 40 total mortality. A second survey in Peristenus stygicus cocoons (Drea et al . January 1982 resulted in the receipt of 1973). Sent to the United States and 665 cocoons from the black wattle mirid cultured, they resulted in the only Lygidolon laevigatum Reuter. From them, recorded establishment, although 167 parasites emerged, comprised of temporary, of an exotic parasite of Mesochorus melanothorax Wilkinson, a mirids (van Steenwyk and Stern, 1977). hyperparasite, and _P. praetor and Additional surveys in France in 1971 PL nigricarpus . F generations of both revealed the presence of three species of Peristenus species were obtained from Peristenus (originally called Lygus lineolaris (Palisot) in the . Leiophron ) These were EL stygicus , P laboratory. No F of EL nigricarpus 2 digoneutis , and P. rubricollis . In 1976, resulted, and only three F 2 adults (no a fourth species, EL adelphocoridis Loan, F 3 ) of P. praetor were obtained (G.L. was found attacking Adelphocoris Snodgrass, pers. comraun.). lineolatus (Loan, 1979). A total of 750 cocoons, including the 40 from Turkey, Schuster (see p. 16) went to Kenya in were sent to the United States in 1971. October 1983. Nymphs of Taylorilygus spp. were collected from grain sorghum In 1972, collections were made in eastern and Lantana camara L. The emerging France and Germany. A total of 2,190 Peristenus specimens were provided nymphs nymphs yielded 270 Peristenus parasites. of T. pallidulus , Lygus hesperus Knight, and L. lineolaris in quarantine at Table 1 is a summary of the number of Stoneville, Miss., but cultures could not Peristenus spp. sent to the United States be maintained beyond the F 2 generation by EPL during 1973-83. This was a period (G.L. Snodgrass, pers. commun.) when a rather consistent effort was made

78 —

to recover natural enemies of these W.R. Nickle as Agamermis near decaudata. mirids. The majority of the collections A nematode was earlier reported by were made in France and Austria. A grand Bilewicz-Pawihska and Kamionek (1973) on total of 14,363 Peristenus spp. were Lygus rugulipennis Mo observations have shipped, most of which were released been made by EPL on the predator complex directly in the field on emergence, but of the pest mirids. some were cultured (Debolt, see p. 83) and the progeny released. CIBC, Delemont Project

This summary refers only to Peristenus This project has been funded by Canada nymphal parasites, and, in fact, the and very closely resembles that of EPL. major effort was to collect them. A In some years, USDA contributed mymarid egg parasite, Erythmelus sp. near financially to the work, and personnel goochi Enock (determ, by G. Gordh) , was from both laboratories worked together in found, but efforts to trap large numbers the field. Collections made in various by placing egg-infested plant material in countries of Europe have resulted in the the field did not succeed. A tachinid, recovery of the same parasite species as Alophora obesa (F.), emerged from adults those reported in the EPL project. There collected in Austria, and 21 puparia and has been no estabLishment of an exotic adults were shipped in 1980. These were species in Canada. Current efforts are released in a field cage in Delaware. In concentrated on obtaining large numbers addition, in 1977, three shipments of two of Peristenus adelphocoridis, because its species of mermithid nematodes were host, Adelphocoris lineolatus, occurs in made. One was tentatively identified by

Table 1 Number of specimens and source country of Peristenus spp. sent to United States by European Parasite Laboratory, 1973-83

Peristenus

Year Country digoneutls styglcus rubricollis adelphocoridis

1973 France 152 1974 Poland — — 85 France 26 60 9 1975 France 73 — 30 1976 France 340 180 124 1977 Austria 120 1/275 — France 631 i/763 1/232 1978 Austria?./ 1,036 41 59 France 2,273 1/ 1,388 l/l81 1979 Austria 7 — — France 1,562 9 — 1980 Spain — 35 — Austria 384 41 76 France 130 — — 1981 Austria 1,261 26 24 France 1,201 5 4 1982 Spain — 88 — France 139 — — 67 1983 Hungary 56 98 — Greece — 30 — Spain — 65 — France 568 76 17 316

Total 9,959 3,180 841 383

L^Some material laboratory reared.

2/ Austrian collections done in cooperation with CIBC, Delemont.

79 .

both North America and Europe. This fact sufficient effort and time, but it implies increased probability of appears unlikely that such a commitment establishment of its European parasites will be made in the near future. in North America. More specific results of this project are contained in informal There are possibilities for work to be annual reports and thus cannot be cited done under cooperative agreements, such or summarized here. as the Binational Agricultural Research and Development Fund agreement with Future Exploration Israel. Special Foreign Currencies still exist in some countries, such as India, A large part of the world remains to be Pakistan, Poland, and Yugoslavia, and explored for natural enemies of Miridae. projects using these funds can be Central and southern Europe, a small initiated through the Office of section of Asia, and four countries on International Cooperation and the African continent have been the only Development, an agency of the USDA. With areas surveyed for natural enemies for additional personnel, the Asian Parasite importation into North America. Not all Laboratory, USDA, could undertake a these surveys were adequate owing to long-term study in Korea, a country very limitations of time, personnel, and similar in climate to large areas of the funding. United States and southern Canada. The exchange programs with the People's Ideally, the first new areas to be Republic of China and the Union of Soviet surveyed should be where adequate Socialist Republics offer possibilities populations of mirids, closely related or for short-term investigations, but identical to pest species of North permission to export the natural enemies America, are known to be present. The needs to be clearly specified at the ecology and biology of these hosts, as outset well as those of the natural enemies, should be thoroughly studied. The Almost nothing is known about mirids or natural enemies most likely to succeed in their enemy complex in South America or becoming established should then be in eastern Africa. It is possible that tested against the proposed target hosts effective and potentially useful natural to determine host suitability. Host enemies exist in these areas. range, predaceous habits, and any phytophagous tendencies should also be CONCLUSIONS evaluated and compared to potential benefits. When results of these studies Surveys in Europe, South Central Asia, are favorable, mass collection and and some African countries during the release should begin and continue for 3-4 1960's and-1970's have resulted in the years to attempt establishment of the discovery of several natural enemies of natural enemy. This should then, of mirids. Although predators and egg and course, be followed by a thorough adult parasites have been observed, they evaluation of the effectiveness of the have not been studied. Importations into established species. In reality, North America have concentrated on however, information on occurrence of hymenopterous parasites of the nymphs. closely related mirids does not usually Apparently none of these have become exist, although the Pakistan and Egypt established though they often attack the projects have provided this information proposed hosts in the laboratory and are in the areas surveyed. Funding and sometimes found in the field for short political considerations often prevent periods after release. Most of the long-term studies in foreign countries, world's agricultural areas, sometimes and lack of culture techniques, including entire continents, have especially for predators and nematodes, received no survey effort. Although precludes host range and other tests. various areas could be explored to some All these obstacles can be overcome with extent, there is a need for a large and

80 long-term commitment by North American Clancy, D.W., and H.D. Pierce. 1966. agricultural research organizations to Natural enemies of some lygus bugs. investigate fully the potential of exotic Jour. Econ. Entomol. 59:853-858. natural enemies of mirids for controlling the pest species of North America. Drea, J.J., L. Dureseau, and E. Rivet. 1973. Biology of Peristenus stygicus REFERENCES CITED from Turkey, a potential natural enemy of lygus bugs in North America. Environ. Bilewicz-Pawinska, T. 1969. Natural Entomol. 2:278-280. limitation of Lygus rugulipennis Popp, by a group of Leiophron pallipes Curtis on Hedlund, R.C., and D. Coutinot. 1984. the rye crop fields. Ekol. Pol., Ser. A, Parasitism of Lygus spp. and Adelphocoris 17:811-825. spp. in central France. Proc. Internatl. Conf. on Integrated Plant Protect., Bilewicz-Pawinska, T. 1974a. Emergence Budapest, Hungary, July 4-9, 1983. and longevity of two species of Peristenus Foerster (Braconidae) under Hoberlandt, L. 1953. Results of the laboratory conditions. Ekol. Pol. Armstrong College Expedition to Siwa 22:213-222. Oasis (Libyan Desert), 1935, under the leadership of Prof. J. Omer-Cooper: Bilewicz-Pawinska, T. 1974b. Hemiptera-Heteroptera. Bui. Soc. Observations of introduction of Entomol. Egypt 37:359-370. Peristenus rubricollis Thomson under laboratory conditions. Bui. Acad. Pol. Linnavuori, R. 1964. Hemiptera of Sci. 22:681-684. Egypt, with remarks on some species of the adjacent Eremian region. Ann. Zool. Bilewicz-Pawinska, T. 1975. Fenn. 1:306-356. Distribution of the insect parasites, Peristenus Foerster and Mesochorus Loan, C.C. 1979. Three new species of Gravenhorst in Poland. Bui. Acad. Pol. Peristenus Foerster from Canada and Sci. 23:823-827. Western Europe (Hymenoptera : Braconidae,

Euphorinae) . Naturaliste Can. Bilewicz-Pawinska, T. 1977. Parasitism 106:387-391. of Adelphocoris lineolatus Goeze and Lygus rugulipennis Popp. (Heteroptera) by Nixon, G.E.J. 1946. Euphorine parasites braconids and their occurrence on of capsid and lygaeid bugs in Uganda alfalfa. Ekol. Pol. 25:539-550. (Hymenoptera: Braconidae). Bui. Ent. Res. 37:113-129.

Bilewicz-Pawinska, T. , and M. Kamionek. 1973. Lygus rugulipennis Popp. (Het.: Priesner, H. , and A. Alfieri. 1953. A Miridae) as a host of a nematode review of the Hemiptera-Heteroptera known (Mermithidae) . Pol. Pismo Entomol. to us from Egypt. Bui. Soc. Entomol. 43:847-849. Egypt 37:1-119.

CIBC (Commonwealth Institute of Taylor, T.H.C. 1945. Lygus simonyi Biological Control). 1979. Reut., as a cotton pest in Uganda. Bui. Possibilities for biological control of Ent. Res. 36:121-148. lygus bugs (Hemiptera: Miridae). Commonw. Inst. Biol. Control, Status Van Steenwyk, R.A., and V.M. Stern. Paper 15, 7 pp. 1977. Propagation, release and

evaluation of Peristenus stygicus , a CIBC. 1981. Investigations on the newly imported parasite of lygus bugs. natural enemies of Lygus spp. and other Jour. Econ. Entomol. 70:66-69. plant bugs (Miridae). Final rpt. [of PL-480 proj. PK-ARS-91], Commonw. Inst. Biol. Control, Pakistan Station, 39 pp. with appendixes and plates. [Unpub.]

81 ,

AUGMENTATION: REARING, RELEASE, AND parasites, Peristenus stygicus Loan, EVALUATION OF PLANT BUG PARASITES imported from Europe, may be an excellent candidate if initial establishment is By Jack W. Debolti/ followed by additional augmentative releases. Augmentation of natural enemies can be defined as any action used to increase The effectiveness of augmentative populations or effectiveness of the releases depends not on the long-term beneficial organisms. As such it can suppression of Lygus spp. but on include environmental manipulations as short-term reductions in populations. well as periodic releases of selected These reductions will be effective if natural enemies. This report deals with they reduce the movement of Lygus spp. the latter factor, specifically the from alternate host plants to crops where potential for using properly timed they cause considerable damage. In the periodic releases of selected parasites case of L. hesperus, reduction of the as a component in Lygus spp. management first two generations on alfalfa in the programs. spring should eliminate several insecticide applications later on cotton, Lygus lineolaris (Palisot) is the major which would have disrupted the entire pest species in the Eastern and Southern beneficial complex there. This would United States and Canada, whereas Lygus save the cotton grower money by reducing hesperus Knight takes over this role in the need to control Lygus spp. and other the Southwestern and Western United secondary pests. States. Of the six North American hymenopterous parasites of Lygus spp. REARING listed by Krombein et al. (1979), two nymphal parasites, the braconids Successful augmentation of Lygus spp. Peristenus pallipes (Curtis) and parasites depends on the timely

Leiophron unif ormis (Gahan) , and an egg availability of sufficient numbers of parasite, the mymarid Anaphes ovi jentatus these parasites. Efficient and highly

(Crosby and Leonard) , are widespread and cost-effective methods will be needed to common enough to be possible candidates meet this goal. At present, few insect for augmentative releases. parasites have been reared outside their host. We must, therefore, still rely on Peristenus pallipes occurs over much of rearing systems that begin with efficient the United States as a parasite of Lygus production of living hosts. lineolaris , but it has not been reported from the Southwest (Clancy and Pierce, In the past, most Lygus spp. were reared

1966). Leiophron unif ormis , the only on green beans, Phaseolus vulgaris L. hymenopterous parasite of Lygus spp. (Beards and Leigh, 1960), or combinations nymphs reported in the Southwest, is also of green beans with other foods such as found in low numbers from the Midwest, heat-killed larvae of the beet armyworra, into Canada, and eastward to New Jersey Spodoptera exigua (Hubner) (Bryan et al. and Delaware. The egg parasite Anaphes 1976) . Rearing systems using Lygus spp. ovi jentatus has been reported from such produced by these methods as hosts have widespread areas as the Southwest, New been described for parasites of mirid York, Indiana, Louisiana, and California nymphs, Peristenus stygicus (Van Steenwyk (Clancy and Pierce, 1966; Stoner and and Stern, 1976) and Leiophron unif ormis Surber, 1969; Sillings and Broersma, (Debolt, 1981), and for the parasite of 1974) . In addition to these native mirid eggs, Anaphes ovi jentatus (Stoner and Surber, 1969). The quality and quantity of parasites and their hosts i^Biological Control of Insects produced by these methods vary greatly Laboratory, Agricultural Research with changes in the quality and Service, U.S. Department of availability of the mirid* s food Agriculture, 2000 East Allen Road, sources. Unfortunately, during late Tucson, AZ 85719.

82 winter and early spring, when parasite to colonize Peristenus pallipes collected cultures should be increased, green beans from New Jersey, and they achieved some are at their lowest availability, poorest initial parasitization. Van Steenwyk and quality, and highest price. This often Stern (1977) reared and released a large requires a shift to other even more number of P_. stygicus adults in an expensive and less satisfactory foods. alfalfa, plot in the San Joaquin Valley of California from May through August 1973. Only recently has Debolt (1982) reported In their study, the alfalfa was strip-cut the first artificial diet suitable for and the cutting cycle was greatly continuous rearing of any Lygus sp. lengthened from 30 to 60 days in order to Improvements in rearing and feeding increase the number of available Lygus. techniques (Patana, 1982; Debolt and A low rate of parasitism was achieved Patana, 1985) have allowed greatly during 1973, and the parasites were increased production of L. hesperus recovered in lower numbers during the nymphs and eggs for parasite production. next two summers. In neither instance At the Biological Control of Insects was any attempt made to augment the Laboratory, Tucson, Ariz. , we routinely parasite populations after the initial expose over 38,000 Ij. hesperus nymphs per release period. week to stygicus and L. uniformis, using only the excess produced by the To make efficient use of parasites in laboratory host culture. In addition, augmentative releases, we need to develop the egg parasite A. ovijentatus has been release techniques that will improve the shown to readily attack and develop well released parasite's effectiveness and in eggs laid in synthetic membranes by survival in the field. The hymenopterous artificial diet-reared L. hesperus parasites of Lygus spp. nymphs can be (Jackson, 1982). Another major target released as adults, cocoons, or as larvae species, L. lineolaris , has recently been in parasitized hosts. Only adult successfully adapted to rearing on the releases have been reported, and this is artificial diet, though initially its usually the only procedure feasible for reproduction was very poor. The effects the immediate release of foreign of such severe laboratory selection on material. Unfortunately, studies have production or effectiveness of parasites not been made of the behavior of the have not been studied. released parasites. Such knowledge might provide clues to the timing and Efforts are continuing to improve the procedures for release. Thus, we have rearing procedures for parasites of Lygus little knowledge as to whether the spp. eggs and nymphs. Although present parasites begin searching for hosts, methods are sufficient to rear several mate, leave the area, or fly to the thousand individuals of L. uniformis , nearest attractive nectar source. Also,

£. stygicus , and A. ovijentatus per week, we can only guess at the best time of day large-scale field testing will require for adult parasite release. With the the development of mechanization and advent of improved rearing techniques, we automation techniques to increase now have available the needed numbers of parasite production. certain parasites to experimentally study these factors. In addition, we can RELEASE determine the potential for release of parasitized hosts or parasite cocoons or The history of parasite releases to both. Successful suppression of Lygus control Lygus spp. in North America has spp. populations possibly may require been summarized in this publication by release of two or all three parasite Coulson (p. 1), Craig and Loan (p. 48), stages to provide a continuity of and Day (p. 20). Most releases have been parasites. of small numbers of imported parasites, and the results have not until now been Rearing procedures being developed for published. Clancy and Pierce (1966) egg parasites may eventually allow their attempted near Riverside, Calif., in 1964 release in large numbers. Releases of

83 — ,

egg parasites, either as adults or in the The use of cages to exclude the parasites host eggs, could be aimed at periods when from certain units may provide one of the host nymphs are not yet available. best methods to utilize the numbers of parasites we currently can produce. Disruption of cultivated hosts of Lygus Leigh and Gonzalez (1976) used this spp. by harvesting and cultural practices technique effectively to study various often produces an extremely unstable predator species attacking L. hesperus on environment, and variable populations of cotton. Lygus hesperus females were both pest and beneficial insects result. caged on cotton plant terminals for a Several studies have indicated higher and limited time in large field cages, some more stable populations of parasites of of which had been treated with Lygus spp. on weeds, even when mixed with insecticide to remove indigenous the cultivated host (Streams et al. species. Predators were then introduced 1968; Sillings and Broersma, 1974; Lim to some of the cages. In this way these and Stewart, 1976; Graham and Jackson, researchers were able to separate the 1982). Given this information, release effects of indigenous predators from of parasites on weed hosts, especially those effects due to the introduced with small numbers of foreign parasites, species. Two advantages of such tests may ensure more rapid and positive are that they can be replicated in a colonization. This could in turn provide relatively uniform habitat such as an material for later rearing and alfalfa field or a large wild host patch augmentation efforts. and that they require only moderate numbers of parasites. Not only would EVALUATION such cage tests demonstrate the effectiveness of the parasite but they The importance of evaluating the could provide data on the efficiency of effectiveness of natural enemies with the parasite and help to determine the studies that include experimental checks numbers needed in open field releases. in paired comparative plots has been These tests could provide information on pointed out by DeBach et al. (1976). the immediate effect of the released This is especially true in evaluating the parasites, but they would not be readily short-term rapid effects we should expect adaptable to studying continuing effects from augmentation programs. due to the growth and harvesting of the host plants. DeBach and Huffaker (1971) discussed three methods of evaluating the When large numbers of parasites are effectiveness of natural enemies available, augmentative releases could be addition, exclusion or subtraction, and evaluated in replicated tests without the interference. The first two are most need for cages. Fields of cultivated likely to be useful in assessing the hosts such as alfalfa are usually benefits of augmenting parasites of abundant enough in one area so that Lygus spp. release and check fields can be replicated throughout an area. Even The last method, interference, has been without knowing the dispersal abilities used mostly with pests that occupy of the pests and parasites, it should be discrete units of habitat such as trees. possible to detect the level of The insecticide interference method may, parasitism increase we would expect from however, be applicable when the dispersal augmentation releases. This would be range of the parasite is known. The especially true if releases were made greatest difficulty with using this during periods with low rates of natural technique for Lygus spp. is that this parasitism of Lygus spp., such as during pest is preyed on by a complex of natural the early months of the year in the enemies. Thus, unless an insecticide is Southwestern United States (Graham et highly specific against the parasite, it al. , 1986) . Monitoring could be would be impossible to determine the continued throughout the season, but the actual causes of pest density changes. effectiveness of the parasites would be

84 harder to determine because of migration samples have been obtained by using sweep into and out of the test fields. Weed nets (Clancy and Pierce, 1966; Hormchan, hosts also occur throughout an ecosystem 1977) or D-Vac suction samplers (Van in patches, which could serve as treated Steenwyk and Stern, 1977). Although both and check plots. Since weed patches are methods have advantages and generally smaller than fields of disadvantages, they provide rapid cultivated hosts, they would require sampling of Lygus spp. and their fewer parasites and might be even easier parasites. When the proper preliminary to replicate. work is done to establish uniform sampling techniques for use on the Eventually the effectiveness of parasite various important Lygus spp. host plants, releases will have to be evaluated on these methods should provide population crops over a relatively wide area. This estimates accurate enough to evaluate is true whether the object is to attack parasite augmentation programs. the Lygus spp. on reservoir hosts to reduce their movement into valuable crops Determination of the proportion of Lygus or to reduce the population directly on spp. parasitized is usually done either such crops. Adequate replication of such by dissection or by rearing the host wide areas is almost impossible to until parasite emergence (Clancy and achieve. Success or failure of these Pierce, 1966; Loan, 1974; Van Steenwyk types of releases over a period of years and Stern, 1977; Graham et al., 1986). will determine the effectiveness of the Dissection of nymphs provides the most system. accurate estimates of the proportion of hosts parasitized, since the results are As Lygus spp. infest a wide range of both not biased by differential mortality cultivated and wild host plants and the between parasitized and unparasitized area covered by certain wild hosts cannot hosts during handling and rearing. be determined accurately in a large Nymphs can be dissected live if numbers ecosystem, intensive sampling of all are small, and larger numbers can be hosts will be impossible. The situation frozen for later dissection (Day, see becomes much more difficult when p. 25). Nymphs can be directly examined attempting to estimate populations on the rapidly, and probably rearing should only diverse hosts of Lygus spp. hosts that , be used when personnel cannot handle the vary widely in their growth habits. number of nymphs or when adult parasite Studies covering large numbers of host or host identification is required. When plants, such as those carried out by nymphs are reared, the proportion Graham et al. (1986) that provide host parasitized should be based only on those range and yearly population trends, that survive until parasite emergence should pinpoint the major sources of (number adult bugs plus number of Lygus spp. adults. Quantitative sampling parasite larvae and cocoons) to eliminate of these hosts, as well as of the crops from the estimate those that die of we seek to protect in an ecosystem, unknown causes (Debolt, 1981). should provide adequate data to assess the impact of augmentative releases. In Since mirid eggs are inserted into plant addition, such sampling of major hosts tissues, it would be very difficult to will also provide data that can be used directly determine parasitism by to construct life tables of Lygus spp. on dissection. Estimates of the proportion these hosts. Studies on these life parasitized can be made by counting mirid tables for critical host plants will eggs in plant stems with the aid of a greatly aid in assessing the importance dissecting microscope and holding samples of the various natural enemies in of plant stems containing eggs for regulating Lygus spp. populations. emergence and identification of mirids and their parasites as described by Both in surveys for native parasites and Graham et al. (1984, 1986). in attempts to evaluate parasite introductions, Lygus spp. nymph and adult

85 REFERENCES CITED Graham, H.M., C.G. Jackson, and J. W. Debolt. 1986. Lygus spp. Beards, G.W., and T.F. Leigh. 1960. A (Hemiptera: Miridae) and their parasites laboratory rearing method for Lygus in agricultural areas of southern hesperus Knight. Jour. Econ. Entomol. Arizona. Environ. Entomol. 15:132-142. 53:327-328. Graham, H.M., C.G. Jackson, and Bryan, D.E., C.G. Jackson, R.L. Carranza, K. R. Lakin. 1984. Comparison of two and E.G. Neeraan. 1976. Lygus hesperus : methods of using the D-vac to sample Production and development in the mymarids and their hosts in alfalfa. laboratory. Jour. Econ. Entomol. Southwest. Entomol. 9:249-252. 69:127-129. Hormchan, P. 1977. Biology of three Clancy, D.W., and H.D. Pierce. 1966. exotic species, and role of native Natural enemies of some lygus bugs. species of the genus Peristenus - Jour. Econ. Entomol. 59:853-858. parasites of tarnished plant bug, Lygus

lineolaris , in Mississippi. Ph.D. DeBach, P., and C.B. Huffaker. 1971. Dissertation, Miss. State Univ., 74 pp. Experimental techniques for evaluation of the effectiveness of natural enemies. In Jackson, C.G. 1982. Parasitism of Lygus Huffaker, C.B., ed., Biological Control, spp. eggs by the mymarid wasp Anaphes pp. 113-140. Plenum Press, New York and ovi jentatus (Crosby and Leonard) . Ph.D.

London. Dissertation, Univ. Ariz. , Tucson, 91 pp.

DeBach, P., C.B. Huffaker, and Krombein, K.V., P.D. Hurd, Jr., A.W. MacPhee. 1976. Evaluation of the D.R. Smith, and B.D. Burks. 1979. impact of natural enemies. Ln Huffaker, Catalog of Hymenoptera in America north C.B., and P.S. Messenger, eds., Theory of Mexico. Vol. 1, 1198 pp. Smithsonian and Practice of Biological Control, pp. Inst. Press, Washington, D.C. 255-285. Academic Press, New York, San Francisco, and London. Leigh, T.F., and D. Gonzalez. 1976. Field cage evaluation of predators for Debolt, J.W. 1981. Laboratory biology control of Lygus hesperus Knight on and rearing of Leiophron unif ormis cotton. Environ. Entomol. 5:948-952.

(Gahan) (Hymenoptera : Braconidae) , a parasite of Lygus spp. (Hemiptera: Lim, K.P. , and R.K. Stewart. 1976.

Miridae) . Ann. Entomol. Soc. Amer. Parasitism of the tarnished plant bug, 74:334-337. Lygus lineolaris (Hemiptera: Miridae), by

Peristenus pallipes and _P . pseudopallipes Debolt, J.W. 1982. Meridic diet for (Hymenoptera: Braconidae). Can. Entomol. - rearing successive generation of Lygus 108 : 601 608 . hesperus. Ann. Entomol. Soc. Amer. 75:119-122. Loan, C.C. 1974. The North American species of Leiophron Nees, 1818, and Debolt, J.W., and R. Patana. 1985. Peristenus Foerster, 1862 (Hymenoptera:

Lygus hesperus . In Moore R.F., and P. Braconidae, Euphorinae) , including the Singh, eds., Handbook of Insect Rearing, description of 31 new species. vol. 1, 488 pp. Elsevier, Amsterdam. Naturaliste Can. 101:821-860.

1982. Graham, H.M. , and C.G. Jackson. Patana, R. 1982. Disposable diet packet Distribution of eggs and parasites of for feeding and oviposition of Lygus Lygus spp. (Hemiptera: Miridae), Nabis hesperus (Hemiptera: Miridae). Jour. spp. (Hemiptera: Nabidae) , and Econ. Entomol. 75:668-669. Spissistilus f estinus (Say) (Homoptera: Membracidae) on plant stems. Ann. Entomol. Soc. Amer. 75:56-60.

86 Sillings, J.O., and D.B. Broersma. 1974. The parasites of the tarnished plant bug Lygus lineolaris in Indiana. Proc. North Cent. Branch Entomol. Soc. Amer. 29:120-125.

Stoner, A., and D.E. Surber. 1969. Notes on the biology and rearing of

Anaphes ovi jentatus , a new parasite of Lygus hesperus in Arizona. Jour. Econ. Entomol. 62:501-502.

Streams, F.A., M. Shahjahan, and H.G. LeMasurier. 1968. Influence of plants on the parasitization of the tarnished plant bug by Leiophron pallipes. Jour. Econ. Entomol. 61:996-999.

Van Steenwyk, R.A., and V.M. Stern. 1976. The biology of Peristenus stygicus

(Hymenoptera : Braconidae) , a newly imported parasite of lygus bugs. Environ. Entomol. 5:931-934.

Van Steenwyk, R.A., and V.M. Stern. 1977. Propagation, release, and evaluation of Peristenus stygicus , a newly imported parasite of lygus bugs. Jour. Econ. Entomol. 70:66-69. .

QUARANTINE PROCEDURES FOR IMPORTED ROLE OF THE QUARANTINE PARASITES OF LYGUS SPP. The role of a quarantine facility on By G.L. Snodgrass and L.R. Ertleii/ receipt of any culture of an exotic parasite species is to check the culture Shipment of exotic parasites of Lygus for unwanted plant material, to

(Heteroptera : Miridae) spp. to a positively identify the parasite, and, quarantine facility in the United States when advisable, to subsequently ship requires prior approval and permits strong, viable specimens. If the issued by the USDA, Animal Plant Health biology of the parasite is well known Inspection Service, Plant Protection and and rearing methods for it have been Quarantine (APHIS, PPQ) . Approval by established, then the quarantine the the State agricultural agency where facility may only need to forward the also is quarantine facility is located culture to its final destination. The required. There must be coordination quarantine facility could also perform and this facility as between the shipper host range studies or increase the packaging, to timing, correspondence, numbers of cultures prior to their routing, and so forth. In addition, the release from quarantine. A quarantine facility must ensure that the quarantine facility can also receive a culture of a proper numbers and life stage(s) of the parasite species, usually in limited for intended host(s) are available numbers from field-collected hosts, the parasites are testing when whose biology is not well known. In received. An excellent discussion of this instance, the quarantine facility to the procedures for shipping parasites must try to simultaneously evaluate the facility is found in Jones a quarantine parasite against a targeted Lygus sp information et al. (1984). Additional and increase the numbers of parasites. on packaging live material for shipment is in Boldt and Drea (1980). Since information on the basic biology of the parasite needed to develop The United States has 20 Federal and rearing methods for the particular State quarantine facilities available species is usually lacking, knowledge of a variety of for the importation wide from rearing a closely related species biological material (Knutson et al., of parasite must be used. Consequently, Research 1982). The Beneficial Insects a proper evaluation of the parasite may ARS Laboratory, the USDA, quarantine not be obtained. If a viable colony of Del., has been the facility in Newark, the parasite is established in parasites main facility for importing quarantine using the targeted Lygus sp. for use in controlling Lygus spp. Many host then additional data can be in , of these parasites were collected obtained on rearing methods, host Europe and propagated at the ARS efficacy, and host range. This European Parasite Laboratory in Sevres, information is critical for propagating France. The ARS research quarantine the parasite and determining when and if facility in Stoneville, Miss., is it should be released from quarantine. involved in evaluating parasites collected In Africa for release against PROPAGATION OF TARGET AND NONTARGET HOSTS Lygus spp.

A quarantine facility must be able to rear not only the intended Lygus host ^/Respectively , Southern Field Crop Insect Management Laboratory, but other insect species used in related Agricultural Research Service, U.S. host range studies. Species of Lygus Department of Agriculture, P.0. Box 225, usually can be successfully reared on Stoneville, MS 38776, and Beneficial one of their plant hosts such as green beans, Phaseolus vulgaris L. which can Insects Research Laboratory, , Agricultural Research Service, U.S. be purchased throughout the year, Lygus Department of Agriculture, 501 South lineolaris (Palisot), L. hesperus Knight, Chapel Street, Newark, DE 19713. L. desertinus Knight, and L. elisus Van

88 ,

Duzee all can be reared on green beans REARING NYMPHAL AND EGG PARASITES (Beard and Leigh, 1960; Butler, 1970; Mueller and Stern, 1973; Parrott et al. Species of Peristenus and its closely 1975). Several artificial diets have related genus Leiophron comprise most of been tested for suitability in rearing L. the known nymphal parasites of Lygus lineolaris and L. hesperus (Landes and spp., whereas all known egg parasites of Strong, 1965; Auclair and Raulston, 1966; Lygus spp. are mymarids in the genera Vanderzant, 1967; Strong and Kruitwagen, Anaphes , Erythmelus , and Polynema (CIBC, however, the only artificial 1969); diet 1979) . Nymphs or eggs of Lygus are on which any rairid has been reared often exposed for parasitization by continuously is that developed by Debolt placing them in cages with adult male ( 1982) for L,. hesperus . and female parasites. Cages vary in size and are commonly ventilated In general, Lygus spp. can be reared cardboard or plastic containers. between 15° and 30°C, at a day length of 14 hours or longer to prevent Adult parasites are provided with a reproductive diapause, and at a relative water source and usually fed honey or a humidity of 50-60 percent. The most honey-sucrose mixture applied to the satisfactory rates of development sides of the cage. A fan may be placed usually occur from 25° to 30° (Ridgway near the cage since the movement of air and Gyrisco, 1960; Leigh, 1963; Champlain through the cage may stimulate mating or and Butler, 1967; Strong and Sheldahl, oviposition (Hormchan, 1977; Porter,

1970; Butler, 1970; Butler and 1979) . To ensure that female parasites Wardecker, 1971; Mueller and Stern, are mated, cocoons or parasitized eggs 1973; Khattat and Stewart, 1977). The can be held individually in gelatin rearing of related beneficial species of capsules until adult emergence. Emerged Hemiptera for host range studies is parasites are sexed, then paired and often more difficult than rearing Lygus observed for mating. Most species of spp. Colonies of a few predaceous Peristenus diapause within a cocoon in species, such as Geocoris punctipes the soil and mate soon after emergence Orius (Say) (Cohen and Debolt, 1983) and (Bilewicz-Pawinska , 1971; Drea et al., insidiosus (Say) (Isenhour and Yeargan, 1973; Van Steenwyk and Stern, 1976;

1981) , can be maintained under Hormchan, 1977). The use of mated laboratory conditions. female parasites is critical because all known Lygus spp. parasites are The eggs or nymphs of other beneficial arrhenotokous, or produce only male species can be collected from the field progeny if unmated. The occurrence of for exposure to the parasite being diapause complicates rearing efforts, tested, but care must be taken to ensure since it lengthens the time required to that they are not already parasitized by increase a parasite culture in numbers. native parasites. This can be It also makes field releases of the accomplished by holding part of the parasite more difficult, since the field-collected eggs or nymphs parasite must emerge when hosts in the separately for observations of native field are in the proper life stage for parasite emergence. Field-collected parasitization. nymphs of predaceous Hemiptera often can be reared by providing them with a water BIOLOGY STUDIES source and lepidopterous eggs or larvae for food, which expands the rearing If a parasite attacks the Lygus nymph or program in order to maintain a supply of egg to which it is exposed and progeny the required hosts. develop successfully, then studies should be made to determine the number of nymphs or eggs parasitized per female. Other criteria such as the sex

89 ratio of the offspring, the occurrence removed from the cages and held for of diapause, and the longevity of the parasite emergence. Nymphs are often adult parasite are very useful in held in cardboard cartons with a evaluating a parasite species prior to substrate in the bottom for parasite its release or in propagating for pupation once the larvae leave the host release. In some cases, parasitization nymph or adult. Depending on the apparently occurs, but no parasite species, larvae of Peristenus and progeny are produced; dissection of the Leiophron can emerge from older nymphs host after parasitization may be or adults (Brindley, 1939; Loan, 1965;

necessary to determine host resistance Drea et al. , 1973; Loan and Craig, 1976; mechanisms, such as encapsulation. Hormchan, 1977; Debolt, 1981). The substrate provided for pupation is Results of laboratory studies can be commonly a layer of vermiculite or affected by environmental conditions layers of black felt. Since some under which the host is exposed and species of Lygus are facultative reared, age of the host egg parasitized, predators (Wheeler, 1976), the pupation density and instar of the host exposed, substrate is usually separated from the and diet of the adult. For example, Van Lygus nymphs by a wire screen or a Steenwyk and Stern (1976) found that the similar device that allows the parasite number of progeny of Peristenus stygicus larvae to crawl through but that Loan decreased when Lygus hesperus was excludes the Lygus nymphs. parasitized in later instars, although a higher percentage of the progeny instars Parasitized eggs may be held in petri were females. Adult longevity was dishes. Cocoons of nymphal parasites inversely related to temperature, and at can be removed from the pupation a day length of 12.75 hours nearly all substrate and held separately or left offspring entered diapause. Debolt undisturbed in the substrate until (1981) found that the maximum progeny emergence. Cold storage at per female of Leiophron unif ormis (Gahan) approximately 10°C for varying periods were obtained when 75 nymphs of of time may be required to break L. hesperus were exposed per female diapause. Some parasites, such as a of .P. parasite; no increase in female Turkish strain stygicus , do not offspring occurred when more than 50 undergo diapause under laboratory hosts per female parasite were exposed. conditions (Drea et al., 1973). The greatest number of progeny per female parasite was produced when hosts HOST RANGE STUDIES in instars two and three were attacked. Stoner and Surber (1969, 1971) studied In nature most parasites attack several the mymarid Anaphes ovi jentatus (Crosby different host species. In the and Leonard) and found that fewer laboratory, the barriers of time and parasites were produced in Lygus eggs as space that separate potential hosts and the age of the exposed egg increased. parasites in nature are absent (Doutt, The rate of development and adult 1959). Consequently, host range studies longevity for both sexes were can be misleading since parasitization temperature dependent. of a species in the laboratory may not occur in nature. Information on the The time that Lygus spp. nymphs or eggs life cycle and host range of a parasite should be exposed to a parasite for in its native country is very useful in parasitization varies. Van Steenwyk and determining whether or not host range Stern (1976) exposed Lygus hesperus studies must be done in quarantine and nymphs to I>. stygicus for 48 hours, in choosing the potential hosts to be whereas Debolt (1981) found that there tested. Host range studies should be was no increase in progeny of Leiophron conducted when little is known about the unif ormis per female parasite when native host range. L. hesperus nymphs were exposed for periods longer than 1 hour. After The beneficial insects to be screened in exposure, Lygus spp. eggs or nymphs are quarantine can be selected by considering

90 ] .

the host range of closely related species REFERENCES CITED of the parasite, if this information is available. Consideration also must be Auclair, J.L., and J.R. Raulston. given to the most abundant hemipterous 1966. Feeding of Lygus hesperus predators that occur in the intended (Hemiptera: Miridae) on a chemically release area of the parasite, and one or defined diet. Ann. Entomol. Soc. Amer. more of these predators should be 59:1016-1017. screened for parasitization by the exotic parasite. The presence of alternate Beard, G.W. , and T.F. Leigh. 1960. A mirid hosts in the release area can be laboratory method for rearing Lygus critical to the establishment of an hesperus Knight. Jour. Econ. Entomol.

exotic parasite of Lygus . Consequently, 53:327-328. the mirid fauna in an intended release

area should be known. Mirid species such Bilewicz-Pawinska , T. 1971. Role of

as those in the genera Ceratocapsus , parasitic Hymenoptera in reduction size

. Pilophorus , Deraeocoris , Phytocoris , and of two species of the genus Lygus

Hyaliodes are predaceous (Kelton, 1980) [Final rpt. of PL-480 proj . E21-ET-11],

and parasitism of them is undesirable. Inst. Ecol. , Pol. Acad. Sci., Warsaw, 54

Therefore, host range studies should also pp . [Unpub. include some of the most abundant predaceous and phytophagous species of Boldt, P.E., and J.J. Drea. 1980. Miridae found in th^ intended release Packaging and shipping beneficial area. A good example of a host range insects for biological control. FAO study where predaceous and phytophagous Plant Protect. Bui. 28:64-71. species of Miridae were screened for parasitism was performed by Jackson and Brindley, M.D. 1939. Observations on Graham (1983) using the native mymarid the life-history of Euphorus pallipes

egg parasite Anaphes ovi jentatus . (Curtis) (Hymenoptera: Braconidae) , a parasite of Hemiptera-Heteroptera Two methods can be used to expose Proc. Roy. Entomol. Soc. Lond. 14:51-56. nontarget hosts to exotic parasites in quarantine. In a no-choice method, the Butler, G.D. 1970. Temperature and the parasite is exposed only to the nontarget development of egg and nymphal stages of host, using the same methods for exposing Lygus desertus. Jour. Econ. Entomol. the eggs or nymphs of the intended Lygus 63:1994-1995. spp. host. If parasitization of the nontarget host occurs in a no-choice Butler, G.D., and A.L. Wardecker. test, then additional tests can be 1971. Temperature and development of

performed where the intended Lygus host eggs and nymphs of Lygus hesperus . Ann. and nontarget host are exposed to the Entomol. Soc. Amer. 64:144-145. parasite simultaneously to determine host selection preference. Champlain, R.A., and G.D. Bulter. 1967. Temperature effects on RELEASE OF PARASITE FROM QUARANTINE development of the egg and nymphal

stages of Lygus hesperus . Ann. Entomol. The decision to release an exotic Soc. Amer. 60:519-521. parasite of Lygus from quarantine is usually made by the quarantine officer CIBC (Commonwealth Institute of

involved and requires the permission of Biological Control) . 1979. the appropriate State and Federal Possibilities for biological control of officials through the use of PPQ Form Lygus bugs (Hemiptera: Miridae). 526. This decision is made after a Commonw. Inst. Biol. Control, Status careful examination of all the available Paper 15, 7 pp. data relating to the parasite and its potential host range.

91 Cohen, A.C., and J.W. Debolt. 1983. Kelton, L.A. 1980. The insects and Rearing Geocoris punctipes on insect arachnids of Canada. Pt. 8. The plant eggs. Southwest. Entomol. 8:61-64. bugs of the prairie provinces of Canada (Heteroptera: Miridae). Pub. 1703. Debolt, J.W. 1981. Laboratory biology Can. Govt. Pub. Centre, Ottawa. and rearing of Leiophron unif ormls

(Gahan) (Hymenoptera : Braconidae) , a Khattat, A.R., and R.K. Stewart. 1977. parasite of Lygus spp. (Hemiptera: Development and survival of Lygus Miridae) . Ann. Entomol. Soc. Amer. lineolaris exposed to different 74:334-337. laboratory rearing conditions. Ann. Entomol. Soc. Amer. 70:274-278. Debolt, J.W. 1982. Meridic diet for rearing successive generations of Lygus Knutson, L., J.R. Coulson, and J.J. hesperus. Ann. Entomol. Soc. Amer. Drea. 1982. Facilities currently 75:119-122. acting as quarantine receiving centers for exotic beneficial organisms in the Doutt, R.L. 1959. The biology of United States. In Information on ARS parasitic Hymenoptera. Ann. Rev. Biological Control Programs by Use of Entomol. 4:161-182. Natural Enemies, Document No. 00061, pp. 19-22. Insect Ident. and Beneficial Drea, J.J., Jr., L. Dureseau, and Insect Introduct. Inst., Beltsville, Md. E. Rivet. 1973. Biology of Peristenus stygicus from Turkey, a potential Landes, D.A., and F.E. Strong. 1965. natural enemy of Lygus bugs in North Feeding and nutrition of Lygus hesperus America. Environ. Entomol. 2:278-280. (Hemiptera: Miridae). I. Survival of bugs fed on artificial diets. Ann. Hormchan, P. 1977. Biology of three Entomol. Soc. Amer. 58:306-309. exotic species, and role of native species of the genus Peristenus - Leigh, T.F. 1963. Life history of parasites of tarnished plant bug, Lygus Lygus hesperus (Hemiptera: Miridae) in the laboratory. Ann. Entomol. Soc. lineolaris , in Mississippi. Ph.D. Amer. 56:865-867. Dissertation, Miss. State Univ. , 74 pp.

Isenhour, D.J., and K.V. Yeargan. Loan, C.C. 1965. Life cycle and 1981. Effect of temperature on the development of Leiphron pallipes Curtis development of Orius insidiosus , with (Hymenoptera: Braconidae, Euphorinae) in notes on laboratory rearing. Ann. five mirid hosts in the Belleville Entomol. Soc. Amer. 74:114-116. district. Proc. Entomol. Soc. Ontario 95:115-121. Jackson, C.G., and H.M. Graham. 1983. Parasitism of four species of Lygus Loan, C.C., and C.H. Craig. 1976. (Hemiptera: Miridae) by Anaphes Euphorine parasitism of Lygus spp. in ovi jentatus (Hymenoptera: Mymaridae) and alfalfa in western Canada (Hymenoptera: an evaluation of other possible hosts. Braconidae; Heteroptera: Miridae). Ann. Entomol. Soc. Amer. 76:772-775. Naturaliste Can. 103:497-500.

Jones, W.A., Jr., J.E. Powell, and Mueller, A.J., and V.M. Stern. 1973. E.G. King, Jr. 1985. Stoneville Effects of temperature on the Research Quarantine Facility: A regional reproductive rate, maturation, longevity and national center for support of and survival of Lygus hesperus and L. research on biological control of elisus (Hemiptera: Miridae). Ann. arthropod and weed pests. Bui. Entomol. Entomol. Soc. Amer. 66:593-597. Soc. Amer. 31(2):20-26.

92 :

Parrott, W.L., J.N. Jenkins, Wheeler, A.G. , Jr. 1976. Lygus bugs as F.G. Maxwell, and M.L. Bostick. 1975. facultative predators. In Scott, D.R., Improved techniques for rearing the and L.E. O’Keeffe, eds. , Lygus Bug: Host tarnished plant bug, Lygus lineolaris Plant Interactions. Univ. Idaho Press, (Palisot de Beauvois) . Miss. Agr. and Moscow. Forestry Expt. Sta. Tech. Bui. 72, 8 pp.

Porter, B.J. 1979. Host selection in Peristenus stygicus Loan (Hymenoptera Braconidae); an approach to the evaluation of host range for parasitoids. M.S. Thesis, Tex. A&M

Univ. , 55 pp.

Ridgway, R.L., and G. Gyrisco. 1960. Effect of temperature on the rate of development of the Lygus lineolaris

(Hemiptera: Miridae) . Ann. Entomol. Soc. Amer. 53:691-694.

Stoner, A., and D.E. Surber. 1969. Notes on the biology and rearing of

Anaphes ovi jentatus , a new parasite of Lygus hesperus in Arizona. Jour. Econ. Entomol. 62:501-502.

Stoner, A., and D.E. Surber. 1971.

Development of Anaphes ovi jentatus , an egg parasite of Lygus hesperus in relation to temperature. Jour. Econ. Entomol. 64:1566-1567.

Strong, F.E., and E. Kruitwagen. 1969. Feeding and nutrition of Lygus hesperus . III. Limited growth and development on a meridic diet. Ann. Entomol. Soc. Amer. 62:148-155.

Strong, F.E., and J.A. Sheldahl. 1970. The influence of temperature on longevity and fecundity in the bug Lygus hesperus (Hemiptera: Miridae). Ann. Entomol. Soc. Amer. 63:1509-1515.

Vanderzant, E.S. 1967. Rearing Lygus bugs on artificial diets. Jour. Econ. Entomol. 60:813-816.

Van Steenwyk, R.A., and V.M. Stern. 1976. The biology of Peristenus stygicus (Hymenoptera: Braconidae), a newly imported parasite of lygus bugs. Environ. Entomol. 5:931-934.

93 .

emerged SUMMARY AND RECOMMENDATIONS from adults of L. lineolaris , L.

elisus , and L. hesperus from alfalfa and By H.M. Grahami^ weeds, but the levels of parasitization are low. Nematodes have been found infesting L. lineolaris in a few instances, and some Lygus spp. have been This publication was prepared by members reported killed by fungi. of a Coordinating Subgroup on Biological Control of Lygus and Other Mirids that Efforts to establish parasites of Lygus was established in 1980 under the USDA, spp. from Europe in North America have been ARS , Working Group on Natural Enemies. unsuccessful. Most of the efforts Its purpose is to review, update, and have involved the braconid Peristenus consolidate information on the pest stygicus Loan, and although parasitized status, general biology, taxonomy, and nymphs were recovered after parasite efforts toward the biological control of releases, the parasites failed to become two genera of mirids, Lygus and permanently established. Smaller

.P . Adelphocoris , in North America. The releases of digoneutis Loan and Lygus spp. —mainly L. lineolaris rubricollis (Thomson) were unsuccessful (Palisot) in the East and L. hesperus also. Likewise, releases of ]?. Knight in the West—are indigenous pests adelphocoridis Loan against Adelphocoris of a wide variety of seed, fruit, lineolatus have not resulted in parasite vegetable, fiber, and forage crops, establishment causing significant economic losses by direct damage, costs of control measures, Explorations in southern Asia failed to and indirect effects of pesticide yield any parasites of Lygus spp. other applications on nontarget organisms, than an egg parasite with a broad host especially entomophagous arthropods and range. A study in Egypt revealed a pollinators. Adelphocoris lineolatus species of Telenomus (family Scelionidae)

(Goeze) , an introduced species, is mainly parasitizing high percentages of eggs of a pest of alfalfa in the Northern United Taylorilygus pallidulus (Blanchard) on States and Canada. Matricaria chamomilla L. None of these parasites were imported. Indigenous parasites attacking Lygus spp. include the mymarid Anaphes ovi jentatus Surveys in South Africa in 1981 found two

(Crosby and Leonard) , which attacks the egg parasites, Chaetostricha spp. (family eggs in a variety of habitats, with Trichogrammatidae) and Telenomus spp. rather high levels of parasitism in some (family Scelionidae ) , and two nymphal instances. Three indigenous species of parasites, Peristenus nigricarpus braconids attack Lygus spp. nymphs. (Szepligeti) and JP. praetor (Nixon)

Peristenus pallipes (Curtis) is reported (family Braconidae) , attacking the mirid from Lygus lineolaris (also Lygidolon laevigatum Reuter on Acacia

A. lineolatus ) on alfalfa and weeds, .P. mearnsii De Wild, in Natal Province. The pseudopall ipes Loan from L. lineolaris on nymphal parasites were shipped to the

Erigeron spp. , and Leiophron unif ormis Stoneville, Miss., quarantine facility,

(Gahan) from L. lineolaris , L. hesperus , but only three survived shipment, and and L. elisus Van Duzee on various crops these failed to reproduce. Additional and weeds. Levels of parasitism by the collections and shipments of these braconids are generally low, but high braconids were made in 1982, and two levels may be reached in some instances. generations of P. praetor and one of _P. Tachinids of the genus Alophorella nigricarpus were produced on Lygus lineolaris in quarantine, but no sustained culture was obtained. Collections were made in Kenya in 1983, ^/Biological Control of Insects and nymphal parasites of Taylorilygus Laboratory, Agricultural Research spp. were obtained. Eight adult Service, U.S. Department of Agriculture, P. nigricarpus and an undescribed 2000 East Allen Road, Tucson, AZ 85719.

94 . .

Leiophron sp. were recovered in The research should be expanded to quarantine. Two generations of _P. include other important mirid species. nigricarpus were reared on Lygus The cotton fleahopper, Pseudatomoscelis hesperus , but no sustained culture was seriatus (Reuter) , is a possible obtained. In late 1985, a shipment of candidate. Besides basic information on the undescribed Leiophron sp. and the ecology and biological control of the _P. nigricarpus was received at Stoneville pest, exploration for exotic natural from the Commonwealth Institute of enemies attacking related genera might be Biological Control in Kenya and is being started reared successfully on L. hesperus and L. lineolaris .

The research to date on the biological control of Lygus spp. and Adelphocoris lineolatus has not yielded successful systems for suppressing populations of the pests, but it has produced a vast amount of basic information on the hosts and natural enemies that is needed for the development of such systems. Future research must build on this information until successful systems can be devised. In the area of classical biological control, the successful culturing of the unidentified Leiophron sp. from Kenya in Lygus hesperus and L. lineolaris provides another species of parasite that might fit into our agricultural systems, but a great deal of basic research must be done before its potential can be determined. Some other areas of the world remain to be explored for other parasites that might have potential for use in North America. These include northeastern Asia, U.S.S.R., and Latin America. Efforts should be made to initiate these explorations. Efforts to use European parasites against A. lineolatus , an introduced species from Europe, should be continued

Research directed toward the development of inoculative or augmentative release of parasites against Lygus spp. in certain situations should continue. A rearing system for L. hesperus based on an artificial diet has made rearing the host and its parasites much more reliable. However, improvements need to be made, especially for rearing the parasites, and the system should be enlarged. A great deal of information on the behavior and biologies of the parasites is needed so that methods can be developed to use them effectively against the pests. When these procedures are accomplished, their feasibility must be tested.

95