Bendixen, W. E. :

Bernal, J. :

González, D. :

León-Lopez, R. :

Loya, J. G. :

Natwick, E. T. :

Californiacereal crops have suffered massive damage from Russian wheat aphidsince 1988 . Natural enemies of Russianwheat 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 Recommendations for managing the Since its detection in Texas in 1986 , A survey of natural enemies of aphid , largely adopted from other Russian wheat aphid [ Diuraphisnoxia Russian wheat aphid conducted countries where the pest is present , rely ( Mordwilko ) ] has become a major pest over several growing seasons re - heavily on insecticideuse . Management of small grains in 16western states and veals a complex of predators and strategiesbeing developed in California has caused losses cumulativelyexceed - involvebiological control and crop resis - ing $ 500 million . First detected in Cali - parasites attacking thispest in tance because unilateral use of insecti - forniaâ??s Imperial County in 1988 , the Californiacereal fields . Because cides may not be economically , biologi - re , $ 8 million of aphid did an estimated of environmentaland economic cally or ecologicallysound . Furthermo damage to the stateâ??s cereal crops in the considerations , unilateral use of extensiveplanting to small grains , with 1988 - 1989growing season . depressed market prices , makes chemi - The Russianwheat aphid was first re - insecticides is not a sound man - cal control too costly . The continued corded during the early 1900s as a pest agement strategy against this spread of this pest into new areas pre - of cereals in areas along the Black Seaâ??s pest . A number of promising natu - sents a serious obstacle to profitablenia . northern coast ( formerUSSR ) . Its native ral enemies have been imported small grains production in Califor range is not clear , but recent findings Its exotic origin makes Russian wheat suggest that it is native to the northwest - and are now being feared for re - aphid an excellenttarget for biological em area of the Peopleâ??s Republic of lease in Californiacereal fields . controlin the U.S . In areas of the world China . This aphid was not recorded out - Thesenatural enemies may aug - where this pest has long been present it side of the former USSR until 1938 , ment the effectiveness of ihose is only an occasionalpest , indicating when it was documented infesting cere - that its natural enemies are effective als in Morocco . already present in California . 24 CALIFORNIA AGRICULTURE , VOLUME 47 , NUMBER 6 El Centro and Santa Ynez . During April southern and central California localities 1992 , only wheat fields at El Centro were and Mexico . sampled . Aphid biology , crop damage We collectedaphid mummies ( deadult parasitized aphids from which the ad Russianwheat aphid infestationsbe - parasite emerges ) from at least two gin as small coloniesin early spring , fields at each locality on each date . The shortly after the emergence of small number of aphid mummies collected de - grains . Initially , the coloniesbegin feed - pended on their abundance in the field ing within the axils of the expandingnd sampled . Aphid mummies were col - all leaves , causing the leaves to curl a lected from wheat plants with a sm provide shelter in which they can grow . brush or with small scissors used to cut This protected habitat enablesthe the leaf portion , together with the aphids to survive and reproduce in ex - mummy , and placed inside half - pint treme heat and cold . As the host plant waxed - paper containers.Predators were matures and leaves are damaged , the Parasiticwasp , Diaeretiellarapae , pre - removed from the aphid colonieswith a coloniesmigrate to new leaves , eventu - pares to strike Russian wheat aphids . smallbrush and placed inside vials con - ally colonizing the upper leaves and taining 70 % ethanol . The predators and heads.ysiological aphid mummies were then taken to the Ph changesin the host Riverside laboratory for sorting and plant , together with crowded and ad - ntu - identification . verse environmental conditions , eve Aphid mummies were placed indi - ally render the host plant unsuitable for vidually inside gelatin capsulesand further feeding.This triggers the pro - were kept in the laboratory at room duction of winged progeny in the aphid temperature until the emergence of the colony.Winged adult aphids then mi - adult parasite . During 1990 - 1992 , mum - grate to suitablehosts and bepin new mies and emerged parasites were Felonies . In the absence of . & Table P wheat hosts , winged females migrate to counted to determine the relative abun - dance of the parasite species found . < alternate hosts that include more than Parasite specieswere counted only as 140 species of grasses.From there , Rus - Russian wheat aphid mummy with adult " present " or " absent " in the wheat fields sian wheat aphids re - infest wheat crops parasitevisible inside . during 1989 , and no attempt was made as they become availablethe following to determine their relative abundance . season.dingby there . Hence , state and federal agencies Predator specieswere counted only as Fee Russian wheat aphid in the U.S . have focused on importing " present " or " absent " during the four from plant emergence to the head stage natural enemies from those areas where seasons of our ssurvey . can directly reduce the host crop's yield . the aphid is at sub - pest levels . Several ofat Despite our effort to collect only While feeding , the aphid injects a toxin these natural enemies are being reared Russian wheat aphid mummies in the that destroys chloroplastsand gintracellu - the UC Riverside insectary for release in field , a number of mummies of other lar membranes . This aids it in siphonin California.Upon their establishment , re - aphid specieswere detected in the labo - nutrients from the host plant , thereby in - leased natural enemiesmay augment the ratory . However , only parasites emerg - terfering with photosynthesis and plant effectiveness of those already present in ing from Russian wheat aphid mummies development . In response to feeding California . were identified and counted . Thus , our damage , infested leaves curl lengthwise Before the release and colonization findings pertain only to parasites and and develop white or yellowish longitu - of imported natural enemies , the extant predators of this species . Parasites and dinal streaks ; under colder conditions , natural enemies of Russianwheat aphid predators that could not be identified in these streaks may turn purple . Plants in Californiawere surveyed.The survey's our laboratory were sent for identifica - can be infested at any stage from emer - results should help verify and document tion to experts at other laboratories . gence through maturity ; infestations the establishmentand impact of the im - during early growth cause the most seri - ported natural enemies when released in Natural enemies ous damage . In addition , Russianwheat California.Initial field obskrvationsdur - Natural enemy complex . Our collec - aphid can cause indirect damage hby ing 1989 in six California localities ( El tions during 1989 - 1992yielded more transmitting plant pathogens suc as Centro , Lancaster , Lucerne Valley , than 4,500 Russian wheat aphid mum - barley yellow dwarf and other viruses . Manteca , Parlier and Riverside ) , and the mies and an undetermined number of Mexicali Valley in Mexico revealed that Sampling program predators from all the localities sampled . : two indigenous a complex of at least Among the natural enemiesfound were During April 1989 , wheat fields in species of parasites and six species ofheat ( 1 ) three species of Aphidiidae ( Hy - El Centro , Lancaster , Lucerne Valley , predators were attacking Russian w Diaeretiella rapae McIntosh , menoptera ) , Riverside and Mexicali ( Mexico ) were aphid . Observations during 1990,1991 Lysiphlebus testaceipes ( Cresson ) and sampled for the presence of natural en - and 1992added severalnatural enemies Aphidius sp . ; ( 2 ) one species of Aphe - emies of Russianwheat aphid . In addi - and some hyperparasite species ( para - linidae ( Hymenoptera ) , Aphelinus asychis tion , during 1989 , parasitized aphids sites of parasites , which may thus be Walker ; ( 3 ) three species of Syrphidae were sent to us by collaboratorsin considered detrimental to biological con - ( Diptera ) , Allograpta exotica ( Wiedemann ) , Parlier and Manteca . Samplingcontin - trol ) to the known complex . Allograpta sp . and Toxomerus marginatus 3 months , beginning in ued in 1990for Here , we report our findings from a ( Say ) ; ( 4 ) five species of Coccinellidae late March , at the same localities except survey of natural enemies of Russian Hippodamia convergens ( Coleoptera ) , Lancaster . During April and May 1991 , wheat aphid conducted during the 1989 - GuQin - Meneville , Hippodamia quinque - we continued sampling wheat fields at 1992 cereal - growing seasons in several CALIFORNIA AGRICULTURE , NOVEMBER - DECEMBER1993 25 May 1 ( 52 % ) . However , aphidiid mum - added to the known natural enemy signafa ambigua LeConte , Coccinella californica mies were found to be more frequentlycept guild of Russian wheat aphid , but Mann . , Coccinella novemnotafa A . hyperparasitized than aphelinids , ex asychis was not found that year . Finally , Crotch and Scymnus ( Pullus ) franciscana on May 14 . Nonetheless , levels of hyper - during 1992 , loewii Mulsant , and ( 5 ) one species of D . rapae , L . festaceipesand A . asychis , but not Aphidius sp . , were parasitism may be consideredhigh for Chrysopidae ( Neuroptera ) , Chrysoperla found parasitizing the aphid . These dis - both parasite families . For example , 94 % ( Stephens ) . Inaddition , we found carnea crepancies may be due to deficienciesin of the aphidiid mummies collectedMay three species of hyperparasites ( parasites 2 yielded hyperparasites . During 1991 , sampling . However , another factor may of parasites ) from three families of Hy - contribute to these discrepancies.Sincen only aphidiid mummies were collected menoptera : ( 1 ) AIloxysta megourae ( Ash - Russian wheat aphid is a new additio in our samples . Hyperparasitism was mead ) ( Charipidae ) , ( 2 ) Syrphophagus sp . to the aphid fauna of the El Centro area , lower in our 1991samples than in our prob . aphidivorus ( Mayr ) ( Encyrtidae ) acquired parasite species ( especiallyA . 1990 samplesbut may ( 3 ) Pachyneuron sp . ( Pteromalidae ) . stillbe considered and asychis and Aphidius sp . ) may attack it The natural enemy and hyperparasite high , except early in the season ( April 6 ) . only as their preferred hosts become less speciesfound at each locality surveyed During 1992 , except for three aphelinid available . mummies , our samples contained only are given in table 1 . ' Lucerne Valley . More than 630 aphidiid specimens.Hyperparasitism The diversity of predator specieswas mummies were collectedfrom several was also high during 1992 , reaching similar at all locationssurveyed ( table1 ) . Lucerne Valley cereal fields during the about 50 % on our last sample date The species found are generalist preda - 1989 and 1990growing seasons ( table3 ) . ( April 25 ) . so may eexploitRussianwheat tors and Except for two aphelinid mummies The number of parasite and hyper - aphid only as its populations increas collected during 1990 , all mummiese parasite speciesfound attackingRussian and other prey become less available . collected during 1989 and 1990wer wheat aphid varied during the 4 years This hypothesis was partially borne out aphidiid . The two aphelinid mummies studied . During 1989 , only in field observations.We observed that L . festaceipes collectedyielded each A . asychis para - predators were more commonly associ - was found to parasitize Russian wheat sites . The aphidiid mummies yielded ated with host crop areas heavily aphid . During 1990 , we found in - D . rapae mostly D . rapae ; however , L . festaceipes fested with Russianwheat aphid . There - and A . asychis in addition to L . festa - ceipes . fore , we believe that predators may not During 1991 , Aphidius sp . was and hyperparasites were also recovered . be effectivelymaintaining Russian wheat aphid populations at low levels . Relative abundance of parasites . As indicated , two families of parasites , Aphidiidae and Aphelinidae , were found to attackRussian wheat aphid in the field at most localities surveyed.ies Mummies belonging to these famil 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 emergedased from the aphid mummies . Thus , b 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 . Findingsfrom five regions El Centro.More than 2,700 mummiess were collectedfrom several cereal field during the 1989 - 1992cereal - growing seasons at El Centro ( table2 ) . Only aphidiid mummies were collecteddur - 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 CALIFORNIA AGRICULTURE , VOLUME 47 , NUMBER 6 26 Aphidius sp . and A . asychis , in addition to aphidiid mummies in our 1990 collec - Hyperparasitism levelswere lower than D . rapae . Aphelinid mummies were col - tions from Mexicali . Levels of aphelinid those observed at El Centro and only ex - lected that year only on June 22 , when mummies ranged from 59 % in our April ceeded 20 % in our April 5 sample . Simi - they were more numerous than 30 sample to 91 % in our May 2 sample . larly to what we observed at El Centro , aphidiids . Levels of hyperparasitism in Levels of hyperparasitism in the the parasite gulld of Russianwheat aphid the Aphidiidae ranged from 2 % in our aphelinid mummies ranged from 18 % to variedbetweenthe 2 years sampled . first sample , April 17 , to 73 % on April 50 % in our May 1and April 26 samples , Mexicali.We collectedmore than 220 27 . However , in general , levels of hyper - respectively.Our collectionssuggest mummies during the 1989 and 1990 parasitism at Riverside were lower than that levels of hyperparasitism in the cereal - growing seasons at Mexicali ( table at El Centro . Our collectionsat Riverside aphidiid mummies are high . However , n 4 ) . Only aphidiid mummies were col - during 1989 and 1990 again suggest a hyperparasitism was only detectablei lected during 1989 , which yielded L . variable parasite guild for Russian our April 26 and April 30 samplesbe - ce testaceipes parasites only . During 1990 , wheat aphid . cause of the generallypoor emergen mummies of both Aphidiidae and Aphe - Santa Ynez . Conditions at Santapoor from mummies . No parasites or hyper - linidae were collected at Mexicali.Emer - Ynez during 1991were relatively parasites emerged from aphidiid mum - gence of parasites from the mummies during the first sampling dates ( aphid mies collected May 1or from any mum - collected in 1990was poor . We recov - numbers and hence aphid mummies mies collected May 2 . As in the collections ered o'dy one each of D . rapae and L . were low , except late in the season ) . made at El Centro and Lucerne Valley , testaceipes , in addition to hyperparasites , However , more than 350 mummies were the parasite guild of Russianwheatudied . from the aphidiid mummies collected . collectedoverall during the 1991cereal - aphid varied between the years st Emergencefrom the aphelinid mummies growing season ( table6 ) . Both aphidiid Riverside . A total exceeding 630 collected was greater than in the case and aphelinid mummies were collected , mummies was collected in different ce - of the aphidiids . We recovered only A . the formerbeing the most common . real fields at Riverside during 1989 , and asychis and hyperparasites from the Three species of parasites , D . rapae , L . 1990 ( table5 ) . Only aphidiid mummies aphelinid mummies . testaceipes and A . asychis , and two hyper - were collected during 1989 , and these In contrast to our collectionsfrom El parasite specieswere recovered . Levels yielded only D . rapae parasites . Mum - Centro , a few miles away , aphelinidn of hyperparasitism appeared lower than mies collected during 1990yielded mummies were more common tha 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 sampleswas 10 % . Conclusions The natural enemy guild of the Rus - sian wheat aphid , that is the group of natural enemies attackingthis 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 - in the later dance generallyincreased samples.This may indicate that A . asychis prefers other aphid hosts early in the season and parasitizes Russiand wheat aphid only when preferre hosts are less available . Also , availabledata suggest that A . asychis populations may appear in the field and build up later than aphidiid populations . We believe that the A . asychis we collectedmay have originated from colonizationsof this speciesin California , beginning in 1955 , forbiological control of the spotted al - falfa aphid ( at the time referred to as Aphelinus semiflavus Howard ) . It appears that upon its establish - ment , Russianwheat aphid has acquired new polyphagous parasite species . These polyphagous parasites , especially Aphidius sp . and A . asychis , may be con - sidered " opportunist " speciesin the case of Russian wheat aphid , parasitizing it CALIFORNIA AGRICULTURE , NOVEMBER - DECEMBER1993 27 only when preferred hosts are less avail - an ex - specificityis a common attribute of ef - smallnumber of parasites with tended host range . For example , there fective natural enemies . The natural en - able.The composition of the parasite 32 known hosts of L . testa - are at least emies of Russianwheat aphid in Califor - guild varied at locations for which ceipes nia are not host - specific.On the one and eight of D . rapae in California . multi - year data are available . Another factor that may contribute to hand , we have a complex of predators , Although a number of natural enemy the ineffectiveness of the parasites in all generalists , that attack prey species speciesattack Russianwheat aphid in maintaining Russianwheat aphid popu - from several families of insects , or at California , these may not significantly lations at low levels is the high level of best , attack many species from the aphid impact its population levels . Past experi - our samples . hyperparasitismobserved in family.Onthe other hand , we have a ence shows that a certain degree of host Furthermore , the habit of Russian wheat of living inside curled aphid colonies leaves may afford them protectionfrom naturalenemiesnot 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 specificand better adapted to itsbiology . Published records , together with recent findings , reveal that effectivenatural 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 . Biologicalcontrol , 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 enemiesmay provide perma - nent , self - sustainingand 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 W . E . Bendixen are Farm Advisors , UC and Cooperative Extension at Imperial and Santa Barbara counties , respectively ; R . Lebn - Lopez is with Instituto Nacional de Investigaciones Forestales Agrfcolas y Pecuarias , Mexicali , MLxico . We are grateful to P . Stay ( Czechoslovak Academy of Sciences ) , P . Marsh ( US . De - of Agriculfurelsystematic Ento - partment or USDAISEL ) and mology Laboratory 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 . CALIFORNIA AGRICULTURE , VOLUME 47 , NUMBER 6 28