Acta Hortic. 1158. ISHS 2017. DOI 10.17660/ActaHortic.2017.1158.14 Proc. I International Symposium on Moringa Eds.: A.W. Ebert and M.C. Palada

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Diseases and pests of moringa: a mini review M.A.U.Mridha1,aandF.N.Barakah21Plant Production Department, College of Food and Agriculture Sciences, King Saud University, PO Box 2640,Riyadh 11451, Saudi Arabia; 2Soil Science Department, College of Food and Agriculture Sciences, King SaudUniversity,POBox2640,Riyadh11451,SaudiArabia.Abstract

The multipurpose uses of moringa – as medicinal plant, its antimicrobialactivities, being a source of nutrition for human food and animal feed and otherenvironmental, industrial uses – make this crop very important. Cultivation ofMoringa oleifera is spreading across theworld under different climatic conditionsthat may expose the plants to different pests and diseases. The present paperhighlightsthestatusofpestsanddiseasesofmoringa.Moringaplantssufferfromfruitrots,stemrots,rootrot,twigcanker,etc.Majorpestsincludepodfly,budworm,hairycaterpillars,redmites,etc.

Keywords:moringa,pests,diseases,reviewINTRODUCTIONMoringa (belonging to Moringaceae family) is a fast-growing, multipurpose treespecies.Thegenuscomprises13species(Mahmudetal.,2010).Thecropiswellknownforits variousmedicinal properties, antimicrobial activities, nutritional value as human foodandanimalfeedandotherenvironmental,industrialandgeneraluses(Adebayoetal.,2011;Anwaretal.,2007;Fahey,2005;Fakurazietal.,2008;Fuglie,1999a,b;Kumaretal.,2009;Paliwaletal.,2011;Mridha,2015)AbriefsummaryoftheusesofmoringacanalsobefoundinaCABIdatasheet,whichisavailableonline(http://www.cabi.org/isc/datasheet/34868).Moringa is also used for ecosystem services, such as erosion control, soilimprovement;ornamental,boundary/barrier/support,intercropping;pollutioncontrol,etc.(http://www.cabi.org/isc/datasheet/34868; Mridha, 2015). The plants serve as animalforage, biogas, fuel, domestic cleaning agent, blue dye, fencing, fertilizer, foliar nutrient,greenmanure,gum,honeyandsugarcanejuice-clarifier,medicine,bio-pesticide,pulp,rope,tannin,waterpurifier, etc.Variouspartsof thisplant suchas the leaves, roots, seed,bark,fruit, flowers and immature pods are used asmedicine againstmultiple human diseases.Thiscrop is thoughttobe indigenousto India. It isgrowingeitherasnativeor introducedplantinmorethan60differenttropicalandsubtropicalcountries(Robiansyahetal.,2014;Sharmaetal.,2011).Moringaisresistanttomostpestsanddiseases.Butdifferentminordiseasesandmanypestsarerecordedfromvariousmoringagrowingcountries.RootrotcausedbyDiplodiasp.,twig canker caused by Fusarium pallidoroseum, and fruit rot caused by Cochliobolushawaiiensisaresomeofthereporteddiseases(PatricioandPalada,2017;Carbungcoetal.,2017;Rajangametal.,2001).Differentfungiandpestsarealsoreportedtoaffectmoringa.Hencethequalityofmoringaproductsshouldbethoroughlymonitoredbeforereachingtheconsumertopreventhealthhazards.Withthisunderstanding,thepresentminireviewwasundertaken to raiseawarenessof the researchersandconsumers to avoidhealthhazards.Becauseofitsmultifarioususes,medicinalpropertiesaswellasenvironmentalimportance,thereisanurgentneedtoassessthestatusofpestsanddiseasesofmoringa.DISEASESOFMORINGAMoringa plants arewidely recognized as resistant plants against themost commonplantpathogenicpestsanddiseasesandmanyresearchersreportedthattheplantsusually aE-mail: mridha52@gmail.com

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donotsuffer fromanyseriousdisease indifferentregionsof theworld.Butundercertainconditionstheplantsmaysufferfromvariouspestsanddiseases.Recentlytheauthorofthepresentpaper reported several pathogenic fungi (Mridha andAl-Barakah, 2015) from theharvestedpodswhicharesoldonthemarketsoftheKingdomofSaudiArabia.Altogethersixdifferentspeciesof fungibelonging to fivegenerawere identified.The identified fungiareAspergillus niger van Tieghem, Aspergillus flavus Link, Alternaria alternata (Fr.) Keissl.,Fusarium oxysporum Schlecht. emend. Snyder Hansen, Macrophomina phaseolina (Tassi)Goid,andRhizopusstolonifera(Ehrenb.)Vuill.(Figure1).

Figure1.Fungiisolatedfrommoringapodscollectedfromdifferentmarkets.

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Mostof thereported fungiarerecognizedasplantpathogenic fungi,whilesomearesaprophytic fungi.This is the first recordof fungiassociatedwithpodsofmoringa. Inourstudy, we have recorded two species ofAspergillus whichmay be detrimental for humanhealth.There is no recordof fungi associatedwithmoringapods sold in themarkets andmeantforhumanconsumption.During an adaptability and horticultural trial with a large number of accessions ofmoringa in the Philippines, Patricio and Palada (2017) observed only stem rot disease.Fungal endophytes associated with leaves ofM. oleifera were isolated, characterized andidentifiedbyCarbungcoetal.(2017)fromthePhilippines.Theyisolatedatotalof24fungalmorphospecies. The identified genera of fungi were Fusarium, Xylaria, Pestalotiopsis,Aspergillus,Nigrospora,Stachybotrys,RhizoctoniaandMacrophomina.Mycobiota associatedwithmoringa on imported seedswere isolated and identifiedfrom Cuba by Martınez de la Parte et al. (2013). A total of 708 isolates belonging to47species of 26 generawere identified by them. They recordedFusarium,Aspergillus andChaetomium. Thesewere the predominant genera constituting 44.35% of all the isolatedfungi.Intheirstudyofstoredandfreshlyharvestedstembarksatroomtemperature,Senuetal.(2012)isolatedandcharacterizedthefungalcontaminantsassociatedwithdeterioratedmoringa.Theyobservedthepresenceoffungalpathogenscausingdeteriorationafter7daysof incubation.AspergillusnigerandAspergillus flavuswere identifiedbytheseresearchers.They recommended that thequality of herbal drugs be thoroughly checkedbeforeuse byhumanbeings.Zhaoetal.(2012)detectedanendophyticNigrosporaspeciesfromtherootsofmoringaforthefirsttime.Rajangam et al. (2001) reported that no major disease in India is affecting theeconomicsofthecrop.However,anewdiseasehasdevelopedintheMaharastraregion.Theyalsomentioned thatpods reachingmaturity showedextensive rot. Thedisease symptomsareobservedallover thesurfaceof thepods,moreconspicuouslyat thestigmaticend.Ongreenpods,ellipticalorelongatedsunkenspotswithreddishbrownraisedmarginscanbeobserved.Diseasedpodsshrinktothinnerdimensionsattheirstigmaticendsthanhealthyones. In advanced stages of disease development, the pods get rotten and dry upprematurely, leaving uneven raised spots over the surface. The causal organism wasidentifiedasDrechslerahawaiiensis.ThisdiseaseappearstobenewlyrecordedformoringainIndia.SeveralotherdiseasescausingminordamagetotreesgrowinginIndiaarereportedbya few researchers: a root rot caused byDiplodia sp. (Ramachandran et al., 1980), a newdisease of edible pods ofM. oleifera in Maharashtra caused by Drechslera [Cochliobolus]hawaiiensis,apreviouslyunreportedhost(KshirsagarandD’Souza,1989).Mandokhotetal.(1994)reportedanewdiseaseofM.oleifera inIndia.ThediseasewascausedbyFusariumpallidoroseumandwasreported forthefirst timeasthecausalagentof twigcankeronM.oleifera.The tree is thecollateralhostofLeveillula taurica, apowderymildewthatcausesseriousdamageinpapaya(CaricapapayaL.)nurseriesinsouthIndia,asreportedbyUllasaandRawal(1984).PESTSOFMORINGAWidespreadofoccurrenceandseveredefoliationofthecropwasnotedinM.oleiferagrowing in agricultural farms of the King Saud University, Saudi Arabia (personalobservationoftheauthor).RecordsofsomemajorandminorpestsofmoringainIndiacanbe found online at http://agridr.in/tnauEAgri/eagri50/ENTO331/lecture26/Moringa/004.html.Thedistributionandstatusofthepestsaswellasthecauseofdamageandtheirmanagementwerereported.ThereportedmajorpestsinIndiaarepodfly(Gitonadistigma),a serious pest of moringa in South India, bud worm (Noordamoringae), a major pest inSouthIndia,leafcaterpillar(Noordablitealis),aseriouspestofdrumsticktrees,especiallyinSouthIndia,hairycaterpillars(Eupterotemollifera,Pericalliaricini,MetanastriahyrtacaandStreblote (Taragama)siva), aredestructiveandare found in the Indiansubcontinent,barkborer (Indarbela tetraonis), long horn beetles (Batocera rubus) are widely distributed all

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overtheIndiansubcontinent.Among theminor pests, aphids (Aphisgossypii) is a polyphagous pest. Nymphs andadults suck vital sap from the twigs.As reproduction ismostlyparthenogenic, populationbuild-up is rapid. Other minor pests are scale insects (Ceroplastodes cajani), bud midge(Stictodiplosismoringae)andleafeatingweevils(Myllocerusspp.).Pests of moringa are also mentioned in another website (TNAU Agrictech, 2016).Theseare:budworm(Noordamoringae),podfly(Gitonadistigma),leafcaterpillar(Noordablitealis), bark caterpillar (Indarbela tetraonis) and hairy caterpillar (Eupterotemollifera)etc. PatricioandPalada(2017)observedredmites(Tetranyctrusurticia),defoliator, leaf-footed bug (Leptoglossus phyllospus) and whiteflies (Bermisia sp.) in the field during anadaptability and horticultural trial with a large number of moringa accessions in thePhilippines and mentioned that the insects cause little damage to the plants. Kant et al.(2017)conductedasurveyofinsectpestsindifferentpartsofM.oleiferaproductionfieldsinSamoaandreportedaminordamageofflowersonly.Theyalsoreportedaplanthopperandstemborercausingminordamagetotheplants.Sattietal.(2013)conductedpreliminarybio-ecologicalstudiesoftheleafcaterpillar(NoordablitealisWalker,Lepidoptera:Pyralidae)inSudan.Theyreportedasuddenoutbreakof unfamiliar caterpillar on M. oleifera that caused severe defoliation to the crop inKhartoumState, Sudan. The results of preliminary investigationson certainbio-ecologicalfeatureswereoutlined,besidestheresultsofsomebotanicalextractsincontrollingthepest.They also mentioned that more emphasis should be given to such an important pest toindicate its distribution range and possible means of eradication, or otherwise effectivemeans of pestmanagement, before it invades new areas in the country. Due to the wideexpansion ofmoringa cultivation in theworld, the pest continuouslywidened its area ofdistribution during the past few years. Caterpillars onmoringawere reported frommostcountries in Southeast Asia, the Middle East and the Arabian Peninsula. In Africa, it wasreported fromEthiopia,Kenya, Somalia, SouthAfrica,Namibia,Gambia,Niger,MadagascarandLaReunion.(Nair,1970;ButaniandVerma,1981;ButaniandVerma,1984;Gillett,1997;Demuelenaere,2001;Parrotta,2001;Anonymous,2012).YusufandYusif(2014)studiedtheleaffeedinglarvaerearedthroughtopupationandto adulthood in Bayero University, Kano State, Nigeria. The adults that emerged wereidentified to be Ulopeza phaeothoracica Hampson. With regard to larval feeding, it wasobserved that the damage caused by the larvaewas extreme on a heavily infested youngmoringatreeat thestudy location.TheyconcludedthatU.phaeothoracica isa leaf feedingpestofM.oleiferaand itsactivitycouldbeofseriousconcernespeciallyonyoungtreesofmoringa,keptunderpoormanagementconditions.Maheshetal.(2014)reportedforthefirsttimeofdrumstickpodfly(Gitonadistigma),apestofmoringainIndia,whichhasbecomeoneofthemostseriouspestsofthecropwithinfestation starting frompod initiation andpersisting till harvest, causing severe damage,especiallyunderpoormanagementconditions.Sahaetal.(2014)discussedtheimportanceofseveralpestsofmoringaandtheirmanagementinapopulararticle.Theydiscussedaboutbark-eatingcaterpillar(IndarbelaquadrinotataWlk.),moringabudworm(NoordamoringaeTams.),moringaleafcaterpillar(NoordablitealisWlk.),hairycaterpillar(EupterotemolliferaWlk.), black hairy caterpillar (Pericallia ricini Fabricius.), fruit fly (Gitona distigmata) andlonghornbeetles(BatocerarubusLinn.).Ojiako et al. (2012) conducted an experiment to determine the insect pests ofM.oleiferaLam.atdifferentstagesofgrowthinthenursery.TheinsectsidentifiedweremainlyZonocerus variegatus Linn. (variegated grasshopper), Musa domestica Linn. (house fly),Formica rufa Linn. (red wood ant), Lagria villosa Fabricus (leaf-eating beetle), Oedaleusnigeriensis Uvarov (Nigerian grasshopper) and Homorocoryphus nitidulus vicinus Walker(edibleor long-hornedgrasshopper).Their resultwas in agreementwith earlierworksofAkanbietal.(2007),whoreportedZ.variegatusasamajorpestofmostvegetablesgrowninsouthern Nigeria. In Puerto Rico, moringa is reportedly very susceptible to attack bytermitesandtheseedsareaffectedbyanunidentifiedinsect(Parrota,2009).

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Rajangam et al. (2001) reported that developing pods are damaged by the fruit flyGitona distigmata which can be effectively managed by adopting integrated pestmanagement(IPM)measures.ButaniandVerma(1981)reported28differentinsectspeciesandtwospeciesofmitesfromIndiaonvariouspartsofdrumsticktrees.Amongthem,majorinsect pests are bark-eating caterpillars (Indarbela quadrinotataWlk., Indarbela tetraonisMoore.),greenleafcaterpillar(NoordablitealisWlk.),budworm(N.moringaeTams.),hairycaterpillar (Euptero temoliferaWlk.),blackhairy caterpillar (Pericalliaricini Fab.), fruit fly(Gitonia distigmata Meigon.) and long horn beetles (Batocera rubus Linn.). Kareem et al.(1974) reported severe damage of moringa pods caused by a fly of the genus Gitona(Drosophilidae:Diptera). Pillai et al. (1979) identifiedHelopeltis antonii Sign, as a pest ofmoringa.VermaandKhurana(1974)recordedInderbelatetraonisasanewhostofmoringagrowninIndia.CONCLUSIONSAlthough itwas reported thatmoringa is not very susceptible to pest and diseases,given the wide spread of moringa cultivation throughout world, under different climaticconditions; it is likely that the plants will be suffering from various important pests anddiseases.Therefore,caremustbetakenregardingthediseasesandpestsofmoringatoavoiddamagetotheplantationsandsubsequenteconomiclosses.ACKNOWLEDGEMENTSThis research was financially supported by the King Saud University, Deanship ofScientificResearchandCollegeofFoodandAgricultureSciences,ResearchCentre.LiteraturecitedAdebayo, A.G., Akintoye,H.A.,Olufolaji, A.O., Aina,O.O., Olatunji,M.T., and Shokalu, A.O. (2011). Assessment oforganic amendments on vegetative development and nutrient uptake ofMoringa oleifera Lam in the nursery.AsianJ.PlantSci.10(1),74–79http://dx.doi.org/10.3923/ajps.2011.74.79.Agrictech, T.N.A.U. 2016. Major insect pests of Moringa http:/www.Agritech.tnau.au.ic/crop_protection/crop_prot_crop_insectveg_Drumstick.html(accessedJanuary1,2016).Akanbi,W.B.,Adebayo,T.A.,Togum,O.A.,Adedeye,A.S.,andOlaniram,O.A.(2007).TheuseofcompostextractsasfoliarspraynutrientssourceandbotanicalinsecticidesinMoringaoleifera.WorldJ.Agric.Sci.3(5),642–652.Anonymous.(2012).NoordablitealisWalker,1859.AfroMoths.http://www.afromoths.net.Anwar,F.,Latif,S.,Ashraf,M.,andGilani,A.H.(2007).Moringaoleifera:afoodplantwithmultiplemedicinaluses.PhytotherRes21(1),17–25.PubMedhttp://dx.doi.org/10.1002/ptr.2023Butani,D.K., andVerma,S. (1981). Insectpestsofvegetables and their control-drumsticks.Pesticides.15 (10),29–32.Butani,D.K.,andVerma,S.(1984).InsectsinVegetables(Delhi,India:PeriodicalExpertBookAgency),pp.356.Carbungco, E.S., Pedroche, N.B., Panes, V.A., and De la Cruz, T.E. (2017). Identification and characterization ofendophytic fungi associated with the leaves of Moringa oleifera Lam. Acta Hortic. 1158, 373–38010.17660/ActaHortic.2017.1158.42.Demuelenaere,E.(2001)Moringastenopetala,asubsistenceresourceintheKonsodistrict.Paperpresentedat:InternationalWorkshopDevelopmentPotentialforMoringaProducts(Dar-Es-Salaam,Tanzania).Fahey, J.W. (2005). Moringa oleifera: a review of the medical evidence for its nutritional, therapeutic andprophylacticproperties.Part1.TreesLifeJ.1(5).Fakurazi,S.,Nanthini,U.,andHairuszah, I. (2008).HepatoprotectiveandantioxidantactionofMoringaoleiferaLam. against acetaminophen induced hepatotoxicity in rats. Int. J. Pharm. 4 (4), 270–275 http://dx.doi.org/10.3923/ijp.2008.270.275.Fuglie,L.J.(1999a).TheMiracleTree:Moringaoleifera:NaturalNutritionfortheTropics(Dakar:ChurchWorldService),pp.68;revisedin2001andpublishedasTheMiracleTree:TheMultipleAttributesofMoringa,pp.172.http://www.echotech.org/bookstore/advanced_search_result.php?keywords=Miracle+Tree.Fuglie, L.J. (1999b).Newuses ofMoringa studied inNicaragua. ECHODevelopmentNotesNo. 68 (North FortMyers,Fla:EducationalConcernsforHungerOrganization(ECHO)).

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