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Acta Hortic. 1158. ISHS 2017. DOI 10.17660/ActaHortic.2017.1158.4 Proc. I International Symposium on Moringa Eds.: A.W. Ebert and M.C. Palada 19 Moringa frequently asked questions M.E. Olson a Instituto de Biologı́a, Universidad Nacional Autónoma de México, Tercer Circuito s/n de Ciudad Universitaria, México DF 04510, Mexico. Abstract The moringa tree Moringa oleifera is increasingly being studied for numerous properties of applied interest. In the course of work on these properties, many questions arise from both scientists and potential consumers. Here I address some of the most common such questions. I explain that moringa’s correct scientific name is Moringa oleifera Lam., and that Moringa pterygosperma is not a synonym but an illegitimate name. The wild range of Moringa oleifera is unknown but it might be native of lowland northwestern India. It is cultivated in all tropical countries, but it is probably best to avoid saying that it is “naturalized” because some uses of this word imply that the plant has become invasive. There are thirteen described species in the genus Moringa, but additional new species probably await description, especially in northeast Africa. Traditionally, leaves of Moringa oleifera, M. concanensis, and M. stenopetala are eaten, and the tubers of young M. peregrina are sometimes eaten roasted. All other species have local medicinal uses. Current commercial use so far emphasizes M. oleifera dried leaf meal in capsules, often touting protein content. Simple calculations show that capsules have negligible protein nutritional value. Such use in pill form rather than as a food leads to the frequent question of whether moringa has “side effects”. A review of studies shows that moringa has low levels of trypsin inhibitors, tannins, saponins, and lectins, meaning that there is no reason to expect that normal levels of consumption would lead to discomfort from these compounds. Nearly 40% of moringa calcium may be present in the form of oxalates, but current data suggest that these are insoluble, excreted, and do not contribute to the formation of kidney stones. Goitrogenic glucosinolates are probably absent, and if present are probably in very low concentrations. Moringa might have abortifacient potential, especially in concentrates. Given its usefulness and relative lack of antinutritional factors, there is global interest in growing moringa, so I examine its climate preferences. Moringa oleifera is a plant of the lowland dry tropics, growing best in places where annual low temperatures do not dip below 15°C, rainfall is less than 1500 mm and distributed in one or two rainy seasons, and below 500 m a.s.l. I conclude by underscoring the need for studies of all of these aspects across the entire diversity within M. oleifera and across the genus. Keywords: Moringa, taxonomy, nomenclature, climate preference, side effects, nutrition INTRODUCTION Moringa oleifera (“moringa”) is of global interest for its nutritional, nutraceutical, and industrial applications, but there are many aspects of basic moringa biology for which information is difficult to come by. This difficulty means that many papers in the applied moringa literature often, and understandably, repeat some misconceptions regarding the plants. To help make this information available in one place, I treat some of these key issues here, as a series of questions. WHAT IS MORINGA’S CORRECT SCIENTIFIC NAME? As with many useful plants, there is some degree of confusion over moringa’s correct scientific name, and, especially in the popular literature, even how to write it. It should go a E-mail: [email protected]

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Acta Hortic. 1158. ISHS 2017. DOI 10.17660/ActaHortic.2017.1158.4 Proc. I International Symposium on Moringa Eds.: A.W. Ebert and M.C. Palada

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Moringa frequently asked questions M.E.OlsonaInstituto de Biologıa, UniversidadNacional Autonoma deMexico, Tercer Circuito s/n de CiudadUniversitaria,MexicoDF04510,Mexico.Abstract

Themoringa treeMoringa oleifera is increasinglybeing studied fornumerousproperties of applied interest. In the course of work on these properties, manyquestionsarisefrombothscientistsandpotentialconsumers.HereIaddresssomeofthemostcommonsuchquestions.Iexplainthatmoringa’scorrectscientificname isMoringa oleifera Lam., and that Moringa pterygosperma is not a synonym but anillegitimate name. Thewild range ofMoringa oleifera is unknown but itmight benativeoflowlandnorthwesternIndia.Itiscultivatedinalltropicalcountries,butitisprobablybesttoavoidsayingthatitis“naturalized”becausesomeusesofthiswordimplythattheplanthasbecomeinvasive.TherearethirteendescribedspeciesinthegenusMoringa,butadditionalnewspeciesprobablyawaitdescription,especially innortheast Africa. Traditionally, leaves of Moringa oleifera, M. concanensis, and M. stenopetala are eaten, and the tubers of young M. peregrina are sometimes eatenroasted.Allother specieshave localmedicinaluses.Current commercialuse so faremphasizes M. oleifera dried leafmeal in capsules, often touting protein content.Simplecalculationsshowthatcapsuleshavenegligibleproteinnutritionalvalue.Suchuse in pill form rather than as a food leads to the frequent question ofwhethermoringahas“sideeffects”.Areviewofstudiesshows thatmoringahas low levelsoftrypsin inhibitors,tannins,saponins,and lectins,meaningthatthere isnoreasontoexpect that normal levels of consumption would lead to discomfort from thesecompounds.Nearly40%ofmoringacalciummaybepresent inthe formofoxalates,butcurrentdatasuggestthattheseare insoluble,excreted,anddonotcontributetotheformationofkidneystones.Goitrogenicglucosinolatesareprobablyabsent,andifpresent areprobably in very low concentrations.Moringamighthave abortifacientpotential, especially in concentrates. Given its usefulness and relative lack ofantinutritional factors, there isglobal interest ingrowingmoringa,so Iexamine itsclimatepreferences.Moringa oleifera isaplantof the lowlanddry tropics,growingbestinplaceswhereannuallowtemperaturesdonotdipbelow15°C,rainfallislessthan1500mmanddistributed inoneortworainyseasons,andbelow500ma.s.l.IconcludebyunderscoringtheneedforstudiesofalloftheseaspectsacrosstheentirediversitywithinM. oleiferaandacrossthegenus.

Keywords:Moringa,taxonomy,nomenclature,climatepreference,sideeffects,nutritionINTRODUCTION

Moringaoleifera(“moringa”)isofglobalinterestforitsnutritional,nutraceutical,andindustrial applications, but there are many aspects of basic moringa biology for whichinformation is difficult to come by. This difficultymeans thatmany papers in the appliedmoringa literature often, and understandably, repeat some misconceptions regarding theplants.Tohelpmakethisinformationavailableinoneplace,Itreatsomeofthesekeyissueshere,asaseriesofquestions.WHATISMORINGA’SCORRECTSCIENTIFICNAME?Aswithmanyusefulplants,thereissomedegreeofconfusionovermoringa’scorrectscientificname,and,especially inthepopular literature,evenhowtowrite it. Itshouldgo aE-mail: [email protected]

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without saying that the correct scientific name format needs to be followed, and this isMoringaoleiferaLam.,withthegenuscapitalized,thespeciesepithetinlowercase,boththegenusandspeciesitalicized,andtheauthoritynotitalicizedbutcapitalizedandabbreviatedfollowingbotanicalconvention.ThismeansthatuseslikeMoringaOleiferaLamandrelatedvariantsthatarefoundabittooofteninthemoringaliteratureareincorrect.“Lam.”isshortfor “Lamarck” and this is sometimeswrittenout, but botanists have a conventional set ofabbreviationsforauthorsandthecorrectoneis“Lam.”inthiscase(Lamarck,1783;McNeilletal.,2012).Another frequent naming issue regardsMoringapterygosperma. This name is oftencited as a “synonym” ofM.oleifera, sometimes used interchangeablywith it, and even asthough it were another species entirely.Moringapterygosperma is none of these. It is anincorrectname,notasynonym,ofM.oleifera.Briefly,thesituationisasfollows.Inthelate1600s,AdriaanvanRheedetotDrakenstein(vanRheede,1698),postedwiththeDutchEastIndia Company in southwestern India, published an early description and illustration ofMoringa oleifera as “mouringou” (along with the name in various languages, including“moringa” inPortuguese). Inhis1753SpeciesPlantarum, Linnaeus citesRheede, andcallsthe plant “Guilandinamoringa,” mistaking it for a legume, Guilandina being a genus oflegumes.SoonbotanistsrealizedthatMoringawasnotalegume,sothegenusMoringawaserected,takingthenamefromGuilandinamoringa(Adanson,1763).Adansondidnotassigntheplant a speciesname,however. Finally, in1783, Jean-BaptisteLamarck,ofLamarckianevolutionfame,gavetheplantforfirsttimethenameMoringaoleifera,referencingLinnaeus,Rheede, and others. In thisway, the nameMoringaoleiferawas established as the officialname for the plant. Because it was Lamarck who first used this term, he is cited as the“authority”orauthorofthename.In1791,JosephGaertnerpublishedthesecondvolumeofhisDeFructibusetSeminibusPlantarum,themostdetailedworkonseedsatthattime.GaertneroverlookedthattheplantweknowasMoringaoleifera had alreadybeennamedby Lamarck.Not onlydidGaertnergiveanewname,Moringapterygosperma,toaplantwithalegitimatename,buthealsowentso faras tocite theverypublications inwhichtheplantwasgiven itsname.Givinganewnametoaplantwhileblandlycitingitspreviouslegitimatepublicationissuchanaffronttostudents of botanical nomenclature that these superfluous names are often not evenincludedinlistsoflegitimatebotanicalsynonyms(e.g.,Olson,2010).Moringapterygospermais thus considerednot a synonymbuta superfluousname forMoringaoleifera.Therefore,thereisnoreasonevertousethenameMoringapterygosperma.WHEREISMORINGANATIVE,CULTIVATED,ANDNATURALIZED?The introduction of nearly every paper on Moringa oleifera applied propertiesincludes a brief overview of moringa’s geographical distribution. Some of these are asaccurateascanbegivencurrentknowledge(e.g.,Morton,1991)andsomeareextravagantintheirbiogeographicalimplausibility,oftenstatingthatmoringaisnativeto“northernAfrica”,“easternAsia”,“Arabia”,“Iran”,“Afghanistan”evenCaribbeanislands,andallnumberofotherplaces where it is definitely not native. Much of this confusion is understandable. Usefulplantsaremovedaroundbypeopleandinhighlytransformedtropicallandscapesthathavebeeninhabitedformillennia,itishardtotellwildfromintroducedplants.Eventheconceptsof“wild”versus“cultivated”or“naturalized”areoftenunclear.What is meant by the “wild” distribution of a plant is the area in which the plantevolved and spread before humans arrived. Its wild habitat is the natural floristicassemblage at the geographical site that the plantwould grow in even in the absence ofhuman intervention. So, even though it is common to seemoringa trees growing and re-seedingontheoutskirtsofvillageshereinMexico,orinPakistan,inMadagascar,westAfrica,andmanyotherplaces,thisdoesnotmeanthattheyaregrowingwildintheseplaces.Iwilltreat this issue indetail in a laterwork,but Iwill note that at themoment, basedon theliteratureandmyownfieldwork,thereissofarevidenceforwildstandsofwhatiscurrentlyregarded as Moringa oleifera only in hilly lowlands of northwestern India (Figure 1).Innumerable reports of “wild” moringas in other parts of India have in my field and

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herbariumworkturnedouttobecultivatedplantsorremnantsofoldcultivation.GivenitsproximitytonorthwesternIndia,itwouldnotbesurprisingtofindwildmoringasineasternPakistanbutsofartherearenoconvincingreports(Stewart,1972;PakistanPlantDatabasewww.tropicos.org/Project/Pakistan).So,thoughthereisstillmuchtobelearned,basedontheliterature(e.g.,Dastur,1951;Verdcourt,1986;Olson,2010)andongoingfieldwork,itissafesttosaythatmoringais“possiblynativetonorthwesternIndia”.

Figure1. Putatively wild plants of Moringa oleifera in subtropical deciduous forest inlowlandnorthwestIndia.Thatsaid,moringa iscultivated inall tropicalcountries,and it isoftensaidthat it is“naturalized”inthesecountries.“Naturalized”isavexedtermbecauseundersomeusagesitis synonymous with weedy or invasive. In others, it can refer to plants that reproducethemselves inanon-nativearea,especiallyaroundhumanenvironments,withoutenteringintoundisturbedhabitat(ColauttiandMacIsaac,2004).ThisisthecaseofM.oleifera,whichdoesre-seeditselfaroundhouses,vacantlots,road,andthemarginsofagriculturalfieldsinmany places in the world. What has never been observed anywhere in the world aremoringasinvadingintactprimaryhabitat.Thisisveryimportantbecauseitmeansthatthereis no reason to think that moringa will become an ecological nuisance, displacing nativeflora. Plants considered weeds or other nuisances can be banned or their movementsotherwiserestrictedbygovernments,hamperingresearchandtrade.Therefore,becauseofits various connotations, I suggest avoiding the term “naturalized” and using only“cultivated.”Tosummarize:moringaisputativelywild,asfarasiscurrentlyknown,inthelowlandsof northwestern India. Moringa is cultivated in other parts of the Indian subcontinent,tropicalAsia,Africa,Madagascar,theAmericas,Australia,andOceania.Itisnotknowntobeinvasive or aweed anywhere. Finally, it isbest to avoid saying thatmoringa isnaturalizedanywhere.HOWMANYSPECIESOFMORINGAARETHERE?Reports of the numbers of species of Moringa vary widely, ranging up to 14(Verdcourt,1986).Basedonmyfieldandherbariumwork,thereare13currentlydescribedspecies(Table1).Verdcourt’s“species14”turnedouttobeMoringalongitubauponvisitingthe locality (Figure 2). There are probably several undescribed species, especially innortheast Africa. Moringa rivae ssp. longisiliqua is very different in flower color fromMoringarivae ssp.rivae and is verypoorly collected. Itmight represent adistinct species,butmaterialissofragmentarythatitisdifficulttosay.SpecimensfromsoutheastofBerbera,Somaliland,(GloverandGilliland1194,intheKewandEastAfricanherbaria)werereferredtoM.pygmaea by Olson and Carlquist (2001) but they might representM. borziana orpossibly an undescribed species. Much more exploration is needed to map out the wilddistributions of Moringa species and the taxonomy of the species. Based on currentknowledge,though,thereare13describedspecies,listedinTable1.

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Table1.CurrentlydescribedspeciesofMoringa.Moringa arborea Verdc.Moringa borziana MatteiMoringa concanensis NimmoMoringa drouhardii Jum.Moringa hildebrandtii Engl.Moringa longituba Engl.Moringa oleifera Lam.Moringa ovalifolia Dinter and A. BergerMoringa peregrina (Forssk.) FioriMoringa pygmaea Verdc.Moringa rivae Chiov.Moringa ruspoliana Engl.Moringa stenopetala (Baker f.) Cufodontis

Figure2. Verdcourt’s “Moringa sp. 14” on theKenya-Somaliaborder east ofWajir turnedouttobeMoringalongituba.WHICHSPECIESOFMORINGAAREEDIBLE?

Moringaoleifera is themostwidelygrownspecies,cultivatedaroundtheworld foravarietyofproducts.InadditiontoM.oleifera,threespeciesareknowntohavesomedegreeofedibility,M.stenopetala,andtoalesserdegreeM.concanensisandM.peregrina.Moringastenopetala is the secondmost-cultivated species ofMoringa. It seems to be found nativeonlyinahandfuloflocalitiesaroundLakeTurkana(MbalukaandBrown,2016),intheGreatRift Valley of northwesternKenya and southwestern Ethiopia. Slightly to the northeast, itformspartofasystemofpermacultureagroforestryinsouthernEthiopiaintheregionoftheKonsopeople.Thisareaisattheupperelevationalmarginofthedrytropics,around1600ma.s.l. People there grow annual vegetable crops in the rainy season, but plant Moringastenopetala trees abundantly in their towns.Moringastenopetala has a very large, waterstoring trunk and holds on to its leaveswell into the dry season. These are eaten by theKonso as an important dry season food (see Jahn, 1991; Forch, 2002; Jiru et al., 2006).Thoughitsgrowthrateandyieldsareimpressive,M.stenopetalagrowsmoreslowlythanM.

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oleiferaanditsyieldsarelower.Itsseedyieldsarelowerandthethick,spongyseedcoatofM.stenopetala makes it even harder to extract the oil, with lower yields and, apparently,lowerquality seedoil andmuch lowerwater clarificationproperties.Moringastenopetalaleaves have a tougher texture to eat than the very soft leaves ofM.oleifera. WhereasM.oleifera grows tall and mast-like during its first year,M.stenopetala tends to formmanystemsfromthebase,formingahugeshrubifitisnotshapedaggressively.

MoringaconcanensisistheclosestlivingrelativeofM.oleifera.Itisnativethroughoutthe lowlanddry tropics of eastern and southernPakistan,muchof India, and a few smalllocalities inBangladesh. It lookssomewhat likeM.oleiferaand isoftenconfusedwith it. Itoften has thicker outer bark than M. oleifera and the leaves have slightly longer pinnasegments thatareonce-pinnateascompared toM.oleifera.Thecommonassertion thatM.concanensishastwicepinnateleavesandthatM.oleiferahas3-pinnateleavesandthatthisfeaturereadilydistinguishesthespecies(Qaiser,1972;Bhandari,1990;Verdcourt,1986)isnot quite true. It is based on the small and fragmentary leaves that are oftenpressed forherbarium specimens. Small leaves ofM.concanensis are indeed often 2-pinnate, but thelarge, mature leaves of M. concanensis often have 3-pinnate sections (Figure 3). Large,mature leaves ofMoringaoleifera are always 3-4 pinnate.What distinguishes themmostclearly are the long leaf tips inM.concanensis,which consist of a long section of pairs ofleaflets, often3-8, in contrast toM.oleifera,which at the leaf tips usually has only 1 or 2pairsofleaflets.

Figure3. Moringaconcanensisleaves.Ontheleft,asmalltwicepinnateleaf.Ontheright,averylargeleaf,showingthatwhenlarge,thereareoften3-pinnatesections,eveninM.concanensis.Theyoungpods,andsometimesleavesandflowersofM.concanensisareoccasionallyeaten locally (e.g., Arinathan et al., 2007), but in general this species is regarded asmedicinal,includinginterveningincholesterollevels,diabetes,andparasiteinfections,muchlikeotherspeciesofMoringa(e.g.,seeAnbazhakanetal.,2007,thoughtheirdescriptionofthespeciesseemsatoddswithitsmorphology).Moringa peregrina is, in turn, the closest living relative to M. oleifera and M.

concanensis(Olson,2002).Itisaslendertrunkedorbushytreewithwispyleavesthatdroptheirleafletsatmaturity.Inthisway,thematureleavesaremadeupofjustthenaked,woodyrachises.Theoilcontained in thehard-shelled,winglessseeds is laboriouslycollectedandsaved formedicinal use, at least in Oman, where it is reportedly taken by the cupful forstomachcomplaints.Theonlyediblepartseemstobethetubersofyoungplants,whichareroastedandeaten(MillerandMorris,1988).OnlyM.oleifera,M.stenopetala,M.concanensis, andM.peregrina are known to haveany degree of edibility. The other species are all used medicinally locally, though. InMadagascar Moringa drouhardii and M. hildebrandtii are classic tomb ornamentals insouthernandwesternMadagascar(seeOlsonandRazafimandimbison,2000).Thebarkof

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the trees is often scraped and gouged. Local people told me that they use the bark indecoctions forbronchial complaints. I asked them if theyeverate the leavesor the seeds,andtheytoldmethattheyareregardedaspoisonous.Moringaovalifolia,fromNamibiaandAngola,alsoseemstobeusedmedicinallybutneverasfood.ThenortheastAfricanendemicsM.arborea,M.borziana,M. longituba,M.rivae, andM.ruspoliana are all usedmedicinally.The roots all seem to be used to treat intestinal parasites in goats and camels, and skinafflictionsinanimals.Moringapygmaeaissogeographicallyrestrictedandsopoorlyknowningeneralthat,whileitmightbeusedsimilarly,thereisnodocumentationofthis.Nopartofanyofthesespeciesisknowntobeeaten.DOMORINGAPILLSORCAPSULESHAVEPROTEINNUTRITIONALVALUE?Themostcommonproductonthemoringamarketcomesintheformofdriedleavesincapsules.Averycommonclaim insupportof thesaleof thesecapsules is thatMoringaoleifera leaves have high levels of protein. Examining these claims makes it clear thatmoringacapsulesareunlikely toprovidedietarily significantamountsofprotein.Moringacapsulesusuallycontainabout400mgofdriedmoringaleafpowder.Moringaleafpowderthatincludesmostlyleaflets,andnotthewoodypetioleandleafrachises,containsabout20-30% protein. 25% of 400 mg = 100 mg protein. World Health Organization standardssuggestthatanaverageadultneeds105mgproteinkg-1bodyweightday-1.Therefore,an80-kgadultneedssome8,400mgproteinday-1.Assumingthatalloftheproteininmoringaisavailabletothebody,dividingtheaveragedailyneedbytheamountofproteininmoringa(100/8400×100)showsthatamoringacapsulecontainsabout1.2%oftheproteinneededevery day. Meeting daily protein intake would require more than 80 moringa capsules.Therefore,itisclearthatmoringacapsulesareneitherasignificantproteinsourceandnoracost-effectiveone.DOESINGESTINGMORINGAPRODUCESIDEEFFECTS?Because moringa is often commercialized as a capsule rather than as a vegetable,many consumers ask whether “taking” moringa produces side effects. In answering thisquestion,itishelpfultostopthinkingofmoringaasamedicineandthinkofitasanutritiousvegetable.Thiswillhelp thinkproperlyhowtoeatmoringa,aswellasguideexpectationsregarding“sideeffects”.Briefly,therearegenerallynosideeffectstoeatingavegetable,butpeople have different reactions. Soybeans, for example, provide high quality protein, butmanypeopleareallergictothem.Iamunawareofanyreportsofmoringaallergy,butthereisnoreasontoassumethatitisimpossible(thoughthereissomeevidencetosuggestthatmoringa actually helps counteract some allergic responses, see for exampleMahajan andMehta,2007;AgrawalandMehta,2008).But“sideeffects”refertoareasonablydependable,undesirablesecondaryeffect,andtherearenumerouscompoundsinplantsthatcancausesuchunwantedeffects.IbrieflyexaminethecontentsofMoringaoleiferaandconcludethatthere is little reason to expect side effects from eating moringa, though its abortifacientpotential at high concentrations requiresmore research. I examine several antinutritionalcompoundsasfollows:TrypsininhibitorsTrypsin is an important digestive protease. Natural selection has favored theproductionofprotease inhibitors inplants, apparently as adefensemechanism,deterringanimals from eating them. There have not been many studies on trypsin inhibitors inMoringa,andthosethathavebeendonehavebeencarriedoutonlyonverylimitedsamples.Based on these studies, though, protease inhibitors seem to be found only in moderateamountsinM.oleiferaleaves,andtheonesthatarethereseemtobeveryheat-sensitive,soaquick cooking deactivates most of them (Vanderjagt et al., 2000). Some nutritious foods,suchassoybeans,arenotoriousfortheirtrypsininhibitors(e.g.,Guillamonetal.,2008).Infact,many legumeswith very high protein contents are not eaten precisely because theyhave such high levels of trypsin inhibitors and other antinutritional factors. Unlike thesespecies, Moringa oleifera is not known for its indigestibility. So, based on the available

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evidenceandalonghistoryofconsumptionbypeople,trypsininhibitorsdonotseemtobepresentinside-effectproducingquantitiesinM.oleifera.TanninsTanninsarepolyphenolsthatinteractwithproteins,oftenbindingtothemandmakingtheminsoluble.Whenproteinsarenotinsolution,theycannotbedigested.So,likeproteaseinhibitors, tannins appear to have arisen and beenmaintained in plants as antiherbivoryagents.MakkarandBecker(1997)foundtanninsinconcentrationsofabout12gkg-1,whichtheauthorsregardedasonlyrepresentingamoderateconcentration.Note,though,thatthestudies that havebeen conductedonmoringahavebeen carriedouton samples gatheredonly in a few geographical regions and therefore might not reflect the variability foundacrossthespecies.Also,theresultsofchemicalstudiescanvarytremendouslydependingonthe exact extraction and sample preparation method used (Hagerman, 1988). This alsomeans that it is sometimes hard to compare between studies. For example, Albrecht andMuck (1991) measured tannin contents in a variety of legumes and found that tannincontentsvariedfrom0to27gkg-1.ThiswouldseemtobearoutMakkarandBecker’s(1997)conclusionthatthe12gkg-1inMoringaoleiferaleavesisindeed“moderate”.However,giventhattheirmethodsdifferedslightly,itishardtoknowjusthowMoringaoleiferatanninlevelscomparetothoseinotherfoods.Inaddition,becauseMakkarandBeckeronlyusedasinglesample, it is hard to know how much variation there is in tannin concentrations acrossMoringa oleifera and the different products made from moringa that people consume.However,incontrasttothingslikegrapes,persimmons,orrawnuts,whicharenotoriousfortheirtannincontent,moringahasnosuchreputationdespitemillenniaofconsumption.So,given the information available, the tannin concentrations seem lowenough that they areunlikelytoproduceunwantedreactionundernormalconsumption.SaponinsFungi seem to be particularly susceptible and saponins might be an evolutionaryresponsebyplantstofungalattack(Osbourn,1996).Theyapparentlyactbydisruptinglipidcellmembranes.Liketannins,theyareunpleasanttastingandpotentiallytoxic.MakkarandBecker(1996)showedthatMoringacontainedsomesaponins(seealsoRichteretal.,2003).Theyfoundsaponinlevelshigherthanthoseinsoybean,butreportedthatthetoxicityofthesaponins inmoringa seems tobevery low.Likeall aspectsofmoringa, systematic studiesacrossthevariabilitywithinM.oleiferaandacrossthegenusareneeded,butbasedontheavailableevidence therewouldseem tobenoreason toavoideatingMoringa inanormaldietbecauseofitssaponincontent(seealsoMakkarandBecker,1997;Gidamisetal.,2003).LectinsLectinsareglycoproteinsthat,wheneatenbypeople,bindtothemucopolysaccharidesprotrudingfromthemembranesofthecellsintheintestinalwall.Wellknownlectinsincludericin and phytohemagglutinin. Lectins are again compounds that plants, being sessileorganismsthatcannotrunawaywhenconfrontedbyapredator,defendthemselvesagainstattack (Peumans and Van Damme, 1995). Makkar and Becker (1996) found no traces oflectinsintheiranalysis,thoughtheseeddoes,famously,havecoagulatingproteins.Thesearetheproteins that areused inmoringawaterpurification (seeSutherlandet al., 1994, alsoCoelho et al., 2009 for othermoringa lectin uses). So, even thoughmoringa is so rich inproteins, lectins do not seem to be important components of the chemical repertoire ofmoringaleaves.CalciumoxalateIt is often said thatmoringa has “more vitamin C than oranges,more calcium thanyogurt, etc…” Olson and Carlquist (2001) showed that therewas abundant calcium in allmoringaparts–butintheformofcalciumoxalatecrystals.Thesecrystalsareanotherlineofplantdefense,thistimeagainstchewingorpiercinginsects.Forhumans,calciumoxalateisworrisomebecauseinthebestcaseitisnotavailabletothebodyandintheworstcasecan

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contributetoformationofkidneystones(FinkielsteinandGoldfarb,2006).Foryearsitwasnotclearhowmuchofthe“morecalciumthanyogurt”wasactuallynutritionallyinaccessiblecalciumoxalate.RadekandSavage(2008)quantifiedtheproportionofcalciuminmoringain the form of oxalate, and it turned out to be a 38%. This percentage would seemdismayinglyhigh,buttwoimportantobservationsemergefromtheirstudy.First,RadekandSavageshowedthatmoringaleavescontainonlynon-solubleoxalates.Thismeansthateventhough thereare largeamountsofoxalates inmoringa leaves, it is found ina formthat issimply excreted by the body. Oxalates that are excreted do not circulate in the body, andthereforecannotcontribute tokidneystone formation.Second,RadekandSavageshowedthatmoringahas totalcalciumvalues thatareextremelyhigh(>20mgg-1ofdry leaf).So,evenwithmore than a third of the calcium being unavailable,moringa offers substantiallevelsofcalciumthatarepotentiallybioavailable.Powderedmilkhasapproximately13mgg-1ofcalcium(USAID,2006).So,moringaleafpowderwouldseemtocomparefavorablynotonlywithpowderedmilkintermsofproteincontentbutalsointermsofcalcium.Evenifalloftheproteinorevenallofthenon-oxalatecalciuminmoringaturnsoutnottobereadilydigestible(andheremoreresearchisneeded),themuchlowercostofmoringameansthatitis a protein and calcium source that is more inexpensive and with a much lowerenvironmental impact than milk. Thus, although a large proportion of the calcium inmoringaisboundupinoxalates,mostoftheseoxalatesarelikelysimplyexcreted,meaningthattheydonotcontributetokidneystones.And,inadditiontocalciumoxalate,thereisstillasubstantialamountofcalciumthatisprobablybioavailable.GlucosinolatesBeyond its well-proven nutritional benefits, one of the main promising aspects ofMoringaoleifera is itsbatteryofantioxidantglucosinolates,ormustardoils.Glucosinolatesare the spicy, sulfur-containing compounds that give radish, cabbage,wasabi, papaya, andotherBrassicaleanplantstheirspiciness,pungency,orsometimesslightlyfetidsmell.Theyarewhatseemtogivemoringaitspotentialpromiseincancerchemoprevention(Guevaraetal.,1999;Faheyetal.,2004;etc.),glucoseregulationfordiabetics(Karetal.,2003;Ndongetal.,2007),andotherpotentialapplications.Glucosinolatesarepotentiallyimportantinconnectionwithsideeffectsbecausesomeof them lead to the formation of goiters. Therefore, a natural question is whetherglucosinolates inMoringaoleifera have thepotential to cause goiters (Abuye et al., 2003).Moringa is amemberofBrassicales, the greatorderofmustard-oilproducingplants. Thismeans that it is a relative, though a bit distant, of themustard family,Brassicaceae.ManyBrassicaceae are well known for containing progoitrin, which, when eaten and then splitapart in the initial stages of digestion, releases goitrogenic oxazolidonethiones. However,progoitrinhasneverbeenidentifiedinanyMoringaspecies.Likewise,noMoringaspeciesisknowntohavehighlevelsofglucosinolatesconstructedaroundanindolegroup(Faizietal.,1995; Guevara et al., 1999). Indole glucosinolates are also important goiter-causingcompounds.Asaresult,thereisnoevidencethatpointsdecisivelytowardariskofgoitersfromconsumingmoringa.However,itcouldbethatsomethiocyanates,thesulfur-pluscyan-group containing compounds common inmoringa, justmight be goitrogenic in very highconcentrations,wellbeyondthosefoundinanormaldiet.This issignificantbecausesomecommercialmoringaproducts includeconcentratesthatverywellmightconcentratesomesubstances excessively, an issue potentially of concern also with regard to abortifacientpotential.AbortifacientpotentialOne aspect of moringa biology that requires attention is its potential to provokeabortion.MoringaisatraditionalabortifacientinIndia(Nathetal.,1992)anddoesseemtoprovokeuterinechangesinratsthathavehadtheirovariesremovedandsootherwiselackfemale hormones (Shukla et al., 1989). In addition, there is a fair amount of researchexamining the ability of moringa to cause abortions in rats. As with most research onmoringa’smedicalandnutritionalpotential,manyhavemethodsthatarehardtointerpret.

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For example, Sethi et al. (1988) appear to have ground upmoringa leaves, extracted thecontentswithethanolandthendriedthis tincturedown(seealsoNathetal.,1992).Theythenadministrated175mgofthispasteperkgofratbodyweight.Fora65-kghuman,thiswouldmean taking11gof thishyper-concentrate. It isnotatall clearhowmanykilosoffreshmoringaleaveswouldbeneededtomake11gofsuchanextract,butitlikelyexceedstheamountthatapersonwouldingestinanymeal.Centuriesofuseasanediblefoodhaveestablishedmoringaasanutritiousadditiontohumandiets,apparentlyincludingpregnantwomen,butitisclearthatmoreresearchwouldbehelpful.Moringa’spotentialabortifacientpotentialatveryhighdosesillustratestheimportantpointthatwell-meaningusagessuchasconcentrates that go far beyond proven dietary doses could reveal potential undesirableeffect.Giventhisevidence,itseemsclearthatdietaryuseofmoringashouldconcentrateonmoringa as a vegetable, a use that is known to be safe and nutritious; concentrates andextractsshouldbeavoideduntilmoreisknownaboutabortifacientpotential.WHERECANMORINGABEGROWN?Becausemoringaissuchausefulplant,peopleworldwidewouldliketogrowit.HereIprovidesomeinformationregardingwheremoringagrowsbest,itsclimatepreferences,andconsiderationsforgrowinginmarginalareas.First,moringaisatropicalplant.Itonlygrowstrulywell in the tropics, and thedry tropics at that. Thekey factors are temperature andmoisture; latitude and elevation inevitably intervene as well. We will look at theseindividually.The firstkeyaspect is theannual lowtemperature. Justbecause itgetshot inDeathValley,orIowa,orParisdoesnotmeanmoringaswillgrowwellthere.Thisisbecausewhatlimitsmoringasmostseverelyistheyearlyabsolute(notmean)lowtemperature.Moringasdonottoleratefrostwell.Moreimportantly,theydonotgrowwellinplacesthatgetbelow10°Cor so, andonly thenwhen such low temperatures are rare. 15°Cas a general low isideal. On the Jalisco coast, at the site of the InternationalMoringa Germplasm Collection(www.moringaceae.org), the lowest low is 17°C, ideal for moringa. There are occasionallows,at3amatthecoldesttimeofyear.Ten(10)degreeweatherfordaysonendisasbadformoringasasafrost.Goodaveragedailytemperaturerangesareinthe20-to35-degreerange. The annual high is important insofar as it is related to the average, but is not animportantconsiderationinselectionareasforgrowingmoringa.Moringasingeneraldonotsuffer from high temperature, and often do not even drop their leaves under hightemperature if there is water in the soil. In any case, tropical areas havemoremoderateclimatesthandesertsandotherextremeplaces,soanywherewiththeminimumthatishighenoughforamoringawillhaveabsolutehightemperaturesthatarealsointhecorrectrange.As to rainfall,practicallyany tropicalarea thatmeets the temperaturerequirementswillmeettheminimumrainfallneedsofmoringa.Theprobleminthetropicsislikelytobetoomuchrainfall.Moringasdobestinareasthatreceivelessthan1.5mofrainperyearandwheretherainfallsinoneortwoconcentratedseasonsduringtheyear,notevenlyallyearround.Thewet tropics,as inrainforestareas,placeswherethings likecacao,mangosteen,tea,oilpalms,orallspicegrowwellareusuallytoowetformoringastogrowsatisfactorily.Moringasdonottoleratewellwaterpuddledaroundtheirroots,orheavy,finesoilwithlittleoxygenaroundtheroots.Ontheotherhand,theyrespondwelltowelldrained,wellaeratedsoil.Fastdraininggravelly soil is ideal, and theywill alsodowell in sandysoils.However,theywill do poorly even on the best soils if they remainwaterlogged. For example, deepvolcanicsoilsareoftenperfectformoringas,butiftheyareinahighrainfallareatheplantswillsufferanyway.Withregardtolatitudeandelevation,moringaisatropicallowlandplant.Moringasingeneral growbest fromsea level to500ma.s.l. or so. In someplaces,moringas cangrowacceptablyuptoabout1000m.Growthattheseelevationswillgenerallynotbeacceptableforcommercialproductionbutmightbesatisfactoryfordomesticuseorasanornamental.Thetreescanoftensurvivebutdefinitelynotthrivebetween1000and1500m.Above1500m is completelyoutof thequestionas faras seriousmoringacultivationgoes.Rememberthatmoringaisatropicalplantandtheseelevationsapplytotropicallatitudes,between23

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northandsouthlatitudeorso.Moringasreallydonotgrowwelloutsideoftheselatitudesandcertainlynotathigherelevations.I offer some tables (Tables 2-4) giving combinations of temperature and rainfall inareaswhere I have seenmoringa growingwell. These illustrate the point thatM.oleiferapreferswarmclimateswithveryhighlowtemperatures.Thehighscanbehigh,butthelowsneedtobehigh.Rainfalltendstobelow,1500mmoroftenmuchless,andishighlyseasonal,usuallywith8monthsorsoofverydryweather.Moringaisalowlandplant,growingbestbelow500ma.s.l.Moringa oleifera will hang on in many marginal places, even flower and fruitingsparingly in places like southern California, the Mexican or Kenyan high plateaus, or theCanary Islands. They can be cultivated, at great expense andmassive carbon footprint, ingreenhouses in cold places like Europe (Forster et al., 2015), or, perhaps even moreunsustainably, with outdoor gas heaters (Figure 4). Given the very fast growth rates of

Moringaoleifera, it seems possible that it could be cultivated as an annual in temperateregionswithadequateyield.Somecultivarsaregrown in Indiaasannuals for theirediblepods, so with their long summer day lengths it could be possible to reach adequatetemperatezoneyieldsdespitetheinappropriateclimate.Table2. Moringa oleifera temperature preferences in degrees Celsius, showing thatmoringasgrowbestinareaswithveryhighminimumtemperatures.Locality Mean annual temp. Max. temp. Min. temp.Tiruchirappalli, India 29 37 21Rupnagar, India 24 40 7Tehuantepec, Mexico 28 35 20Antanimeva, Madagascar 24 33 13IMGC, Jalisco, Mexico 26 33 16Mandera, Kenya 29 40 20Kitui, Kenya 25 35 16Accra, Ghana 27 32 22Barranquilla, Colombia 28 33 23Chiquimula, Guatemala 26 35 18Depto. León, Nicaragua 27 35 20

Table3. Moringa oleifera precipitation preferences (ppt in cm), showing that moringasgrowbestinareasthathaverelativelylowandseasonalrainfall.Locality Mean Ann Ppt Ppt wet Mo Ppt dry Mo Ppt wet qtr Ppt dry qtrTiruchirappalli, India 860 192 9 453 39Rupgnagar, India 944 307 8 694 55Tehuantepec, Mexico 860 216 2 511 7Antanimeva, Madagascar 665 165 2 457 10IMGC, Jalisco, Mexico 818 225 1 566 13Mandera, Kenya 247 85 1 138 3Kitui, Kenya 421 128 1 205 5Accra, Ghana 786 194 10 421 57Barranquilla, Colombia 778 192 0 437 2Chiquimula, Guatemala 696 158 0 384 3Depto León, Nicaragua 1458 386 0 855 1

Mean Ann Ppt = Mean annual precipitation; Mo = month and Qtr = quarter, i.e. 3 month period, so it rains 192 mm in the wet month in Barranquilla, 437 in the wet quarter, 0 mm in the driest month, and 2 mm in the driest quarter.

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Table4.Moringaoleiferaelevationalpreferencesinma.s.l.Locality ElevationTiruchirappalli, India 84Rupnagar, India 260Tehuantepec, Mexico 41Antanimeva, Madagascar 146IMGC, Jalisco, Mexico 74Mandera, Kenya 221Kitui, Kenya 574Accra, Ghana 8Barranquilla, Colombia 40Chiquimula, Guatemala 339Depto León, Nicaragua 87

Figure4. Moringa drouhardii being grown outside with the benefit of gas heaters, TheHuntington,SanMarino,California.CONCLUSIONS–THENEEDFORFURTHERSTUDIESEven thoughpeoplehavebeeneatingmoringa for thousandsof years, all aspectsofmoringa needmore study.Most of the studies that have been carried out have examinedvery small samples of moringa germplasm. Virtually no effort has been made to studysamplesfromacrosstheentiregenusMoringaandincludingthefullgeneticdiversityofM.oleifera.Thestudiesthathavebeencarriedoutarehardtocomparewithoneanotherandtheirmethodsmake their relevance to humannutritiondifficult to interpret at times (forexample,themassiveabortifacientdosesgiventorats).Anystudiesinhumanshaveinvolvedvery fewsubjects.Relatively fewof these studiesare inprestigious international journals.Withtheeaseofcommunicationaffordedbytoolssuchasemailandvideoconferences,plusthe relative ease of sending material or traveling, there is every reason to expect thatmoringa scientists can forge a global collaboration to produce globally comprehensive

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applied and basic data. Only in this way can we take moringa science from its currentsituationofindicatinggreatpromisebutbasedonverylocalstudies;onlyinthiswaycanwetakemoringafrombeingaplantofgreatpromiseandmuchanecdotalevidencetoonewiththefullbackingofsolidscientificresearch.ACKNOWLEDGEMENTSThisworkwassupportedbyTreesforLifeandbyprojectIT200515oftheProgramadeApoyoaProyectosdeInvestigacioneInnovacionTecnologica,UNAM.LiteraturecitedAbuye,C.,Urga,K.,Knapp,H.,Selmar,D.,Omwega,A.M.,Imungi,J.K.,andWinterhalter,P.(2003).AcompositionalstudyofMoringastenopetalaleaves.EastAfrMedJ80(5),247–25210.4314/eamj.v80i5.8695PubMed.Adanson,M.(1763).FamillesdesPlantes.IIPartie(Vincent,Paris).Agrawal, B., and Mehta, A. (2008). Antiasthmatic activity ofMoringaoleifera Lam: A clinical study. Indian JPharmacol40(1),28–31.PubMedhttp://dx.doi.org/10.4103/0253-7613.40486Albrecht,K.A.,andMuck,R.E.(1991).Proteolysisensiledforagelegumesthatvaryintanninconcentration.CropSci.31(2),464–469http://dx.doi.org/10.2135/cropsci1991.0011183X003100020048x.Anbazhakan, S., Dhandapani, R., Anandhakumar, P., and Balu, S. (2007). Traditional medicinal knowledge onMoringaconcanensisNimmoofperambalurDistrict,Tamilnadu.AncSciLife26(4),42–45PubMed.Arinathan,V.,Mohan,V.R.,Britto,A.,andMurugan,C.(2007).WildediblesusedbyPalliyarsofthewesternGhats,TamilNadu.IndianJ.Tradit.Knowl.6,163–168.Bhandari,M.M.(1990).FloraoftheIndianDesert.Revisededition.(MPSRepros),pp.435.Coelho, J.S.,Santos,N.D.,Napoleao,T.H.,Gomes,F.S.,Ferreira,R.S.,Zingali,R.B.,Coelho,L.C.,Leite,S.P.,Navarro,D.M., and Paiva, P.M. (2009). Effect ofMoringaoleifera lectin on development andmortality of Aedesaegyptilarvae.Chemosphere77(7),934–938.PubMedhttp://dx.doi.org/10.1016/j.chemosphere.2009.08.022Colautti,R.I.,andMacIsaac,H.J.(2004).Aneutralterminologytodefine‘invasive’species.Divers.Distrib.10(2),135–141http://dx.doi.org/10.1111/j.1366-9516.2004.00061.x.Dastur,J.F.(1951).UsefulPlantsofIndiaandPakistan(D.B.TaraporevalaSons&Co.).Fahey,J.W.,Dinkova-Kostova,A.T.,andTalalay,P.(2004).The“Prochaska”microtiterplatebioassayforinducersofNQO1.InMethodsinEnzymology,Vol.382,ParteB,H.Sies,andL.Packer,eds.(SanDiego,California:ElsevierScience),p.243–258.Faizi,S.,Siddiqui,B.S.,Saleem,R.,Siddiqui,S.,Aftab,K.,andGilani,A.H.(1995).Fullyacetylatedcarbamateandhypotensive thiocarbamate glycosides from Moringa oleifera. Phytochemistry 38 (4), 957–963. PubMedhttp://dx.doi.org/10.1016/0031-9422(94)00729-DFinkielstein, V.A., and Goldfarb, D.S. (2006). Strategies for preventing calcium oxalate stones. CMAJ 174 (10),1407–1409.PubMedhttp://dx.doi.org/10.1503/cmaj.051517Forch, W. (2002). Case study: the agricultural system of the Konso in South-Western Ethiopia. FWU WaterResourcesPublications(Germany:UniversityofSiegen),http://fwu.fb10.uni-siegen.de/bkd/FWU_WRP.htmForster,N.,Ulrichs,C.,Schreiner,M.,Arndt,N.,Schmidt,R.,andMewis, I. (2015).Ecotypevariability ingrowthandsecondarymetaboliteprofileinMoringaoleifera:impactofsulfurandwateravailability.J.Agric.FoodChem.63(11),2852–2861.PubMedhttp://dx.doi.org/10.1021/jf506174vGidamis,A.B.,Panga,J.T.,Sarwatt,S.V.,Chove,B.E.,andShayo,N.B.(2003).Nutrientandantinutrientcontentsinraw and cooked young leaves and immature pods ofMoringaoleifera Lam. Ecol. Food Nutr. 42 (6), 399–411http://dx.doi.org/10.1080/03670240390268857.Guevara, A.P., Vargas, C., Sakurai, H., Fujiwara, Y., Hashimoto, K.,Maoka, T., Kozuka,M., Ito, Y., Tokuda, H., andNishino,H. (1999).Anantitumorpromoter fromMoringaoleiferaLam.Mutat.Res.440 (2),181–188.PubMedhttp://dx.doi.org/10.1016/S1383-5718(99)00025-XGuillamon,E.,Pedrosa,M.M.,Burbano,C.,Cuadrado,C.,Sanchez,M.deC.,andMuzquiz,M.(2008).Thetrypsininhibitorspresentinseedofdifferentgrainlegumespeciesandcultivar.FoodChem.107(1),68–74http://dx.doi.org/10.1016/j.foodchem.2007.07.029.Hagerman, A.E. (1988). Extraction of tannin from fresh and preserved leaves. J. Chem. Ecol.14 (2), 453–461.PubMedhttp://dx.doi.org/10.1007/BF01013897

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Sethi,N.,Nath,D.,Shukla,S.C.,andDyal,R.(1988).Abortifacientactivityofamedicinalplant"moringaoleifera"inrats.AncSciLife7(3-4),172–174PubMed.Shukla, S., Mathur, R., and Prakash, A.O. (1989). Histoarchitecture of the genital tract of ovariectomized ratstreated with an aqueous extract of Moringa oleifera roots. J Ethnopharmacol 25 (3), 249–261. PubMedhttp://dx.doi.org/10.1016/0378-8741(89)90031-7Stewart,R.R.(1972).AnAnnotatedCatalogueoftheVascularPlantsofWestPakistanandKashmir(Karachi).Sutherland, J.P., Folkard, G.K., Mtawali, M.A., and Grant, W.D. (1994).Moringaoleifera as a natural coagulant.Paperpresentedat:20thWEDCConference,AffordableWaterSupplyandSanitation(Colombo,SriLanka).USAID.(2006).Commoditiesreferenceguide.Factsheet:nonfatdrymilk(USAID).vanRheede,H.A.(1698).HortusIndicusMalabaricus.Volume6,TomeII.(Amsterdam:JohannisvanSomerenandJoannisvanDyck).Vanderjagt,D.J.,Freiberger,C.,Vu,H.-T.N.,Mounkaila,G.,Glew,R.S.,andGlew,R.H.(2000).Thetrypsininhibitorcontentof61wildedibleplantfoodsofNiger.PlantFood.HumanNutr.55,335–346.Verdcourt,B.(1986).Moringaceae.FloraofTropicalEastAfrica(TaylorandFrancis).