Biology of barley shoot fly Delia flavibasis Stein (Diptera: Anthomyiidae) on resistant and susceptible barley cultivars

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The biology of barley shoot fly Delia flavibasis was studied using resistant (Dinsho and Harbu) and susceptible (Holker) barley cultivars at Sinana Agricultural Research Center, Ethiopia. A higher number of eggs was laid on Holker (17 eggs/female)
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  ORIGINAL PAPER Biology of barley shoot fly  Delia flavibasis  Stein (Diptera:Anthomyiidae) on resistant and susceptible barley cultivars Muluken Goftishu   Tadele Tefera   Emana Getu Received: 20 June 2007/Revised: 9 September 2008/Accepted: 24 September 2008/Published online: 31 October 2008   Springer-Verlag 2008 Abstract  The biology of barley shoot fly  Delia flavib-asis  was studied using resistant (Dinsho and Harbu) andsusceptible (Holker) barley cultivars at Sinana Agricul-tural Research Center, Ethiopia. A higher number of eggs was laid on Holker (17 eggs/female) than on Din-sho (11 eggs/female) or Harbu (12 eggs/female).However, there were no differences between cultivars inpreoviposition and total reproductive periods. Theshortest time required to complete larval, pupal and totaldevelopmental stages from egg to adult emergenceoccurred when the insect was reared on the cultivarHolker. Pupal weight, adult emergence and adult lon-gevity did not differ between cultivars. The female tomale sex ratio was 1:1. This study enabled us tounderstand the duration of each of the life stages of   D. flavibasis , which will undoubtedly aid researchers andgrowers to design a sustainable management strategyagainst barley shoot fly. Keywords  Barley    Delia flavibasis    Life cycle   Pest management    Resistant cultivar Introduction Two barley shoot fly species  Delia arambourgi  Seguy(Davidson 1969) and  D. flavibasis  Stein (Tafa 2003) areknown to occur in Ethiopia, inflicting considerable yieldlosses. Both species belong to the order Diptera and familyAnthomyiidae.  Delia flavibasis  has recently been recordedfrom Ethiopia (Tafa et al .  2004).  Delia flavibasis  isreported as a major pest of barley (  Horedum vulgare  L.) inEthiopia and Kenya (Macharia and Mueke 1986; Tafa2003). Infestation level of   D. flavibasis  in Bale highlands,Ethiopia, frequently reaches 100% on susceptible barleycultivars and causes considerable yield loss. Because of itsdevastating effect especially on malt barley, improvedcultivars and exotic germplasms, the pest has become amajor constraint to barley cultivation in the Bale highlandsof Ethiopia (Amare 1993; Tafa et al .  2004).Besides the main host barley, shoot fly survives onseveral alternative hosts in the grass family, like maize(  Zea mays ), wheat ( Triticum  spp.), blurish millet ( Pen-nisetum americanum ) and a few grasses (Hill 1987). Hostpreference study of   D. flavibasis  conducted at the SinanaAgricultural Research Center (SARC) with barley, teff,wheat, oat and maize revealed that barley and teff were themost preferred (SARC 2004).Studies conducted on this pest focused on managementaspects, viz., cultural, chemical, host plant resistance andthe resistance mechanisms (Thewodros 1982; Hussien et al . 1993; Berhane et al. 1996; Tafa 2003; SARC 2004). However, information on life cycle, nature of attack andover seasoning or diapausing, which are essential for Communicated by M. Traugott.M. Goftishu    T. TeferaDepartment of Plant Sciences, Haramaya University,P. O. Box 138, Dire Dawa, EthiopiaE. GetuDepartment of Biology, Addis Ababa University,P. O. Box 1176, Addis Ababa, Ethiopia Present Address: T. Tefera ( & )Division of Entomology, Department of Crop Science,Georg-August-University Goettingen, Grisebachstr. 6,37077 Go¨ttingen, Germanye-mail: tadeletefera@yahoo.com  1 3 J Pest Sci (2009) 82:67–71DOI 10.1007/s10340-008-0222-0  making decisions concerning  D. flavibasis , are lacking.Such information is imperative for developing a soundstrategy for shoot fly management. This study, therefore,reports on the fecundity and phenology of   D. flavibasis under laboratory and field conditions. Materials and methods FecundityThe fecundity of   D. flavibasis  was studied on a susceptiblebarley cultivar, Holker, and two relatively resistant culti-vars, Dinsho and Harbu (SARC 2004). The resistantcultivars were food barley developed by the SARC, Ethi-opia, from the Ethiopian barley landraces. Holkar is anintroduced improved malt barley cultivar and is susceptibleto the pest. Barley seedlings with dead hearts as a result of   D. flavibasis  infestation were collected from the field andkept in cages in the laboratory until the emergence of adultflies. A pair of newly emerged flies, 24 h old, were releasedinto individual cages (30 by 20 by 20 cm) having fivenewly emerged seedlings per cage of 1.1-growth stage (firstleaf unfolded) (Zadoks et al. 1974) for oviposition. Thecage had a plastic cover with a plastic mesh in the middleto allow air circulation. The cages were arranged in acompletely randomized block design with five replications.Adults were provided with diet prepared from glucose,brewers yeast and distilled water at the ratio of 4:7:10,respectively (Kasana and AliNiazee 1994). Cages wereexamined two times daily (in 12-h interval) to determinepreoviposition period, number of eggs per female and totalreproductive period. Data were recorded on days to ovi-position, total number of eggs per day and totalreproductive period. Eggs were removed at each time of data collection.Laboratory and field phenology of   D. flavibasisEgg stage The developmental period of   D. flavibasis  was studied onsusceptible barley cultivar, Holker, and two relativelyresistant cultivars, Dinsho and Harbu. For this study,freshly laid eggs, age less than 24 h, were collected fromthe field and transferred to individual seedlings in pots(25 cm in diameter) in the laboratory (21–23  C). Twelveseedlings of each of the three cultivars were raised in eachpot and thinned to ten before egg inoculation. Each seed-ling was inoculated with two eggs of   D. flavibasis  byplacing them at the base of each plant at 1.1-growth stage(Zadoks et al .  1974). This was done using sterile camel hairbrush (Delobel and Unnitahn 1983; Ortega et al. 1980). The pots were arranged in a completely randomized block design with four replications. A fluorescent lamp was hungabove the rearing pots and artificial light was supplementedfor 12 h daily during the experimental period. A total of 80eggs were used for each cultivar both in the laboratory andin the field. The same experiment was repeated in the field.In the field, the pots were housed in screen cage (41 by 50by 60 cm) made of wooden frame covered with whitemuslin cloth to protect from oviposition by the adult fly.Seedlings were examined four times at 4-h interval per dayto observe egg hatching. Data on the number of hoursrequired for hatching was recorded.  Larval stage After egg hatching, the duration of larval development wasassessed on the three barley cultivars in the pot experiment.A total of 56 and 52 larvae on each cultivar were used forthe laboratory and field experiments, respectively. Obser-vations were made four times daily at for hour interval untilprepupation commenced and the total number of days topupation recorded. Pupal stage To determine prepupal (last larval instar becomesinactive, stop feeding, leaves the seedling and burirsitself in the soil) and pupal developmental time, seed-lings of the three barley cultivars with dead heartshaving last larval instar of   D. flavibasis  were carefullyuprooted. The prepupae were placed in moistened soil ina 14 cm diameter Petri dish and kept at room tempera-ture in the laboratory (20–23  C) and in the screen cagein the field. The purpose of adding soil to petridisheswas to provide the pupae with suitable conditions similarto the natural habitat (Bullock  1965). A completelyrandomized block design with four replications was used.Observations were made on 48 and 40 pupae collectedfrom each cultivar both in the laboratory and in the field,respectively. Each petridish was examined four times perday at 4-h interval. Records were taken on prepupal andpupal developmental time and pupal weight. Pupae wereweighed using WA 80 analytical electronic balancehaving sensitivity of 80/0.0001 g. All pupae wereweighed and carefully returned to the respective Petridishes in the soil to determine adult emergence.  Adult stage To determine adult emergence period, pupae were col-lected from each Petri dish of each cultivar and kept inrearing cages (30 by 20 by 20 cm). A completely ran-domized block design with four replications was used. 68 J Pest Sci (2009) 82:67–71  1 3  Observations were made on 36 and 28 flies on each cultivarin the laboratory and in the field, respectively. Each cagewas examined four times daily at 4-h intervals until adultflies emerge. At emergence, adults were carefully removedusing siphon trap and were placed in another cage. Theflies were provided with diets prepared from glucose,brewers yeast and distilled water at the ratio of 4:7:10,respectively (Kasana and AliNiazee 1994). Data wererecorded on adult emergence and longevity period of adultflies.Statistical analysisData on the time required for preoviposion, total repro-duction, egg hatching, larval stage, pupal stage, adultemergence, longevity, total developmental time and pupalweight were subjected to analysis of variance (ANOVA).Number of eggs per female was transformed using squareroot (  ffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi  X þ 0 : 5 p   ) to stabilize the variance before beingsubjected to ANOVA. Whenever the  F   test was significant( P \ 0.05), least significant difference (LSD) was used formean separation. Data were analyzed using a general linearmodel (PROC GLM, SAS Institute 1999–2000). Results Fecundity of   D. flavibasis As observed in the laboratory and in the field, eggs maybe found laid singly or in groups. There were significantdifferences ( P \ 0.05) in number of eggs ovipositedbetween the barley cultivars. The highest number of eggs(17.9) was laid on the susceptible cultivar, Holker, andthe least on Harbu (12.3) and Dinsho (11.5) (Table 1).However, no significant differences were observedbetween cultivars in preovipostion and total reproductiveperiods. The egg of   D. flavibasis  is white and elongate-ovoid in shape, resembling grains of rice. It has longi-tudinal ridges or strips when observed under amicroscope.Phenology of   D. flavibasisEgg stage Significant difference ( P \ 0.05,  df   =  2,  F  value  =  5.79)was observed in the time needed for egg hatching betweenthe cultivars (Table 2) in the laboratory experiment. Ashorter time from egg to larval stage was required for thecultivar Holker than for Dinsho or Harbu.  Larval stage The number of days required for the development of larvaevaried significantly ( P \ 0.05,  df   =  2,  F  value  =  12.18)among cultivars (Table 2). Larvae required a shorter timeto reach the prepupal stage on the susceptible cultivar thanon the resistant cultivars under both laboratory and fieldcondition. Pupal stage The number of days required for prepupal and pupal stageson Holker was higher (2.26 days) than that on Harbu andDinsho under laboratory condition (Table 2). However, inthe field, significantly fewer days were required to reachthe pupal stage on Holker than on Harbu and Dinsho. Therewas no difference among cultivars in pupal weight underboth laboratory and field conditions. Puparia, formed of thehardened larval skin as a protective container for the pupae,were ovoid in shape. Newly formed pupae were lightbrown in color and slowly turned to dark brown with age.Pupation took place in the soil within 1–3 cm depthamongst the roots. Observation under field conditionsshowed that, in rare cases, pupation also took place insidethe basal stalk of barley. In the present study, no evidenceof diapause was obtained; all larvae and pupae, which werereared in the laboratory, completed their cycle withoutinterruption, which indicates that  D. flavibasis  did notdiapause at the immature stages.  Adult stage Adult emergence and longevity required 7–9 days andwere not affected by cultivars under either laboratory orfield conditions (Table 2). The total developmental period(from egg to adult 10 emergence) was significantly( P \ 0.05,  df   =  2,  F  value  =  14.43) shorter on the suscep-tible cultivar compared to the resistant cultivars in thelaboratory and field. Table 1  Mean  ?  SE number of eggs, preovipositon period and totalreproductive period of   Delia flavibasis  on three barley varieties in thelaboratoryVariety Number of eggs/femalePreovipositionperiod (days)Total reproductiveperiod (days)Dinsho 11.50  ±  2.33b 3.53  ±  0.24 5.03  ±  0.20Harbu 12.33  ±  2.78b 3.50  ±  0.22 5.02  ±  0.24Holker 17.90  ±  2.62a 3.50  ±  0.31 5.35  ±  0.22LSD 4.42 NS NSMeans within a column followed by the same letter are not significantat  P \ 0.05  NS   not siginificantJ Pest Sci (2009) 82:67–71 69  1 3  Discussion Thepresentstudydemonstratedtheeffectofbarleycultivarson  D. flavibasis  fecundity and phenology. The susceptiblecultivar,Holker,ispreferredforovipositionthanDinshoandHarbu. Tafa (2003) reported a similar trend in the egghatching time of   D. flavibasis  on different barley cultivarsinoculated with eggs of   D. flavibasis  under laboratory con-ditions. He found significant differences between thesusceptible(60.00 h)andresistant(78.00 h)barleycultivarsfor the time required for egg hatching. Previous studiesconducted on  D. arambourgi  (Bullock  1965) and  D. platura (Hill 1987) indicated 72–96 h for egg hatching. Occasion-ally,  D. flavibasis  may oviposit on the undersurface of olderleaves. Under normal conditions, young barley seedlings(two to three leaf stages) are most preferred for oviposition.However,oviposition canoccur ontillersof older plants andtheir leaves. On susceptible cultivars, which are recurrentlyinfested, oviposition lasts for a longer period. Preliminaryobservationmadeduringthefieldstudyrevealedthatmostof the adults trapped from barley seedlings and from newlyploughed lands are females. The females visit these areasprobably to lay their eggs on barley seedlings and to createconducive environment for the larvae. We observed thatadult  D.flavibasis aremostactiveduringlatemorning(9:30–10:30 am)andlateafternoon(4:00–5:00 pm).Adultfliesareusually found on newly ploughed moist soil and newlyemerging seedlings during this time of the day.Generally, fewer numbers of eggs were laid by  D. flavibasis  in this study as compared to 100 eggs per femaleby  D. radicum  (Hill 1987) and about 238 eggs per femaleby  A. soccata  (Sileshi and Lakra 1994). This may reflectthe differences in oviposition potential among the dipteranspecies. Diet is also a relevant factor in variation inovipostion. According to Jones et al. (1992), lack of proteinat the adult stage is an important constraint to the repro-ductive success of many muscoid dipterans. McDonald andBorden (1996) found that elimination of protein from thediet of female  D. antiqua  often resulted in lower sexualattraction, reproductive competency and fecundity.The damaging stage of   D. flavibasis  is the larval stage.Infestation commenced with a mine in the first or secondleaf or both and the larvae make its way down through thetissues to the growing point. The attack results in death of the central shoot, producing dead heart. Following deadheart formation, the larvae may quit the shoots and minethrough the leaves of the seedlings. In the field, the minedleaves collapse at their weakened bases, lying flat on thesoil surface. Similar observations were reported byDavidson (1969) on  D. arambourgi . On the other hand,Bullock (1965) observed that this type of attack by  D.arambourgi  is only occasional in Kenya. The larvae of   D.arambourgi  bore directly into the central shoot afterclimbing above the first leaf sheath. Field observations inthe current study revealed that most of the attacked seed-lings had both the first and second leaves mined. It wasobserved that, occasionally, a seedling may host more thanone larva and the larvae may leave a seedling and boreanother seedling in the vicinity. Davidson (1969) reportedsimilar observations for  D. arambourgi.  The variations innumber of days required for larval and pupal stages of   D. flavibasis  under both laboratory and field conditionsbetween the susceptible and resistant cultivars may beattributed to the existence of antibiosis in resistant culti-vars. Tafa (2003) reported antibiosis mechanism of resistance to  D. flavibasis  in different barley cultivars, viz.,PGRCE/E 1799, PGRCE/E 4414, PGRCE/E 4409,PGRCE/E 4282 and Arusso to a lesser degree. Table 2  Developmental time of   Delia flavibasis  and adult longevity on three barley varieties (mean  ?  SE) in the laboratory and fieldVariety Egg hatching(h)Larval stage(days)Prepupalstage (days)Pupal stage(days)PupalweightAdultemergence(days)Adultlongevity(days)Total time(egg–adultemergence)Laboratory experimentDinsho 74.45  ±  4.12a 13.14  ±  1.81a 1.68  ±  0.21b 13.81  ±  1.52a 3.20  ±  0.31 8.81  ±  1.25 8.61  ±  2.01 40.54  ±  4.01aHarbu 77.59  ±  6.04a 12.60  ±  1.52a 1.61  ±  0.32b 13.58  ±  1.81a 3.15  ±  0.29 8.54  ±  1.48 8.54  ±  1.80 39.56  ±  3.42aHolker 68.40  ±  3.01b 11.35  ±  1.05b 2.26  ±  0.55a 11.94  ±  1.03b 3.48  ±  0.34 8.41  ±  1.23 8.90  ±  2.30 36.81  ±  2.81bLSD 6.72 0.91 0.30 0.56 NS NS NS 2.06Field experimentDinsho 72.43  ±  3.52 13.24  ±  1.04a 1.65  ±  0.30 13.99  ±  2.03a 3.06  ±  0.42 7.86  ±  0.46 7.37  ±  1.48 39.67  ±  3.32aHarbu 75.81  ±  5.21 13.20  ±  1.92a 1.79  ±  0.41 13.60  ±  1.82a 3.20  ±  0.23 7.83  ±  0.23 7.54  ±  1.50 39.62  ±  3.04aHolker 77.74  ±  5.00 12.35  ±  0.42b 1.82  ±  0.34 11.50  ±  0.81b 3.50  ±  0.27 7.30  ±  0.51 8.10  ±  2.00 36.21  ±  2.40bLSD NS 0.74 NS 0.63 NS NS NS 2.83Means within a column followed by the same letter are not significant at  P \ 0.05  NS   not significant70 J Pest Sci (2009) 82:67–71  1 3  The shortest time required to complete developmentalstages from egg to adult on the susceptible cultivar, Holker,indicates the suitability of the cultivar to the shoot fly.However, owing to its high demand by malt industries inEthiopia, Holker fetches high prices and farmers prefer tocultivate Holker than the other cultivars. Therefore, thiscultivar needs to be protected against shoot fly infestation.It has been reported that one principal component of shootfly management is adjustment of sowing dates (SARC2004). In the region, farmers very often sow barley in thebegging of June. The present study indicates that, onegeneration requires about 36 days on the susceptible cul-tivar, Holker. Hence, delayed sowing might have cropgrowth stages coinciding with high population levels and,consequently, infestation might increase. In spite of somedegree of infestation by shoot fly, early sown barley cul-tivars recovered from shoot fly damage and gave relativelybetter yield by fully exploiting the available moisture(SARC 2004).The present study indicates that, after egg hatching, thelarvae feed on the barley shoot for 11–13 days, causing adead heart, before they enter into the soil for pupation.Application of insecticides, if feasible, therefore, shouldfocus on the early larval stages. The insecticides, carbo-furan, aldicarb, cyfluthrin and deltamethrin are reported tobe effective against the shoot fly (Thewodros 1982; Hus-sien et al. 1993). Information on the life cycle of barleyshoot fly as determined in the current study will aidresearchers and growers in designing a sustainable man-agement strategy against this pest. References Amare A (1993) Infestation and damage level of barley shoot fly(  Delia arambourgi ) at Sinana. In: Proceedings of the JointConference of the Ethiopian Phytopathological Committee andthe Committee of Ethiopian Entomologists, Addis Ababa,Ethiopia, 5–6 March 1992. Crop Protection Society of Ethiopia(CPSE), Addis Ababa, p 28Berhane L, Hailu G, Fekadu A (1996) Barley production andresearch. In: Gebre H, van Leur (eds) Barley research inEthiopia: past work and future prospects. Proceedings of the firstbarley research review workshop, Addis Ababa, Ethiopia, 16–19October 1993. Institute of Agricultural Research (IAR), AddisAbaba, Ethiopia/International Center for Agricultural Researchin Dry Areas (ICARDA), Aleppo, Syria, pp 1–8Bullock JA (1965) The control of   Hylemya arambourgi  Seguy(Diptera: Anthomyiidae) on barley. Bull Entomol Res 55:645–661Davidson A (1969) Effect of some systemic insecticides on aninfestation of the barley fly  Delia arambourgi  in Ethiopia. EastAfr Agric For J 34:422–425Delobel AGL, Unnitahn GC (1983) Effects of constant temperatureon the charactersitcs of populations of   Atherigona soccata Rondani (Diptera: Muscidae). Acta Oecol Oecol Appl 4:351–368Hill DS (1987) Agricultural insect pests of temperate regions andtheir control. Cambridge University Press, Cambridge, 659 ppHussien MLA, Melde C, Wetzel T (1993) Investigations on theeffects of seed treatment of winter wheat with Decis (delta-methrin), Filitox (metamidophos) and Baythroid (cyfluthrin)against larvae of the wheat bulb fly (  Delia coarctata  Fall).J Phytopathol Plant Prot 28:147–154Jones CJ, Milne DE, Patterson RS, Schreiber ET, Milio JA (1992)Nectar feeding by  Stomoxys calcitrans  (Diptera: Muscidae)effect on reproduction and survival. Environ Entomol 21:141–147Kasana A, AliNiazee MT (1994) Effect of constant temperature ondevelopment of the walnut hsuk fly,  Rahgoletis completa .Entomol Exp Appl 73:247–254Macharia M, Mueke JM (1986) Resistance of barley varieties tobarley fly  Delia flavibasis  Stein (Diptera: Anthomyiidae). InsectSci Appl 7:75–77McDonald RS, Borden JH (1996) Dietery constraints on sexualactivity, mating success, and survivorship of male Delia antiqua.Entomol Exp Appl 81:243–250Ortega A, Vasal SK, Mihn J, Hershey C (1980) Breeding plantsresistance to insects. Wiley, Chichester, 683 ppSAS Institute (1999–2000) PROC GLM. SAS Institute, Cary, NC, 50ppSileshi G, Lakra RK (1994) Off-season survival of the sorghum shootfly  Atherigona soccata  Rondani (Muscidae: Diptera) in Alemayaregion of Ethiopia. Afr Crop Sci J 7:97–104Sinana Agricultural Research Center (SARC) (2004) Entomologyprogress report ,  1996–2004. Sinana Agricultural ResearchCenter, Robe, BaleTafa J (2003) Mechanism(s) of resistance in barley accessions toshoot fly ,  Delia flavibasis  Stein (Diptera: Anthomyiidae). MScthesis, School of Graduate Studies of Alemaya University, 73 ppTafa J, Tadesse G, Sakhuja PK (2004) Ovipositional antixenosis insome barely accessions to barely shoot fly. Pest Manag J Ethiop8:51–57Thewodros M (1982) Studies on the sorghum shoot fly,  Atherigona varia var.  soccata  Rondani (Diptera: Muscidae) with specialreference to its biology and control measures. MSc thesis, AddisAbaba University, 88 ppZadoks JC, Chang TT, Konzak CF (1974) A decimal code for thegrowth stages of cereals. Weed Res 14:415–421J Pest Sci (2009) 82:67–71 71  1 3
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