Natural Enemies of Russian Wheat Aphid Identified in California
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California cereal crops have suffered massive damage from Russian wheat aphid since 1988. Natural enemies of Russian wheat aphid 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 pest 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 aphids 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 barley 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 (Hymenoptera), Aphelinus 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.