w ww . e l s e v i e r . c o m / l o c a t e / b j p
Original
Article
Medicinal
plants
in
the
diet
of
woolly
spider
monkeys
(
Brachyteles
arachnoides
,
E.
Geoffroy,
1806)
–
a
bio-rational
for
the
search
of
new
medicines
for
human
use?
Liége
M.
Petroni
a,
Michael
A.
Huffman
b,
Eliana
Rodrigues
a,∗aCentrodeEstudosEtnobotânicoseEtnofarmacológicos,DepartamentodeCiênciasBiológicas,UniversidadeFederaldeSãoPaulo,SãoPaulo,SP,Brazil bPrimateResearchInstitute,KyotoUniversity,Kyoto,Japan
a
r
t
i
c
l
e
i
n
f
o
Articlehistory: Received15April2016 Accepted18September2016 Availableonline12October2016
Keywords: Zoopharmacognosy Ethnomedicine Woollyspidermonkeys Diet
Atlanticforest Medicinalplants
a
b
s
t
r
a
c
t
Thepresentstudyaimedtocomparetheplantfooddietofwoollyspidermonkeys(Brachyteles arach-noides)inhabitingIntervalesStateParkinSãoPaulo,Brazil,withmedicinalplantspeciesusedbyhumans inthesurroundingareasofthepark.ThedietofagroupofwoollyspidermonkeyslivinginanAtlantic for-estareawasrecordedduring43monthsoffieldwork.Fifty-threespecies(87fooditems)wererecorded. PlantspecimenswerecollectedandidentifiedattheUniversityofSãoPauloandtheBotanicalInstitute ofSãoPauloState.Usingsemi-structuredinterviews,ethnomedicinaldatawerealsocollectedfromfour preselectedrespondentsregardingthehumantherapeuticvalueoftheseplants.Thestudyshowedthat 24.5%(13/53)ofthesespeciesareusedbyresidentsaroundtheparkformedicinalpurposes.Ofthese thirteen,sevenspeciesalsohavevalidatedpharmacologicalproperties,andthreeareutilizedbylocal residentsforsimilarmedicinalpurposes.Overlapintheplantfood/medicinaldietofwoollyspider mon-keypopulationselsewherewerealsonoted,suggestingpotentialoverlapintheirmedicinalvaluefor humansandprimates.Thesimilaritiesbetweentheingestionofplantsbyprimatesandtheir medici-nalusebyhumansprovideabio-rationalforthesearchofbioactiveplantsintheprimatediet.Further detailedinvestigationoftheirpharmacologicalandphytochemicalvalueiswarranted.
PublishedbyElsevierEditoraLtda.onbehalfofSociedadeBrasileiradeFarmacognosia.Thisisanopen accessarticleundertheCCBY-NC-NDlicense(http://creativecommons.org/licenses/by-nc-nd/4.0/).
Introduction
Mostprimateshaveadiverseplantbaseddiet,fromwhichthey obtaintheneeded caloriesand nutrientsnecessary for survival andreproduction(Oats,1987;Altmann,1998;Lambert,2011).The majorplantdietarystrategiesarefrugivoryandfolivory, supple-mentingthiswithseeds,sap,barkandflowers(Carvalho,1996; Lambert,2011).However,plants provide more then just nutri-ents.Plantsalsocontainavarietyofsecondary metabolitesthat have largelybeen viewedasdeterring primatesfrom eatthem (Glander,1982).Ithasalsobeenshownthatmanydifferentprimate species ingestplants containingboth nutritional and medicinal value,suggestingthatthesesecondarymetabolitescouldactually bebeneficialtothehealthoftheuser(e.g.Sifaka:Carraietal.,2003; gorilla:CousinsandHuffman,2002;chimpanzee:Huffman,2003; Kriefetal.,2005,2006;Japanesemacaque:MacIntoshandHuffman, 2010).
∗ Correspondingauthor.
E-mail:e.rodrigues@unifesp.br(E.Rodrigues).
Buildingontheworkofanimalself-medication,anidentified pathforthediscoveryofnewdrugsofpotentialvaluetohumans isbasedontheevaluationofthemedicinalpotentialofthediet ofgreatapes,OldWorldmonkeysandprosimians(Ohigashietal., 1994;Huffmanetal.,1998;Kriefetal.,2004).Thebasicpremise ofthisprocess,alsoknownaszoopharmacognosy(Rodriguezand Wrangham,1993)isthatanimalsutilizeplantsecondary metabo-litesand othernon-nutritionalsubstancesin thediet asa form ofpassivepreventionortreatmentfordiseasessuchasparasite infection(Huffman,1997).Huffmanpointsoutthatthechallenge ofinterpretingself-medicationinanimalsistodistinguishbetween possibleindirectmedicinalbenefitsderivedfromlimitedingestion ofplantsrichinsecondarycompoundsofbiologicalsignificance (medicinalfoods),versusthelimitedandsituationspecific inges-tionof non-nutritionalitemsthatare processedsolelyfor their therapeuticmedicinalproperties(e.g.Huffmanand Seifu,1989; Huffmanetal.,1993).Onething,thatsetsmedicinalfoodsapart fromnormaldietaryfooditemshighinnutritionalvalue,is the biologicalpropertiespresentindietaryitemseatenatseasonally limited periodsin smallamounts,withnosigns of illness,that haveuseinhumantraditionalmedicineforailmentscommonto
http://dx.doi.org/10.1016/j.bjp.2016.09.002
Brazil
N
Xitué Ecological station
Ribeirão Grande
State of São Paulo
Carlos Botelho State Park Intervales State Park Alto da Ribeira
State Park
Atlantic Ocean
0 6 12
0 1.000 2.000 3.000 Km
18 24 Km
Paraná S
E W
N
S E W
Fig.1.LocationofIntervalesStatePark,SãoPaulostate,RibeirãoGrandemunicipality(24◦12′to24◦25′Sand48◦03′to48◦30′W).
bothhumansandanimals.Theplantdietofneo-tropicalprimate hasremainedunder-studiedandunderreportedintheseaspects (Janzen,1978;Glander,1994).
Brazilhasanincalculablewealthoftraditions,customsand cul-turaltraitsthatstilllinger,especiallyintraditionalsocieties.Plants comprisepartoftheidentityofa groupofpeoplebecausethey reflectwhattheyareandwhattheythinkaswellastheir relation-shipswiththeirsurroundings(Medeirosetal.,2004).Therefore,the useofplantsfortherapeuticpurposesispartofasocialand eco-logicalcontext,andmostofthespecificitiesofsuchusecanonlybe understoodinthiscontext.
Understandingtheroleofplantsinthedietofneo-tropical pri-matesandhowtheseplantsmaybeusedtopromotehealthisa potentialnewavenuetohelpunderstandthebiologicalbasesand originsoftraditionalpracticeswithineffortstodeveloppotential bioactivecompounds.Using this bio-rational,thepresent study aimedtocomparetheplantscontainedinthedietofwoollyspider monkeys(Brachytelesarachnoides)inhabitingIntervalesStatePark inSãoPaulo,Brazil,totheplantspeciesusedinhumanmedicine aroundthepark.
Materialsandmethods
Ethics
ThisstudywasapprovedbytheUnifespEthicsCommittee (CEP-UNIFESP)undertheprocessnumber031538/2016,andTermsof Consent(TCLE)wereobtainedfromrespondents.
Studyareaandgroups
IntervalesStatePark(ISP)islocatedinthesouthernregionofthe stateofSãoPaulo,headquarteredinthemunicipalityofRibeirão Grande(24◦12′to24◦25′Sand48◦03′to48◦30′W).ISPhasanarea
of49,888haandisconnectedtothreeotherConservationUnits: CarlosBotelhoStatePark,XituéEcologicalStationandAltoRibeira StatePark(Fig.1).
AccordingtoTheIUCNRedListofThreatenedSpecies,B. arach-noideshasbeencategorizedasanendangeredspeciessince1982. InBrazil,thedistributionofwoollyspidermonkeysiscurrently
restricted toisolated, scatteredareas becauseof anthropogenic disturbances,rangingfromdeforestationtoindiscriminate hunt-ing (Lemos de Sá, 1988).The group of woolly spidermonkeys reportedhereconsistedof39individualsoccupyinganareaofuse of1216.35ha(Petroni,1993,2000).
Speciesandfooditemsusedbywoollyspidermonkeys
Abehaviouralstudyofwoollyspidermonkeyswasconducted during43monthsoffieldwork,from1989to1990andfrom1994to 1997,byoneoftheauthors(Petroni,L.M.).Thedailyactivitiesofthe woollyspidermonkeyswererecordedadlibitum(Altmann,1974). Thepresentstudyperformedaqualitativeanalysisofthedietofthe groupstudied.Thecalculationoftheintakeofeachfooditemwas basedonthenumberofobservationsinwhicheachitemwas con-sumedbywoollyspidermonkeys.Thesamplesofplantspecimens observed in the diet of monkeys werecollected for identifica-tionpurposesusingthedrymethod(Morietal.,1985)consisted of the following: branches, flowers or fruits knocked down or pickedfromtreetopsbythemonkeys.Fooditemswereclassified intoflower,fruit,andleafcategories.Alloftheplantspecimens wereidentifiedbyresearchersfromtheUniversidadedeSãoPaulo, DepartmentofEcologyandfromtheBotanicalInstituteofSaoPaulo State,andtheirexsiccatesweredepositedin thecorresponding herbaria.
Ethnomedicine
Theusesofplantsbyprimatesandhumanswereorganized,and theirbiologicalactivitiesasreportedinthepharmacological sci-entificliterature,aswellasotherstudiesondietofwoollyspider monkeys,wereassessedtoimpartgreaterrobustnesstothedata, enablinginferencesonanypotentialbioactivecompounds.Oneof thelimitationsofourstudyisthatwedidnotcollectspecificdata onthehealthofindividualswhenfeeding.Thiswasnotapartof initialstudy.
Resultsanddiscussion
Plantfooddietofwoollyspidermonkeys
ThedietofwoollyspidermonkeysrecordedatIntervalesState Parkcontained53plantspecies,fromwhich87differentitemswere eaten;leaves,fruitsandflowers.Anequalnumberofleaves(45.5%) andfruit(45.5%)itemswererecognized,withflowers(9%) repre-sentingonlyasmallproportionofthediet.Thesespeciesbelonged to27families(Box1).Amongthem,Myrtaceaehadthegreatest numberoffoodspecies(n=10)represented,followedbyFabaceae s.l.(n=8),Lauraceae(n=4),Moraceae(n=3),Celastraceae, Euphor-biaceae, Rubiaceae, Sapotaceae and Urticaceae (two species each).The remainingfamilies wererepresented byone species each.
InordertoanalyzethedietofIntervalesStateParkwoolly spi-dermonkeys compared withthatof B. arachnoidespopulations elsewhere,wecomparedourlistwithpublishedrecordsinthe liter-ature(Box1).Thesitesforwhichliteraturewasavailableincluded twostates ofsoutheasternBrazil:state ofSãoPaulo: Intervales StatePark,municipalityofRibeirãoGrande(VieiraandIzar,1999), FazendaBarreiroRico,municipalityofAnhembi(Assumpc¸ão,1983; Milton,1984;Martins,2008),CarlosBotelhoStatePark, municipal-ityofSãoMiguelArcanjo(Talebietal.,2005;Buenoetal.,2013); andstateofMinasGerais:FazendaMontesClaros,municipalityof MontesClaros(Brozek,1991).Acompletecomparisonwas diffi-cult,asthepartconsumedwasnotalwaysindicatedandinsome instancesplantfoodswereonlylistedtothegenuslevelor incom-pletespeciesweregiven.
FooditemsinspeciesfromtheMyrtaceaefamily(n=17), fol-lowedbythoseofLauraceae(n=5)andFabaceaes.l.(n=3)were recognizedforB.arachnoidesatCarlosBotelhoStatePark(Moraes, 1992).Thesefamiliesareamongthemostcommonintheregion oftheIntervalesandCarlosBotelhoStateParks(Hueck,1972).In MinasGeraisstate,foodplantspeciesfromthefamiliesFabaceae s.l.,MyrtaceaeandMoraceaewereamongthemaindietary com-ponentsofB.arachnoidesthere(Brozek,1991).
Overall,fifteenspeciesinthesamegenuswererecordedinthe dietsofthesedifferentpopulations;sevenofwhichwerethesame species (markedwithan asterisk in Box 1).Ten out of the fif-teenspecieshadatleastonepartofthesameplantconsumedby monkeysatoneormoreothersites.Themainitemsreportedtobe consumedwereleaves,fruitsandflowers.Amongtheplantfood itemsmentionedinBox1,whoseingestedpartswerereported, therewasapredominanceoffruit(70%),followedtoamuchlesser extent by leaves(20%), seeds (5%) and flowers (5%). The main foodsourceofBrachytelesisfruit.However,Martins(2008)found that dependingonlocation habitat,fruitconsumption occupies between21%and 71%of theaverageannualfeedingtime ofB. arachnoides.
AstudyconductedbyMilton(1984)inBarreiroRico,SãoPaulo state, found a higher number of leaves in the diet of woolly spider monkeysthan in a study conducted byStrier (1986) in MontesClaros,MinasGeraisstate,whereahighernumberoffruits wasobserved.Thesedietarydifferencesaremainlyrelatedtothe
existence of a higher number of species that provide fruits in MontesClarosthaninBarreiroRico(Strier,1986).
Ethnomedicinalandpharmacologicalpropertiesofthediet
Evidenceforpossiblemedicinalactivityinthedietofwoolly spidermonkeys,eitherethnomedicinallyorpharmacologically val-idated, was recognized in 37.7% (20/53 species) of the species listedinBox1.Ofthese,thirteenwerereportedbythefourlocal respondentsasbeingusedforethnomedicinalpurposes,fourteen hadreportedpharmacologicalactivity,whilesevenhadboth eth-nomedicinalandpharmacologicalrecords.
Theethnomedicinalusesdescribedforthesespecieswere; lax-ative/purgative (n=5), wound healer, cold remedy (n=3 each), stimulant,bronchitis,ulcers/gastritis,hoarseness,warmsthebody (n=2each).Otherlessfrequentlylistedproperties,representedby onespecieseachwere,asthma,fracture,hypotensive,aphrodisiac, postpartumweakness,hepatitis,rheumatism,cleanser,infection, clottingagent,digestive(n=1each).Somespecieshad multiple uses reported, e.g. Tapirira guianensiswas used as a purgative, woundhealerandothertreatmentforcuts.Thefactthatthe indica-tiontofightacoldisalmostalwaysaccompaniedbytheexpression warmsthebodystandsout.Accordingtorespondents,the sensa-tionimpartedisthatofcomfortbecausethebodybecomeswarm, mitigatingtheundesirablecoldsymptoms.
Twenty-sixpercent(14/53)ofthefoodplantspeciesinBox1 have pharmacologicalproperties. However,of thethirteen eth-nomedicinalplantspeciesreportedbytherespondents,onlyseven had reported pharmacological uses. Of these, three have uses similar to the biological activity reported in the scientific lit-erature (markedwith two asterisks in Box 1).The human use ofaroeira (TapiriraguianensisAubl.) asawound andcut healer matcheditsanti-bacterialpharmacologicalactivity(Roumyetal., 2009).ThespeciesCrotonurucuranaBaill.,knownaspau-sangue (dragon’sblood)usedasawoundhealer,wasstudiedbyPeresetal. (1997),whofoundantimicrobialactivity.Whilejatobá(guapinol), HymenaeacourbarilL.,indicated forcold symptoms,hasshown immunomodulatory activity(Rosárioet al.,2008), although the plantpartsstudiedinthepharmacologicalliteratureandtheparts indicatedbytherespondentsofthisstudywerenotalwaysthe same(Box1).
Zoopharmacognosyandethnomedicine
Asmentionedbefore, amongthe53plantsconsumedby pri-matesinthepresentstudy,thirteenarealsousedinlocalhuman medicine.However,weobservedlittlesimilaritywhencomparing thepartsofthethirteenplantsusedbybothbytherespondentsand primates.Humansusethefollowingplantpartsformedicinal pur-poses:bark(fourplantspecies),seeds(3),leaves(2),root,fruit,sap, oil,resin,core,latexandvine(oneeach);whileforthesethirteen plants,theprimatesmostlyconsumedfruits(ninespecies)and/or leaves(8).
Onepossibleexplanationforthisdifferenceisthatfolkmedicine hasmanyplantspreparationforms,predominating istheuseof leavesandbarkintheirrecipes.Whileprimateshaveaconsistently frugivorousdietwheninhabitinglessdisturbedhabitats,asisthe casehere.Theirpredominantfooditemisfruit.Moreover,thefruits arerarelyusedinhumanmedicine.Inthissense,aconvergencewas notexpected.
Box1:The53plantfoodspeciespresentinthedietofwoollyspidermonkeys(Brachytelesarachnoides)atIntervales StatePark,SãoPaulo,Brazil.Plantpart(s)consumed,theirlocalethnomedicinal,pharmacologicalpropertiesandfood itemsreportedatotherB.arachnoidesstudysites.
Family Species[voucher]–plant
partconsumed
Vernacularname Ethnomedicinaluses (plantpart)
Pharmacologicalproperties Plantfoodsreportedat othersites
Anacardiaceae TapiriraguianensisAubl. [256464]–Le
Aroeira,roeirão, roeira-brava
Laxative/purgative, woundhealerb(Ba)
Anti-protozoaland anti-bacterialb(Roumy
etal.,2009)
N.d.f.
Annonaceae GuatteriaaustralisA.St-Hil. [262336]–Fr,Le
Reticueiro – Antiplasmodialactivity
(Fischeretal.,2004)
N.d.f.
Araceae PhilodendronimbeSchott
exEndl.hort.exEngl. [249754]–Fr,Le
Trucuá – N.d.f. Philodendron
appendiculatum,P. corcovadenseKunth.,P. crassinerviumLindl.,P. exymiumSchott.,P. martianumandP. obliquifolium–Fr(Vieira andIzar,1999)
Araliaceae Scheffleracalva(Cham.)
Frodin&Fiaschi[347509]– Le
Mandioqueiro – N.d.f. N.d.f.
Boraginaceae CordiasellowianaCham.a
[263105]–Le
Louro – N.d.f. Cordiasellowianaa–Fr
(Martins,2008)
Canellaceae Cinnamodendrondinisii
Schwacke[397239]–Fr,Le
Pimenteira – Antibacterial,Antifungal
andTrypanocidalactivity (esssentialoil)(Andrade etal.,2015)
N.d.f.
Celastraceae Cheilocliniumserratum
(Cambess.)A.C.Sm. [252697]–Fr,Le
Cipotá – N.d.f. N.d.f.
Maytenuscestrifolia
Reissek[309097]–Fr
Carrapateiro – N.d.f. N.d.f.
Combretaceae BuchenaviakleiniiExell [129533]–Fr,Le
Amarelinho – N.d.f. N.d.f.
Euphorbiaceae Alchorneatriplinervia
(Spreng.)Müll.Arg.a
[205189]–Le
Tapiaeiro-miúdo, tapiá
– Anti-inflammatoryactivity
(Lopesetal.,2010); Antibacterialactivity–Le (Calvoetal.,2010); Gastroprotectiveeffect (Limaetal.,2008)
Alchorneatriplinervia
(Spreng.)Müll.Arg.a–
n.d.f.(Milton,1984)
CrotonurucuranaBaill. [291906]–Le,Fl
Pau-sangue, sangueiro
Woundhealerb(Sa) Alleviatepainassociated
withgastrointestinaland otherrelateddisorders–Sa (Raoetal.,2007); Antidiarrhoealeffect–Sa (Gurgeletal.,2001); Antimicrobialactivityb
(Peresetal.,1997)
CrotonfloribundusSpreng. –Fl(Milton,1984)
Fabaceaes.l. Copaiferatrapezifolia
Haynea[254711]–Le
Pau-óleo,capaúva, capaúba
Bronchitis, laxative/purgative, ulcers/gastritisand infection(Oil)
N.d.f. CopaiferalangsdorfiiDesf.
–n.d.f.(Milton,1984);C. langsdorfii–Se(Assunc¸ão, 1983);Copaifera trapezifoliaa–Fr(Bueno,
2013)
HymenaeacourbarilL.a
[251741]–Fr,Le
Jatobá Clottingagent(Ba),
coldremedyb, bronchitis,rheumatism, laxative/purgative(Ba, Re)
Immunomodulatory activityb(Rosarioetal.,
2008)–Se
Hymenaeacourbarila–Fr
(Martins,2008);H. courbarila–n.d.f.(Milton,
1984);H.courbarila–Le
(Assunc¸ão,1983)
IngamarginataKunth. [254729]–Fr,Le
Ingá-mirim, inga-feijão
– N.d.f. Ingastriata–Fr(Martins,
2008);I.striata–Se(Milton, 1984);I.sessilisa–Le
(Talebietal.,2005)
Ingasessilis(Vell.)Mart.a
[256195]–Fr,Le
Ingá-macaco – N.d.f.
Piptadeniaadiantoides
(Spreng.).J.F.Macbr. [373254]–Fr
Gambaeiro – Leishmanicidal(Campos
etal.,2008)
Piptadeniagonoacantha– n.d.f.(Milton,1984)
Pseudopiptadenia warmingii
(Benth.)G.P.Lewise M.P.Lima[285783]–Le
Calvin – N.d.f. N.d.f.
SwartziaacutifoliaVogel [159775]–Le
Box1:(Continued)
Family Species[voucher]–plant
partconsumed
Vernacularname Ethnomedicinaluses (plantpart)
Pharmacologicalproperties Plantfoodsreportedat othersites
Tachigalidenudata(Vogel) Oliveira-Filho[254424]–Le
Pascoré,pasquaré – N.d.f. N.d.f.
Lauraceae Beilschmiediaemarginata
(Meisn.)Kosterm.[101743] –Fr,Le
Canela-batalha, canela-bataia
– N.d.f. N.d.f.
Ocoteadiospyrifolia
(Meissn.)Mez[331471]–Fr, Le
Canela-nhutinga Aphrodisiac,warmsthe body,coldremedy, hoarseness(Fr,Se)
Acaricidalactivity(Dos Santosetal.,2013)
Ocoteacorymbosa–Fr (Martins,2008);O. odorifera(Vell.)Rohwera–
Le(Talebietal.,2005);O. spixianaNees.,O.acutifolia
Nees.,Ocoteasp.–Le (Milton,1984);O.spixiana– Fr(Assunc¸ão,1983)
OcoteaodoriferaRohwera
[300387]–Fr,Le
Canela-sassafrás Stimulant,coldremedy, hoarseness,warmsthe body(Ba,He)
Antifungaleffects–Le (Yamaguchietal.,2011); Antimicrobial(DeSouza etal.,2004)
Ocoteaporosa(Nees& Mart.)Barroso[204129]– Fr,Le
Canela-amarela – N.d.f.
Magnoliaceae MagnoliaovataA.St.-Hill. [253046]–Le
Pinho-bravo – Antipyreticand
anti-inflammatory(Kassuya etal.,2009);Insecticidal activity(Coelhoetal., 2006);Hypoglycemiceffect –Le(Moratoetal.,1989)
N.d.f.
Malvaceae Spirothecarivieri(Decne.) Ulbr.[13075]–Fr,Le,Fl
Figueira-mata-pau – N.d.f. N.d.f.
Melastomataceae Tibouchinapulchra(Cham.) Cogn.[286821]–Le,Fl
Manacá-da-serra – N.d.f. N.d.f.
Meliaceae Cabraleacanjerana(Vell.)
Mart.[248092]–Le
Canjarana, canharana
– N.d.f. Cabraleasp.–n.d.f.(Milton,
1984) Menispermaceae AbutaselloanaEichler
[318838]–Fr
Grão-de-mico,buta Postpartumweakness
(Li)
N.d.f. n.d.f.
Moraceae FicusinsipidaWilld.
[247888]–Fr,Le
Figueira-branca – Anthelminticactivity–La
(deAmorimetal.,1999)
Ficussp.–Fr(Milton,1984)
FicusorganensisMiq. [374561]–Fr,Le
Figueira – N.d.f.
Soroceabonplandii(Baill.) W.C.Burger,Lanj.&Wess. Boer.[318828]–Fr
Laranjinha Ulcers/gastritis(Le) N.d.f. N.d.f.
Myristicaceae Virolabicuhyba(Schottex Spreng.)Warb.[288360]– Fr,Le
Bucúva,bucuveira Laxative/purgativeand digestive(Se)
Analgesicactivity–Le (Kuroshimaetal.,2001)
N.d.f.
Myrtaceae Campomanesiaguaviroba
(DC.)Kiaersk.[304809]–Fr, Le
Guabirova, guabiroba
– N.d.f. Campomanesiasp.–Fr
(Martins,2008)
Eugeniaburkartiana
(D.Legrand)D.Legrand [312083]–Fr
Murta – N.d.f. Eugeniapyriformis,E.
ligustrina,Eugeniasp.–Fr (Martins,2008);Eugeniasp. –Fr(Talebietal.,2005);
Eugeniasp.–Fr(Assunc¸ão, 1983)
Eugeniapruinosa
D.Legrand[262439]–Fr
Murta – N.d.f.
Myrceugeniamyrcioides
(Cambess.)O.Berg[262327] –Fr
Cafeeiro Stimulant(Se) N.d.f. N.d.f.
Myrciaanacardiifolia
Gardner[313862]–Fr
Goiabinha – N.d.f. N.d.f.
MyrciagrandifoliaKiaersk [254610]–Fr,Le,Fl
Murta – N.d.f. N.d.f.
MyrciamacrocarpaBarb. Rodr.[246584]–Fr
Goiabinha,murta – N.d.f. N.d.f.
MyrciapubipetalaMiq. [250041]–Fr
Murta – N.d.f. N.d.f.
Myrciariafloribunda
(H.WestexWilld.)O.Berg [292773]–Fr,Le,Fl
Arac¸azinho – N.d.f. Myrciariasp.–Fr(Milton,
1984)
Psidiumlongipetiolatum D.Legrand[293823]–Fr,Le, Fl
Arac¸á-piranga – N.d.f. N.d.f.
Nyctaginaceae Guapiraopposita(Vell.) Reitz[246573]–Le
Abobreiro, carne-de-vaca
Box1:(Continued)
Family Species[voucher]–plant
partconsumed
Vernacularname Ethnomedicinaluses (plantpart)
Pharmacologicalproperties Plantfoodsreportedat othersites
Ochnaceae QuiinaglazioviiEngl.
[290593]–Fr
Jerivazinho – N.d.f. N.d.f.
Phyllanthaceae Hyeronimaalchorneoides
Allemão[296596]–Fr,Le,Fl
Recurana, aricurana
– N.d.f. N.d.f.
Phytolaccaceae PhytolaccadioicaL. [288761]–Fr,Le,Fl
Embueiro – Antifungalactivity–Fr(Di
Libertoetal.,2010)
N.d.f.
Rubiaceae Bathysaaustralis(A.St.-Hil.) K.Shum.[358307]–Le
Fumo-bravo, fumeiro
– N.d.f. N.d.f.
Posoquerialatifolia(Rudge) Roem&Schult.[350771]– Fr
Laranja-de-macaco – N.d.f. N.d.f.
Sapotaceae ChrysophyllumvirideMart.
&Eichler[275282]–Fr,Le, Fl
Bujoeiro, pau-marfim
– N.d.f. N.d.f.
Pouteriabullata(S.Moore) Baehnia[32105]–Fr
Guapeva-branca Woundhealerand
hepatitis(LaandFr)
N.d.f. Pouteriabullataa–Fr
(Buenoetal.,2013)
Solanaceae SolanumrufescensSendtn.
[305753]–Le
Quina-branca Laxative/purgative(Ba, Ro)
N.d.f. N.d.f.
Urticaceae CecropiaglazioviiSnethl. [309099]–Fr,Le
Embaúba Asthma,fracture,
cleanser,hypotensive
(Br)
Antisecretoryandantiulcer activities(Souccaretal., 2008);Antidepressant-like effect(Rochaetal.,2007); Anxiolytic-likeeffects (Rochaetal.,2002)
N.d.f.
Coussapoamicrocarpa
(Schott)Rizzini[268699]– Fr,Le
Figueira-mata-pau – N.d.f. N.d.f.
aThematchesbetweentheplantspeciesconsumedbywoollyspidermonkeysobservedinthepresentstudyandreportedatotherB.arachnoidesstudysites. b Localethnomedicinalvalueisconsistentwithreportsfromthepharmacologicalliterature.
Ba,bark;Sa,sap;Br,bract;Ro,root;La,latex;Li,liana;He,heartwood;Fr,fruit;Re,resin;Le,leaves;Fl,flowers;Se,seeds;N.d.f.,nodatafound.
Whilepharmacologicalliteraturecorroboratedsomeofthe bio-logicalactivityobtainedfromourinterviews,thisoverlapisnotthe mostoutstandingaspectofthisstudy.Rather,itisnotablethat thir-teenspeciesofatotalof53plantspresentinthedietofmonkeys areincludedinthemedicinalrepertoireofpeoplelivingaround thepark.Severalstudieshavepreviouslyshownastrong correla-tionbetweentheplantsusedbyprimatesforself-medicationand plantspeciesusedinthetraditionalmedicinesoflocal communi-ties(Baker,1996;Gottliebetal.,1996;Huffman,1997;Cousinsand Huffman,2002;Kriefetal.,2005).
Kriefetal.(2005)alsofoundthatseveralplantspeciesincluded inthedietofchimpanzeesareusedbytraditionalhealersinlocal communitiesinAfrica.Whencorrelatingtheseplantswiththe eth-nomedicinalliterature,thoseauthorsfoundthatatleast35(21.5%) ofthe163speciesincludedinthedietofchimpanzeesareused intraditional medicine,including inthetreatmentof intestinal parasites,skininfectionsandrespiratorydiseases.Huffman(1997, 2003)alsoreportedintwo studiesofchimpanzees,that22% of thedietcontainedmedicinalplantsusedspecificallyagainst para-sitesbypeopleinAfrica.Also,astudyconductedbyMacIntoshand Huffman(2010)verifiedthat21.9%oftheplantfooditemsoften Japanesemacaquetroopsalsocontainedantiparasitic andother medicinalproperties.Theresultsofthepresentstudyaresimilar tothatreportedabove;i.e.24.5%(13/53)oftheplantsinthedietof thewoollyspidermonkeysmatchedtheplantsusedinlocalhuman medicine.
Thesestudiesshowthatalmostonequarterofplantsfoundin thedietsofprimateshavesomemedicinalvaluetohumans.This isinterestingasitindicatesacommonalitybetweenhumansand non-humanprimatesintheirselectionofplants.Furtherstudies shouldinvestigatetherelativemedicinalandnutritionalvalueof theseplants.
Cousins and Huffman (2002) indicated a strong correlation betweentheplantsusedbygorillasandtheplantsusedbylocal
communitiestotreatparasitic,fungal,viral,cardiacand respira-torydiseases.Theseusescorroboratethedatafoundinthepresent studybecausemanyofthosetherapeuticuseswerealsoreported herein.
Itis interestingthat five(38.5%) oftheplantsrecognizedby respondentsinourstudyasbeingmedicinalareusedaslaxatives and purgatives,i.e. TapiriraguianensisAubl., Copaifera trapezifo-lia Hayne, Virola bicuhyba (Schott ex Spreng.) Warb., Solanum rufescens Sendtn. and H.courbaril L. Anotherfive species have anti-parasiticactivitiesintheliterature(Box1),includingthe fol-lowingactivities;leishmanicidal:Piptadeniaadiantoides(Spreng.) J.F.Macbr.,(Camposetal.,2008),anthelmintic:FicusinsipidWilld. (deAmorinetal.,1999),antiplasmodial:GuatteriaaustralisA. St-Hil. (Fischer et al., 2004), trypanocidal: Cinnamodendron dinisii Schwacke(Andradeetal.,2015)andacaricidal:Ocoteadiospyrifolia (Meissn.)Mez(DosSantosetal.,2013)(Box1).
Amongtheplantspresentinthedietofwoollyspidermonkeys, inadditiontothetherapeuticusesoutlinedabove,wefoundtwo toxicplants,PhytolaccadioicaL.(Ashafaetal.,2010)andFicus insip-idaWilld(deAmorinetal.,1999).Thesameplantpartsshowntobe toxicarethepartsconsumedmostbythewoollyspidermonkeys whiletheyareactivelyavoidedbyotherprimatessuchas chim-panzees(Gustafssonetal.,2016).Thisshouldbeexaminedmore closelyinfuturestudies.
Conclusion
The relationships between plants, primates and humans observed in the present study indicate potential bioactive compoundstobeexaminedinfuturepharmacologicaland phyto-chemicalstudies,especiallythoseplantswithantiparasiticactivity. Bothaspectscouldsignificantlycontributetoimprovingthequality oflifeoflocalcommunitiesandtothesustainabilityoftheAtlantic Forest,especiallyatthestudysite.
Ethicaldisclosures
Protectionofhumanandanimalsubjects. Theauthorsdeclare thatnoexperimentswereperformedonhumansoranimalsfor thisstudy.
Confidentialityofdata. Theauthorsdeclarethatnopatientdata appearinthisarticle.
Righttoprivacyandinformedconsent. Theauthorsdeclarethat nopatientdataappearinthisarticle.
Authors’contributions
LPandERhavetogetheridealizedthisstudy.LPhascollected dataamongthemuriquisandERhascollectedtheethnomedicinal dataamongtheinterviewees.MAHcontributedtothewriting, anal-ysisandliteraturesearch.Allauthorshavereadthefinalmanuscript andapprovedsubmission.
Conflictsofinterest
Theauthorsdeclarenoconflictsofinterest.
Acknowledgements
WethankthepeoplelivingaroundIntervalesStateParkwho participatedin theinterviewsforproviding theirknowledge on themedicinaluseofplantsandhelpingtocollectandidentifythe speciesincludedinthedietofwoollyspidermonkeys:LuísAvelino, Ditinho,JoãoVazand Tonico.WethankSônia Aragaki,Eduardo GomesandWaldirMantovaniforhelpwithidentifyingtheplant species.WethanktheFundac¸ãoFlorestalparaaConservac¸ãoea Produc¸ãoFlorestaldoEstadodeSãoPauloforthelogisticalsupport andforallowingustoconductthisstudyatIntervalesStatePark. WethankFAPESP,CNPq,CAPES,Fundac¸ãoOBoticáriodeProtec¸ão àNatureza,andtheWorldWideFundforNaturefortheirfinancial support.Wealsothanktwoanonymousrefereesfortheirhelpful suggestionsinimprovingthispaper.
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