Russian An introduced of small grains in the High Plains

A brief history of the invasion Russian wheat pre- The , Diuraphis noxia fer to feed in rolled leaves on (Mordvilko), is native to the steppe country of southern the upper parts of the plant Russia. It was first detected in North America near (Figure 4). Greenbugs typi- Mexico City in 1980 and was discovered near Lubbock, cally are found on the under- Texas, in March 1986. By sides of lower leaves and do the fall of that year, infesta- not cause leaf rolling. Damage Figure 4. Leaf unrolled to tions were reported in New to wheat plants is noticeable expose Russian wheat aphids Mexico, Oklahoma, Colorado, from a distance. Besides rolled Nebraska, Wyoming and leaves and trapped heads, Kansas. Russian wheat aphid feeding causes purple or white longi- The aphids spread rapidly tudinal streaking on the leaves throughout wheat-produc- (Figure 5). Leaves damaged ing regions of the western by greenbugs turn brown and United States and proved appear scorched. When search- to be well adapted to the ing for the Russian wheat arid conditions of the High aphid in wheat, it is often use- Plains. Following introduc- Figure 1. ful to look for damage first tion, the Russian wheat aphid then for the aphids. Figure 5. Purpling caused hundreds of millions of dollars in wheat and and rolling of leaves production losses through reduced yields and Biology and life history pesticide treatment costs. Annual direct yield losses The Russian wheat aphid reproduces asexually. All peaked at $274 million in 1988 but dropped to less than aphids are female, and each gives birth to live daugh- $10 million by 1993. Russian wheat aphid still appears ters carrying embryonic granddaughters. This telescop- periodically across the High Plains in southwestern ing of generations, combined with rapid, asexual repro- Wyoming, southeastern Nebraska, eastern Colorado duction is the key to the explosive population growth and New Mexico, western Kansas and the panhandles achieved by many aphid species. of Oklahoma and Texas (Figure 1). In Asia, the Russian wheat aphid may produce a Description and damage sexual generation in the fall, with mated females laying The Russian wheat aphid is a small, lime-green eggs that overwinter. Although sexual females have aphid with a distinctive football-shaped body been found in North America, males have not, and it (Figure 2). The legs, antennae and cornicles are short appears that the aphid population reproduces without compared to most other sexuality. This inability to produce overwintering eggs aphids. Viewed from may have limited the northern range of the Russian the side, the terminal wheat aphid in North America. The aphid is more cold segment of the abdo- tolerant than greenbugs, however, and easily survives men has a supracaudal Kansas winters. structure that looks Russian wheat aphid nymphs are relatively sed- like a double tail. The entary and gregarious on the plant, forming dense greenbug is similar in Figure 2. Russian wheat aphid colonies. As colonies increase in size, the aphids benefit color (Figure 3), but the from feeding as a group, developing and reproducing dark green stripe, long at higher rates and reducing their individual risk of antennae and cornicles, attack by natural enemies.There are four or five molts which are often longer from first instar to reproductive adult. Maturation than the body, make requires from nine to 55 days depending on tempera- it easy to distinguish ture. Low temperatures delay development and repro- from the Russian wheat duction, but temperatures above 25 ºC (77 ºF) cause aphid. Figure 3. Greenbug mortality. Each wingless adult can produce as many

Kansas State University Agricultural Experiment Station and Cooperative Extension Service 1 five or six nymphs per day in warm weather, or only In Kansas, the most critical period for Russian wheat one every 10 or 20 days when temperatures approach aphid survival is during the summer between wheat freezing. harvest and wheat emergence. Cool- or warm-sea- Unlike most aphids, the Russian wheat aphid feeds son grasses that remain alive during the summer are on wheat until the plant is mature and can often be important for Russian wheat aphid survival during this found in developing heads. When the wheat plant period. According to studies in Colorado, Canada wild dries down as it matures or in response to heavy aphid rye, Elymus canadensis (L.), and crested wheat grass, feeding, an increased proportion of the immature Agropyron cristatum (L.) are two of the most important aphids develop wings that look like shoulder pads on summer hosts for the Russian wheat aphid. Prolonged third and fourth instar nymphs. drought can force grasses to die or go dormant, reduc- ing the chances of the pest surviving the summer. These winged, or alate, adults differ in biology and appearance from their apterous (wingless) sisters. They Neglected volunteer wheat can be just as impor- may feed for several days on the plant where they were tant to Russian wheat aphid survival as the presence born, but they do not begin reproducing. Rather, they of wild hosts. Some years immigration from infested soon respond to sunlight by flying and may be carried crops a long distance away also has a considerable on wind currents for long distances. Their function is to effect. Fields do not have to be close to alternate hosts seek a suitable host plant and initiate a new colony. to become infested. When descending from the sky, the Russian wheat Resistant varieties aphid responds only to the green or yellow-green Various genetic sources of resistance to Russian color of young plants and the contrast with dark back- wheat aphids were identified in the late 1980s, and two grounds. Consequently, infestations often begin along were eventually incorporated into commercial wheat field borders where the contrast between young plants varieties. One source developed by K-State is available and bare soil is greatest. In natural plant communities, in the variety Stanton (derived from PI 220350 contain- an alate aphid must probe and sample many plants ing the resistance gene designated Dny). The other, before finding a suitable one, but host location is hardly developed by scientists in Colorado, is in the varieties a problem for Russian wheat aphids that light on a Halt, Yumar, Prowers and Prairie Red (derived from PI wheat field. With significant wing muscles and fat bod- 372129 containing the resistance gene Dn4). ies that store energy for flight, alate aphids have small K-State research shows that resistant varieties dra- reproductive organs and produce few daughters. The matically reduce the reproductive rate and nymphal daughters invariably develop into wingless adults survival of Russian wheat aphid. The effect of natural accelerating colony growth in the second generation. enemies is usually greater on aphid colonies feeding The Russian wheat aphid is capable of modifying on resistant plants than on susceptible ones. Resistance growth of the host plant. Longitudinal leaf rolling screening typically is performed in a greenhouse using allows high density colonies to form in a protected heavy aphid infestations without natural enemies, so location, somewhat like the galls formed by other varieties demonstrating resistance under these condi- aphids. Rolled leaves may create a favorable micro- tions perform well in the field where biological control climate for the aphid colony, buffering it from tem- lends a helping hand. perature extremes and reducing the risk of desiccation There was concern that breeding for plant resis- when relative humidity is low. In addition, many larger tance might make the aphids less suitable as food for aphid predators and parasitoids that attack Russian natural enemies, but it actually can enhance biological wheat aphids are less likely to encounter them in rolled control. Russian wheat aphids and greenbugs grown leaves or less inclined to forage in such close quarters. on resistant varieties are as nutritious and acceptable Aphids hidden in rolled leaves are better protected for predators as those grown on susceptible varieties. from contact insecticides even if they are susceptible to In fact, the aphids may be stressed in various ways by them. Consequently, materials with systemic activity the resistant plant, making them more vulnerable to are superior for Russian wheat aphid control. natural enemies. For example, significant numbers of Host plants aphids are dislodged from plants by foraging preda- A variety of wild grasses can serve as host plants tors, and some die. The aphids feeding on resistant for the Russian wheat aphid and may be important for plants may be smaller, weaker and less likely to return aphid survival when cereal crops such as wheat and to the plant once dislodged. Because resistant varieties barley are not available. In order to persist in a region, exhibit less leaf rolling when infested, the aphid colony Russian wheat aphid must have host plants year is more exposed to natural enemies and abiotic sources round. Cool-season grasses important for this of mortality. include wheat grasses, bromegrasses, wild ryes and Biological control jointed goatgrass. Jointed goatgrass is exceptionally Faced with astronomical aphid populations and suitable because of its close relationship with wheat. declining wheat production in the late 1980s, the U.S. Although reproduction tends to be lower on warm-sea- Department of Agriculture mounted an unprecedented, son hosts such as grama grasses and pearl millet, they far-reaching program to explore the ancestral range of can serve as potential hosts. 2 the Russian wheat aphid and find natural enemies. At Natural enemies of the Russian wheat aphid least 120 scientists from 20 countries participated in the program, which imported more than 12 million benefi- cial of at least 24 species. These insects were cul- tured, mass produced and released at numerous sites in 16 states for about five years. The majority of these insects were already represented in the United States by similar, locally adapted native species. Of the introduced insects, one species of parasitic wasp, albipodus, has conclusively established, Figure 9. Hover fly Figure 10. Scymnus beetle but its effect on Russian wheat aphid is limited to a small portion of the aphid’s current range. On the other hand, the number of native predators and parasitoids capable of preying on and parasitizing Russian wheat aphids have gradually increased, and some have extended their range to coincide with regions now infested by the Russian wheat aphid. Two factors have contributed to the gradual, area- wide decline of Russian wheat aphid: the development Figure 11. Scymnus beetle Figure 12. Aphelinid wasp larva among aphids and distribution of resistant varieties in the most seri- (Aphelinus spp.) ously affected regions, and gradual increases in the populations of native natural enemies. Because of the an ideal foraging environment because their own risk failure of the classical program against this aphid and of predation and parasitism is reduced. Several of these the potential non-target effects of introduced biologi- are shown above. Clockwise, from left they include cal control agents, it is generally agreed that massive, small hover flies (Diptera: Syrphidae) (Figure 9). Small indiscriminate introduction of exotic species should ladybeetle species in the genus Scymnus have larvae not be the first response in the event of an invasion of with distinctive waxy filaments and can also be found another aphid pest of small grains. feeding in Russian wheat aphid colonies (Figures 10 and 11). The introduced parasitic wasp Aphelinus albipodus Natural enemies (: ) and other native Aphelinus Predators and parasitoids that attack other grain spp. are small and stealthy and forage effectively in aphids also feed on the Russian wheat aphid, but rolled leaves (Figure 12). not all are effective at reaching them in rolled leaves. Various entomopathogenic fungi can cause diseases Exclusion cage studies in western Kansas indicate in Russian wheat aphids, but most require substan- that the convergent lady beetle, tial humidity to be effective, which makes them a less Hippodamia convergens Figure 6 ( ), likely cause of death in arid regions where the aphid is also the key predator of green- most prevalent. bug in the region, is one of the most important natural controls. Evolution of the Russian wheat aphid The seven-spotted lady beetle, In spring of 2003, outbreaks of Russian wheat aphid Coccinella sepempuncata, is com- in commercial wheat fields of Prairie Red were discov- mon in wheat fields in early spring ered in several counties in eastern Colorado. This led to Figure 6. Convergent and may play a role in reducing suspicions that a new genetic strain, or biotype, of this lady beetle Russian wheat aphid numbers. aphid had evolved with the ability to overcome resis- Similarly, Aphidiid wasps, includ- tance in these varieties. ing the greenbug parasitoid Lysiphlebus testaceipes (Figure 7) also attacks and This is not surprising because many greenbug develops on the Russian wheat biotypes have evolved over the years and overcome aphid. various sources of wheat and sorghum resistance. Extensive acreages have been planted to Russian wheat Wasps in the genus Praon aphid-resistant varieties in the worst affected areas belong to the same family but over the past decade, and this could have generated form dis- strong selection pressure that favored aphids with Figure 7. Aphidiid wasp tinctive resistance-breaking mutations. mummies with a pedestal-like structure It is surprising, however, that two separate and (Figure 8). Other smaller predators supposedly distinct sources of resistance should be and parasitoids that normally have overcome in a single evolutionary event. Although no little effect on greenbug popula- genetic changes have yet been characterized in aphid tions have found Russian wheat Figure 8. Mummified clones established from the Colorado infestations, aphid colonies in rolled leaves are aphid (Praon sp.) bioassays performed at K-State have measured 3 improved performance on resistant varieties. In fact, Deciding when to treat for Russian wheat aphids is this new "biotype 2" Russian wheat aphid appears based on economic thresholds. The economic threshold more virulent to virtually all commercial wheat variet- is where the damage from the aphid equals the cost ies grown in Kansas than the original biotype 1, and of control.The economic threshold during the jointing the progresson of damage symptoms is far more rapid, stage can be estimated using the formula: especially between 65° and 75°F. Often a resistant variety is more productive than ET = (CC × 200) ÷ (EY × MV) susceptible alternatives when under pest pressure, but ET = economic threshold or the percent of tillers less productive in its absence. Similarly, the altered that needs to be infested to justify treatment genetics that enable an insect to overcome a particular CC = control cost per acre source of plant resistance may not perform as well on EY = expected yield per acre other varieties. This may explain why many regions MV = market value per bushel sampled in eastern Colorado in 2004 were found to contain both aphid biotypes. Laboratory tests have If populations are below the threshold, then the shown that biotype 2 performs better on varieties damage that the aphids are expected to cause will not expressing resistance to biotype 1 than on related vari- exceed the treatment cost and treatment is not needed. eties that lack the resistance gene. Cultivars bred for After the flowering stage, substitute 500 for the 200 in resistance to biotype 1 have not been widely grown in the numerator of the formula. Note, after heading it Kansas because they often do not yield as well as in the takes even higher levels of Russian wheat aphid to jus- absence of significant Russian wheat aphid pressure. tify control. More tests are underway to study the diversity For information on pesticides labeled for Russian of Russian wheat aphid populations. There may be wheat aphid control, check the current version of the several biotypes of this aphid in the United States. K-State Research and Extension publication MF-745, Preliminary results from Kansas tests show that the Wheat Insect Management Guide. old biotype seems predominant at the locations tested. However, biotype 2 could be present in counties near Photo credits the Colorado border based on its predominance in Figure 1: Elliott, N.C., Hein, G.L., Carter, M.R., Burd, reports from eastern Colorado during 2004. J.D., Holtzer, T.O., Armstrong, J.S., and Waits, D.A. These changes are a reminder that insect popula- 1998. Russian wheat aphid (Homoptera: ) tions are dynamic and can change over time. Growers ecology and modelling in Great Plains agricultural should select wheat varieties adapted to their area and landscapes, pp 31-64. In S. S. Quisenberry and F. B. use resistant varieties where insect pressure warrants. Peairs [eds.], Response Model for an Introduced Pest They also must remain alert for Russian wheat aphid - The Russian wheat aphid. Fig. 1, p. 33. Thomas populations that adapt to damage-resistant varieties. Say Publications, Entomological Society of America, Lanham, Maryland. Russian wheat aphid management Figures 2 and 3: Frank Peairs, Colorado State University When natural enemies and host-plant resistance fail, producers must rely on insecticides to limit aphid dam- Figures 4 and 5: Phil Sloderbeck, Kansas State University age. Two insecticide options are currently available. Figures 6, 9 and 10: J. P. Michaud, Kansas State University One option is to use a seed treatment, which can pro- Figure 7: Texas A&M Extension Service vide early season protection but is only cost effective where there is a high probability of significant Russian Figure 8: Tom Fasulo at University of Florida wheat aphid activity. The other option is to use insecti- Figure 11: J. Castner, University of Florida cides to reduce aphid numbers after populations have Figure 12: Urs Wyss, Kiel University, Germany been detected in the field.

J. P. Michaud and Phillip E. Sloderbeck

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Kansas State University Agricultural Experiment Station and Cooperative Extension Service MF-2666 May 2005 K-State Research and Extension is an equal opportunity provider and employer. Issued in furtherance of Cooperative Extension Work, Acts of May 8 and June 30, 1914, as amended. Kansas State University, County Extension Councils, Extension Districts, and United States Department of Agriculture Cooperating, Fred A. Cholick, Director. 4