California cereal crops have suffered massive damage from Russian since 1988.

Natural enemies of identified in California

J. Bernal o D. Gonzalez o E.T. Natwick o J.G. Loya o R. Leon-Lopez o W. E. Bendixen

A survey of natural enemies of Since its detection in Texas in 1986, Recommendations for managing the Russian wheat aphid conducted Russian wheat aphid [Diuraphisnoxia aphid, largely adopted from other (Mordwilko)]has become a major countries where the pest is present, rely over several growing seasons re- of small grains in 16 western states and heavily on insecticide use. Management veals a complex of predators and has caused losses cumulatively exceed- strategies being developed in California parasites attacking this pest in ing $500 million. First detected in Cali- involve biological control and crop resis- California cereal fields. Because fornia’s Imperial County in 1988, the tance because unilateral use of insecti- aphid did an estimated $8 million of cides may not be economically, biologi- of environmental and economic damage to the state’s cereal crops in the cally or ecologically sound. Furthermore, considerations, unilateral use of 1988-1989 growing season. extensive planting to small grains, with insecticides is not a sound man- The Russian wheat aphid was first re- depressed market prices, makes chemi- agement strategy against this corded during the early 1900s as a pest cal control too costly. The continued of cereals in areas along the Black Sea’s spread of this pest into new areas pre- pest. A number of promising natu- northern coast (former USSR). Its native sents a serious obstacle to profitable ral enemies have been imported range is not clear, but recent findings small grains production in California. and are now being feared for re- suggest that it is native to the northwest- Its exotic origin makes Russian wheat lease in California cereal fields. em area of the People’s Republic of aphid an excellent target for biological China. This aphid was not recorded out- control in the U.S. In areas of the world These natural enemies may aug- side of the former USSR until 1938, where this pest has long been present it ment the effectiveness of ihose when it was documented infesting cere- is only an occasional pest, indicating already present in California. als in Morocco. that its natural enemies are effective

24 CALIFORNIA AGRICULTURE, VOLUME 47, NUMBER 6 southern and central California localities El Centro and Santa Ynez. During April and Mexico. 1992, only wheat fields at El Centro were sampled. Aphid biology, crop damage We collected aphid mummies (dead Russian wheat aphid infestations be- parasitized from which the adult gin as small colonies in early spring, parasite emerges) from at least two shortly after the emergence of small fields at each locality on each date. The grains. Initially, the colonies begin feed- number of aphid mummies collected de- ing within the axils of the expanding pended on their abundance in the field leaves, causing the leaves to curl and sampled. Aphid mummies were col- provide shelter in which they can grow. lected from wheat plants with a small This protected habitat enables the brush or with small scissors used to cut aphids to survive and reproduce in ex- the leaf portion, together with the treme heat and cold. As the host plant mummy, and placed inside half-pint waxed-paper containers. Predators were Parasitic wasp, Diaeretiellarapae, pre- matures and leaves are damaged, the pares to strike Russian wheat aphids. colonies migrate to new leaves, eventu- removed from the aphid colonies with a ally colonizing the upper leaves and small brush and placed inside vials con- heads. taining 70% ethanol. The predators and Physiological changes in the host aphid mummies were then taken to the plant, together with crowded and ad- Riverside laboratory for sorting and verse environmental conditions, eventu- identification. ally render the host plant unsuitable for Aphid mummies were placed indi- further feeding. This triggers the pro- vidually inside gelatin capsules and duction of winged progeny in the aphid were kept in the laboratory at room colony. Winged adult aphids then mi- temperature until the emergence of the grate to suitable hosts and bepin new adult parasite. During 1990-1992, mum- Felonies. In the absence of .&Table mies and emerged parasites were P wheat hosts, winged females migrate to counted to determine the relative abun- < alternate hosts that include more than dance of the parasite species found. Russian wheat aphid mummy with adult 140 species of grasses. From there, Rus- Parasite species were counted only as parasite visible inside. sian wheat aphids re-infest wheat crops "present" or "absent" in the wheat fields as they become available the following during 1989, and no attempt was made there. Hence, state and federal agencies season. to determine their relative abundance. in the U.S. have focused on importing Feeding by Russian wheat aphid Predator species were counted only as natural enemies from those areas where from plant emergence to the head stage "present" or "absent" during the four the aphid is at sub-pest levels. Several of can directly reduce the host crop's yield. seasons of our survey. these natural enemies are being reared at While feeding, the aphid injects a toxin Despite our efforts to collect only the UC Riverside insectary for release in that destroys chloroplasts and intracellu- Russian wheat aphid mummies in the California. Upon their establishment, re- lar membranes. This aids it in siphoning field, a number of mummies of other leased natural enemies may augment the nutrients from the host plant, thereby in- aphid species were detected in the labo- effectiveness of those already present in terfering with photosynthesis and plant ratory. However, only parasites emerg- California. development. In response to feeding ing from Russian wheat aphid mummies Before the release and colonization damage, infested leaves curl lengthwise were identified and counted. Thus, our of imported natural enemies, the extant and develop white or yellowish longitu- findings pertain only to parasites and natural enemies of Russian wheat aphid dinal streaks; under colder conditions, predators of this species. Parasites and in California were surveyed. The survey's these streaks may turn purple. Plants predators that could not be identified in results should help verify and document can be infested at any stage from emer- our laboratory were sent for identifica- the establishment and impact of the im- gence through maturity; infestations tion to experts at other laboratories. ported natural enemies when released in during early growth cause the most seri- California. Initial field obskrvations dur- ous damage. In addition, Russian wheat Natural enemies ing 1989 in six California localities (El aphid can cause indirect damage by Natural enemy complex. Our collec- Centro, Lancaster, Lucerne Valley, transmitting plant pathogens such as tions during 1989-1992 yielded more Manteca, Parlier and Riverside), and the yellow dwarf and other viruses. than 4,500 Russian wheat aphid mum- Mexicali Valley in Mexico revealed that mies and an undetermined number of a complex of at least two indigenous Sampling program predators from all the localities sampled. species of parasites and six species of During April 1989, wheat fields in Among the natural enemies found were: predators were attacking Russian wheat El Centro, Lancaster, Lucerne Valley, (1)three species of Aphidiidae (Hy- aphid. Observations during 1990,1991 Riverside and Mexicali (Mexico) were menoptera), Diaeretiella rapae McIntosh, and 1992 added several natural enemies sampled for the presence of natural en- Lysiphlebus testaceipes (Cresson) and and some hyperparasite species (para- emies of Russian wheat aphid. In addi- Aphidius sp.; (2) one species of Aphe- sites of parasites, which may thus be tion, during 1989, parasitized aphids linidae (), asychis considered detrimental to biological con- were sent to us by collaborators in Walker; (3) three species of Syrphidae trol) to the known complex. Parlier and Manteca. Sampling contin- (Diptera), Allograpta exotica (Wiedemann), Here, we report our findings from a ued in 1990 for 3 months, beginning in Allograpta sp. and Toxomerus marginatus survey of natural enemies of Russian late March, at the same localities except (Say); (4) five species of Coccinellidae wheat aphid conducted during the 1989- Lancaster. During April and May 1991, (Coleoptera), Hippodamia convergens 1992 cereal-growing seasons in several we continued sampling wheat fields at GuQin-Meneville, Hippodamia quinque-

CALIFORNIA AGRICULTURE, NOVEMBER-DECEMBER 1993 25 signafa ambigua LeConte, Coccinella May 1 (52%).However, aphidiid mum- added to the known natural enemy californica Mann., Coccinella novemnotafa mies were found to be more frequently guild of Russian wheat aphid, but A. franciscana Crotch and Scymnus (Pullus) hyperparasitized than aphelinids, except asychis was not found that year. Finally, loewii Mulsant, and (5) one species of on May 14. Nonetheless, levels of hyper- during 1992, D. rapae, L. festaceipes and Chrysopidae (Neuroptera), Chrysoperla parasitism may be considered high for A. asychis, but not Aphidius sp., were carnea (Stephens). In addition, we found both parasite families. For example, 94% found parasitizing the aphid. These dis- three species of hyperparasites (parasites of the aphidiid mummies collected May crepancies may be due to deficiencies in of parasites) from three families of Hy- 2 yielded hyperparasites. During 1991, sampling. However, another factor may menoptera: (1)AIloxysta megourae (Ash- only aphidiid mummies were collected contribute to these discrepancies. Since mead) (Charipidae), (2) Syrphophagus sp. in our samples. Hyperparasitism was Russian wheat aphid is a new addition prob. aphidivorus (Mayr) (Encyrtidae) lower in our 1991 samples than in our to the aphid fauna of the El Centro area, and (3) Pachyneuron sp. (Pteromalidae). 1990 samples but may still be considered acquired parasite species (especially A. The natural enemy and hyperparasite high, except early in the season (April 6). asychis and Aphidius sp.) may attack it species found at each locality surveyed During 1992, except for three aphelinid only as their preferred hosts become less are given in table 1. mummies, our samples contained only available. ' The diversity of predator species was aphidiid specimens. Hyperparasitism Lucerne Valley. More than 630 similar at all locations surveyed (table 1). was also high during 1992, reaching mummies were collected from several The species found are generalist preda- about 50% on our last sample date Lucerne Valley cereal fields during the tors and so may exploit Russian wheat (April 25). 1989 and 1990 growing seasons (table 3). aphid only as its populations increase The number of parasite and hyper- Except for two aphelinid mummies and other prey become less available. parasite species found attacking Russian collected during 1990, all mummies This hypothesis was partially borne out wheat aphid varied during the 4 years collected during 1989 and 1990 were in field observations. We observed that studied. During 1989, only L. festaceipes aphidiid. The two aphelinid mummies predators were more commonly associ- was found to parasitize Russian wheat collected yielded each A. asychis para- ated with host crop areas heavily in- aphid. During 1990, we found D. rapae sites. The aphidiid mummies yielded fested with Russian wheat aphid. There- and A. asychis in addition to L. festa- mostly D. rapae; however, L. festaceipes fore, we believe that predators may not ceipes. During 1991, Aphidius sp. was and hyperparasites were also recovered. be effectively maintaining Russian wheat aphid populations at low levels. Relative abundance of parasites. As indicated, two families of parasites, Aphidiidae and , were found to attack Russian wheat aphid in the field at most localities surveyed. Mummies belonging to these families can be distinguished before emergence of the adult parasite. Aphidiid parasites produce tan or light-brown mummies; aphelinid parasites produce black mum- mies. This difference in color was used to separate mummies from both families and was especially useful in determin- ing the parasite family to which the mummy belonged when no adults emerged or hyperparasites emerged from the aphid mummies. Thus, based on mummy counts, we were able to de- termine the relative abundance of both parasite families and the incidence of hyperparasitism in each of those families on Russian wheat aphid. Following, we summarize our findings at each locality surveyed. Findings from five regions El Centro. More than 2,700 mummies were collected from several cereal fields during the 1989-1992 cereal-growing seasons at El Centro (table 2). Only aphidiid mummies were collected dur- ing 1989. During 1990, both aphidiid and aphelinid mummies were collected; overall, aphidiid mummies were more abundant than aphelinid mummies. During 1990, aphidiid mummies ac- counted for more than 70% of the mum- mies collected on each date, except on

26 CALIFORNIA AGRICULTURE, VOLUME 47, NUMBER 6 Hyperparasitism levels were lower than aphidiid mummies in our 1990 collec- Aphidius sp. and A. asychis, in addition to those observed at El Centro and only ex- tions from Mexicali. Levels of aphelinid D. rapae. Aphelinid mummies were col- ceeded 20% in our April 5 sample. Simi- mummies ranged from 59% in our April lected that year only on June 22, when larly to what we observed at El Centro, 30 sample to 91% in our May 2 sample. they were more numerous than the parasite gulld of Russian wheat aphid Levels of hyperparasitism in the aphidiids. Levels of hyperparasitism in varied between the 2 years sampled. aphelinid mummies ranged from 18%to the Aphidiidae ranged from 2% in our Mexicali. We collected more than 220 50% in our May 1and April 26 samples, first sample, April 17, to 73% on April mummies during the 1989 and 1990 respectively. Our collections suggest 27. However, in general, levels of hyper- cereal-growing seasons at Mexicali (table that levels of hyperparasitism in the parasitism at Riverside were lower than 4). Only aphidiid mummies were col- aphidiid mummies are high. However, at El Centro. Our collections at Riverside lected during 1989, which yielded L. hyperparasitism was only detectable in during 1989 and 1990 again suggest a testaceipes parasites only. During 1990, our April 26 and April 30 samples be- variable parasite guild for Russian mummies of both Aphidiidae and Aphe- cause of the generally poor emergence wheat aphid. linidae were collected at Mexicali. Emer- from mummies. No parasites or hyper- Santa Ynez. Conditions at Santa gence of parasites from the mummies parasites emerged from aphidiid mum- Ynez during 1991 were relatively poor collected in 1990 was poor. We recov- mies collected May 1 or from any mum- during the first sampling dates (aphid ered o'dy one each of D. rapae and L. mies collected May 2. As in the collections numbers and hence aphid mummies testaceipes, in addition to hyperparasites, made at El Centro and Lucerne Valley, were low, except late in the season). from the aphidiid mummies collected. the parasite guild of Russian wheat However, more than 350 mummies were Emergence from the aphelinid mummies aphid varied between the years studied. collected overall during the 1991 cereal- collected was greater than in the case Riverside. A total exceeding 630 growing season (table 6). Both aphidiid of the aphidiids. We recovered only A. mummies was collected in different ce- and aphelinid mummies were collected, asychis and hyperparasites from the real fields at Riverside during 1989, and the former being the most common. aphelinid mummies. 1990 (table 5). Only aphidiid mummies Three species of parasites, D. rapae, L. In contrast to our collections from El were collected during 1989, and these testaceipes and A. asychis, and two hyper- Centro, a few miles away, aphelinid yielded only D. rapae parasites. Mum- parasite species were recovered. Levels mummies were more common than mies collected during 1990 yielded of hyperparasitism appeared lower than at other localities sampled. The number of parasites, or hyperparasites, emerging from the mummies collected at Santa Ynez, was exceptionally low. Overall, emergence of parasites and hyperpara- sites from our samples was 10%. Conclusions The natural enemy guild of the Rus- sian wheat aphid, that is the group of natural enemies attacking this pest, at the localities studied is comprised of at least four parasite and nine predator species (table 1).At all localities studied, D. rapae was the most common parasite, except at Mexicali, where A. asychis was more common. However, at localities where A. asychis was collected, its abun- dance generally increased in the later samples. This may indicate that A. asychis prefers other aphid hosts early in the season and parasitizes Russian wheat aphid only when preferred hosts are less available. Also, available data suggest that A. asychis populations may appear in the field and build up later than aphidiid populations. We believe that the A. asychis we collected may have originated from colonizations of this species in California, beginning in 1955, for biological control of the spotted al- falfa aphid (at the time referred to as Aphelinus semiflavus Howard). It appears that upon its establish- ment, Russian wheat aphid has acquired new polyphagous parasite species. These polyphagous parasites, especially Aphidius sp. and A. asychis, may be con- sidered "opportunist" species in the case of Russian wheat aphid, parasitizing it

CALIFORNIA AGRICULTURE, NOVEMBER-DECEMBER 1993 27 only when preferred hosts are less avail- specificity is a common attribute of ef- small number of parasites with an ex- able. The composition of the parasite fective natural enemies. The natural en- tended host range. For example, there guild varied at locations for which emies of Russian wheat aphid in Califor- are at least 32 known hosts of L. testa- multi-year data are available. nia are not host-specific. On the one ceipes and eight of D. rapae in California. Although a number of natural enemy hand, we have a complex of predators, Another factor that may contribute to species attack Russian wheat aphid in all generalists, that attack prey species the ineffectiveness of the parasites in California, these may not significantly from several families of , or at maintaining Russian wheat aphid popu- impact its population levels. Past experi- best, attack many species from the aphid lations at low levels is the high level of ence shows that a certain degree of host family. On the other hand, we have a hyperparasitism observed in our samples. Furthermore, the habit of Russian wheat aphid colonies of living inside curled leaves may afford them protection from natural enemies not adapted to searching in such concealed niches. The impact of the extant natural en- emies on Russian wheat aphid popula- tions may be augmented by introducing natural enemies more specific and better adapted to its biology. Published records, together with recent findings, reveal that effective natural enemies of this pest ex- ist where it has long been present at low levels. These areas should be explored, and the natural enemies of Russian wheat aphid found, imported to and colonized in California. Because of envi- ronmental and economic considerations, management of Russian wheat aphid in California should not rely mainly on us- ing insecticides. Biological control, coupled with plant resistance, may be a more judicious approach toward manag- ing this pest in California. Many natural enemies of Russian wheat aphid have been imported through university and federal efforts and are now being reared at insectaries in the western United States, including the insectary at Riverside. Imported natural enemies may provide perma- nent, self-sustaining and economical control of Russian wheat aphid in Cali- fornia and should be exploited.

J. Bernal, D. Gonzdez and J. G. Loya are Graduate Student, Entomologist and Visit- ing Researcher, respectively, Department of Entomology, UC Riverside; E. T. Natwick and W. E. Bendixen are Farm Advisors, UC Cooperative Extension at Imperial and Santa Barbara counties, respectively; R. Lebn-Lopez is with Instituto Nacional de Investigaciones Forestales Agrfcolas y Pecuarias, Mexicali, MLxico. Weare grateful to P. Stay (Czechoslovak Academy of Sciences), P. Marsh (US. De- partment of Agricul furelsystematic Ento- mology Laboratory or USDAISEL) and M. Schaufl(USDA1SEL) for assistance with parasite and hyperparasite identifications, K. S. Hagen (UC Berkeley)for assistance with Coccinellidae identifications and F. C. Thompson (USDAISEL)for assistance with identification of Syrphidae. M. L. Flint, C. Summers and J. R. Quezada assisted with collections from Manteca and Parlier.

28 CALIFORNIA AGRICULTURE, VOLUME 47, NUMBER 6