Russian : natural enemies, resistant wheat offer potential control rz D. Gonzalez a Charles G. Summers o Calvin 0. Qualset u> 2 f Adult Russian wheat aphid.

wears. Coordinated research to de- and social costs or the concerns associated velop economically and environ- with COmba~gRwA tati ions with insecticides. At present, insecticides are management the only RWA control tactic available to strategies for this is in California farmers. Continued use of these progress. agents will destroy native natural enemies, accelerate dev~opm~tof insecticide re- In March 1986, Russian wheat aphid sistance in RWA and other pests, (RWA),Diuruphis noxiu (Mordvilko),was and upset se~ndarypests. The results, first reported present in the United States, short-term, are induced pest outbreaks. causing crop losses in small grains in The results, long-term, are cont~ation Texas. Since then, it has spread, infesting of soil and watert wildlife losses, and gen- View of aphid from above showing characteris- small grains in Oklahoma, Kansas, Ne- eral en~o~ent~degradation. Economi- tic short antennae, double tail, and very short braska and South Dakota and moving cdy, too, the extensive acreage planted cornicles (small tubelike projections on each west to California, Oregon and Washing- with small gains, depressed markets and side of the aphid). ton. Crop losses in 1988 were an estimated decreased prices make unilateral chemical $130 million, 2.4 times greater than in protection a poor option. 1987. Losses since 1986 have exceeded ~u~he~ore,~~ea~edsmall grains $500 million. nonnally host native natural enemiesf pro- Russian wheat aphid is a small, pale viding natural control of potential p~ma~ green insect, often covered with a white and second^ pests in their crops and in powdery coating of wax. It prefers to colo- adjacent crops. ~~~ncingb~olo~cd con- nize areas deep in the whorl or beneath trol of RWA wiB ~e insecticide USE the leaf sheath, but as aphid numbers in- and permit maximum impact from native crease, the entire plant may be colonized. natural enemies in cereais and associated A cool-season aphid, it causes damage agroecosystems. from late fall through spring. While feed- After a 3-year exploration for RWA ing, RWA injects into the plant a toxic sa- natural enemies in Central Asia, D. liva that destroys chlorophyll, resulting in GonzAlez and others documented that white or cream-colored streaks on stems RWA has not been a pest on small grains. and leaves. The toxin also causes leaves to In these areas the aphid has been associ- twist and curl like a soda straw. ated with cereals for more than 50 years. In California, wheat and are ap- In the 3 years of exploration several poten- parently the most susceptible crops, fol- tially effective species (or biotypes) of lowed by rye and triticale. Oats also host natural enemies and many different poten- RWA, but suffer only marginal injury. The tially resistant wheat varieties have been RWA does not attack or injure corn, rice, identified from in and around Central or sorghum. It does, however, colonize Asia. These should be evaluated in the many native and introduced grasses. United States to advance biological controt The aphid first appeared in Imperial and host plant resistance of RWA. County in March 1988 and in Yolo County Our ongoing and proposed assessment the following May. It has since spread to of biological controI/hos~plant resis- all of California's major cereal-growing re- tance/chemical assessment (economic gions (fig. 1).Losses in California's cereal thresholds] are summarized here. The re- crops during the 1988-1989 growing sea- port reflects a summary of RWA research 9 son, including control costs, are estimated coordinated by UC researchers D. f at $8 million, according to the Great Plains Godezand C. G. Summers in biologicd Typical Russian wheat aphid damage showing Agricultural Council. Losses in rangeland control, C. G.Summers and C. 0. Qualset curled leaf and white streaking. grasses have not been determined. in host plant mistance, and C.G. Summers

32 ~ALIFORNIAAGRICULTURE, VOLUME 46, NUMBER 1 in the season and are rarely land valley, southern coastal valley, cen- inside curled leaves. There- tral inland valley and northern inland val- fore, effective biological con- ley. These represent the climatic zones in trol will require importing which most wheat is grown in California. new and exotic natural en- They also represent varied environmental emies from Central Asia, and climatic conditions under which the where natural enemies control impact against RWA of the same exotic this aphid. species and/or biotypes of natural en- Foreign exploration. Sci- emies can be assessed. entists in State Agricultural Experiment Stations (SAES), Migration and flight activity USDA-AgnculturalResearch With the aid of a statewide network of Service (ARS), and the USDA- suction traps (fig. l), UC scientists are and Plant Health In- studying migration and flight activity of spection Service (APHIS) co- RWA. These studies are part of a larger operated in 1988-1991 to migration study being conducted through- import and establish natural out the aphid’s range. A pattern of migra- enemies of RWA in the tion and movement of winged is United States. Foreign explo- emerging that will help determine ration has resulted in importa- whether planting dates can be manipu- tion and culture of more than lated within the constraints of field access, 124 source populations of wheat maturity and crop rotation to avoid natural enemies, including or escape these dispersal flights and thus parasites and predators. These prevent infestation when the crop is im- foreign explorations also pro- mature and most susceptible. While too duced information on (1) the few data have been collected to describe a frequent occurrence (in several locations in predictable pattern of aphid movement, a Fig. 1. Current distribution of Russian wheat several countries) in or near Central Asia small flight apparently occurs in fall and a aphid in California and location of suction of several parasite species routinely associ- much larger flight during spring (fig. 2). traps. ated with low densities of RWA, (2) effec- Occasionally, small flights occur in mid- tive parasitization of RWA under a wide winter. Planting so that cereals do not in migration and economic thresholds. range of climatic conditions, and (3) para- emerge until after the fall flight but mature Our studies are based on observations and sitization of RWA inside curled leaves. to at least flowering before the spring reports on RWA in fields in and around This information, plus experience with the flight may enable growers to avoid much Central Asia as well as on previous experi- imported natural enemies, causes us to be- of the wheat injury caused by RWA. Plant- ences in alfalfa with spotted alfalfa aphid lieve that five of the exotic parasites merit ing trials that encompass dates from Octo- and blue alfalfa aphid. Both alfalfa pests further study: D. rapae, asyckis, ber through February are underway at the initially caused extensive damage in al- Aphelinus varipes, Aphidius colemani and Kearney Agricultural Center and West falfa throughout the western United Apkidius matricarae. Side Field Station to obtain empirical data States, but the combination of biological Introduction of exotic parasites. The on aphid numbers and veld response as control and host plant resistance reduced five species of RWA parasites noted have they relate to time of planting and infesta- both pests to little economic siwcance. been released, in collaboration with tion. USDA-APHIS, in selective fields in Biological control California’s Imperial, Riverside, Santa Bar- Economic thresholds In California, biological control efforts bara, Fresno, Sacramento, and Yolo coun- Short-term, chemical intervention of- against RWA include a preliminary assess- ties, with the assistance of local farm advi- fers the most effective and immediate con- ment of native natural enemies attacking sors. Sites for release were selected on the trol of RWA. Development of economic RWA before introduction of exotic en- basis of variations in different habitats and thresholds for RWA is underway at the emies; foreign exploration to determine climatic patterns in the following growth Kearney Agricultural Center as part of a the type and extent of mortality factors as- zones: southern low desert, southern in- cooperative Western Regional project. sociated with RWA outside the United 500 - These thresholds will be dynamic and re- States, where this species has existed in flect the plant growth stage (age) at initial 450 - --,-Westside - Fresno Co. low numbers for a long time, and prelimi- 13- Chico - Butte Co. infestation and the degree of aphid dam- 400 - + Davis - Yolo Co. nary selective introduction of five exotic 2 350- + Lancaster - Lo9 Angeles Co. age (number of tillers infested) and aphid parasite species. 300- density. Preliminary data show that aphid Surveys for native natural enemies. $ 250- infestations on young plants can result in Indigenous primary parasites attacking 2 200 - extensive plant mortality and that plants RWA in the United States include 150- are susceptible to injury and yield loss as Lysiphlebus testaceipes, Diaeretiella rapae and 100 late as head emergence (table 1). Apkelinus varipes. Several species of 50 Russian wheat aphid is susceptible to coccinellid and dipterous predators also 0 of the common insecticides used for Jan Feb Mar Apr May Jun JuI Aug Sep Oct all attack RWA and other aphids-on small Sample date aphid control in small grains; there are no grains. However, the extant aphid natural Fig. 2. Flight pattern of Russian wheat aphid known cases of aphid resistance. The enemy species in the United States do not representing the high desert (L.A. Co.), San aphid is, however, difficult to control be- effectively control RWA. In California, na- Joaquin Valley (Fresno Co.), Sacramento Val- cause of its ability to roll leaves into a tive natural enemies are associated with ley (Yolo Co.) and Northern Sacramento Valley tubelike structure that insecticides cannot only moderate to high RWA numbers late (Butte Co). penetrate. Therefore, treatment decisions

CALIFORNIA AGRICULTURE, JANUARY-FEBRUARY 1992 33 should be made before injury reaches this sidered resistant. Those ranking 4 to 6 tension personnel in those areas and from stage. Some control may be obtained after showed some streaking and chlorosis (yel- published reports, we believe that RWA in this stage if the weather is warm and the lowing) and were regarded as intermedi- California can be managed effectively. insecticide chosen has some vapor or sys- ate in response. Plants rated 7 to 9 exhib- Considering the wide range of habitats temic action. Insecticide treatments at ited extensive chlorosis and streaking, and climatic conditions that RWA occu- planting are not recommended because were often near death, and were consid- pies in westem North America (from cen- there are no procedures available to pre- ered susceptible. Emphasis was placed on tral Mexico to Canada and particularly dict whether a field is infected with RWA. wheat and triticale because these two California),we propose several strategies Likewise, such treatments will not last sources, if resistant, can be used directly in to reduce its economic impact. For ex- long enough to provide protection developing resistant wheat varieties for ample, several combinations of host plant throughout the period for potential injury. California,but the tests also included bar- varieties and natural enemy species and/ Growers should contact their local farm ley and rye. or biotypes will be needed to effectively advisor for information on economic Two UC Davis primary octoploid triti- reduce RWA numbers in different envi- thresholds as they develop and proper cales (CI81 and CI82), developed in a ronments. Our future plans include assess- choice of insecticides. breeding program at Davis in the 1970s ing the effectiveness of introduced biologi- and found to be resistant in Oklahoma, cal control agents, host plant resistance, Host plant resistance also were resistant at the Kearney Agricul- and economic threshold information and The development of host plant resis- tural Center (2.0 and 2.5 scores, respec- resources. Ultimately, integration of this tance offers the most economical and least tively). The third triticale, CI87, was inter- information will result in a workable plan environmentally disruptive strategy for mediate in score (5.5) and probably is not for managing RWA in field situations. managing RWA in California. Combined useful for breeding. First, however, we need detailed evalua- with biological control provided by preda- A group of 99 durum wheat breeding tions of available natural enemy and plant tors and parasites already described, these lines from UC Davis and from ICARDA species and/or biotypes to select optimal strategies could largely eliminate the need did not show useful resistance. However, species, insect and plant races or biotypes for chemical intervention. Evaluations of in a group of 103 Iranian bread , 9 for the different California wheat growth RWA resistance under California field scored 2 and 27 scored 3; thus, more than areas. We will continue to screen available conditions have been made with wheat 25% of that group were worthy of more material for genetic resistance. When and triticale germplasm from UC Davis, testing. Previously, workers in South Af- found, these entries will be distributed to International Maize and Wheat Improve- rica and at several U.S. sites found that others and used to enhance RWA resis- ment Center (CIMMYT Mexico), Interna- some wheats from West Asia have good tance in California wheats. Russian wheat tional Center for Agricultural Research in resistance to RWA. California and aphid resistance will be combined with re- the Dry Areas (ICARDA Syria), and Iran. CIMMYT common wheat breeding lines sistance to Septoria tritici blotch, barley yel- Material has been employed from breed- and varieties uniformly were susceptible, low dwarf virus, stripe rust and leaf rust ing programs in Oklahoma, Colorado and with average scores of 7.65 and 7.66, re- so that California wheat production will the USDA National Small Grains Collec- spectively. This confirms the need for in- be protected against major pests and tion at Aberdeen, Idaho. Communication troducing resistance genes into California pathogens with minimal use of pesticides. with workers in Colorado, Idaho, Oregon wheats. Meanwhile, hexaploid triticale va- Resistance to RWA should be introduced and Oklahoma has been maintained to rieties adapted to California conditions ap- into barley as well. In biological coittrol a avoid duplication of efforts. peared to be damaged less by RWA search will continue for the most effective Materials were tested at the Kearney (means score of 5.3 for 23 included in the RWA natural enemy biotype and/or spe- Agricultural Center in Parlier. Entries test) than currently available common cies. We will concentrate in the Tian Shan were hand-planted in mid-December, with wheat varieties (mean score of 7.11, and and Kunloon mountain valleys of China, each entry replicated twice. Beginning in could be considered for production in ar- where for more than 20 years RWA has early February, plants were infested eas where RWA infestation is anticipated been known to occur infrequently. When weekly with greenhouse-reared RWA. In- to be heavy or for forage uses of cereal RWA are present, numbers are low and festations continued until plants began grains until effective resistance is devel- are always associated with the presence of flowering. Following flowering, plants oped. several natural enemies. were rated visually for their reaction to A breeding program to introduce host RWA on a 1-to-9 scale. Plants rated 1 to 3 plant resistance genes from nonadapted D. Gonzrilez is Entomologist, UC Riverside; C. showed little or no injury and were con- wheats to California varieties was initiated G. Summers is Associate Entomologist, UC in 1990. For 15 crosses, pollen from two re- Berkeley (located at Kearney Agricultural Cen- sistant accessions was taken directly from ter), and C. 0. Qualset is Professor, Agronomy the test plot at KAC to greenhouse-grown and Range Science, UC Davis. plants at Davis. PI94460 (score 2.0) and The authors acknowledge funding for por- PI294994 (score 2.0) were used as resistant tions of this research from the California Wheat sources. Six additional crosses involved Commission, the California Crop Improvement PI137739 and PI94355 as resistant sources. Association, the UCIPM Project, USDA- Fl's have been backcrossed to California APHIS,USDA-ARS, and USDA-CSRS Spe- breeding lines and varieties and grown in cial Grant No. 90-34205-5174. The authors the summer nursery in 1991. Hybrid seeds wish to thank A. Newton, H. Vogt, C. Wick, S. were shared with CIMMYT-Mexico where Scardaci, W. Johnson,P. Mauk, R. Coviello,A. Fl's were grown in 1990-1991. Fulton, W.Bentley, W. Chaney, S. Orloff, W. Bendixen, E. Natwick, R. Deerberg, L. Wendel Summary (USDA-APHIS),R. Leon-Lopez (INIFAP),as Based on personal observations in and well as 1. Zhang, G. Zhang and R. Wang of the around Central Asia, unpublished infor- People's Republic of China for assistance with mation from farmers, researchers and ex- many aspects of this research.

34 CALIFORNIA AGRICULTURE, VOLUME 46, NUMBER 1