Insectsasfoodandfeed: environmentalimpact

DennisG.A.B.Oonincx Promotors Prof.DrA.vanHuis PersonalchairattheLaboratoryofEntomology WageningenUniversity

Prof.DrJ.J.A.vanLoon PersonalchairattheLaboratoryofEntomology WageningenUniversity

Othermembers Prof.DrW.H.Hendriks,WageningenUniversity DrT.V.Vellinga,LivestockResearch,WageningenUniversityandResearchCentre

Germany DrP.G.Jones,WalthamCenterforPetNutriton,MarsPetcare,Leicestershire,UK

ThisresearchwasconductedundertheauspicesoftheGraduateSchoolof Insectsasfoodandfeed: environmentalimpact

DennisG.A.B.Oonincx

Thesis

atWageningenUniversity

inthepresenceofthe

tobedefendedinpublic onTuesdayϲJanuary2015 atϰp.m.intheAula. DennisG.A.B.Oonincx

PhDthesis,WageningenUniversity,Wageningen,NL(2015) Withreferences,withsummariesinDutchandEnglish

Abstract thedemandforanimalbasedproteinisontheincrease.Tomeetthisincreased

andaresuggestedtobeproducedmoresustainably.

ammonia,aswellascarbondioxideemissionandaveragedailyweightgainof

(expressedasCO2 ammoniaandeithercomparableorloweramountsofGHGthanpigs. ResultsfromChapterϯwereusedinĂLifeCycleAssessmentconducted animalprotein.ThischaptershowsthatmealwormsshouldbeconsideredĂmore sustainablesourceofedibleprotein,andthatĂlargepartoftheirenvironmental impactisduetothefeedtheyconsume. wereformulatedsuchthattheyvariedinproteinandfatcontent.Thesedietswere

InChapterϲthesuitabilityofchicken,pig,andcowmanurewascompared asfeedforlarvaeoftheBlackSoldierFly,whichinturncouldbeusedasfeedfor

vi Abstract onmoistenedmanure.Whereassurvivalwashighonallthreetestedsubstrates,

topreventthisinordertomakeitecologicallysound.Furthermore,toimprove animalsareevaluatedbasedonbothliteraturedata,anddatagatheredinthis thesis.Furthermore,prospectsforinsectsasfoodorfeedareputforward,

vii viii Tableofcontents

Tableofcontents

Abstract vi

Chapter1 1

Chapter2 19

Chapter3 51

Chapter4 71 Ăhumanproteinsourceʹlifecycleassessment Chapter5 83

Chapter6 115 pig,orcowmanure Chapter7 Generaldiscussion 133

145 References

182 Summary

186

190 Acknowledgements

193 Curriculumvitae

194

197 

198

ix

Chapter1

D.G.A.B.Oonincx Chapter1

TheClassInsectacomprisesmostspeciesofalltaxaintheAnimalKingdom.The numberofdescribedspeciesisaboutonemillion(Ødegaard2000;Finlay,Thomas etal.2006).Fromthose,atleast1900insectspecieseatenbyhumanshavebeen documentedinliterature,andthetotalnumbercanbeexpectedtobewellover

acrosstheglobe.InmosttemperatezoneslikeEurope,NorthAmericaandthe

However,countriesinthetemperatezonelikeJapanandChinaarenotable

predominantlycollectedfromnature.Therefore,theiravailabilityisinmanycases

Imbrasiabelina (Westwood);Lepidoptera:Saturniidae)isavailabletwiceĂyear(IllgnerandNel 2000). derivedproductsareusedbyhumans.Thebestknown,andbestacceptedproduct

2010).Otherinsectproductsthatareeatenaremushrooms(Termitomycesspp.) emergingfromthefungigardenoftermites(vanHuis1996).Also,thesoilof termitemoundsiseaten,whichistermedgeophagy(Luoba,Geissleretal.2004).

(Dominy,Davoustetal.2004).However,ithasalsobeensuggestedthatgeophagy

Geissleretal.2004). asE120.Itismadefromcochineal(Dactylopiuscoccus(Costa);Homoptera:

2 1

History

ThehistoryofentomophagybyhominidsstartsbeforetheexistenceofHomo sapiens

madesuitablebytheearlyhominoidAustralopithecusrobustustŽdigintotermite

. Basedontheanalysisofcoprolites,insectswereeateninNorthandMiddle insectsstemsfromthePaleolithicarea(approximately6000BC),whenHomohabilis evolvedtoH.sapiens

InthegreatBasinareainNorthAmerica,theremainsoflargeamounts ofMormoncrickets(Anabrussimplex togetherwiththeremainsofotheringredientsof“Desertfruitcake”werefoundin

feastfortheirking(Berenbaum1995).Romanaristocratsatetheirlocustshoneyed

3 Chapter1 ofinsectscomesfromĂplayofAristophanes(425BC),whowritesthatlocustswere

Someyearslater,inhisHistoriaanimalium onwhenintheirlifecyclethetasteofcicadaswasthesweetest(Thompson1910). theBible.ForinstanceintheOldTestamentfoodlaws:“...youmayeatanykind honey.Around23AD,StrabodescribeshowAfricanpeoplecaughtlocusts:“The inhabitantscatchthembythrowingintotheravinesmaterialswhichcauseĂgreat accountsbyDioscoridesthattheLibyansconsumedlocusts(OsbaldestonandWood 2000).PlinytheElderwritesinhisencyclopediaonnaturalhistory(approximately larvae,whichlivedinoaktrees,asdelicaciesandthatthewealthyParthiansate whichpossiblyarethelarvaeorpupaeofXylophagus(Diptera:Xylophagidae)and ofPontustoeatĂlocust,andhewillthinkitscandalous.ForceĂSyrian,anAfrican, orArabiantoswallowworms,hewillhavethesamecontemptforthem”.Several

1995).

Damiri,publishedatthedawnofthe15thcentury.Around1600,LeoAfricanus

renewedinterestinentomologystartsinthelateRenaissance

4 th 1 thatthisspecieswaspoisonouspreventedthepeoplefromconsumingit(de

thesewerethelarvaeofthedungbeetle(Copris(CatharsiusͿmolossus(Fabricius); Bombyx mori insects,forinstancePalmweevilsinthewestIndieswerealsoeatenbytheFrench

 Attheendofthe19th

withother“odd”foodtypeswhichareconsidereddelicacies,suchaseel,seaslugs,

asanargumentforentomophagyintheWesternworld(Howard1916;Holt1995).

Piophilacasei(L.);Diptera:Piophilidae),whichare

Entomophagyinnon-Westerncultures

5 Chapter1

KruseandKwon2004;vanHuis2005),andSouthandCentralAmerica(Ruddle

Some500yearsago,theEuropeanscameintocontactwiththeindigenous

Oryctesspp.(Coleoptera:

RepublicofCongo,Ăsurveyindicatedthatduringthemainseason2.36kgof insectswasconsumedpercapita,permonth.Thisamountsto19.6gramsof surveysconductedatAmazoniantribesreportedthat2.6%and~6%oftheprotein

6 TheMopanecaterpillar,oneofthemostcommonlyconsumedinsectsin 1 asprocessedfoodandinrestaurants(Alloteyetal.2003),butitisalsoexported totheUSAandKorea(Mpuchane,Gasheetal.2000).similarexampleofinsects beingexportedasfoodtoĂWesterncountryarebeepupaefromJapansentto

1960).Also,theThaiGiantwaterbug(Lethocerusindicus

pricesareaskedforantlarvaeandpupae,(Liometopumapiculatum(Wheeler); Hymenoptera:Formicidae)(200$/kg),whiteagaveworms(Aegialehesperiaris (Walker);Lepidoptera:Hesperiidae)(250$/kg),andlarvaeoftheredagaveworm (Xyleutesredtembacheri(Hamm);Lepidoptera:Cossidae)(200$/kg)usedinthe

Elorduy1997a).Thepriceforthesecollectedinsectshasincreasedgreatlyinthe lastdecades;supposedlythepricefor“escamoles”was35$/kgandthepricefor increaseissuggestedtobetheincreasedwealthofMexicansthathavemovedfrom ruralareastotheUSA,andwhowishtoretaintheirculinaryhabits. 

Certainspeciesofinsectsareseenasacceptablefood;commoditygoods.Forthe

7 Chapter1

(Gonimbrasiazambesina͖Lepidoptera:Saturniidae),tofeedontheregenerated

2005). instance“Axayacatl”(Hemiptera:Corixidae),havebeenculturedinMexicobefore

Anaphe infractaWalsingham(

50x50x50cmcage.Theauthorsconcludedthattherearingofthisspecieswould larvaeof

InwesternAfrica,larvaeofthepalmweevil(Rhychophorousspp.; presentthere.Thebeetlesovipositindecayingpalmtreesfromwhichthelarvae

Rhychophorousferrugineus etal.2013). Ifsustainableinsectrearingsystemsareestablished,theseaidtothe inthesustainableeconomicdevelopmentofĂregion(Illgneretal.2000).Another before,cochinealisusedasĂreddye.Itisculturedinseveralcountries,amongst

8 spp.;Cactaceae:Caryophyllales) 1 Besidesproducinginsectsforfood,theycanalsobeusedasĂfeed sourceforlivestock,forinstancepoultry(MunyuliBinMushambanyiandBalezi 2002).AnextensivewayofproducingtermitesforfeedisknownfromBurkina certaininsectculturesistheabilitytoconvertbiomaterialsthatwouldotherwise

ofsuchĂsystemisthatitallowsforĂmorecontrolledproductregardingboth forbirds,lizardsoramphibians,whichissoldthroughthepettrade.Thistypeof businesshasbeenaroundforĂfewdecadesanditseemslikelythatfurtherprocess

whicharethenplacedinĂseparatecageaccordingtoageorstageofdevelopment

 Insectrearing,whencomparedtoinsectgathering,hasthedisadvantage environment.Becauseinsectsdependonenvironmentaltemperatureforgrowth

9 Chapter1

Foodsafety

al.2006).

(Looyetal.2013).Furthermore,certainspeciesofinsectsnaturallycontaintoxins, usedasĂdefenceagainstpredators.This,however,neednotbeĂreasontodiscard themasfood.Forinstance,thelarvaeofCirinafordaWestwood(Lepidoptera:

Abatanetal.2002).IntheWesternworld,whereinsectsarenormallyrearedrather

Ăhammermill.InĂcontrolledenvironment,procedurescanbedevelopedto

ofanimaloriginarethemostimportantsourceofzoonosis,andSalmonellaspp. andCampylobacter (Valkenburgh,R.vanOosterometal.2007).Sinceinsectsaretaxonomicallyand instanceEnterobacteriaceae(whichincludeEscherichiacoliandSalmonellassp.), similarlevelsasfoundinunprocessedplantbasedfoodstemmingfromagricultural

Researchperformedonthelessermealworm(Alphitobiusdiaperinus(Panzer); thatbothlarvaeandadultsarecapableofharbouringEscherichiacoliforatleast

10 10days(McAllister,Steelmanetal.1996).Anearlierstudyreportedtheability ofA.diaperinustoharbour Wray1995).Inboththesestudiestheanimalswereinoculatedwiththepathogens, 1 apthostforthepathogen.similarstudyonturkeybroilersalsoindicatedthe possibilityofSalmonellaandEscherichiatransmissionbyA.diaperinus(Harein 1972).  Althoughcockroachesaregenerallyseenasvectorsofdisease,ithasbeen cockroaches(Periplanetaamericana(L.),and (L.);Dictyoptera; etal.2007).InĂstudyonP.americanainMorocco,elevenspeciesofpathogenic studiesinFrance(Rivault,Cloarecetal.1993).ForP.americana͕itwasshownthat

studyonthepresenceofprotozoaandhelminthsincockroachesindicatesthat

summary,itcanbeassumedthatcertainpathogenscanbedistributedbycertain arepresentinedibleinsects,inordertodevelophygienicrearingprotocolsfor methodsinordertoguaranteefoodsafety.

Reasonsforentomophagy

hasnot froglegshavebeenaccepted(KiuchiandTamaki1990;Illgneretal.2000;Gullan andCranston2005).Foodchoiceisdeterminedbycultural,psychological,and

11 Chapter1

ofnewfooditemsisgreaterforproductsofanimaloriginthanforotherfood lowsocialstatusmightbeanimportantrestraintforWesterners(Nielsen2000).It entomophagy,theyaremoreinclinedtosurmounttheiraversion(Mignon2002;

Mushambanyietal.2002). availabilityofinsectsasfoodforhumans.However,insectsaresuggestedtobe

1995;Looyetal.2013).Itissuggestedthatinsectscancontributetohealthyageing andthereforecouldbecomeĂnormalpartofthedietforWesternersbytheend healthvalueintheWesternworld,shouldbeexplored.

animals(Premalatha,Abbasietal.2011).femaleHousecricket(Acheta

(L.);Diptera:

12 eclosion,andĂfemaleofthesuperworm(Zophobasmorio(Fabricius)Coleoptera; 1 cows,pigs,orevenchickens.



Looyetal.2013).Thisseemsplausiblebecauseinsects,unlikeendotherms,donot useenergyobtainedfromfeedtomaintainĂconstantbodytemperature.Therefore,

HousecricketshavebeenreportedtohaveĂfreshweightECIof95%onĂ

ThesevaluesareonĂfreshweightbasis,inwhichthemoisturecontentof

HousecricketsĂdryweightECIof27%wasreported(Woodring,Roeetal.1977;

from35to44%andbetween53and73%formealworms(Tenebriomolitor(L.); Coleoptera:Tenebrionidae)whenthesespeciesarerearedonorganicwastesof vegetableorigin.

lesssuitablediets.ECI,however,isĂcrudemeasurethatdoesnotdiscriminate

13 Chapter1 above90%hasbeendescribedforcopperandzincinthebruchidbeetle(Bruchidius sahlbergi(Schilsky);Coleoptera:Chrysomelidae)(Ernst1992).However,inthe samestudythenutrientECIforcalciumandmagnesiumwasbelow20%.These

specieswithĂminimaluseofresources.

Sustainability 

andlanduse(Mollenhorstetal.2004).Thelivestocksectorisanimportant

etal.2010;Steinfeld2012).Thisincreaseindemandgoeshandinhandwithan increaseincarbonemissionsandassuchwithenvironmentalproblemsonĂglobal

foodsource(Hardouinetal.2003;Barwa͖Das,Gangulyetal.2009;Premalathaet al.2011;Looyetal.2013).

14 1

Stumm1994;Cazemier,Hacksteinetal.1997;Kammann,Heppetal.2009).The

assessment(LCA),shouldbeimplemented.

“Waste”asĂsubstrate  AccordingtoKollikkatharaetal.(2009)“Wasteissimplyresourcesoutofplace”. Insmall,closedsystems,whereresourcesarelimited,theurgencytoavoidwaste ismostapparent.Severalauthorshavesuggestedtouseinsectstoconvertwaste

Musca (L.);Diptera:Muscidae)(ElBoushy1991;ElBoushyandvanderPoel 2000). whichareusedbothasfoodforpeopleandasfeedforpoultry(Pereira,Ferrarese Filhoetal.2003).Thisspeciescanbeproducedonmulberryleavesandthe

ecologically,andeconomically,soundproduct.

15 Chapter1

Outlineofthisthesis and,forĂvarietyofinsectspecies,addsexperimentaldataregardingtheirchemical feedtobodymass,inordertodeterminethevalidityofthesearguments.ChapterϮ altered. species(T.molitor͕ ͕LocustamigratoriaL.(Orthoptera:Acrididae), PachnodamarginataDrury(Coleoptera;Scarabaeidae),and Serville

speciesofmealworms(T.molitorandZ.morioͿisexamined.Thisisdonebymeans

mealwormsreadyforfurtherprocessing).Presenteddataareexpressedaskgof combinedtoformulatefourdiets,varyinginproteinandfatcontent.Thesedietsare testedonfourinsectspecies(T.molitor͕ ͕H.illucensandB.dubia), arereported.Thegoalofthisexperimentwastodeterminethesuitabilityofthese pigsandcowsisusedasĂsubstratetorearlarvaeofH.illucens͘ManureisĂtrue

hadthreegoals:(1)todeterminethesuitabilityofthesetypesofmanureasĂ substrateforH.illucens

16 1

feed.

17

Chapter2

Publishedin:

London,UK,AcademicPress. Chapter2

Abstract nutrientcontentofĂvarietyofcommerciallyraisedinsectsandcomparethose valuestothedataavailableforwildinsects.Thesedataarediscussedinlightof

Keywords

20 InsectsaregenerallyconsideredĂgoodsourceofmostnutrients(DeFoliart1992) al.2005)andthosecommerciallyreared(SimpsonandRaubenheimer2001;Finke 2

etal.2010). stageofdevelopment(McClements,Lintzenichetal.2003),diet(Calvez1975;

amountofnutrientswhentheseareexpressedasfreshmaterial.WhilewaterisĂ

Oonincxetal.2012b;Finke2013).

21 Chapter2

Nutrientcontentofinsects

Proteinandaminoacids

 Theproteincontentofinsectsishighlyvariableandrangesbetween7.5% etal.2002;Punzo2003;Oonincxetal.2010a;Oonincxetal.2011;Oonincxet

2013). Aminoacidsarethebuildingblocksofproteins.Certainaminoacidsareknownas

aminoacids.Theaminoacidsintableϭtogethertypicallyaccountforover90% ofthecrudeproteininmostinsectspecies.Thesmallamountofnitrogenthatis notaccountedforbytheseaminoacidsislikelyduetoothernitrogencontaining duringproteinhydrolysis.

mostcomparisonshavebeenmadeusingmorecommonlaboratoryanimals,such

22 asratsorchickens(Finke2002;Finke2013). L.)larvaeand

L.)fedtomountainchicken frogs(Leptodactylusfallax

( 2

TenebriomolitorL.)was75%when

(AnabrussimplexHaldeman)orHousecricketswerethesolesourceofprotein,the

Onifade,Oduguwaetal.2001).Similarly,methionineandcysteinewerecalculated Zophobasmorio F.),larvaeoftheGreaterwaxmoth(Galleriamellonella larvae(BombyxmoriL.),honeybeelarvaeandpupae(ApismelliferaL.),adult Walker)and ChilecomadiamooreiSilva)(Finke2002;Finke2013).Assuch

beenproposedthatadultpasserineshaveĂpreferenceforspiders,drivenbyĂneed forenhancedlevelsofmethionine,cysteineorperhapstaurinebytheirgrowing chicks(RamsayandHouston2003).

23 Chapter2



eitherobtainedandstoreddirectlyfromĂdietarysourceorsynthesizedfrom

AsĂdietarycomponent,fatisnotonlyanimportantenergysource,butmayalso

1997;Yang,Siriamornpunetal.2006;Finke2013).AsĂruleofthumb,mostadult, wildinsectscontainlessthan10%fatonĂfreshweightbasis(Fast1970;Leaseand Wolf2011). adulthoodinmigratorylocusts(LocustamigratoriaL.).Theadultweightinthis

(Thompson1973).Incertainspecies,themaleshaveĂhigherfatcontentthan thefemales(NakasoneandIto1967;Fast1970).Forspecieswheremalecombat iscustomary(forinstanceOdonata),thiscanbeexplainedbyĂneedforgreater energyreserves.InseveralfamilieswithintheorderLepidoptera,malescontain femaleshavegreaterfatreservesthanmales(Zhou,Honeketal.1995;Nestel, Papadopoulosetal.2005;Leaseetal.2011).Inspeciesthatuseaccumulated

thewildseemtohaveĂlowerfatcontentthaninsectswhicharecommercially produced(Finke2002;Yangetal.2006;Oonincxetal.2012b;Finke2013).This

acidsarestoredintheinsectfatbody,makingupover90%ofthetotalfatbodylipid

24 2

1997;Yangetal.2006).Forinstance,thefatoftheChinesegrasshopper(Acrida cinerea

Lopezetal.2002).similartrendwasreportedforcommerciallyraisedfeeder insects(Finke2002).

1)species,2)developmentalphase,3)diet,and4)environmentalfactorssuchas temperature,lightandhumidity.

25 Chapter2

1973;Finke2013).

vertebrates,denovo

tosynthesizethem(Bender2002).Thisalsoappearstobetrueformostinsect

Periplaneta americana synthesizeddenovo

Carbohydrates

GryllusbimaculatusDeGeer),polysaccharide

1973)andfreecarbohydratecontentofthefatbodyinfemalesofthisspeciesis

26 2007;LeaseandWolf2010;Oonincxetal.2012b;Finke2013).Whileinsects 2

2002;WhitakerJr,Dannellyetal.2004;Donoghue2006;German,Nagleetal. 2010).

 While“harderbodied”insectslikeadultbeetlescontainedhigherlevels

27 Chapter2

Minerals

playĂprimaryroleinhelpingmaintaintheskeletalstructureinvertebrateswhile basebalance.Thetracemineralsplaywiderangingrolesrangingfromoxygen nothaveĂmineralizedskeleton.Calciumlevelsaretypicallylessthan0.3%dry etal.2011;Oonincxetal.2012b;Finke2013).Thehigherlevelsofcalcium

Oonincxetal.2011;Oonincxetal.2012b;Finke2013).Theexoskeletonofmost

Ămineralizedexoskeletoninwhichcalciumandothermineralsareincorporated

Muscaautumnalis

OtherinvertebratessuchasmillipedesandisopodsalsohaveĂmineralized

nestlinggrowth(Gravelandetal.1994;BurešandWeidinger2003). Thephosphoruscontentoffeederinsectsismuchhigherthancalciumlevelsin

28 etal.2011;Oonincxetal.2012b;Finke2013).Mostinsectswouldlikelycontain sincethephosphorusininsectsislikelytobereadilyavailableaswasshownfor

 Mostspeciesoffeederinsectscontainlevelsofmagnesiumrangingfrom 2 feederinsects.ItseemslikelythatbothcalciumandmagnesiumformĂcomplex bredinsects(Finke2002;Oonincxetal.2011;Oonincxetal.2012b;Finke2013) insects(Reichleetal.1969;LevyandCromroy1973;Studier,Keeleretal.1991; StudierandSevick1992;Oyarzun,Crawshawetal.1996).Levelsofpotassium thechloridecontentoffeederinsectswithvaluesrangingfrom0.16ʹ0.97%

zinc,copperandmanganese.Whilethehighfatlarvalstageofsomespeciesof

1992;Punzo2003).  InsectsaregenerallyĂgoodsourceofzincwithvaluesforcommercially

Finke2002;Punzo2003;Oonincxetal.2012b;Finke2013)͘Thesevaluesare

29 Chapter2 similartothoseobtainedforwildcaughtspecies(Levyetal.1973;Punzo2003). Copperincommerciallyraisedfeederinsectsrangedfrom3.1to51.2mg/kgdry

aretypicallygoodsourcesofcopper.Wildcaughtinsectsalsoappeartocontain

 Levelsofmanganeseinfeederinsectsrangefrom1.5to364mg/kgdry

thisspeciesareunclear.Somespeciesofstoredproductinsectscontainelevated levelsofzincandmanganeseintheirmandiblespresumablytohardenthemin

Punzo2003). twelvespeciesoffeederinsectsanalyzed,onlysixhadanydetectableiodinewith brood(pupaeandlarvae)didnotcontaindetectablelevelsofiodine(Finke2005). Nootherdataareavailableconcerningtheiodinecontentofinsects. Asisthecaseforiodinethereareonlylimiteddataontheseleniumcontentof elevenspeciesoffeederinsectscontainseleniumatlevelsrangingfrom0.27to

30 Vitaminsandcarotenoids

VitaminA  VitaminplaysĂroleinĂwidevarietyofphysiologicalprocessesincluding limiteddataregardingthevitamincontentofwildinsectsandmostspeciesof 2 migratorylocustsfedĂgrassdietsupplementedwithwheatbranandfreshcarrots

2011).

Pernisapivorus

carotenoidcontentitmaybethatdietsfedtocommerciallyraisedinsectsdonot

Levi,Zivetal.2012).Carotenoidsarefoundathighlevelsinmanyspeciesofwild

Andersson2007;Eeva,Helleetal.2010;Oonincxetal.2011;Finke2013).The

31 Chapter2

Jonesetal.1996;Miller,Greenetal.2001;Pessier,Linnetal.2005;Hoby,Wenker etal.2010).

VitaminD

speciesofcommerciallyraisedinsectsdetectednovitaminalthoughthethreshold

3

ϯ(Finke2013)͘Thesevaluesare isnoanalysisofthevitamincontentofwildinsectsavailableforcomparison. content.However,itseemslikelythatexposuretoultravioletlightistheappropriate

1996;Oonincxetal.2010a).

VitaminE varyingamountsofvitaminE.BothHousecricketsandyellowmealwormshave beenshowntocontainwidelyvaryinglevelsofvitaminE.ValuesforHousecrickets

32 (Microcentrumrhombifolium(Saussure))(Finke2002;Oonincxetal.2012b;Finke 2013).Therearefewdataonthevitamincontentofwildinsects,althoughthey appeartocontainvitaminatlevelsonthehigherendoftherangeorexceeding

B-Vitamins 2 commoncommerciallyraisedfeederinsects(Finke2002;Finke2013).Thereismuch

oroxygen.Thereforevaluesobtainedbyanalysingdriedinsectsthathavebeen livewholeinsects.Thisalsomeansthatcommerciallyavailabledriedwholeinsects

Thiamine(vitaminB1 associatedwithenergymetabolism(Thurnham,Benderetal.2000).number ofspeciesoffeederinsectsincludingHousecrickets,adultYellowmealworms,

2006).WhenanalysedusingĂmicrobiologicalmethod,highlevelsofthiamine werereportedfortheAfricanpalmweevillarva(Rhynchophorusphoenicis(F.)) Ustaterpsichore(Maassenand

(Macrotermessubhyalinus

ZaireanalysedusingĂmicrobiologicalmethodalsocontainedlowlevelsofthiamine

33 Chapter2

2 ofĂvarietyofothernutrients(Thurnhametal.2000).Mostspeciesofcommercial

theseinsectswerekeptdry(adults)orstoredin70%alcohol(larvae).Since orresultedfromlossesduringstoragepriortoanalysis.

 Niacin(vitaminB3 (Thurnhametal.2000).Itappearstobeabundantininsectswithcommercially

(Finke2002;Finke2013).varietyofdriedinsectspeciestypicallyconsumed lepidopteranlarvaehavebeenanalysedforniacin.Eventhoughtheseinsectswere

 Pantothenicacid(vitaminB5

 Pyridoxine(vitaminB6ͿplaysanimportantroleinĂvarietyofmetabolic

34 raisedinsectsappeartobegoodsourcesofpyridoxinewithvaluesrangingfrom

Yellowmealwormbeetles(Jonesetal.1972;Finke2002;Finke2013).Mostinsect species,however,fallinĂfairlynarrowrangebetweenϲand10mgpyridoxine/kg

obtainedareĂresultofthesmokinganddryingprocessusedtopreservethedried insectproduct. 2

Folicacid(vitaminB9 metabolism(Thurnhametal.2000).UsingĂchemicalmethodcommerciallyraised insectswereshowntocontainhighlevelsoffolicacidrangingfromĂlowof1.57

lightandoxidizingagentsthelowvaluesseemlikelyĂresultofthesmokingand dryingprocessusedtopreservethedriedinsectproduct.

Cobalamin(vitaminB12ͿisfoundexclusivelyinproductsofanimaloriginandplaysĂ

larvaecontainnodetectablevitaminB12 otherspeciesaregoodsourcesofvitaminB12

12 commerciallyraisedspecies.

VitaminC oxidant.Insectscontainsomevitaminandithasbeensuggestedthatcertain insects,forinstancethegrasshopperMelanoplussanguinipes(F.),useenzymesto

35 Chapter2

2006).Mostotherspeciesinwhichvitaminwasdeterminedcontainedlowlevels

Yellowmealwormscontainedlevelssimilartothosereportedforhoneybees(Finke

Ingeneral,thelipidcontentofwildinsectsisapproximately30%forlarvaeand priortometamorphosis(Fast1970).Thisdependstosomedegreeonwhether speciesundergoĂcompletemetamorphosis(holometabolousspecies;forinstance Yellowmealworms)oranincompletemetamorphosis(hemimetabolousspecies;for instanceHousecrickets).  LarvaeofholometabolousspecieshaveĂhigherfatcontentthanadults (Punzo2003;Leaseetal.2011).Yellowmealworms,forexample,increasetheir fatreservesduringlarvalgrowth(McClementsetal.2003).Thesefatreserves

2002;Leaseetal.2011;Oonincxetal.2012b).similartrendisseeninfruit mealwormschanges;glycine,tryptophanandtaurinecontentincrease,while wellasĂspeciesofnoctuidmoth( Walker)alsoincreased

betweenmalesandfemales(Nakasoneetal.1967).Inthevelvetbeancaterpillar, totallipidcontentdecreasesduringmetamorphosis,aswouldbeexpected.

36  Unlikeholometabolousinsects,hemimetabolousadultstendtohaveĂ higherfatcontentthannymphs(Leaseetal.2011).Thisholdstrueforcertain studiesconductedonMigratorylocusts,butnotall(Oonincxetal.2010a; 2

proteinandĂlowerfatcontentthansmallandmediumHousecrickets(Finke2002; nymphsandadultsofthisspecies(Finke2002).InĂstudyonthreecockroach (Kirby))and Hissingroaches(Gromphadorhinaportentosa contentandcrudeproteincontent,andĂconcomitantdecreaseinfatcontent,was notedbetweensmallandmediumspecimens.Theoppositechangewasnoted

insectitselfcanalsobealteredtoĂcertainextentthroughthediet.Forinstance,

37 Chapter2 larvaeincreasestheirwatercontent(64vs.59%)(Machin1975). Forthemacronutrients,itseemsthatinsectfatcontentishighlyvariableand

Ăcertainamountofproteinincreasesitsfatreserve,thepercentageofprotein

2011).Thismightbethereasonwhytheproteincontentstaysconstantduring adulthoodifĂproteinsourceisavailableandproteincontentdecreasesifonlyĂ carbohydratesource,whichcanbeconvertedtofat,isavailableaswasshownin (Wiedemann))(Nesteletal.2005). Althoughthepercentageofproteincanbealteredthroughthediet,itseems

thelarvae.  Asstatedbefore,thecrudefatcontentofinsectscanbealteredbythe

fatcontentthanthosefedthecommercialcricketdiet.Duringthisperiodthefat contentdecreasedforallthreegroups,whichledtoĂconcomitantriseinthe energycontentinthethreeexperimentaldietsthaninthedietprovidedbefore adultsduringthosethreeweeksandassuchtheirfatcontentwouldbeexpected todecrease(McClementsetal.2003).

38 2

Whiletheelevatedcarotenelevelscouldbeduetogutloading,itseemslikelythat

ParusmajorL.)have yellowmealworms(Senaretal.2010). suchasCdandPb,canoccurincertaininsectspecies(Zhang,Songetal.2012).

39 Chapter2

numberofenvironmentalfactors,suchastemperature,lightandhumidity,can

Temperature dependstoĂlargedegreeontheenvironmentaltemperature.Therefore,within growthrateshouldincreasewithhighertemperatures(Alietal.1977;Hanson

highertemperatures,adultsizegenerallyseemstodecrease;Ăcolderenvironment

Schistocercagregaria Forsskål)andmigratorylocustswhereadultbodyweightsarehigherwhenreared suitablewhenappropriatehumidityisprovided(Hamilton1936).Lastinstar

isalsohighestat34°C.Bothgrowthrateandmortalityaredecreasedat27°C. Thelowestadultfreshweightisachievedatambienttemperaturesaround10°C,



40 ladybeetle(CoccinellaseptempuctataL.)andtheAsianladybeetle(Harmonia axyridis increasesfatstorageatelevatedtemperaturescomparedtonormaltemperatures malesatnormaltemperatures,butĂsimilarfatcontentatelevatedtemperatures. Theauthorssuggestedthattemperaturesbeforeeclosiondeterminethefat contentofadultsinbothspecies(Krengeletal.2012).Thecarbohydrateand proteincontentofbeanbeetles(Acanthoscelidesobtectus(Say))islowerat20°C 2

Humidity

levelsofhumidity,withinanappropriaterange,seemtodecreasedevelopment thecaseofincreasingtemperatures,thisincreaseingrowthratedoesnotseem toleadtoĂlowerbodymassinadults.Forinstance,thebodymassofthepine caterpillar(DendrolimustabulaeformisTsaietLiu)increaseswithhigherhumidity species(L.migratoriaandS.gregaria)indicateddevelopmentispossiblebetween

speciescanabsorbwaterfromthesubstrate,therebyincreasingitsfreshweight

41 Chapter2

RH,forinstancethedevelopmentoffungiand/ormites(Machin1975).The

1950;Machin1975). othervariablescanplayĂroleaswell.TheAsianladybeetletendstogrow largerathigherhumiditylevels(between30and90%)iffedwiththeaphid Acyrthosiphonpisum(Harris)butnotwhenfedonfrozeneggsof kuehniella  Itseemsthatbodyweightanddevelopmentrateofinsectsishigheratthe topoftheirRHrange.Also,themoisturecontentofinsectsseemstoincreaseatĂ

Photoperiod

photoperiods(upto24hours)increasetheirgrowthrate.Possibly,thefoodintake could,however,alsobeduetoconcomitantlyhighertemperatures.Atconstant comparedto12hoursoflight,butadultweightwassimilar(Berkvens,Bonteetal. Nezara viridula(L.))thatmainlyfeedsatnight,hasanincreaseintherateofdevelopment withanincreasedphotoperiod(10vs.14hours)(Alietal.1977;Sheareretal. 1996).Thisincreaseindevelopmentalratecoincidedwithanincreaseinbody weightwhenreaching,andduringadulthood,especiallyforfemales(Alietal. 1977).Shortphotoperiodscaninducediapause,whilelongerphotoperiodsare

beensuggestedthattheproteincontentofadultsincreasesmorerapidlyifkept

concomitantchangesintemperature.

42 availability

tobeevaluatedinthebroadercontextofĂcompletediet,madeupofĂnumberof 2



thishasbeenreportedtobebetweenϯand10%(Cauchie2002).Forthecommonly rearedHousecrickets,thelarvaeoftheGiantwaxmothandthegiantmealworm (hormonallytreatedT.molitor

caterpillars(ClanisbilineataͿwasshowntobesimilartothatforcasein(Xia,Wuet al.2012).TheChinesegrasshopperA.cinereashowedĂslightlyhighertrueprotein andBlair1993).Forbroilers,renderedbeefmealcanbereplacedbyĂmealofthe termite F.,orthecockroach L.,withsimilar

43 Chapter2

thedustcanadhere.ThesamepowderusedforpinheadoradultHousecrickets

Finke2005).

Gutloading

GutloadingisthetermusedfortheprovisionofĂspecialdiettoinsects, shortlybeforetheinsectswillbeconsumed.Whenthisdiet,whichcontainshigh levelsofthedesirednutrient(s),isconsumedbytheinsectitwillbepresentin consumed.Duetothenatureofgutloading,itissuitableforalmostallnutrients

ofwaxmothlarvae,Housecrickets,Yellowmealwormlarvaeandsilkwormlarvae

Anderson2000;Klasing,Thackeretal.2000;Finke2003;Finke,Dunhametal.

44 2005).Chemicalanalysisofthedietprovidedmightbenecessarytoverifythetrue calciumfromgutloadedYellowmealwormsfedhighcalciumdietswasshownto bereadilyavailabletogrowingchicksshowingitsusefulnessinprovidingavailable insectsseemstovaryslightly.ThisislikelyĂresultoftheinsectspeciesbeing 2 hoursappearstoresultinsimilarlevelsofnutrientsintheintactinsect.When oftheinsectshavebeenobserved(Klasingetal.2000).InYellowmealwormsĂ or72hours,resultedinslightlyhigherCa:P(Anderson2000;Klasingetal.2000).

(Anderson2000).However,otherstudiesreportthehighestcalciumcontent

ofthepalatabilityofthegutloadingdiet(McComb2010). somethingtotakeintoaccountwhendesigningĂgutloadingdiet(Anderson

provisionofcarrotsorcertainotherfruitsorvegetablesduringthelast24hours instance,accumulatesmorecarotenoidsonĂhighcarotenoiddietthantheHouse cricketorthebandedcricket(Gryllodessigillatus 2012).  studyinwhichYellowmealwormsweregutloadedwithchicken undetectablelevelswerepresentinmealwormsprovidedĂwheatbrandiet (Klasingetal.2000).

45 Chapter2

containingthedesirednutrients,suchthatthepowderadherestotheoutsideof theinsect.Whentheinsectiseaten,thepowderontheoutsideisalsoingested.

in90seconds(Lietal.2009).Foranimalswhichimmediatelyconsumetheirprey,

calciumcarbonatedustshavebeenreported(Winn,Dunhametal.2003).The

enhancingthenutrientcontentisobviouslyunsuitable.studywiththeWyoming toad(Bufobaxteri rate,whichinturnmightbecausedbydecreasedpalatabilityduetothevitamin powder(Lietal.2009).studyofPuertoRicancrestedtoads(Peltophrynelemur

46 andMitchell2005).TheLessermealwormAlphitobiusdiaperinus(Panzer)has 2 Salmonellaspp.withbothlarvaeand adultsbeingabletocarrySalmonellaspp.bothexternallyandinternally(Crippen, Salmonellacouldbedetectedinnewlyemerged metamorphosis(Crippen,Zhengetal.2012).Sinceseveralspeciesofgrainbeetles (Tenebriosp.andZ.morioͿarecommonlyusedasfeederinsectsitseemslikely thatthesespeciescouldserveasĂvectorofSalmonellaspp.andotherpathogenic microorganisms.Tominimizethisrisk,feederinsectsshouldbeobtainedfrom

Toxins

DanausplexippusL.)andmilkweedbugs(OncopeltusfasciatusDallas) fedcontrolleddietscontainingcommercialfeedingredientsthatareusedtofeed fromtheirdietaslongasthedietwasproperlymadeandstored. Ingredientscommonlyusedincommercialinsectdietscanbecomecontaminated

47 Chapter2

priortouseshouldbestoredproperlyandperiodicallycheckedtoinsuretheyare freeofmoldswhichmightproducemycotoxins.

Anaphespp.), thiamine,pyridoxine,taurine,andothernutrientscouldalsoserveasĂsubstrate AnaphepupaehasbeenassociatedwithĂ

Watanabeetal.2000).Theextenttowhichthiaminasesarefoundinotherspecies

Conclusions  InsectsareĂgoodsourceofmanynutrientsalthoughformostnutrientsthevalues whichtheyareraised.Ingeneralmostspeciesappeartobegoodsourcesofamino

invertebratesthathavebeendustedorgutloadedtoprovideĂwiderangeof

48 Table1:Typicalaminoacidcontentofsomecommonfeederinsects(allvaluesexpressedas mgaminoacid/gcrudeprotein).

AminoAcid Mean Range Alanine 71.4 40.9ʹ101.1 Arginine 56.6 41.4ʹ75.5 65.6ʹ95.0 9.1 5.6ʹ21.3 2 GlutamicAcid 114.5 Glycine 54.7 22.1ʹ37.9 Isoleucine 42.6 32.3ʹ50.3 Leucine 76.2 Lysine 56.9 Methionine 17.0 10.7ʹ29.6 Phenylalanine 34.9 26.2ʹ43.7 Proline 33.9ʹ77.0 Serine 35.1ʹ77.0 Threonine 36.6 Tryptophan 9.0 5.2ʹ17.3 Tyrosine 56.3 31.2ʹ79.9 Valine 56.1 Taurine 1.5

49

Chapter3

speciessuitableforanimalorhuman

Loon,andA.vanHuis

Publishedin: PLoSOne5:e14445. Chapter3

Abstract

Background oneofthebiggestproblemssocietyiscurrentlyfacing.Thelivestocksectorisone ofthelargecontributorsofanthropogenicGHGemissions.Also,largeamounts ofammonia(NH3 bylivestock.Thereforeothersourcesofanimalprotein,likeedibleinsects,are currentlybeingconsidered.

Methodology/PrincipalFindings

2Ϳ

4Ϳandnitrousoxide

(N2O)aswellasNH3 edible:Tenebriomolitor͕ ͕Locustamigratoria͕Pachnoda marginata,and

ϮandGHGs.TheinsectsinthisstudyhadĂ

ThesamewastrueforCO2

3byinsectswaslowerthanfor

ThisstudythereforeindicatesthatinsectscouldserveasĂmoreenvironmentally

andNH3 cycleanalysis.

Keywords:Greenhousegasemission,edibleinsect,ammonia,averagedailygain,

52 climatechange(Steinfeldetal.2006;IPCC2007).ThemostimportantGHGsare carbondioxide(CO2),methane(CH4Ϳandnitrousoxide(N2O).Sincetheendofthe th andCHϰ 4andN2Khave

2͘ByassigningCO2

onĂCO2 4hasĂGWPof25,andN2

2 2

bytheanimalsectorare:9%forCO2 3 energyexpenditures,feedtransport,animalproductprocessing,animaltransport,

4 fromfarmanimalmanure)and65%forN2K(farmmanureandurine)(Steinfeld etal.2006).DirectCO2

sourceofCOϮ(Steinfeldetal.2006).Therespiredcarbon,whichcomesfromthe

2intheairandstoredinanorganiccompound

realisedandCO2 therebyĂrelevantindicatorfortheenvironmentalimpact(deVriesanddeBoer 2010).

(NH3 soil(Aarnink,Keenetal.1995).AlthoughnotconsideredĂGHG,NH3canindirectly contributetoN2Kemission(Steinfeldetal.2006),asconversiontakesplaceby

responsiblefor64%ofallanthropogenicNH3emissions(Steinfeldetal.2006).

ThemainsourceofgaseousNH3 inmammals(Cole,Clarketal.2005).Besidestheseenvironmentalproblemsthe animalwelfare(Thorne2007).

53 Chapter3

mainlybythreefactors:entericCH4

4andN2 insectspecies.COϮ

3emissions

Materialsandmethods

Animalsandhousing

Tenebriomolitor Housecrickets L.(Orthoptera:Gryllidae),thirdandfourthstage nymphsofMigratorylocustsLocustamigratoriaL.(Orthoptera:Acrididae),third larvalstagesunbeetlesPachnodamarginataDrury(Coleoptera;Scarabaeidae) Serville (Dictyoptera:Blaberidae).Currently,T.molitor͕ andL.migratoriaare considerededible,whileP.marginataandB.dubia

(Bruins2001;Friederichetal.2004).

chambers,T.molitorandP.marginata

54 surfaceareafor andB.dubia cmindiameter),werestackedtoĂheightof30cminthewiredcages,whileforL. migratoria commercialinsectrearingcompanies(Table1).Allanimalmassesreportedare providedinTable1.

Diet

Tenebriomolitorlarvaewererearedin300Őmixedgrainsubstrate(wheat, 3 wheatbran,oats,soy,ryeandcorn,supplementedwithbeeryeast)withontop

wasprovidedwithchickenmash(501g)withcarrot

Locustamigratoriawasprovidedwithwheatbran(70g;ArieBlokAnimal

LoliumperenneL.)wasprovideddaily(463 Őinthreedays).ThegrasswasgrownbyUnifarm,WageningenUniversityand Researchcentre,Wageningen,TheNetherlands. PachnodamarginatalarvaewerekeptinĂpeatmosssubstrate(2.0kgper

wasprovidedwithĂchickenmashdiet(199g)andcarrots

͕P.marginataand B.dubiawereprovidedbyKrecaV.O.F,Ermelo,TheNetherlands.Thecarrotsand T.molitorwereprovidedbyInsectra,Deurne, TheNetherlands.

55 Chapter3

Gasmeasurements 

2andCHϰweremeasuredeveryϵ

2andCHϰ

2andCH4ofinsects,feed,andsubstrate. TheexactairvolumesweremeasuredwithĂcalibratedSchlumbergerG1.6dry gasmeterandcorrectedformeasuredairtemperatureandpressure.CO2and

CH4

2(type

Uras3G,HartmannandBraun,Frankfurt,Germany)andCH4(typeUras10E, HartmannandBraun,Frankfurt,Germany).Therefreshedairvolumewassetso thatCO2 asfromtheincomingair,anairsamplewastakenforN2

2

2Kwasdetectedwithanelectroncapturedetector(ECD).

NH3

3gas

2 2 usedinĂformulaadaptedfromWheeler,K.D.Caseyetal.(2003): 3 ERсEmissionrateofN2Kс[N2O]change(ppmdž10 ͿdžVV(m /day)dž44(g/mol)ͬ 0.0224(m3

dayperiodwasusedtodeterminetheaverageN2

NH3

3

CO2

56 producedamountsofCH4andN2 4͕

2K(IPCC2007). Meanbodymasswascalculatedbyaveragingthebodymassatthestart oftheexperimentandthebodymassattheendoftheexperiment.Average

Ϯ

TodetermineCO2

Ϯ recalculatedtokgofliveinsect. 3

TheN2KandNH3

N2

3

2andCH4 wasdonebymeansofSPSS15.0.

Results

2isexpressedperkilogramofmeanlivebodymass(BM)per day(24hours)andperkilogramofmassgain(Table2)andtheaveragedailygain

4͕N2O,CO2 3͕are expressedperkilogramofmeanlivebodymass(BM)perday(Table3)andper kilogramofmassgain(Table4).

57 Chapter3

ADGandCOϮ

ADGvariedbetween4.0%(P.marginataͿand19.6%(L.migratoriaͿwith

2 B.dubiaͿto110(L. migratoriaͿŐperkgBM/day.Also,theCO2

species(Table5).CO2 forL.migratoria Ϯ L.migratoria

2byB.dubia.

Pachnodamarginata Ϯperkgofmassgain(1,539 g/kg),whichwasmorethandoubletheamountofL.migratoria͘

CH4

P.marginataandB.dubia͕but notforthethreeotherspecies.Pachnodamarginataproducedmorethanthree

ϰperkgofmassgainthanB.dubia(4.9vs

ϰperkgBM(0.16Ővs ADG(4.0%vs6.1%).

N2K

N2 T.molitorandL. migratoria 2KbyL. migratoria T.molitor,this toĂmuchhigherADGofL.migratoria.

NH3

NHϯwasproducedby L.migratoria,andB.dubia

3emissionlevelswerefoundfor (6.4and 4.4mg/kgBM/day),L.migratoria(5.6and3.9mg/kgBM/day),andB.dubia(3.4 and2.6mg/kgBM/day).

58 Discussion

Insects,beingpoikilotherms,donotusetheirmetabolismtomaintainĂbody temperaturewithinnarrowranges,contrarytohomeothermicanimals.Thisis

CO2

2 (BaileyandSingh1977;TerblancheandChown2007),temperature(Emekci,

Ϯ/ kgBM/daywasreportedforAnabrussimplex

CO2/kgBM/dayforthelocustSchistocercaamericana(Orthoptera:AcrididaeͿ (GreenleeandHarrison2004)and94g/kgBM/dayforadultTriboliumcastaneum

2͘ThismighttoĂlargeextentbe 3 explainedbyadlibitumfeedingduringtheexperimentthathasbeenreported

2 forT.molitor T.molitor growinglarvaeareexpectedtohaveĂhigherCO2 rangeofCO2 T.molitoriscomparabletothefactorialmetabolic Cicindela

therebyCO2 (M)wasdescribedbyKleiber(1961)asсaMb͕inwhichĂisĂconstantandďс

Wheatley2004;daSilva,Garciaetal.2006).Forpoikilothermsvaluesbetween 0.67and1.0havebeenreportedandĂcomparisonofseveralarthropodspecies

2007).ThevaluechosenforďhasĂlargeimpactonthemetabolicweightand therebythecalculatedCO2

2 metabolicweightforthestudiedinsectspecies(Table5).ForL.migratoriaCO2

11%and34%oftheCO2

TheCO2

59 Chapter3

2 2

2 kg)waseither39%(minimumvalues)or129%(maximumvalues)whencompared

2

depends,amongstothers,onlifephase.Therefore,whereavailable,literaturedata

CH4

scarabbeetlesproduceCH4 methanobacteriaceaeinthehindgut(Egert,Wagneretal.2003).

WefoundlargevariabilityfortheN2Kemissionrates.Earlierstudiesin layinghensusingĂsimilarmethodfordeterminingN2

Fabbrietal.2007).However,otherauthors(Wathes,Holdenetal.1997;Chadwick,

2O/kgBM/dayand52mg

N2

N2

andthereforeonCO2 feedintakeusinggravimetricmethods(AxelssonandÁgren1979)andcan

Casasetal.2005).OurreportedCO2

2 thesubstrateofP.marginata(92.5%)wasmostlikelyduetolargeamountsof fungalbiomassobservedinthemixedfeedandsubstratewheninsectswere

60 2 bythesubstrate.Nofungalgrowthwasapparentduringtheexperimentson feedingP.marginata

P.marginatalarvaeandthesubstrate andBrune2007)offungalbiomassorthroughunknownchemicalorcombined

Ϯ

Ϯ separately.

Ϯ

2 2ismuchhigher forL.migratoria 3

Ϯistheϳ°ChighertemperatureL.migratoriawaskeptat,

2 L.migratoriaisexpectedtoresultinhigher ofCOϮ. ͕ĂlowerADGandincreased

Ϯperkg

Ϯperkgmassgain explainedbyĂdecreaseinADG(from9.0to7.2%). didnot produceCH4͕butN2

2 2

N2

andproducingN2K(Wrageetal.2001).Althoughweincluded

ϯ

NHϯ pH,windspeed,housingtype,andsubstrate(CaseyandHolden2006;Faulkner

61 Chapter3

Inthecurrentexperiment,ĂclearNHϯ amountsofNHϯ ͕L.migratoriaand

B.dubia 3

InallcasesNH3 L.migratoria B.dubia and

3

NH3 3 emission,increasedfromdayonetodaythreeinB.dubia(1.57to4.29mg/kgBM/ day)and 3

experiments.ForL.migratoriaNH3emissiondidnotincreasebetweendayϭand

3 Thismightbecausedbythefaecesofthisspeciesthat,contrarytothoseofB. dubiaor

WeconcludethatP.marginataandT.molitorprobablydidnotemitNH3͘Poultry

3emissionrates substrate. ThepresenceofsubstratesforP.marginataandT.molitorinthisstudy correspondedwithlowerNH3 exchangeinthecontainerisinhibitedbythesubstrateandthereforelessemission ofNH3wasmeasured.However,itcouldalsobethatthesespeciesproduceless

NH3.

AllinsectspeciesinthisstudyproducedmuchloweramountsofNH3 (3.0to5.4mg/kgBM/dayfor andB.dubiaͿthan

speciesandtowhatextentNHϯ frameisused.

Conclusions

bothGHGandNH3

62 emissionsofedibleinsectspeciesismostrelevantwhenbasedonCO2 ofmassgain.InthatwayĂcomparisonoftheselectedspecieswitheachother

thandocumentedforpigswhenexpressedperkgofmassgainandonlyaround 1%oftheGHGemissionforruminants.

ThemeasuredNH3emissionlevelsofallinsectspeciesinthisexperimentwere lowerthanreportedNH3

livestock,whileCO2

ThisstudythereforeindicatesthatinsectscouldserveasĂmoreenvironmentally

GHGandNH3emissions.completelifecycleanalysisforspeciesofedibleinsects 3

Acknowledgements

TheauthorswouldliketothankJeanSlangenoftheWUREnvironmentalSciences Groupforhishelpwiththeanalysisofnitrousoxide.Thecommercialrearing ofthismanuscript.

63 Chapter3

64 Table2:CO2

Species CO2(g/kgBM/day) CO2(g/kgmassgain) ADG(%) Pachnodamarginata(n=4) 50ц22a a 4.0ц2.1%a Tenebriomolitor(n=4) 61ц9b 1,031ц349b 7.3ц2.5%b 19ц3c 337ц51c 6.1ц0.7%c d a 7.2ц3.4%b Locustamigratoria(n=6) 110ц21e 734ц119d 19.6ц2.1%d Pigs  3.2ц0.53% 0.3ц0.07% BMсBodyMass ADGсAveragedailygain 3

65 Chapter3

66 3

67 Chapter3

Table5:CO2 b)     Species b=0.67 b=0.75 Pachnodamarginata(n=4) 7 11 17 Tenebriomolitor(n=4) 3 7 12 2 4 6 4 14 Locustamigratoria(n=6) 9 17 29 Pigs 63 50 41 50 31 21

Table6:CalculatedCO2 perkgofanimalbodymass.

Species ŐCO2/kgBMofinsect Pachnodamarginata 46.2 92.46% Tenebriomolitor 2.2 0.4 2.31% 0.9 1.34% Locustamigratoria 3.3 3.04%

68 3

69

Chapter4

Environmentalimpactofthe humanproteinsourceʹlifecycle assessment

D.G.A.B.OonincxandI.J.M.deBoer

Publishedin: PLoSOne7:e51145. Chapter4

Abstract

sustainablesourceofanimalprotein.However,fewexperimentaldataregarding

fromeithermilk,chicken,porkorbeefresultinhighergreenhousegasemissions, demonstratesthatmealwormsshouldbeconsideredĂmoresustainablesourceof edibleprotein.

Keywords: edibleinsect,mealworm,Tenebriomolitor͕Zophobasmorio

72 Thedemandforfoodofanimaloriginisrisinggloballyandisexpectedtoincrease

Steinfeld2012).Currently,thelivestocksectorusesabout70%ofallagricultural land(Steinfeldetal.2006;Foleyetal.2011)andisresponsibleforabout15%of thetotalemissionofanthropogenicgreenhousegas(GHG)(Steinfeldetal.2006; sourceofGHGemissions(Steinfeldetal.2006;Pan,Birdseyetal.2011)andoneof

Variousauthorshavesuggestedinsectsasanenvironmentallymorefriendly

4

GHGemissions,andotherenvironmentalparameters,suchaslandorfossil

hasbeenusedforvariousanimalproducts(deVriesetal.2010).Although livestockarewidespread,toourknowledge,ĂLCAofanyinsectspeciesusedas twotenebrionidspecies,viz.theYellowmealworm(TenebriomolitorͿandthe Superworm(Zophobasmorio sourcesofanimalprotein,suchasmilk,chicken,porkandbeef.

73 Chapter4

Materialsandmethods

assesseduptothemomentthatthefreshproductleavesthefarmgate.

T. molitor Z.morio43%)andtheaveragepercentageofreportedcrudeprotein T.molitor53%;Z.morio45%)(Bernardetal.1997;Barkeret areconsumedbyhumansasthewholeanimal.Proteincontent(Smil2002;FAO andotherfactors.InthisstudyweusedthedatareportedbydeVriesetal.(2010).

2 2 2͕CH4͕andN2K emissions.TheconversionfactortoCO2 2͕25forCH4 2K (IPCC2007).Landusewasexpressedinm2peryear,andfossilenergyuseinmega

mealwormspecies(Figure1).ThedietconsistedoffreshcarrotsandĂmixed grainfeed(i.e.wheatbran,oats,soy,ryeandcornsupplementedwithbeer

74 bydividingtheamountofconcentratesusedbytheamountoflivemealworms produced. Eggcartonsareusedtoincreasethesurfaceareafortheadult mealworms.Fortheenvironmentalimpactoftheeggcartons,dataforrecycled

fromtheDutchpowergrid. regardingGWP,EU,andLU(Table1)werebasedonEcoinvent(Ecoinvent2004) andnewdatafromtheDutchanimalfeedindustry(BlonkandResearch2011). naturalgas,electricityandwater. TheLUofthefarmandthedirectGHGemissionsfromthemealworms wereaddedtothisdata.DirectGHGemissionforZ.morioandT.molitorwere 4

Finally,thetotalGWP,EU,andLUweredividedbykgoffreshmealworm,

Results

2.

TheGWPofonekgoffreshmealwormswas2.7kgofCO2 theuseofelectricity. TheEUofonekgoffreshmealwormswas34MJ,ofwhich31%results theuseofelectricity.

75 Chapter4

TheLUofonekgoffreshmealwormswas3.6m2

Whenexpressedperkgofedibleprotein(Figure2)theGWPwas14kg 2 ofCO2 remainthesame.

Discussion

withotherfoodsourcesofanimalorigin.

beefarecausedbythreemainfactors;1)entericCH4

MealwormsdonotproduceCH4(Oonincxetal.2010b)andhaveĂhigh T.molitorand1500 eggsinoneyearforaZ.morio isshort;T.molitorreachesadulthoodin10weeksandZ.morioin3.5months (Friederichetal.2004). forthemealwormsinthisstudy(2.2)wassimilartovaluesreportedforchicken

improvementisexpectedtobehigherformealwormscomparedtothemore

nostandardmethodforprocessingandstoring. Weassessedthreeindicatorstoprovideinsightinthesustainabilityof

76 Mealworms,beingpoikilothermic,dependonsuitableambienttemperatures larvaeinthissystemproduceĂsurplusofmetabolicheat,whichcouldbeusedto

4 al.2011;Panetal.2011).SlowingdowntheexpansionofagriculturallandisĂ

Conclusions porkandbeef.However,mealworm,whenconsideredasĂhumanproteinsource,

77 Chapter4

Acknowledgements

TheauthorskindlyacknowledgeRolandandMichelvandeVenforproviding

Flowsenteringthecompanyareon

78 4

Figure2:Environmentalimpactofmealwormscomparedtootheranimalproducts. edibleprotein.Resultsfromthisstudydepictedingreen.Minimum(blue)andmaximum

79 Chapter4

Table1:Resourceuseperyearandenvironmentalimpact. (GWP),energyuse(EU)andlanduse(LU)areexpressedperunitofinputbasedon

2 Resource TurnoverͬYear GWPkgCO2 EUMJ LUm Carrots(kg) 260000 0.12 0.16 Mixedgrains(kg) 0.51 4.79 1.39 Eggtrays(kg) 262 13.70 0.10 Gas(MJ) 0.07 1.20 0.00 Electricity(MJ) 0.20 3.17 0.00 Water(M3) 211 0.32 5.55 0.04 Animal(kg) 0.01 0.00 0.00 Farm 1 0 0.00

Absoluteand

2  GWP(kgCO2 EU(MJ) LU(m )  Carrots(kg) 14.27% 4.31 0.51 14.39% Mixedgrains(kg) 1.11 10.47 31.09% 3.03 Gas(MJ) 0.70 26.26% 11.71 34.77% 0.00 0.02% Eggtrays(kg) 0.00 0.12% 0.04 0.13% 0.00 0.01% Electricity(MJ) 0.45 17.06% 7.13 21.17% 0.01 0.24% Water(M3) 0.00 0.03% 0.01 0.04% 0.00 0.00% Animal(kg) 0.01 0.29% 0.00 0.00% 0.00 0.00% Farm 0.00 0.00% 0.00 0.00% 0.01 0.20% Total 2.65 100.00% 100.00% 3.56 100.00%

80 4

81

Chapter5 crudeproteincontentandlipid ondietscomposedoforganicby- products

D.G.A.B.Oonincx,S.vanBroekhoven,A.vanHuis,andJ.J.A.vanLoon Chapter5

Abstract

bodymass.Therefore,insectsmightbeĂfoodand/orfeedsourcewithlow





YellowmealwormsandHousecricketswassimilartothatreportedforpigs.Onthe

Keywords:

84 Fourspeciesonorganicby-products

Severalinsectspeciescanbeproducedforfoodand/orfeed(Bondariand

andarableland(Steinfeldetal.2006;Steinfeld2012).ForĂlargepart,these indicatorsofenvironmentalimpactaredeterminedbytheamountoffeedused

variables,fourinsectspecies,twoedibleforhumansandtwosuitableasanimal feed,wereselected. environmentalimpactofthisprocessisallocatedtothevariousproducts,which 5 productsarebecomingincreasinglyimportantfeedingredients(Wilkinson2011).

85 Chapter5

Materialsandmethods

Insects

( dubia (L.); Tenebriomolitor(L.);Coleoptera: Tenebrionidae),andtheHousecricket( (L.);Orthoptera: Gryllidae)͘Adult maintainedattheLaboratoryofEntomology,WageningenUniversity.Thesetwo specieshadbeenrearedonchickenfeedforoverfouryears(Opfokmeelfarmfood, wereprovidedbyKrecaV.O.F.(Ermelo,TheNetherlands).Forallspecies,larvaeor nymphswererandomlyallocatedtocontrolandexperimentalgroupswithin24 hoursofegghatch( andH.illucensͿorbirth(B.dubia).

wereselected:beetmolasses(RoyalCosun,Breda,TheNetherlands),potato steampeelings(HedimixBV,Boxmeer,TheNetherlands),spentgrainsand

theseingredientsfourexperimentaldiets;witheitherĂhigh,orĂlowprotein content(HPorLP),andĂhigh,orĂlowfatcontent(HForLF)wereformulated (Table1).DietsweremixedinĂMagimixCS5200foodprocessor(MagimixLTD,

(Deurne,TheNetherlands)providedthesecondcontroldietforYellowmealworms

86 Fourspeciesonorganicby-products

(TM2).ForBSFsthechickenfeeddietusedfortheBSFcolonyattheLaboratoryof EntomologyofWageningenUniversity(Wageningen,TheNetherlands)servedasĂ

Experimentalsetup

 placedinthecontainertoprovideĂhidingplaceforthenymphs.Nymphswere providedwithfourgramsofeitheranexperimentaldiet,orcontroldiet(BD). inĂcornerofthecontainer. OnehundredBSF wereprovidedwithfourgramsofeitheranexperimentaldiet,orcontroldiet(HI). Foreachgramofdiet,approximatelytwomlofwaterwasaddedbymeansofĂ syringe.  ofeitheranexperimentaldietorĂcontroldiet(TM1orTM2).Insomerearing experimentalandcontroldiet.ForthelarvaethatwereallocatedtoĂtreatment  5 andϯcmindiameter)wereplacedineachcage.Nymphswereprovidedwithone gramofeitheranexperimentaldietorcontroldiet(AD).Furthermore,Ăwater dispenser(GebroedersdeBoon,Gorinchem,TheNetherlands),withĂpieceof

Foreachspecies,sixreplicatecontainersperdietarytreatmentwereset

morewasaddedtoensureadlibitumfeeding.WaterfortheHousecricketswas

87 Chapter5

wasobserved.Thismomentwaschosenbecausemostspecimenspercontainer wouldbeexpectedtobeintheirlastlarvalornymphalstage,whichiswhenBSFs andYellowmealwormsarenormallysold,andwhenHousecricketshavethe

Chemicalanalysis

Nitrogen(N)andphosphorus(P)contentofthediets,insectsandfaeces andKryskalla(2003),andWcontentaccordingtoRowlandandHaygarth(1997).

allprovidedfeedhadbeeningested.BoththeFCRandtheECIcanbecalculated isexpressedonĂDMbasis.FCRsforconcentrates(feedswithĂhighnutrient density)excludetheweightofprovidedcarrots.

calculatedastheamountofEintheinsectsatthemomentofharvest,dividedby bythetotalweightofdietprovided.

88 Fourspeciesonorganicby-products

performedusingSPSS19.0.

Results

carrots,usedasĂsourceofmoistureformealwormsinthecarrot(C)treatments,

TFA;Table3).ThemainFAintheHPLFdietwasC13:0(62%ofTFA).Inthecontrol

 5 highestECIofallspecies.BoththisspeciesandtheBSFsgenerallyhadlowFCRs andconcomitantlyhighECIscomparedtotheothertwospecies.TheBSFstended

BSFs.ProvisionofcarrotincreasedFCRsontheLPdiets,andECIsonalldiets.For Housecrickets,FCRsdidnotvaryduetodietarytreatment.TheirFCRsweresimilar tomealworms,buttheECIoftheHousecricketswasthelowestofthespecies

89 Chapter5

lowerontheHPHFdietthanontheADdiet(23vs.41%).

diet,thesurvivalratewasmuchlowerthanontheHPHFdiet(47vs.

survival(>20%).ForHousecrickets,survivalratewaslowonalldiets,exceptfor ontheHPHFandBDdiets,whilethiswasprolongedtoalmosttenmonthsonthe

withlowerDMpercentagesondietswithcarrots.ForHousecricketstheDM contentwaslowerthanfortheotherspecies(~25%). andHousecricketshadhigherCPcontents.OntheHPLFandBDdiets,CPcontent theHPHFandLPLFdietsresultedinintermediateCPcontents.ForBSFs,CP contentwaslessvariable,althoughontheHPHFdietCPcontentwashigherthan ontheLPdiets.ForYellowmealworms,CPcontentwassimilaronmostdiets.

90 Fourspeciesonorganicby-products

However,theLPHFdietsupplementedwithcarrot,resultedinĂlowerCPcontent crickets,dataonCPwereavailableonlyfortheHPHFandADdietwhichresulted

(Rс0.546;Wс0.001),butthiswasnotshowninHousecrickets(Pс0.11).

ForthisspeciesthelowestWcontentwasfoundontheLPHFdiet.TheWcontentof BSFontheHIdietwassimilartoHPdietsbuthigherthanthoserearedonLPdiets. whensupplementedwithcarrots.

comparedtotheotherdiets.ForBSFstheTFAcontentdidnotvaryoverdietary treatments,andvalueswereinthesamerangeasforYellowmealworms.Forthe

TFAcontentthantheHPLFdietandtheHPdietssupplementedwithcarrot.House

(Figure1). limitedamountofsample,FAdataonHousecricketsisavailableforonlythree 5 waspresentinallinsectsamples,inBSFstheycontributedbetweenĂthirdtohalf

InHousecricketsC20:3n3contributed0.4%toTFAonthethreediets analysed,andC22:6n3contributed0.1%toTFAontheHPdiets,whereasthese

91 Chapter5

FAswerenotdetectedinotherspecies(Datanotshown).Furthermore,both HousecricketsonHPHF,andBSFsonLPHFcontained0.1%C20:5n3,whileinthe otherspeciesthisFAwasnotdetected.

Discussion

addedvaluewould,however,stronglydependonwhethertheirdietcouldalsobe wouldbeusedbytheseanimals.TheFCRforconcentratesofYellowmealworms commerciallyproducedmealworms(2.2)providedwithcarrots(Oonincxetal. 2012a).TheseFCRs,andtheFCRofHousecricketsontheADdietaresimilarto

92 Fourspeciesonorganicby-products

2011).WithĂ50%increaseindemandofanimalbasedproteinexpectedby

HPdietsresultedinlowerFCRsandhigherECIsformostspecies.However,inthe

PeriplanetaamericanaͿproducemethane bymeansofendosymbionts(Hacksteinetal.1994;Oonincxetal.2010b).The cockroachendosymbiont convertsnitrogenouswasteproducts,

ThehighwatercontentofcarrotsmightbeexpectedtoincreasetheFCRforall periodsofcarrotprovision,andhencetheprovisionoflargeramountsofcarrot. ourtreatments,comparedtotreatmentswherenocarrotwasprovided.More whenĂsourceofwaterwasprovided(Fraenkel1950).Withoutcarrots,Yellow 5 mealwormFCRsweresimilartothoseofHousecrickets.PublishedFCRvalues comparedtoourresults.Furthermore,theirlowDMcontentresultinthelowest ECIsofthespeciesstudied,whichwerealsolowcomparedtoliteraturevalues

itcouldalsobeduetoĂdensovirus(AdDNV),presentinmostEuropeanand

Szelei,Woodringetal.2011;Pham,Yuetal.2013).

93 Chapter5

arestronglycorrelated.Whereasalldietswereacceptedbythefourspecies,

etal.1959;Diener,Zurbruggetal.2009).ThisissimilartoourHPHFandHIdiet,

TMdietswereintermediary.ThissuggeststhatproteincontentisĂdetermining factorfordevelopmentandsurvival.furtherfactorcouldbetheinclusionof containsimportantgrowthfactorsforYellowmealworms(Fraenkel1950). andHPHFdietsweresimilartothosereportedbyUrsandHopkins(1973b) wasprovidedasĂwatersource.Theincreasesinsurvivalandshorteningof theseparameters(Cohen2003).

otherdiets.Furthermore,survivalrateswerelowinthisspeciesonalldiets,with

94 Fourspeciesonorganicby-products

CrudeproteinandTFAcontentvariedbetweenspeciesanddependedon thediet.BSFsandYellowmealwormshadĂlowCPcontentandhadconsiderable

lowerCPcontentandĂhighTFAcontent.InAmericancockroachesuricacid (whichcontainsN)isstoredwhenprovidedwithhighproteindiets(Mullinset

muchlargerthanintheotherthreespecies.ForthosethreespeciesCPandTFA contentswerewithinpublishedvalues,however,theWcontentofBSFswerelower,

AlthoughCPandWcontentwerecorrelatedwithinĂspecies,theywere mostdietshigherCPcontentscoincidedwithhigherWcontents,thiscouldalso betweenCPandP. 

5 chainaresuggestedtopredominateinDipterans(Fast1970),however,inthe BSFsinthisstudyC12:0wasdominant.AlsoC14:0waspresentinhigherlevels

metabolizedtoC12:0whenloweramountsoffatareprovided,whereasFAsare

95 Chapter5

diet.

fairlyconstant.

AD,

oftheseFAsintheHPLFtreatmentmighthavecausedtheprolongeddevelopment andlowsurvivalonthatdiet.Onthethreedietarytreatmentsanalysed,Ăsmall

(~0.1%ofTFA).TheseFAswerenotdetectedintheotherspeciesanalysed,orin

denovosynthesisofC20:3n3andC22:6n3,is new.

monogastricanimalsitcanbealteredthroughdiet(Koubaetal.2011).Similarly,

96 Fourspeciesonorganicby-products

Conclusions

Acknowledgements

provisionofinsectsandinsectfeed.

5

97 Chapter5

Table1:Inclusionpercentageoffeedingredientstoexperimentaldiets

Spent Beer Cookie Potatosteam Beet Diet grains yeast remains peelings molasses Bread HPHF 60% 20% 20% HPLF 50% 30% 20% LPHF 50% 50% LPLF    30% 20% 50%

98 Fourspeciesonorganicby-products

Table2 DM)ofdietswithhigh(HP)andlow(LP)protein,andhigh(HF)andlow(LF)fatcontents. Diet DM% Protein(%DM) Phosphorus(%DM) HPHF 95.0% 21.9 9.5 0.56 HPLF 95.1% 22.9 1.0 0.53 LPHF 12.9 14.6 0.22 LPLF 14.4 2.1 0.21 TM1 17.5 4.9 0.25 TM2 17.1 4.2 0.54 AD 17.2 4.0 0.66 HI 90.0% 19.1 3.5 0.67 BD 2.7 0.60 Carrot 9.1% 5.9 1.6 0.25 Controldietsfor:Tenebriomolitor(TM), (BD), (AD),and (HI)

5

99 Chapter5

100 Fourspeciesonorganicby-products

5

101 Chapter5

102 Fourspeciesonorganicby-products

Table5: acids(TFA),of (BD), (HI),Tenebriomolitorwithout(TM)

Species Diet DM(%FM)  CP(%DM)  W(g/kgDM)  TFA(%DM)  BD HPHF 32.7ц2.72 ab 60.7ц1.59 a 6.0ц0.16 a 19.6ц0.59 ab HPLF 33.7ц1.53 bc 72.5ц1.25 b a ab LPHF c 37.5ц0.99 c b 40.2ц2.69 c LPLF 27.6ц1.71 a d a 20.5ц0.30 b  BD 31.6ц1.36 ab b 6.2ц0.45 a a HI HPHF a 46.3ц0.93 a ab a HPLF 35.6ц2.45 a 43.5ц3.00 ab ab a LPHF 35.1ц1.97 a b 6.7ц1.34 a a LPLF 35.3ц2.36 a b 6.4ц0.32 a 33.5ц3.17 a  HI a ab 9.7ц1.13 b 25.4ц3.99 a TM HPHF 41.5ц0.37 a 53.6ц0.45 b ab 26.5ц1.10 ab HPLF 36.7ц3.65 abc 53.5ц1.25 b ab 23.0ц1.31 a LPHF 37.2ц2.76 abc ab LPLF ab 47.5ц1.26 ab ab abc TM1 ab 52.4ц0.36 b 9.7ц0.26 b 27.0ц1.02 ab  TM2 39.2ц1.27 ab 49.2ц1.01 ab 7.7ц0.40 a 30.9ц0.37 bc HPHF 32.3ц2.90 cd 51.3ц1.09 b ab 22.6ц1.36 a HPLF bcd 53.3ц1.13 b ab 23.6ц1.59 a 5 LPHF bcd a ab 27.2ц0.99 ab LPLF 30.2ц1.29 d ab 7.9ц0.06 ab ab TM1 35.0ц2.05 bcd 50.4ц1.94 b 9.2ц0.27 ab ab  TM2 36.0ц0.96 abc ab 7.9ц0.24 ab 34.5ц3.27 c AD HPHF 25.7ц2.67 a a a a HPLF a LPHF 25.1ц5.24 a LPLF a  AD 24.1ц1.52 a a a 17.4ц1.61 a

103 Chapter5

Table6: Species Diet C14:1 C16:0 C16:1 BD HPHF 0.1ц0.02 a 17.7ц1.04 a 1.0ц1.34 a 1.6ц1.39 a HPLF 0.0ц0.04 b 21.6ц0.37 b 0.2ц0.02 a b LPHF 0.2ц0.02 c 22.2ц0.62 b 0.2ц0.00 a b LPLF 0.1ц0.02 b 20.9ц0.37 b 0.2ц0.01 a 7.7ц1.46 b  BD 0.0ц0.01 b a 0.2ц0.04 a a HI HPHF 0.4ц0.01 a 17.0ц0.16 a 0.5ц0.06 ab 2.9ц0.21 a HPLF 0.9ц0.10 b b 0.1ц0.03 c 6.6ц0.90 b LPHF 0.6ц0.04 c 14.4ц1.74 ab 0.6ц0.21 b 3.4ц0.11 ac LPLF 0.7ц0.03 c 11.6ц1.24 b 0.2ц0.01 ac 4.7ц0.51 c  HI 0.3ц0.01 a 12.7ц0.91 b 0.2ц0.02 ac 3.4ц0.06 ac TM HPHF 0.0ц0.00 ab 15.5ц0.33 a 1.1ц0.05 ab 2.0ц0.01 ab HPLF 0.0ц0.01 cd 17.2ц0.24 bcd 1.1ц0.06 ab 2.9ц0.17 c LPHF 0.0ц0.00 b 16.4ц0.57 abc 1.1ц0.09 b 1.4ц0.05 d LPLF 0.0ц0.00 cde 16.6ц0.29 abcd 0.9ц0.03 abcd 1.7ц0.11 abd TM1 0.0ц0.00 cde 16.0ц0.36 ab 0.7ц0.05 cdef abd  TM2 0.0ц0.00 cde 15.3ц0.23 a acdef 2.1ц0.10 b HPHF 0.1ц0.00 f 20.2ц0.29 e 0.6ц0.04 ef 1.7ц0.04 abd HPLF 0.0ц0.01 cde d 0.9ц0.02 abcdf c LPHF 0.0ц0.00 ad bcd 1.0ц0.14 abd 1.6ц0.19 ad LPLF 0.0ц0.01 ce 17.7ц0.20 cd cdef 2.0ц0.16 b TM1 0.0ц0.00 e 17.4ц0.36 bcd 0.6ц0.09 ef 1.7ц0.07 abd  TM2 0.0ц0.01 ce 16.4ц0.14 abc 0.7ц0.03 cef 1.9ц0.07 ab AD HPHF 0.1ц0.01 a a 0.3ц0.04 a 1.5ц0.16 a HPLF 0.0ц0.04 b a 0.4ц0.21 a a LPHF LPLF  AD 0.0ц0.00 b 25.1ц0.42 a 0.3ц0.03 a a

104 Fourspeciesonorganicby-products

Table6: (BD), - cens(HI),Tenebriomolitor (AD),

Species Diet C10:0 C12:0 C13:0 C14:0 BD HPHF 0.0ц0.04 a 0.3ц0.09 a 3.1ц0.09 ab 2.6ц0.20 a 0.1ц0.01 ab HPLF 0.0ц0.00 a 0.2ц0.04 b ad 1.7ц0.13 b 0.0ц0.03 c LPHF 0.0ц0.00 a 0.5ц0.03 c 1.5ц0.10 c 3.9ц0.07 c 0.1ц0.01 a LPLF 0.0ц0.00 a 0.2ц0.01 b 2.9ц0.06 b 1.4ц0.09 bd 0.1ц0.01 abc  BD 0.0ц0.00 a 0.2ц0.04 b 4.0ц0.37 d 1.1ц0.07 d 0.1ц0.01 bc HI HPHF 0.7ц0.09 a a 2.4ц0.04 a 7.4ц0.16 a 0.0ц0.02 a HPLF 1.3ц0.07 b bc 2.4ц0.37 a 9.5ц0.36 b 0.0ц0.01 a LPHF a ab a a 0.2ц0.02 b LPLF 1.2ц0.04 b c a 9.0ц0.14 b 0.0ц0.01 a  HI 0.9ц0.15 a 46.6ц1.52 bc 2.4ц0.39 a 9.2ц0.35 b 0.1ц0.02 c TM HPHF 0.0ц0.00 a 0.3ц0.01 a 2.3ц0.09 a abcde 0.1ц0.02 ab HPLF 0.0ц0.00 a 0.5ц0.25 a 2.7ц0.16 a 4.9ц0.12 abc 0.2ц0.04 abc LPHF 0.0ц0.00 a 0.3ц0.06 a 3.3ц1.30 a 5.5ц0.54 c d LPLF 0.0ц0.00 a 0.3ц0.03 a 2.1ц0.05 a abcd 0.4ц0.03 ce TM1 0.0ц0.00 a 0.4ц0.02 a 2.2ц0.09 a 4.7ц0.12 abcde 0.1ц0.01 ab  TM2 0.0ц0.00 a 0.3ц0.03 a 2.0ц0.04 a 4.4ц0.29 abde 0.5ц0.11 e HPHF 0.0ц0.00 a 0.3ц0.03 a 2.7ц0.15 a 4.7ц0.23 abcde 0.1ц0.01 a HPLF 0.0ц0.00 a 0.3ц0.02 a 2.6ц0.16 a 3.7ц0.03 de 0.2ц0.00 ab LPHF 0.0ц0.00 a 0.4ц0.06 a 2.2ц0.10 a 5.1ц0.43 bc 0.5ц0.01 e LPLF 0.0ц0.00 a 0.3ц0.01 a 2.4ц0.23 a 3.9ц0.17 ade 0.3ц0.03 bc 5 TM1 0.0ц0.00 a 0.3ц0.02 a 2.4ц0.12 a 3.6ц0.40 e 0.1ц0.04 ab  TM2 0.0ц0.00 a 0.3ц0.05 a a abde 0.2ц0.01 abc AD HPHF 0.0ц0.00 a 0.2ц0.04 a 2.9ц0.44 a 2.5ц0.22 a 0.1ц0.01 a HPLF 0.0ц0.00 a 0.1ц0.13 a a 1.4ц1.46 a a LPHF LPLF  AD 0.0ц0.00 a 0.1ц0.03 a 3.5ц0.35 a 0.7ц0.03 a 0.0ц0.00 a

105 Chapter5

Table6: Species Diet CLA9c11tr C20:4n6 C24:1 BD HPHF a 1.1ц0.10 a 0.7ц0.04 a ab 0.1ц0.07 a HPLF 1.7ц0.13 b 0.3ц0.02 b 0.0ц0.01 b 0.0ц0.02 a 0.0ц0.00 a LPHF 7.3ц0.17 c 0.4ц0.01 b 1.0ц0.01 c 0.1ц0.01 ab 0.0ц0.00 a LPLF 7.0ц0.17 c 0.7ц0.03 c 0.0ц0.00 b 0.1ц0.02 ab 0.0ц0.00 a  BD a c 0.1ц0.01 d 0.2ц0.01 b 0.0ц0.04 a HI HPHF 17.1ц0.35 a 1.5ц0.02 a 0.3ц0.01 a 0.2ц0.01 a 0.0ц0.00 a HPLF 3.6ц1.59 b 0.6ц0.17 b 0.0ц0.05 b 0.6ц0.16 b 0.0ц0.00 a LPHF cd bc 0.3ц0.03 a 0.1ц0.01 a 0.0ц0.00 a LPLF 6.0ц0.62 bc 1.0ц0.11 c 0.0ц0.00 b 0.1ц0.03 a 0.0ц0.00 a  HI 9.4ц0.56 d b 0.0ц0.01 b 0.0ц0.00 a 0.5ц0.92 a TM HPHF ab a 0.2ц0.00 a 0.3ц0.04 a 0.0ц0.00 a HPLF c 0.1ц0.02 b 0.0ц0.00 b b 0.1ц0.05 b LPHF 16.3ц0.62 de 0.2ц0.03 bc 0.2ц0.03 ac 0.0ц0.00 c 0.0ц0.00 a LPLF 17.5ц0.64 ef 0.4ц0.06 cd 0.0ц0.01 b 0.0ц0.02 c 0.0ц0.00 a TM1 25.5ц0.26 ab 0.9ц0.02 a 0.0ц0.00 b 0.0ц0.00 c 0.1ц0.02 abc  TM2 24.5ц0.46 a 0.5ц0.07 de 0.0ц0.00 b 0.0ц0.01 c 0.0ц0.00  HPHF 21.3ц0.06 fg 0.9ц0.02 a 0.2ц0.02 ac 0.3ц0.02 a 0.1ц0.01 bc HPLF 14.0ц0.47 cd 0.2ц0.01 bc 0.0ц0.00 b b 0.1ц0.02 bc LPHF e 0.3ц0.02 bcd 0.2ц0.02 c 0.0ц0.01 c 0.0ц0.00 a LPLF 19.2ц0.24 ef 0.5ц0.04 de 0.0ц0.00 b 0.0ц0.00 c 0.0ц0.01 a TM1 b 1.3ц0.17 f 0.0ц0.00 b 0.0ц0.03 c 0.1ц0.02 ac  TM2 23.9ц0.31 ag 0.7ц0.01 ae 0.0ц0.00 b 0.0ц0.00 c 0.0ц0.04 a AD HPHF 30.1ц1.19 ab 1.5ц0.10 a 0.4ц0.03 a 0.0ц0.03 a 0.1ц0.03 a HPLF 23.6ц6.30 a 0.4ц0.14 b 0.1ц0.25 a 0.0ц0.02 a 0.0ц0.00 b LPHF LPLF  AD 34.9ц1.12 b 1.2ц0.09 c 0.1ц0.04 a 0.0ц0.00 a 0.1ц0.01 a

106 Fourspeciesonorganicby-products

Table6 Species Diet BD HPHF 6.5ц0.26 a 0.7ц0.07 a 42.5ц0.91 a 0.5ц0.03 a HPLF 4.2ц0.07 b 0.0ц0.03 b b 0.2ц0.01 b LPHF 3.7ц0.32 b 0.3ц0.31 ab c 0.4ц0.00 c LPLF 4.4ц0.61 b 0.0ц0.02 b 53.1ц1.17 d 0.3ц0.02 d  BD 7.7ц0.44 c 0.1ц0.03 b c 0.4ц0.01 ac HI HPHF a 0.2ц0.04 a 15.9ц0.32 a 0.3ц0.02 ab HPLF 2.0ц0.05 a 0.0ц0.02 b b 0.5ц0.07 b LPHF a 0.2ц0.04 a a 0.2ц0.04 c LPLF a 0.0ц0.00 b 10.3ц0.95 b 0.2ц0.07 ac  HI 2.1ц0.23 a 0.0ц0.00 b 10.2ц0.30 b 0.7ц0.04 d TM HPHF 3.1ц0.06 a 0.1ц0.02 a 43.1ц0.61 ab 0.2ц0.01 ab HPLF 4.1ц0.36 ab 0.0ц0.00 b 51.7ц1.25 c 0.1ц0.01 c LPHF 4.0ц0.50 ab 0.1ц0.03 ac 49.5ц0.41 cde 0.1ц0.01 c LPLF 4.0ц0.02 ab 0.0ц0.00 b cde 0.1ц0.01 c TM1 3.5ц0.21 ab 0.0ц0.00 b 43.0ц0.60 abf 0.2ц0.03 a  TM2 a 0.0ц0.01 bc 45.4ц0.23 bg 0.2ц0.02 a HPHF 4.4ц0.13 b 0.2ц0.03 d 40.3ц0.33 af 0.3ц0.01 b HPLF 4.0ц0.07 ab 0.0ц0.00 b 51.5ц0.62 ce 0.1ц0.02 c LPHF ab 0.0ц0.03 bc deh 0.1ц0.01 c LPLF 3.7ц0.23 ab 0.0ц0.00 b gh 0.1ц0.01 c TM1 3.3ц0.34 a 0.0ц0.00 b 40.1ц1.56 f 0.3ц0.04 ab  TM2 3.2ц0.06 a 0.0ц0.00 b bgh 0.2ц0.02 ab AD HPHF a 0.5ц0.03 a 24.6ц1.51 a 0.5ц0.03 a 5 HPLF ab 0.3ц0.34 ab 26.9ц6.30 a 0.4ц0.10 a LPHF LPLF  AD 7.9ц0.27 b 0.2ц0.05 b 23.6ц0.90 a 0.4ц0.05 a

107 Chapter5

Table7: tein,andhigh(HF)andlow(LF)fat,andcontroldietsprovidedto ͕Herme- ͕Tenebriomolitor(withoutandwithcarrot),and ͘ Treat Tenebrio Tenebriomolitor Acheta ment Diet dubia illucens molitor withcarrot HPHF 10.7 16.2 11.1 32.1 23.7 15.3 HPLF 4.9 7.2 102.1 66.0 29.0 LPHF 13.5 9.1 79.1 57.7 LPLF 6.2 10.4 6.1 40.6 35.4  TM1 11.1   26.6 20.9 TM2 13.5   45.2 32.4  AD 16.4 22.2 HI 20.1 15.1 BD 14.5 22.1 Carrot      Controldietsfor:Tenebriomolitor(TM), (BD), (AD), and (HI)

108 Fourspeciesonorganicby-products

5

109 Chapter5

110 Fourspeciesonorganicby-products

5

Figure1: (A), (B),Tenebriomolitorwithoutcarrot(C),Tenebriomolitorwithcarrot(D) and

111 Chapter5

Figure2 (BD), illucens(HI),Tenebriomolitor(TM),and

112 Fourspeciesonorganicby-products

5

113

Chapter6

manure

D.G.A.B.Oonincx,A.vanHuis,andJ.J.A.vanLoon Chapter6

Abstract

Anexperimentwasconductedtocomparethesuitabilityofchicken,pig,andcow (L.);Diptera:

vs. whiletheECIforphosphoruswashighestoncowmanure.Substratenitrogen contentdecreasedinchickenmanure,butwerestableinpigandcowmanure.

larvae,allowingmorerapiddevelopment.

Keywords:

116 nitrogen(N)andphosphorus(P)intheformofmanureandurine.Concomitant ammonia(NH3 nutrientscontainedinfeedareexcretedasmanure(Steinfeld2012).Innatural systems,manureandotherdecayingorganicmaterialsarebrokendownby

(

Elwert,Knipsetal.2010;Sealeyetal.2011).AsĂdietingredient,BSFlarvaeand

etal.2006;FAO2012),whichisexpectedtoleadtofurtherpriceincreases.IfBSF asanimalfeed,thiscoulddecreasetheenvironmentalimpactofthelivestock sector.Furthermore,thiswoulddecreasetheneedforfeedimports,andthereby thepressureonunsustainablesourcesofdietaryproteincurrentlyused,such 6 comparisonofthesuitabilityofmanuresasfeedforBSFs.Furthermore,these asfeedforBSFlarvae.

117 Chapter6

Materialsandmethods

Freshchicken,pig,andcowmanure(faeces)wascollectedattheanimal

G.R.VeermanBV,Olst,TheNetherlands).

andmixedwithϰmloftapwaterinordertocreateĂdietwithĂwatercontentof andthetopwassealedwithĂlid.EggmasseswerecollectedfromtheBSFcolony maintainedattheLaboratoryofEntomology,WageningenUniversity,Wageningen, TheNetherlands.ThiscolonywasrearedforoverϰyearsonĂchickenfeeddiet of70%,andĂphotoperiodof12h.Onehundredemergedlarvae,lessthan24Ś old,wereplacedinĂcontainer.Thereweresixreplicatesforeachtreatmenti.e.

areconsideredappropriateforthisspecies(May1961;Holmes,Vanlaerhoven duringtheexperiment.photoperiodof12hourswasprovidedbyanarrayof

i.e.more

118 manurewasaddedforlargerlarvaethanforsmallerones.Foreachgramof manureprovidedtothelarvae,approximatelyϮmloftapwaterwasadded.Ifthe

datenoted.Allanimalsfromthatcontainerwereharvestedwithforceps,counted, theirintegumentwereremovedbywashinginĂstandardkitchensieveunder

Todeterminethesurvivalrate,thenumberofliveBSFsattheendofthe

wasdried,weighed,cleanedwithwater,dried,andweighedagain,inorderto inthecontainer.Thefreshweightoftheresidualmaterialinthecontainer,the sampleoftheresidualmaterial,togetherwiththeweightoftheresidualmaterial thatadheredtothelarvae,wasconsideredthetotalresidualmaterial.DM contentofthemanureprovided,thesampledresidualmaterial,andtheBSFyield

6 Chemicalanalysis

Totalnitrogen(N)andtotalphosphorus(P)contentofthemanure, residualmaterial,andharvestedBSFswasanalysedattheChemicalBiological SoilLaboratory(WageningenUR,Wageningen,TheNetherlands)asdescribedby

119 Chapter6 toRowlandetal.(1997).

contentwascalculatedbydividingP2O5contentby2.3.

Results oftheBSFlarvaewashigheronpigmanurethanonchickenmanure(Pс0.019), forBSFlarvaeonchickenandpigmanure,butwhenfedoncowmanurethis waslonger,viz.

(20days).Theyieldonthischickenfeeddietwasalsohigher(11.6Őfreshweight, 4.21ŐDM),aswastheDM%(36.25%).

120 (3.97;Table2).

provided.Itwassimilarintheresidualmaterialfromthechickenandpigmanure manuretreatment(3.06). TheDMweightofthemanurewasreducedby~37%inallthree manure.

Discussion

humidity(Holmesetal.2012),feedavailability(Furmanetal.1959;Dieneretal. manuretypesweresuitableasfeed. However,theBSFlarvaeonoursubstratesreachedtheprepupalstage

6 dietfortendays(Li,Zhengetal.2011),beforetheyreceivedĂmanurediet.In

BSFlarvaerearedondairymanurefromhatching,tookapproximately120days todevelopinprepupae(Sealeyetal.2011).Thesedataindicatethatlarvalage

121 Chapter6 animals(Hansen,Nelssenetal.1993;Gorka,Kowalskietal.2009;Delcroix,

Katz2014).Furtherstudiesshoulddeterminewhichdietshouldbeprovided processing.

asours).Whereastheamountsaresimilartoourstudyweprovidedthistotal offeedleadstolowerECIs(Dieneretal.2009).SimilartoDieneretal.(2009)we changesincolourandtextureoftheresidualmaterial,comparedtothemanure

16%onpigmanurewassuggestedbyNewton,Sheppardetal.(2005).However,

wouldindicatethatĂsurplusoffeedwasprovided.SuchĂsurpluswouldleadto etal.2009).OurEcontentsweresimilartomostpublishedvalues,exceptfor ofthecommerciallyobtainedBSFlarvae.Larvaeshowfeedsearchingbehaviour

larvalEcontents,weassumethatingeneralourfeedingregimeapproximatedad

122 libitum VariablevaluesofprepupalfreshweightofBSFshavebeenreported: manureitwasbetween0.137and0.179Őwhen40%reachedtheprepupal averageweightwassimilarbetweentreatments,butatthelowendoftheabove

studyhadnotyetreachedtheprepupalstage. TheaverageDMcontentoftheBSFsinourstudy(~20%)wasonthelow diets,henceyieldsshouldbereportedbothasfreshanddryweight. publishedvalues(Table5).WhileWcontentreportedbyNewtonetal.(2005)for

vs. themomentofsampling.Furtherstudiesshouldbeconductedtoprovideaccurate weightofBSFlarvae. twomanuretypes(Pс0.002).Inalltreatmentsthesewereatthelowendofthe publishedrange,aspresentedinTable5. Beforedrying,theDMcontentofdairymanurewas12%whichislower thanreferencevaluesforDutchfarms(57.3%),whileDMcontentofpigmanure washigher(34.4vs͘26%)(denBoeretal.2012).Inourstudy,waterwasaddedto 6 atthebeginningoftheexperimentforallthreemanuretypes.Thisislowerthan theexperimentmakesitimpossibletoevaluatethechangeinDM%between themanureandtheresidualmaterial,duetoBSFprocessing.Whilemoststudies withBSFlarvaeonchickenanddairymanurereportincreasedDMpercentages

123 Chapter6

decreasetheDM%ofchickenmanure(AxtellandArends1990).Factorssuchas

Duringourexperiment,thetotalamountofDMwasreducedby~37%.

freshmanure,whereasourshadbeendried.

ChickenmanuregenerallycontainsmoreEthanmanurefromother livestock(Nahm2003).TotalEcontentofthechickenmanureinourstudywas vs.4.47%DM);as wasthecaseforpigmanure(2.55vs͘3.04%DM),andcowmanure(2.74vs͘2.73%

manures. Approximately70%ofEinchickenmanureisintheformofuricacid

experiment.BecausepartoftheEinpigmanureisintheformofammonia(Canh,

vs. rearedonchickenorcowmanure,whichindicatesthatpigmanurecouldbemore Luciliaserricataon

Inourstudy,chickenmanurecontainedlessWthanmanurefrompigs

124 1997;Malley,McClureetal.2005). theresidualmaterialforthethreetypesofmanure.Thiscanbeexplainedbythe ofEintheformofammonia.

i.e.areaswherethe year.InmanyEUmemberstateslessthan170kgtotalEperhacanbeapplied iftheEcontentofĂmanureisassociatedwithanamountofWthatexceeds

Verloop2010).Topreventthis,farmsproducingbothanimalsandcropsprefer

processingbyBSFlarvaecouldenablefarmerstousetheprocessedmanureas 6

125 Chapter6

Conclusions

BSFlarvaecandeveloponthethreemanuretypesstudied.However,their manureprocessingcapacityofthesystem.Furthermore,increasedprocessing measureswouldhelptomakemanureprocessingwithBSFsenvironmentally sound,andeconomicallyviable.

Acknowledgements theirhelpingatheringthetestedmanure.WearegratefulforthehelpofIng T.Zandstrawiththedryingandmillingofthemanure.Furthermore,wekindly

126 Table1 eitherchicken,pigorcowmanure(n=6) Manure Survivalrate(%) Yield(gfreshweight) Chicken a 144.0ц33.12a a Pig 97.0ц4.73b a 6.90ц1.400a Cow ab 214.5ц21.56b 7.43ц1.414a

6

127 Chapter6

128 6

129 Chapter6

130 6

131

Chapter7

Generaldiscussion

D.G.A.B.Oonincx Chapter7

Fundamentalentomologyhasfocusedoninsectmolecularbiology,genomics, biologicalcontrol,plantresistance,integratedpestmanagementanddevelopment

ofthe20th

(LarsenandvonIns2010),buttheincreaseofpapersonentomophagyhassteeply

between2007and2013. Thereasonsforthisincreasedinterestistheurgencytosustainablyrespondtothe increasedprosperityindevelopingcountries,expectedtoleadtoanincreasedper

and5)possibilitytousewasteasfeed. Ithastobetakenintoaccountthatduetothenumberofinsectspecies willgivesomegeneralizedstatementsvalidforĂgreatnumberofspecies.Insect andcows.Thesespecieswereselectedbecausetheyprovidethebulkofanimal proteinintheWesterndiet.

134 Generaldiscussion

Survivalforanimalspeciesdependsonmanyfactors,forinstancethe

presenceofĂdensovirusinthatspecies,whichincreasesmortality(Szeleietal. betweenfourandsevenpercentforchicken(Ross2011),approximatelythree

(Korpelainen1990),aswellasduetothepresenceofcertainsymbionts(Narita, Kageyamaetal.2007;Cordaux,Bouchonetal.2011).InYellowmealwormsthe

described,however,thecauseofthisisnotreported(Gobbietal.2013). 7

135 Chapter7

ThevalueslistedinTableϭshowthatmanyinsectspeciesproducemore

Table1: chicken,pigsandcows

Species Housecricket Yellowmealworm 112 Migratorylocust 90 35

Chicken Pig Cow 5

animalsorhumansthatconsumethem. areabsorbed.Thisdependsonthespecies,itsdevelopmentstage,itschemical

136 Generaldiscussion wasdeterminedinaninvitro

invivotrial

insectspecies.

Thisapproachissuitableifinsects,orevenĂsingleinsectspecies,makeupthe completedietofthetargetspecies.However,ifwetakehumansasanexample, proteinandfat,andtoolowincarbohydrates.Sinceinmostcasestheinsectwill onlybeĂpartofthediet,Ămoreappropriateapproachwouldbetocomparethe purpose.AnexampleofthiscanbefoundinTable2,inwhichthechemical

consideredashighasforbeef.

7

137 Chapter7

Table2 of50ŐDM      YellowMeal House Migratory Dietarycomponent Beef worm Cricket Locust Protein 49.1 66.6 65.0 55.0 Fat 54.1 34.0 63.1 Metabolizableenergy 9.2 11.0 Minerals     Calcium 2.6 4.5 1.1 Phosphorus 76.6 52.2 34.6 Magnesium 30.9 16.1 7.1 Sodium 6.7 20.7 9.5 Potassium 16.3 20.5 12.1 Chloride 15.1 22.7 NA NA Iron 33.5 Zinc 55.7 70.2 51.0 Copper 35.6 44.7 75.1 5.2 Manganese 29.7 NA NA Iodine 15.4 23.5 NA NA Selenium 57.1 53.6 NA Vitamins     VitaminE ND 30.5 NA 2.7 VitaminC 3.2 9.7 NA ND Thiamin 30.0 6.2 NA 410.1 NA 16.9 Pantothenicacid 74.7 NA NA Niacin 29.7 34.6 NA 21.5 Pyridoxine 62.5 22.0 NA Folicacid 103.0 NA 3.7 71.6 50.2 NA NA VitaminB12 35.3 NA Choline 44.0 NA 19.0 VitaminK NA NA NA 2.5 NAсNotavailable.NDсNotdetected.DataadaptedfromGarrowandJames2000;Fin ke2002;FAOandWHO2007;OonincxandvanderPoel2011,andHaytowitzetal.2012.

138 Generaldiscussion

Sustainability

elsewhereinthischapter.

(Oonincxetal.2010b).Fromthat,andpreviousstudies(Hacksteinetal.1994; Egertetal.2003),itisclearthatcertaingroupsofinsects,suchascockroaches, scarabs,andtermites,producemethaneduetobacterialsymbionts.Methane isĂpotentgreenhousegas(GHG),whichcangreatlycontributetotheGlobal

( andlarvaeoftheSunbeetle(PachnodamarginataͿproduce mealworms,whenexpressedperkgofmassgain(Oonincxetal.2010b).Similarly

2 occurbetweeninsectspecies.However,whenexpressedinCO2

7

139 Chapter7

mealworms(Oonincxetal.2012a).IthasĂstrongimpactonGHGemissionsand

isanimportantfactor(Herreroetal.2013a).Itseemsthatininsectsprotein

toreachadulthoodininsects,whereasthelipidcontentisvariable(Oonincxetal. 2011).

andthereforenotaccountedforintheFCR,anFCRlowerthanunityispossible. animalsareprovidedinTable3.ForcowstheFCRispresentedonĂDMbasis forMigratorylocustsishigherthanfortheotherinsectspeciesbecauseitsfeed

Nostudieshavebeenpublishedinwhichthesamedietwasprovided

thattheFCRoftheseinsectsaremostsimilartochicken,onthelowsideofpigs,

140 Generaldiscussion

ForbroilerstheADGisapproximately5.5%(Ross2011),whichissimilartofourof higherADG(19.6%)(Oonincxetal.2010b). Wheninsectsareusedasfoodanotherrelevantfactoristheedible

Table3: chicken,pigsandcows

Species FCR Housecricket Yellowmealworm 100 Migratorylocust 100 Chicken Pig 53 Cow

anddeFoliart(1991)

7

141 Chapter7

“Waste”asfeed

Cerealgrainsareregularlyusedasfeed,however,thesecouldalsobedirectlyused asfood(Wilkinson2011).Thereforeitismoresensibletouseotheringredients cockroachspeciescanbegrownonĂlargevarietyofsubstrates.However,many otherspecies,forinstanceMigratorylocusts,acceptĂmuchsmallerrangeof

animalfeedingredientstheyshouldnotbeconsideredwaste.Ifwasteisseenas resourcesoutofplace(Kollikkatharaetal.2009),animalmanuredoesfallunder

BSFswasevaluatedinChapter6.AlthoughtheBSFlarvaehadĂlowmortality,

indicatesthatmanurecouldbeusedasĂpart(eitherduringĂcertainperiod,or asaningredient)ofthelarvaldiet.However,withintheEuropeanUnion,products suchasmanure,orpartsofanimalsthatarenot,ornotanymore,intendedfor

Insummary,theargumentthatinsectscanusewasteasfeed,isvalidforĂ

aidthesustainabledevelopmentoftheinsectproducingsector.

Thefuture

orfood.Theabundanceofinsectspeciesshouldbeusedtodeterminewhich

142 Generaldiscussion

invitro andinvivo theconsumingspecies.CurrentlyinsectsareconsideredmainlyasĂsourceofhigh asrelevant.Thesecouldserveasnutrientsforhumansandanimals,butcould alsobeusedforotherpurposes,suchasbiofuels(Yang,Lietal.2012;Zheng, Houetal.2012;Zheng,Lietal.2012;Zheng,Houetal.2013;YangandLiu2014),

2014).Lastly,beforeinsectsareusedasĂsourceoffoodorfeedonĂlargescale withintheWesternworld,methodstoguaranteefeedandfoodsafetyneedto bedeveloped(Veldkamp,Duinkerkenetal.2012;Belluco,Losassoetal.2013; CaparrosMegido,Sablonetal.2013;Lv,Liuetal.2013;Spiegel,Noordamet

vanBroekhovenetal.2014). developmentoftheinsectproducingsector.Thisdevelopmentshouldbefueled

7

143 144 References

References

Aarnink,A.J.A.,Keen,A.,Metz,J.H.M.,Speelman,L.andVerstegen,M.W.A.

57. Adamolekun,B.(1993).Anaphevenataentomophagyandseasonalataxic syndromeinsouthwestNigeria.TheLancet341:629.

Anaphevenata

(Nsenenegrasshoppers)inCentral

Tenebriomolitorlarvae.JournalofAgriculturalandFoodChemistry50:

Aidley,D.J.(1976).Increaseinrespiratoryrateduringfeedinginlarvaeof armyworm,Spodopteraexempta

theediblelarvaofCirinaForda(Westwood).AfricanJournalofBiomedical

Schistocercagregaria

145 Dactylopiuscoccus inpricklypearplantsintheopenandinmicrotunnelgreenhouses.

septem:cumsingulorumiconibusadviuumexpressis,ApudClementem Ferronium,pp767.

NezaraviridulaL.

of

Anderson,S.J.(2000).Increasingcalciumlevelsinculturedinsects.ZooBiology19:

stalkingthewild.com/why_not_bugs.htm.

Axtell,R.andArends,J.(1990).Ecologyandmanagementofarthropodpestsof

Bailey,C.G.andSingh,N.B.(1977).Energybudgetfor 

146 References

fourteenspeciesofedibleinsectsinsouthwesternNigeria.AfricanJournal

2013,2013,fromwww.indexmundi.com.

adultsofLocusta Beenakkers,A.M.T.andScheres,J.M.J.C.(1971).Dietarylipidsandlipid Locustamigratoria͘InsectBiochemistry1:

lipidsandlipoproteins,andtheirroleinphysiologicalprocesses.Progress

pp450.

147 ofmankindinearlyandrecentyears.TheAmericanMuseumJournal21:

PublishingCompany,Reading.

Harmoniaaxyridis(Pallas)(Coleoptera:Coccinellidae).

Bernays,E.A.,Chapman,R.F.,MacDonald,J.T.andSalter,J.E.R.(1976).The degreeofoligophagyinLocustamigratoria(L.).EcologicalEntomology1:

Bodenheimer,F.S.(1951).Insectsashumanfood;Ăchapteroftheecologyof man.TheHague,Dr.W.Junk,Publishers,pp352

metamorphosisofthenoctuidmoth Wlk.Insect

148 References

L.,larvae Ictaluruspunctatus Oreochromisaureus

thehousecricketandtheAmericancockroach.InsectBiochemistryand

Bosch,G.,Zhang,S.,Oonincx,D.G.A.B.andHendriks,W.H.(2014).Protein

Bruins,E.(2001).GeïllustreerdeTerrariumencyclopedie.Lisse,TheNetherlands.,

BombyxmoriL.Annalesdela

CaparrosMegido,R.,Sablon,L.,Geuens,M.,Brostaux,Y.,Alabi,T.,etal.(2013).

149 Casey,J.W.andHolden,N.M.(2006).Greenhousegasemissionsfrom

Cazemier,A.E.,Hackstein,J.H.P.,OpdenCamp,H.J.M.,Rosenberg,J.andvan

Palmworm:(Rhynchophorouspalmarum

Chadwick,D.R.,Sneath,R.W.,Phillips,V.R.andPain,B.F.(1999).UK inventoryofnitrousoxideemissionsfromfarmedlivestock.Atmospheric

extractsof

Chown,S.L.,Marais,E.,Terblanche,J.S.,Klok,C.J.,Lighton,J.R.B.,etal.(2007). Scalingofinsectmetabolicrateisinconsistentwiththenutrientsupply

(L.),alongwithbaselinevaluesforfeedingrates,

Springs,AR,USA.

Measures.Rome,pp16. Cohen,A.C.(2003).InsectDiets:ScienceandTechnology,CRCPress,London,UK, pp324. Cole,N.A.,Clark,R.N.,Todd,R.W.,Richardson,C.R.,Gueye,A.,etal.(2005).

150 References

caterpillar,

Cordaux,R.,Bouchon,D.andGrève,P.(2011).Theimpactofendosymbiontson

mealworm,Alphitobiusdiaperinus

Salmonellathrough metamorphosisinthelessermealworm,Alphitobiusdiaperinus

926.

daSilva,J.K.L.,Garcia,G.J.M.andBarbosa,L.A.(2006).Allometricscalinglaws

twocommonIndianAcrididadults(Orthoptera:Acrididae)inlaboratory

Dashefsky,H.S.,Anderson,D.L.,Tobin,E.N.andPeters,T.M.(1976).Face

(AlphitobiusdiaperinusͿtocarriageof inpoultry.

151 CochinealDactylopiuscoccusCosta(Rhyncota:Dactylopiidae):

ImprimerieRoyale.

deVries,M.anddeBoer,I.J.M.(2010).Comparingenvironmentalimpactsfor livestockproducts:reviewoflifecycleassessments.LivestockScience

DeFoliart,G.(1992).Insectashumanfood;GeneDeFoliartdiscussessome

DeFoliart,G.R.(1995).Edibleinsectsasminilivestock.Biodiversityand

DeFoliart,G.R.(2002).Thehumanuseofinsectsasfoodresource:Ăbibliographic

human%20use%20of%20insects. DeFoliart,G.R.(2005).Anoverviewofroleofedibleinsectsinpreserving

Delcroix,J.,Gatesoupe,F.J.,Desbruyères,E.,Huelvan,C.,LeDelliou,H.,et

developmentofseabasslarvae,Dicentrarchuslabrax͕andassociated

Demmers,T.G.M.,Burgess,L.R.,Short,J.L.,Phillips,V.R.,Clark,J.A.,etal.

152 References

Demmers,T.G.M.,Phillips,V.R.,Short,L.S.,Burgess,L.R.,Hoxey,R.P.,etal.

measurementmethodsandtheammoniaemissionfromnaturally

Voedergewassen.Wageningen,WageningenURLivestockResearch,pp24. Diener,S.,Zurbrugg,C.andTockner,K.(2009).Conversionoforganicmaterial

PhoenixWorms( ͿingestedbyMountainChickenFrogs (Leptodactylusfallax

HenryG.Bohn,pp216.

Duncan,F.D.,Krasnov,B.andMcMaster,M.(2002).Metabolicrateandrespiratory

Ecoinvent(2004).FinalReportsEcoinvent2000.S.C.f.L.C.Inventories. Dubendorf,Switzerland,SwissCentreforLifeCycleInventories.

153 Egert,M.,Wagner,B.,Lemke,T.,Brune,A.andFriedrich,M.W.(2003).Microbial

larvaofPachnodaephippiata(Coleoptera:Scarabaeidae).Appliedand

Eghball,B.,Power,J.F.,Gilley,J.E.andDoran,J.W.(1997).Nutrient,carbon,and

theoilsofsomepopularinsectsconsumedinsouthernNigeria.African

ElBoushy,A.R.andvanderPoel,A.F.B.(2000).HandbookofPoultryFeedfrom Waste,ProcessingandUse.Dordrecht,TheNetherlands,KluwerAcademic Publishers,pp409.

Elwert,C.,Knips,I.andKatz,P.(2010).novelproteinsource:Maggotmealofthe

Emekci,M.,Navarro,S.,Donahaye,E.,Rindner,M.andAzrieli,A.(2002). Triboliumcastaneum(Herbst)atreducedoxygen

Emekci,M.,Navarro,S.,Donahaye,E.,Rindner,M.andAzrieli,A.(2004). Rhyzoperthadominica(F.)atreducedoxygen

Bruchidius sahlbergi(Coleoptera:Bruchidae)inseedsofAcaciaerioloba͘Journalof

154 References

Bangkok,FAO,pp456. FAO(2009).HowtoFeedtheWorldin2050.Rome,pp35.

Fast,P.G.(1970).Insectlipids.Progressinthechemistryoffatsandotherlipids

6574. Ferguson,G.W.,Jones,J.R.,Gehrmann,W.H.,Hammack,S.H.,Talent,L.G.,etal. (1996).IndoorhusbandryofthepantherchameleonChamaeleo[Furcifer] pardalis

ofinsectprotein.PhDthesis,UniversityofWisconsin.

Finke,M.D.(2003).Gutloadingtoenhancethenutrientcontentofinsectsasfood

115. Finke,M.D.(2013).Completenutrientcontentoffourspeciesoffeederinsects.

1750.

155 commercialgutloadingproductsforimprovingthecalciumcontentof crickets, JournalofHerpetologicalMedicineand

AnabrussimplexHaldeman)whenusedasĂ

Finlay,B.J.,Thomas,J.A.,McGavin,G.C.,Fenchel,T.andClarke,R.T.(2006).

Folch,J.,Lees,M.andSloaneStanley,G.H.(1957).simplemethodforthe

TenebriomolitorL.

Eristalistenax

Friederich,U.andVolland,W.(2004).BreedingFoodAnimals:LiveFoodfor

contentofmulberrysilkmoth(Bombyxmori)larvae.JournalofZooand

XenopuslaevisandRana catesbeiana

156 References

(Linnaeus)as Ăfactorinthenaturalcontrolof (Linnaeus).Journalof

Geophagy,ironstatusandanaemiaamongpregnantwomenonthecoast

German,D.P.,Nagle,B.C.,Villeda,J.M.,Ruiz,A.M.,Thomson,A.W.,etal.(2010).

SouthernAppalachianhardwoodforest:numbers,biomassandmineral

(Diptera:

Goldsmith,T.H.andWarner,L.T.(1964).VitamininthevisionofInsects.The

rumendevelopmentincalves.JournalofPhysiologyandPharmacology60,

driedTenebriomolitor

Locustamigratorianymphswhenfeeding.Physiological

intheAmericanlocustSchistocercaamericana

157 andmanurehandling.JournalofAgriculturalEngineeringResearch59:

GrootKoerkamp,P.W.G.,Metz,J.H.M.,Uenk,G.H.,Phillips,V.R.,Holden,M.

buildingsinNorthernEurope.JournalofAgriculturalEngineeringResearch

gasemissionsfrombroilerhousesinFrance.BioresourceTechnology96:

Gullan,P.J.andCranston,P.S.(2005).Theinsects:anoutlineofentomology,

Hale,O.M.(1973).Dried

Locustamigratoria migratoioides Schistocercagregaria(Forsk.),Nomadacris septemfasciata

humidityonthesurvivalanddevelopmentofpinecaterpillars, Dendrolimustabulaeformis(lepidoptera:lasiocampidae).InsectScience

158 References

withindigenousspeciesinthetropics.LivestockResearchforRural

itsassociatedenvironmentinĂturkeybrooderhouse.Environmental

Harper,L.A.,Flesch,T.K.,Powell,J.M.,Coblentz,W.K.,Jokela,W.E.,etal.(2009).

Herrero,M.andThornton,P.K.(2013b).Livestockandglobalchange:Emerging

159 Chamaeleo calyptratus

(Gryllus

Gryllusbimaculatus. (Wirkungvonkonstantenundtagesperiodischalternierenden

adulterGryllusbimaculatus

Howard,L.O.(1916).LachnosternalarvaeasĂpossiblefoodsupply.Journalof

bodyandMalpighiantubulesofthetenebrionidbeetle,Zophobasatratus͗

IPCC(2007).SummaryforPolicymakers.͘Cambridge,UnitedKingdomandNew

160 References

Isaksson,C.andAndersson,S.(2007).Carotenoiddietandnestlingprovisioning

572.

Tenebriomolitor

April.pdf.

Entomophagy:keytospaceagriculture.AdvancesinSpaceResearch41:

Katayama,N.,Yamashita,M.,Wada,H.andMitsuhashi,J.(2005).Entomophagyas

Acheta

Klasing,K.C.,Thacker,P.,Lopez,M.A.andCalvert,C.C.(2000).Increasingthe calciumcontentofmealworms(TenebriomolitorͿtoimprovetheir

Microbiologicalaspectsofprocessingandstorageofedibleinsects.Food

161 carbohydratelevelsofGalleriamellonella Pyralidae)inconstantlightnessanddarkness.PakistanJournalof

Kollikkathara,N.,Feng,H.andStern,E.(2009).purviewofwastemanagement

Krengel,S.,Stangl,G.I.,Brandsch,C.,Freier,B.,Klose,T.,etal.(2012).

duringpreimaginalandyoungadultperiodonbodyweightandfatbody contentofmatureCoccinellaseptempunctataandHarmoniaaxyridis

Kroon,L.J.M.,Holtslag,A.A.M.andKrol,M.C.(2009).Inleidingatmosfeer(in Dutch).Wageningen,WageningenUniversity. Kruse,M.andKwon,C.(2004).Edibleinsects,importantsourceofproteinin centralafrica.FAOnewsroom.

Illinois.PaperNo024212. Lamiaa,B.,Mariam,L.andAhmed,A.(2007).Bacteriologicalanalysisof Periplanetaamericana L. (Diptera;Muscidae)intendistrictsofTangier,Morocco.AfricanJournalof

(Diptera,

162 References

Lease,H.M.andWolf,B.O.(2011).Lipidcontentofterrestrialarthropods

Tenebrio molitor

laboratorycomparisonofnitrousoxideanalysisinwesternCanada.

Li,H.,Vaughan,M.J.andBrowne,R.K.(2009).complexenrichmentdiet improvesgrowthandhealthintheendangeredWyomingToad(Bufo baxteri

nitrogenbythehumivorouslarvaofPachnodaephippiata(Coleoptera͗

Lighton,J.R.B.andFielden,L.J.(1995).Massscalingofstandardmetabolism

163  densovirus,isolatedfromtheEuropeanhousecricket,hasevolvedan

offatbodystoresduringadultdevelopmentoffemalecrickets,Gryllus bimaculatus Tenebriomolitorinlowoxygenlevels.Journal

Luoba,A.I.,Geissler,P.W.,Estambale,B.,Ouma,J.H.,Magnussen,P.,etal.(2004).

Tenebriomolitorlarvaethroughdietary

Machin,J.(1975).WaterbalanceinTenebriomolitor

May,B.(1961).TheoccurrenceinNewZealandandthelifehistoryofthesoldier

164 References

McAllister,J.C.,Steelman,C.D.,Skeeles,J.K.,Newberry,L.A.and Gbur,E.E.(1996).ReservoircompetenceofAlphitobius diaperinus(Coleoptera:Tenebrionidae)forEscherichiacoli (Eubacteriales:Enterobacteriaceae).JournalofMedicalEntomology33:

amphibianspecies.MSc.Thesis,NorthCarolinaStateUniversity,pp129.

cricket, McFarlane,J.E.(1962).comparisonofthegrowthoftheHousechricket (Orthoptera:Gryllidae)rearedsinglyandingroups.CanadianJournalof

McMichael,A.J.,Powles,J.W.,Butler,C.D.andUauy,R.(2007).Food,livestock

 and isolateswerepresent.EnvironmentalEntomology10:

insects.Berkely,TenSpeedPress,pp191.

groupsofNortheastIndia,PapuaNewGuinea,AustraliaandNewZealand.

165 Anoliscarolinensis).

Zophobas morio

Metalsinmandiblesofstoredproductinsects:dozincandmanganese

 Imbrasiabelina͘FoodControl11:453.

Mullins,D.E.andCochran,D.G.(1975).NitrogenmetabolismintheAmerican

(Anapheinfracta

TenebriomolitorL.

166 References

rearing (Orthoptera:Gryllidae)asĂnoveltyfood,

housecricket, ͕whenfedtobroilerchicks.Poultry

Bombyx mori Narita,S.,Kageyama,D.,Nomura,M.andFukatsu,T.(2007).Unexpected

Wolbachia Euremahecabeduringlarval

press,pp496.

developmentofladybirdHarmoniaaxyridis(Coleoptera:Coccinellidae).

Newton,G.L.,Booram,C.V.,Barker,R.W.andHale,O.M.(1977).Dried illucenslarvaemealassupplementforswine.JournalofAnimalScience

Newton,L.,Sheppard,C.,Watson,D.W.andBurtle,G.(2005).Usingtheblack

ofswinemanure.NorthCarolina,AnimalandPoultryWasteManagement Center,NorthCarolinaStateUniversity,Raleigh,Nc.͕pp17.

167 

190. Nicks,B.,Laitat,M.,Vandenheede,M.,Desiron,A.,Verhaeghe,C.,etal.(2003). Emissionsofammonia,nitrousoxide,methane,carbondioxideandwater

Nishimune,T.,Watanabe,Y.,Okazaki,H.andAkai,H.(2000).Thiaminis decomposedduetoAnaphe

Onifade,A.A.,Oduguwa,O.O.,Fanimo,A.O.,Abu,A.O.,Olutunde,T.O.,etal.

Ϳfedtorats.Bioresource

Oonincx,D.G.A.B.anddeBoer,I.J.M.(2012a).Environmentalimpactofthe

Assessment.PLoSOne7:e51145.

168 References

Oonincx,D.G.A.B.,Stevens,Y.,vandenBorne,J.J.G.C.,vanLeeuwen,J.P.T.M.

BiochemistryandPhysiologyPartB:BiochemistryandMolecularBiology

Locustamigratoria).Zoo

PLoSOne5:e14445. Osbaldeston,T.A.andWood,R.(2000).Dioscorides:Demateriamedica,Ibidis Press,Johannesburg.

Ϳandstomach contentsfromwildtamanduas(Tamanduatetradactyla).ZooBiology15:

Pan,Y.,Birdsey,R.A.,Fang,J.,Houghton,R.,Kauppi,P.E.,etal.(2011).largeand

(Diptera:

DepartmentoftheInterior,USGeologicalSurvey. ͘

(Orthoptera:Gryllidae).

169 Lethocerusindicus

Pereira,N.R.,FerrareseFilho,O.,Matsushita,M.andSouza,N.E.d.(2003). BombyxmoriL.chrysalis

Pessier,A.P.,Linn,M.,Garner,M.M.,Raymond,J.T.,Dierenfeld,E.S.,etal.(2005). Bufospp.).AAZV,AAWV, AZA/NAGJointconference,Omaha,NE,pp57.

densovirus, miniambidensovirus,fromcrickets.

Piao,S.,Fang,J.,Ciais,P.,Peylin,P.,Huang,Y.,etal.(2009).Thecarbonbalanceof

Pliner,P.andPelchat,M.L.(1991).Neophobiainhumansandthespecialstatusof

(common

University,pp107.

466.

170 References

economyofpeopleoftheruralareasofMexico.EcologyofFoodand

measurestopreservethem.JournalofEthnobiologyandEthnomedicine

Tenebriomolitor(Coleoptera͗Tenebrionidae)torecycleorganicwastes

220.

171 Raubenheimer,D.andSimpson,S.J.(2003).Nutrientbalancingingrasshoppers: Behaviouralandphysiologicalcorrelatesofdietarybreadth.TheJournalof

Reichle,D.E.,Shanks,M.H.andCrossley,D.A.(1969).Calcium,potassium,and

Rivault,C.,Cloarec,A.andGuyader,A.L.(1993).Bacterialloadofcockroachesin

onfeeding,growth,andmetabolismduringthelastlarvalstadiumofthe femalehousecricket, ͘JournalofInsectPhysiology26:

cricket,

RossBreedersLimited12.

415. Ruddle,K.(1973).Thehumanuseofinsects:examplesfromtheYukpa.Biotropica

Russo,A.,Cocuzza,C.E.,Vasta,M.C.,Simola,M.andVirone,G.(2006).Life Piophilacasei

SantosOliveira,J.F.,PassosDeCarvalho,J.,BrunoDeSousaR,F.X.andSimao,M.

736.

172 References

Sealey,W.M.,Gaylord,T.G.,Barrows,F.T.,Tomberlin,J.K.,McGuire,M.A.,et al.(2011).SensoryanalysisofRainbowTrout,Oncorhynchusmykiss͕fed enrichedBlackSoldierFlyprepupae, ͘Journalofthe

Wageningen,WageningenUR,pp16.

Drosophilamelanogaster

inmanuremanagementsystemsforcagedlayinghens.Environmental

Sheppard,C.D.,LarryNewton,G.,Thompson,S.A.andSavage,S.(1994).

173 the5thinstarnymphsofLocustamigratoria͘EntomologiaExperimentalis

dietarynutrients:behavioralmechanisms.PhysiologicalEntomology10:

Simpson,S.J.andRaubenheimer,D.(2001).Thegeometricanalysisofnutrient

439. Simpson,S.J.,Raubenheimer,D.,Behmer,S.T.,Whitworth,A.andWright,G.

Schistocercagregaria͘The

andRelatedInvertebrates.NewYork,JohnWiley,pp1016.

Comprehensiveinsectphysiologybiochemistryandpharmacology.G.A.

ExperimentalisetApplicata39:47.

totalcarbohydrate,lipidandproteinamountsofthebeanbeetle, AcanthoscelidesobtectusSay(Coleoptera:Bruchidae).PakistanJournalof

174 References

Oncorhynchusmykiss͘Journal

Starkie,W.J.M.(1909).TheAcharniansofAristophanes,MacmillanandCompany, limited.

WorkshopSustainableProteinSupply.Amsterdam.

Steinfeld,H.,Gerber,P.,Wassenaar,T.,Castel,V.,Rosales,M.,etal.(2006).

319.

increasingthecalciumcontentofwaxmoth(GalleriamellonellaͿlarvae.

caterpillars,pupae,cocoonsandadultsoftheeasterntentmoth, Malacosomaamericanum

Studier,E.H.andSevick,S.H.(1992).Livemass,watercontent,nitrogenand

175 Acheta

(RoleofRodents,Frogs,Snails,andInsectsforSustainableDevelopment).

Glossinamorsitans centralis Thompson,D.(1910).TheworksofAristotle.Vol.4.HistoriaAnimalium,Oxford:

Thorne,P.S.(2007).Environmentalhealthimpactsofconcentratedanimalfeeding

271.

161.

WallStreetJournalCCXXXVI:1.

ProceedingsoftheSixthandSeventhDr.SchollConferencesonthe

176 References

anddevelopmentoftwostrainsofTenebriomolitorL.(Coleoptera,

TenebriomolitorL.(Coleoptera,

Valkenburgh,S.,R.vanOosterom,O.Stenvers,M.Aalten,M.Braks,etal.(2007).

Tenebrio molitor vanHuis,A.(2005).InsectseateninAfrica(Coleoptera,Hymenoptera,Diptera,

Edibleinsects:futureprospectsforfoodandfeedsecurity.FAOForestry Paper(FAO).

Ăfeasibilitystudy.Wageningen,TheNetherlands,WageningenUniversity,

Jong,G.A.H.,etal.(2014).Housedustmite(DerƉ10)andcrustacean

177 UR,Livestockresearch.

UR,Livestockresearch. Verstegen,M.W.A.,VanDerHel,W.,Brandsma,H.A.,Henken,A.M.andBransen,

Volkova,V.V.,Bailey,R.H.andWills,R.W.(2009).Salmonella

ChinesegrasshopperAcridacinerea(Thunberg)forbroilers.AnimalFeed

Wathes,C.M.,Holden,M.R.,Sneath,R.W.,White,R.P.andPhillips,V.R.(1997).

methane,carbondioxide,dustandendotoxininUKbroilerandlayer

178 References

Winn,D.,Dunham,S.andMikulski,S.(2003).Foodforinsectsandinsectsas

ofSierraLeone:Towhichisadded,anaccountofthepresentstateof medicineamongthem,CambridgeUniversityPress.

2

andmetabolismtoageinthelarval,femalehousecricket.Journalof

Wrage,N.,Velthof,G.L.,vanBeusichem,M.L.andOenema,O.(2001).Roleof

Clanisbilineata(Lepidoptera),anedibleinsect.JournaloftheScienceof

wastesintooilvia (Diptera:Sarcophagidae)larvae

e45940.

Chrysomyamegacephala

149.

Bombyxmori͕

179 ofgreasefromyellowmealwormbeetle(TenebriomolitorͿasĂnovel

207. Zhou,F.,Tomberlin,J.K.,Zheng,L.,Yu,Z.andZhang,J.(2013).Developmental

weight,fatcontentandsurvivalinCoccinellaseptempunctata

180 References

181 Summary

InterestintheusageofinsectsasĂsourceoffoodandfeedisincreasing.Thisis

arablelandandareresponsibleforapproximately15%ofthetotalemissionsof

emphasizesonĂvarietyofinsectsthatarecommonlyusedasfeedorfood.The nutrientcontentofcommerciallyraisedinsectsisreviewedandcomparedtodata availableforwildinsects.Furthermore,thesedataarediscussedinthelightof

currentlyusedtoenhancethenutrientcontentofcommerciallyproducedinsects

͘Furthermore,carbondioxide

(CO2

2

4),ĂpowerfulGHG,which comparableorloweramountsofGHGthandescribedinliteratureforpigs,and

2

182 Summary perkgofmetabolicweightandperkgofmassgain,whichindicatesĂhigherfeed

3Ϳby

mealwormsshouldbeconsideredĂmoresustainablesourceofedibleprotein. Furthermore,itshowsthatĂlargepartoftheenvironmentalimpactofmealworm withwhichthisisconvertedintobodymass.InLCAsenvironmentalimpactis consideredtohaveĂlowerenvironmentalimpactthanmainproducts.

InChapterϱfourdietsformulatedsuchastovaryinproteinandfatcontent

Yellowmealworms,

cockroachesprovedtobehighlydependentondiet.BSFsontheotherhand,

Yellowmealworm mealwormsandHousecricketswassimilartopigsandlowerthanforpoultry.

183 economicvalue,areconsideredtohaveĂnegligibleenvironmentalimpact.Inthe value.Hence,ifaninsectisrearedonmanuretherewouldbenoenvironmental impactallocatedtothefeedusedbytheinsect.InChapterϲthesuitabilityof chicken,pig,andcowmanurewascomparedasfeedforlarvaeoftheBSF.Newly indicatedthatthetestedsubstratescouldbeconsideredsuitable.However, chickenandcowmanure,whereastheECIforphosphorouswashighestoncow manure.Substratenitrogencontentdecreasedinthechickenmanure,butwere

thisinordertomakeitecologicallysound.Itwasalsoconcludedthatshorter

animalsareevaluatedbasedonbothliteraturedata,anddatagatheredin

thisistrueforĂlimitednumberofinsectspeciesonly,anddependsstronglyon

184 Summary

185 Deinteresseinhetgebruikvaninsectenalsbronvanvoedselvoormensen

systemengebruikenmomenteel70%vandebeschikbarelandbouwgrond broeikasgassen.Verscheideneauteurshebbengesuggereerddatinsecten

 InHoofdstukϮwordtdevoedingswaardevaninsectenbesproken.Dithoofdstuk legtdenadrukopinsectensoortendievaakgebruiktwordenalsvoedselof besprokenenvergelekenmetdataoverwildeinsecten.Vervolgenswordendeze

waarvanbekendisdatzedechemischesamenstellingvaninsectenbeïnvloeden, besproken.Techniekendiemomenteelgebruiktwordenomdevoedingswaarde vancommercieelgeproduceerdeinsectenteverbeteren,inclusief“gutloading”

3Ϳvan

vankoolstofdioxide(CO2

186 2

4),waardoorhunbroeikasgas

Echter,alleinsectensoortenindezestudiehaddeneenhogeregroeisnelheid, literatuurbeschrevenvoorvarkensenveelminderdandatgeproduceerdwordt doorrundvee.DatgoldookvoordeCO2

deNH3

3

vanmelk,kip,varkenofrundvleesgaatgepaardmeteenhogereuitstootvan alseenmeerduurzamebronvaneetbaareiwit.Ooktoontdezestudieaandat omgezetinlichaamsmassa.

werdenalscontrolegebruikt.Hettoevoegenvanwortelen,welkediendealseen

187 behalvevandewapenvlieg.Ontwikkelingsduurwerdsterkbeïnvloeddoorhet aangebodendieet.Beschikbaarheidvanwortelvoorgewonemeelwormen

chemischesamenstelling.Degewonemeelwormenendehuiskrekelshadden

metdievanvarkensenlagerdandievoorkippen.Echter,doordehogereeetbare

waarde,wordtalsneutraalgezien.IndeNederlandsecontextismesteen

overlevingvandelarvenlietziendatdegetestesubstratengeschiktwaren.Echter,

nodigomhetecologischverantwoordtemaken.Ookdientdeontwikkelingsduur zouditgedaankunnenwordendoordelarveneenvoedzaamstartdieettegeven, waardoorzezichsnellerontwikkelenwanneerzeovergeschakeldwordenopmest.

188 gebruikenalsvoedsel,geldtditslechtsvooreenbeperktaantalsoortenendit

189 Acknowledgements

anttomeand/wouldliketothankthemfortheirhelp,ideas,guidanceordistrac

Firstofall/wanttothankmypromotors,ArnoldandJoop.Thetwoofyouhave keeninterestinthetopicofentomophagy,/wouldneverhavehadthechanceto workonthisimportanttopic.AlthoughyouareĂtropicalentomologist,andhence wereavailable,thankyouforthat.Yourexperiencewasveryvaluabletome,and /havelearnedĂlotfromyourviewontheplaceofscienceinsociety.Joop,your backgroundinphysiologywas,ofcourse,ofgreatimportanceformywork.You

Atourlaboratory,manyotherpeoplehavehelpedme,eachintheirownway.

mas.Tila,nodoubtyouweretheclosesttome.Wespokeaboutentomology, complished,and/amhappywesharedanislandintheopenseaofourlab.Nina andCindy,thankyoubothforyourhelpintransformingthereadingversionofthis fortherearingwork,butalsoforyouradvice.Youhavedecadesofvaluableexpe rience,andarepartofthebackboneofourgroup.Ofcourse,/needtothankmy

Someofyouhavesincebecomecolleagues,andothershavestartedcareerselse where.Yourworkinourlabhasprovidedvaluabledata,butmoreimportantlyyou havetaughtmemuchonsupervising.Lastly,/wanttothankmyothercolleagues asĂgroup.BecauseĂgroupweare,andassuchyouhavecreatedĂpleasantenvi ronmenttoworkin. Withinouruniversity/havehadtheprivilegetoworkwithseveralothergroups,

190 Acknowledgements

somethinghereandnow,tosomethingreal.

Assaid,theVenikhasplayedanimportantroleinthisdevelopment,and/want

Marian,whoseemstoknoweveryonewhohasusedthewordinsectandfoodin onesentence,andbringsthesepeopletogether.TheCalisfamily,whoweremost meattheirkitchentable./hopetoworkwithyouforyearstocome.Lastly/want tothanktheVandeVenfamilyforopeningthedoorsoftheirfacilitytomeand therebyshowingtheworldthattheirmealwormsareĂsustainablesourceofpro tein.

Besidesthesepeoplewhosupportedmeinmywork,/wanttothankthepeople thatsupportedmeoutsidemywork.Firstofallmygrandparents,whotoldmeto studyaslongas/could,andsupportedmetodoso.Myparentswhosupported meindoingwhat/wasdoing,althoughwhatitactuallywasmightnothavebeen clear.Mom,wheneveryouvisitedthedaypassedasifitwasanhour,andatthe

Myfriends,Hilbert,Linda,Eelco,Mark,Marc,YuriandJeroen,alsoknownas“the guys”;weknoweachotherthroughourhobby,butyouaresomuchmoretome. ofyouthat/wasabletotravel.Yuri,youalwaysbringĂsparkleinlife,andĂhug whenitisneeded.Mark,youareĂstraightshooterandĂstraightthinker,your analysesmakelifeclear.Marc,youareĂneighborandĂfriendinone,andthe muchneededcoolnessfactorofthegroup.Jeroen,youarethenextbestthing youhelpedĂlot.

Lastly,/wanttothankMandy.YouhavesupportedmethroughoutmyPhDperiod,

ĂlocalmarketinLaos,orbakingcricketcookies,youwerethereforme.YouareĂ partnerinmanywaysandwordsarenotenoughtoexplainhowfortunate/feelto bewithyou.

191 CurriculumVitae

192 CurriculumVitae

Dennis G.A.B. Oonincx was born on September 14, 1979 in  completed Ă Bachelors degree in Economics at the Avans UniversityofAppliedSciencesintheNetherlands.In2002he startedhisstudyofAnimalScienceatWageningenUniversity.

theLaboratoryofEntomologyatWageningenUniversity.Theresultsofthisresearch arepresentedinthisthesis.DuringhisPhDhestayedinvolvedinresearchonvitamin sourceoffeedandfood.

193 Peer-reviewed:

Bosch,G.,S.Zhang,D.G.A.B.Oonincx

Finke,M.D.andD.G.A.B.Oonincx

London,UK,AcademicPress.

etal. beardeddragons(

andI.J.M.deBoer(2012).Environmentalimpactofthepro

sessment.PLoSOne7(12):e51145.

Locustamigratoria).ZooBiology30(1):

͕Y.Stevens,J.J.vandenBorne,J.P.vanLeeuwenandW.H.

venilebeardeddragons(

vanLoon,etal.

PLoSOne5(12):e14445.

194 Popular:

(2009).PreferredHatchingTime;Eeninteressantfenomeen

͕S.vanBroekhoven,A.vanHuisandJ.J.A.vanLoon.Feed

͕J.P.vanLeeuwen,W.H.HendriksandA.F.B.vanderPoel. Pogonavit- ). vanZanten,H.H.E.,H.Mollenhorst,D.G.A.B.Oonincx͕P.Bikker,B.G.Meerburg, etal.Fromenvironmentalnuisancetoenvironmentalopportunity:house

195 196 ImkeJ.M.deBoer

University,Wageningen,TheNetherlands

HenryvandenBrand

WageningenUniversity,Wageningen,TheNetherlands

SarahvanBroekhoven LaboratoryofEntomology,PlantSciencesGroup,WageningenUniversity, Wageningen,TheNetherlands

MarkD.Finke MarkFinkeLLC,RioVerde,Arizona,USA

MarcelJ.W.Heetkamp

WageningenUniversity,Wageningen,TheNetherlands

ArnoldvanHuis LaboratoryofEntomology,PlantSciencesGroup,Wageningen University,Wageningen,TheNetherlands

LaboratoryofEntomology,PlantSciencesGroup,Wageningen University,Wageningen,TheNetherlands

JoopJ.A.vanLoon LaboratoryofEntomology,PlantSciencesGroup,Wageningen University,Wageningen,TheNetherlands

197 Reviewofliterature(6ECTS)  Insectsashumanfoodsource;past,presentandfuture(2009)

 AnassessmentofcommerciallyrearedinsectsasĂhumanfoodsource

  Advancedfoodanalysis;VLAG(2010) 

Laboratorytrainingandworkingvisits(1.5ECTS)  2001)  );Universidadde Alicante(2012)



 (Zophobasmorio (2011)  Zoobiology:thesilkwormBombyxmoricansustainthegrowthoftheleopard geckoEublepharismacularius



Competencestrengtheningͬskillscourses(4.5ECTS)  

198   Sciencethepressandthegeneralpublic;SENSE(2009)   Teachingandsupervisingthesisstudents;DO(2010) 

 

  NederlandseEntomologendag(2009) 

 39th  9th 

 43th  Insectstofeedtheworld;Ede,theNetherlands(2014) 

   

SupervisionofĂMScstudents  Greenhousegasemissionsbyinsects   Alphitobiusdiaperinuslarvae

199 200