Matauschek2010 TaxonPhylogenDistribSaguinusPeru Thesis

GttingerZentrum
frBiodiversittsforschungundkologie
GttingenCentreforBiodiversityandEcology
TAXONOMY,PHYLOGENYAND
DISTRIBUTIONOFTAMARINS(GENUS
SAGUINUS,HOFFMANNSEGG1807)
DissertationzurErlangungdesDoktorgradesder
MathematischNaturwissenschaftlichenFakulttender
GeorgAugustUniversittzuGttingen
vorgelegtvon
Dipl.Biol.
ChristianMatauschek
aus
Mnchen
Gttingen,Dezember2010
Referent:Prof.Dr.EckhardW.Heymann
Koreferent:Prof.Dr.PeterM.Kappeler
TagdermndlichenPrfung:
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Contents
GENERALINTRODUCTION.........................................................................................................1
1.1
1.2
1.3
1.4
THETAMARINSOFTHEGENUSSAGUINUS(HOFFMANNSEGG1807) ....................................................... 2
OVERVIEWOFTHECURRENTSTATUSOFTAMARINTAXONOMY ............................................................... 2
GEOGRAPHICORIGINANDDISPERSALOFSAGUINUS ........................................................................... 10
SPECIFICQUESTIONS .................................................................................................................... 13
2 COMPLETEMITOCHONDRIALGENOMEDATAREVEALTHEPHYLOGENYOFCALLITRICHINE
PRIMATESANDALATEMIOCENEDIVERGENCEOFTAMARINSPECIESGROUPS .............................. 15
2.1 INTRODUCTION ........................................................................................................................... 17
2.2 METHODS .................................................................................................................................. 18
2.2.1
Laboratorymethods ........................................................................................................ 18
2.2.2
Phylogeneticanalysis....................................................................................................... 20
2.2.3
Estimationsofdivergenceages ....................................................................................... 21
2.3 RESULTS ..................................................................................................................................... 22
2.3.1
Phylogeneticreconstructions........................................................................................... 23
2.3.2
Estimatesofdivergenceages........................................................................................... 25
2.4 DISCUSSION ................................................................................................................................ 26
2.4.1
PhylogeneticrelationshipswithintheCallitrichinae........................................................ 27
2.4.2
PhylogeneticrelationshipswithinthegenusSaguinus.................................................... 27
2.4.3
TaxonomicimplicationsforthedifferentSaguinusspeciesgroups ................................. 29
2.4.4
Biogeographicimplications.............................................................................................. 30
3 MITOCHONDRIALPHYLOGENYOFTAMARINS(SAGUINUS,HOFFMANNSEGG1807)WITH
TAXONOMICANDBIOGEOGRAPHICIMPLICATIONSFORTHES.NIGRICOLLISSPECIESGROUP......... 33
3.1 INTRODUCTION ........................................................................................................................... 35
3.2 METHODS .................................................................................................................................. 36
3.2.1
Samplingsitesandsamplecollection .............................................................................. 36
3.2.2
Laboratorymethods ........................................................................................................ 39
3.2.3
Statisticalmethods .......................................................................................................... 40
3.3 RESULTS ..................................................................................................................................... 42
3.4 DISCUSSION ................................................................................................................................ 48
3.4.1
ThestatusofS.tripartitus................................................................................................ 48
3.4.2
ThestatusofS.melanoleucus.......................................................................................... 49
3.4.3
ThestatusofS.fuscicollissubspecies .............................................................................. 49
3.4.4
ThestatusofS.n.nigricollisandS.graellsi ..................................................................... 50
3.4.5
Speciesconceptsandgeneraltaxonomicimplications .................................................... 51
3.4.6
Biogeographicimplications.............................................................................................. 53
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4 THERANGEOFTHEGOLDENMANTLETAMARINSAGUINUSTRIPARTITUS(MILNEEDWARDS,
1878):DISTRIBUTIONSANDSYMPATRYOFFOURTAMARINSINSOUTHERNCOLOMBIA,ECUADOR
ANDNORTHERNPERU ............................................................................................................... 55
4.1 INTRODUCTION ........................................................................................................................... 57
4.2 THEDISTRIBUTIONOFSAGUINUSTRIPARTITUS.................................................................................. 57
4.3 SYMPATRY .................................................................................................................................. 64
4.3.1
Saguinusfuscicollislagonotus(JimnezdelaEspada,1870) .......................................... 64
4.3.2
Saguinusnigricollisnigricollis(Spix,1823) ...................................................................... 68
4.3.3
Saguinusnigricollisgraellsi(JimnezdelaEspada,1870)............................................... 70
4.4 SYMPATRY,BODYSIZEANDECOLOGICALNICHES ............................................................................... 74
4.5 GEOGRAPHICRANGES,SYMPATRY,ANDTHETAXONOMYOFSAGUINUSNIGRICOLLISANDS.FUSCICOLLIS .... 77
GENERALDISCUSSION ............................................................................................................ 80
5.1
5.2
5.3
SUMMARYOFRESULTS ................................................................................................................. 80
THEIMPORTANCEOFEXTANTFIELDSAMPLINGFORPHYLOGENETICSTUDIES ........................................... 83
METHODICALAPPROACH:CANMITOCHONDRIALDNASERVEASASUCCESSFULTOOLINTAMARIN
TAXONOMY?.......................................................................................................................................... 84
5.4 SPECIESCONCEPTSANDSPECIESDELIMITATIONSANDTHEIREFFECTONCONSERVATIONISSUES .................. 85
5.5 THERELEVANCEOFMOLECULARSTUDIESFORTHEUNDERSTANDINGOFAMAZONIASDIVERSITYAND
BIOGEOGRAPHY ...................................................................................................................................... 87
5.6 OUTLOOK ................................................................................................................................... 88
SUMMARY .................................................................................................................................... 89
ZUSAMMENFASSUNG.................................................................................................................... 91
BIBLIOGRAPHY .............................................................................................................................. 93
APPENDIX ................................................................................................................................... 101
DANKSAGUNG............................................................................................................................. 109
CURRICULUMVITAE .................................................................................................................... 110
ERKLRUNGBEREIGENELEISTUNGEN ...................................................................................... 111
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1 GeneralIntroduction
Primatesareoneofthemostdiverseorderswithinthemammals.About634taxaareknown
to science so far (Mittermeier et al., 2009). But the taxonomy of primates is still a field of
greatdiscussionanddynamics.Manynewspecieshavebeendescribedinrecentyears,oth
erslumpedtogether,becausenewmolecularmethodsoffernewpossibilitiestoreviewmor
phological similar taxa on a molecular basis and new species concepts prevailed (Groves,
2004).
Aswellasthenumberofnewlydescribedprimatespeciesincreased,thenumberofprimates
appearingontheIUCNredlistofthreatenedspeciesincreasedoverthepastyears.47.8 %
werelistedasthreatenedinthe2008redlist(Mittermeieretal.,2009)Someevenfaceex
tinction within the near future. The need for space of the exploding human population
causesarapidlossofhabitatforprimatesandotheranimalsandplantsaswell.Inmanyre
gionsofthetropicshuntingformeatisamajorthreatforthedecliningnumbersofprimates
(Strier,2007).Sotheresearchonprimatediversitymoreandmoregetsimportantinconser
vationissues.
To contribute to the illumination of primate taxonomy and diversity five research projects
havebeenestablishedbytheGermanPrimateCentre(DPZ)andtheUniversityofGttingen,
fundedbytheWGLPaktfrWissenschaftundInnovation.Theprojectsareconcernedwith
five primate genera, which are poorly understood in their taxonomy and biogeography:
crestedgibbons(genusNomascus)andleafmonkeys(genusPresbytis)insoutheasternAsia,
baboons (genus Papio) in southern Africa, sifakas (genus Propithecus) in Madagascar and
tamarins (genus Saguinus) in the Amazon basin of South America. The obtained results of
these projects contribute to draw broader picture of primate diversity and evolution and
shouldbedirectlyconducivetoconservationmatters.Thisparticularstudywillbeconcerned
withthetamarins(genusSaguinus).
1.GeneralIntroduction
1.1 ThetamarinsofthegenusSaguinus(Hoffmannsegg1807)
Tamarins(Saguinus)belongtotheCallitrichinae,smallbodiedNewWorldprimates,andare
oneofthemostdiversegroupsofprimates.Theyaredistributedthroughoutnorthernand
westernAmazoniauptonorthwesternColombiaandPanama.Tamarinsinhabittropicalfor
ests,openwoodlands,andsecondarygrowth.Thedietoftamarinsconsistsoffruit,sap,nec
tar, insects and small vertebrates (Garber, 1993). They are diurnal and arboreal. Head and
body length is 175310 mm, tail length is 250440 mm, and body mass is usually 225600
grams (Hershkovitz, 1977). Due to their small body size they lost one set of molars. Their
nails look like claws, which enable them to climb on trunks and trees like squirrels
(Thorndike,1968).Theyregularlyproducetwins,whichareraisedinacooperativebreeding
system,wherepredominantlythemalescarrytheinfants(RotheandDarms,1993).Theso
cial organization varies from one male one female to multimalemultifemale groups. Nor
mallyeachgroupholdsonlyonereproductivefemale(Eppleetal.,1993;Digbyetal.2007).
Groupsizenormallyrangesfrom2to13(Digbyetal.,2007).
1.2 Overviewofthecurrentstatusoftamarintaxonomy
The tamarins (Saguinus) belong to the subfamily Callitrichinae, which comprises six other
genera:theGoeldi`smonkey(Callimico),dwarfmarmosets(CebuellaandCallibella),Atlantic
marmosets (Callithrix), Amazonian marmosets (Mico), and lion tamarins (Leontopithecus)
(Rylands and Mittermeier, 2009). The positions of Leontopithecus and Saguinus within the
subfamilyhavenotbeenfullyresolvedsofar;differentstudiesrevealdifferentarrangements,
witheitherSaguinusorLeontopithecusasbasalcallitrichines(seeCortsOrtiz,2009).
ThetaxonomyofthegenusSaguinusismainlybasedontheworkofHershkovitz(1977).All
ofthefollowingstudiesconcernedwithtamarinsystematicsarerestinguponhistaxonomy
basedonmorphologicaldata,mainlythecolorofthepelage.Heidentified33differenttaxa
(Tab.1.1),whicharegroupedinto10speciesandthreesectionsandsixspeciesgroups(Fig.
1.1).
Table 1.1 The traditional taxonomy of Hershkovitz (1977) compared to a recent taxonomy of Groves (2005).
Speciesdivisionsaremarkedwithlines.
Hershkovitz1977
Groves2005
S.nigricollis group
S.nigricollisnigricollis
S.nigricollishernandezi
S.nigricollisgraellsi
S.graellsi
S.fuscicollisfuscicollis
S.fuscicollisfuscus
S.fuscicollisfuscus
S.fuscicollisavilapiresi
S.fuscicollisavilapiresi
S.fuscicolliscruzlimai
S.fuscicolliscruzlimai
S.fuscicollisilligeri
S.fuscicollisleucogenys
S.fuscicollisnigrifrons
S.fuscicollislagonotus
S.fuscicollisweddelli
S.fuscicollisprimitivus
S.fuscicollisprimitivus
S.fuscicollismelanoleucus S.melanoleucus
S.fuscicolliscrandalli
S.fuscicollisacrensis
S.fuscicollistripartitus
S.tripartitus
S.mystaxgroup
S.mystaxmystax
S.mystaxmystax
S.mystaxpluto
S.mystaxpluto
S.mystaxpileatus
S.pileatus
S.labiatuslabiatus
S.labiatuslabiatus
S.labiatusthomasi
S.labiatusthomasi
S.labiatusrufiventer
S.imperatorimperator
S.imperatorimperator
S.imperatorsubgrisescens S.imperatorsubgrisescens
S.inustusgroup
S.inustus
S.inustus
S.midasgroup
S.midasmidas
S.midas
S.midasniger
S.niger
S.bicolorgroup
S.bicolorbicolor
S.bicolor
S.bicolorochraceus
S.martinsiochraceus
S.bicolormartinsi
S.martinsimartinsi
S. oedipus group
S.leucopus
S.leucopus
S.oedipusoedipus
S.oedipus
S.oedipusgeoffroyi
S.geoffroyi
Hershkovitz (1977) divides the genus Saguinus into a hairyfaced, mottlefaced and bare
faced section. Within the hairyfaced tamarins he describes three distinct species groups.
3
TheS.nigricollisspeciesgroupincludestheblackmantletamarinS.nigricolliswiththreesub
speciesandthesaddlebacktamarinS.fuscicolliswith14subspecies.TheS.mystaxspecies
group consists of the mustached tamarin S. mystax with three subspecies, the redbellied
tamarin S. labiatus (two subspecies) and the emperor tamarin S. imperator also with two
subspecies(Hershkovitz,1977,1979).ThetwosubspeciesofS.midasformthethirdspecies
groupofhairyfacedtamarins.ThemottledfacetamarinS.inustuswasplacedinitsownsec
tionandallremainingspeciesarelistedasthebarefacedtamarinscontainingtwospecies
groups:TheS.bicolorgroup,consistingofasinglespecies,thepiedtamarinS.bicolor(with
threesubspecies)andtheS.oedipusgroupwithtwospecies,thecottontoptamarinS.oedi
pus(twosubspecies)andthewhitefootedtamarinS.leucopus(Fordistributionareasofthe
speciesgroupsseeFig.1.2).
Fig1.1ThenominatespeciesofthesixSaguinusspeciesgroups.StephenD.NashConservationInternational.
This classical tamarin taxonomy was reviewed few times and changed on some aspects
(CoimbraFilho,1990;Rylandsetal.1993;Rylandsetal.,2000;Groves,2001).Table1.1gives
anoverviewofthetraditionaltamarintaxonomyandthedifferencestonewlydatedtaxon
omy(Groves,2005).
TheinterspecifictaxonomicrelationshipsofSaguinusarequiteunsolved.Craniometricaland
dentalanalysessupportedthedivisioninthethreesectionsonlypartially(NatoriandHani
hara1988).Thefewgeneticstudiesthathavebeendonetoclarifytheinterspecificrelation
shipofSaguinusdonotsupportasplitintohairyfacedandbarefacedtamarins.Sequence
dataofthe2microglobulinnucleargeneshowedthatthebarefacedtamarinsdidnotform
asingleclade(Canavezetal.,1999).Tagliaroetal.(2005)alsoargueagainstamonophyletic
barefaced group, on the basis of the ND1 mitochondrial gene. The barefaced character
seemstohaveevolvedmorethanoncewithinthetamarins(Croppetal.,1999;Canavezet
al.,1999;Tagliaroetal.,2005).GeneticanalysisonthebasisofmitochondrialDNAsupportsa
divisionofSaguinusintotwoclades,nomatterofhairyorbarefaced:asmallbodiedanda
largebodiedclade.ThesmallbodiedcladeconsistsonlyoftheS.nigricollisgroupwhileall
otherspeciesformthelargebodiedclade(Croppetal.,1999).
Fig.1.2.DistributionareasofthesixSaguinusspeciesgroups.
5
ThetamarinsoftheS.midasgroupofnortheasternAmazoniaarequitelarge,comparedto
therelativelysmalltamarinsoftheS.nigricollisgroup.Hershkovitz(1977)liststhemastwo
subspecies(S.m.midasandS.m.niger)ofasinglespeciesS.midas.ThetaxonomyofS.mi
dasasasinglespecieswithtwosubspecieswasadoptedbyMittermeier(1988)andCoimbra
Filho(1990).ButRylandsetal.(2000)andGroves(2001)listthemastwodistinctspeciesS.
midasandS.niger.Vallinotoetal.(2006)foundthemdistinctonthebasisofmtDNAanalyses
andshowedthatdifferentpopulationsofS.nigerhavebeenisolatedforalongtimeaswell.
They share some dental and cranial characters, like the reduction of the entoconid on M1
andthelossoftheinferiorpetrosalsinusforamen,withthesocalledbarefacedtamarinsof
theS.oedipusandtheS.bicolorgroup,andexclusivelywiththeS.bicolorgroupaderived
formofthepremetacristidonP2(Natori,1988).TheS.bicolorgrouptraditionallyconsistedof
onespecies,thepiedtamarinS.bicolorwiththreesubspecies(S.b.bicolor,S.b.martinsi,S.
b.ochraceus)(Hershkovitz,1977;CoimbraFilho,1990;Rylandsetal.,1993).Inmorerecent
taxonomies,Rylandsetal(2000)andGroves(2001)dividethemintotwospeciesS.bicolor
andS.martinsi(withtwosubspeciesS.m.martinsiandS.m.ochraceus).Groves(2001)as
sumesthatS.m.ochraceusmaybeindeedastabilizedhybridformbetweenS.bicolorandS.
martinsi,duetoobservationsoncaptivehybridizationexperiments.
The other tamarins, which share the barefaced character with the S. bicolorgroup, are
groupedintotheS.oedipusandtheS.inustusspeciesgroups(Hershkovitz,1977).Thelatter
consistsonlyofonespecies,themottledfacetamarinS.inustus.Thisspeciesisnotverywell
knowntoscience.Inmorphologicalregarditseemsthatthisspeciessharesonlythederived
dentalenamelstructurewithotherspeciesgroups,inthiscasewiththehairyfacedandS.
bicolor species groups (Natori and Hanihara, 1988). The only molecular study including S.
inustus delivered no clear results,because only a small amount of sequence data could be
generatedforthisspecies(Croppetal.,1999).
TheS.oedipusgrouphasthenorthernmostdistributionofallcallitrichineprimates(Fig.1.1).
WithintheS.oedipusgroupHershkovitz(1977)originallydescribedtwospecies:S.leucopus
andS.oedipuswithtwosubspeciesS.o.oedipusandS.o.geoffroyi.Butmostauthorshave
listed the three taxa as three distinct species (Rylands et al., 1993; Rylands et al., 2000;
Groves,2001).Morphologicallytheycanbedistinguishedfromallhairyfacetamarinsbythe
narrowmaxilla(NatoriandHanihara,1988).
In contrast to the previously described species groups, the representatives of S. mystax
grouparedistributedsouthoftheAmazonriver.Theyoccurinsympatrywithdifferentrepre
sentativesoftheS.nigricollisgroupalmostthroughouttheirrangeandcommonlyformsta
bile mixedspecies troops with them (Heymann and BuchananSmith, 2000). This species
groupischaracterizedbysomespecificmorphologicalattributes,likethelengthoftheinci
siverelativetothewidth(Natori,1988).CraniometricaldataplacesthemneartotheS.nigri
collisgroup(NatoriandHanihara,1988).Incontrasttothis,firstgeneticapproachesindicate
acloserrelationshiptotheotherSaguinusspeciesthantotheS.nigricollisgroup(Croppet
al.,1999;Tagliaroetal.,2005).TraditionallytheS.mystaxgroupconsistsofthemustached
tamarinS.mystaxwiththreesubspecies,thewhitelippedorredbelliedtamarinS.labiatus
with two subspecies and the emperor tamarin S. imperator with also two subspecies
(Hershkovitz,1977,1979).WithinS.mystaxthedistinctionbetweenthedifferentsubspecies
is not very clear. Two of the three traditionally featured subspecies, S. m. pluto and S. m.
pileatus, are only known from few museum specimens, with partly uncertain localities. So,
thetaxonomicstatusofthesetamarinsisascrypticastheirdistributionareas.Groves(2001)
arguestogivefullspeciesranktotheredcappedtamarinS.pileatus,whichisfeaturedasa
subspeciesofS.mystaxbyotherauthors(Hershkovitz,1977;Rylandsetal.,1993).Tradition
allytwosubspeciesofthewhitelippedtamarinS.labiatusarerecognized(Hershkovitz,1977;
CoimbraFilho,1990;Rylandsetal.,1993).Butsomeevidenceisgivenbyexaminationofthe
colorpatternofthecrownspotsofmuseumspecimens,thattheremaybeanothersubspe
ciesS.l.rufiventer(Groves,2001;Rylandsetal.,2000).ThesubspeciesS.l.thomasiwaslong
timeonlyknownfromthetypelocality,whichisratherdistanttothedistributionareasofthe
other whitelipped tamarins. It was also described north of the Amazon river, but remains
cryptic(Hershkovitz,1977;Silva1988).WithintheS.mystaxgroupthetwosubspeciesofthe
emperortamarinS.imperatorseemonlytobedistantlyrelatedtotheothertaxa,regarding
craniometricaldata(HaniharaandNatori,1989).
ThespeciesgrouponwhichwillbegiventhemainemphasisinthisstudyistheS.nigricollis
group, which is the most widely distributed and most diverse group (Fig. 1.3). Hershkovitz
(1977)groupedthe17taxaintotwospecies,theblackmantledtamarinS.nigricollis(bizonal
7
colorpattern)andthesaddlebacktamarinS.fuscicollis(trizonalcolorpattern).Hedescribes
14taxaofsaddlebacktamarins,differentincolorpatternanddistribution,whichheallcon
sidersassubspeciesofonewiderangingspeciesS.fuscicollis.Heexplainstheseparation,as
wellastheradiationofthedifferentsubspecies,withthetheoryofmetachromismbasedon
thecoatcoloration(Hershkovitz,1968,1977).Thistheoryofreconstructingmammalradia
tions by means of bleaching and saturation of coat coloration was already highly disputed
decadesago(Lawlor,1969).
ThedifferentsubspeciesofS.fuscicollisare,inmostcases,clearlyseparatedbyriverchan
nels, where they often occur within sight and calling distance to each other on opposite
banksofariver(Hodun,1981)(Fig.1.3).Whereasrelativeagreementbetweenthedifferent
authorsexistswithregardtothenumberofdifferenttaxawithinthesaddlebacktamarins,
thestatusofthedifferenttaxaasspeciesorsubspeciesisfairlycontroversial.Sometaxahave
onlybeendescribedfromveryfewmuseumspecimens,withanoftendoubtfullocation,like
S. f. primitivus and S. f. cruzlimai. Their distribution areas were placed by Hershkovitz only
due to some uncertaininformation of the type localities. For many interfluvial areas is not
evenknownwhichtypeoftamarinsexists.OneoftheseareasisthelargeareabetweenRio
NapoandRioPutumayoinPeru,forexample.Recentlyanewtaxon,S.f.mura,wasdescribed
inBrazil(Rheetal.,2009).
Fig.1.3ThePeruviantaxaoftheS.nigricollisgroupandtheirschematicdistributionbetweenthemajorrivers.
TamarindrawingsbyStephenD.NashConservationInternational.
The goldenmantle tamarin S. tripartitus, considered as a subspecies of S. fuscicollis by

Hershkovitz, was given full species rank by other authors referring on the grounds of sup
posedsympatrywithS.f.lagonotus(Thorington,1988).Fromthemorphologicalandecologi
cal point of view, the differences between S. tripartitusand S. f. lagonotus seem not to be
biggerthandifferencesbetweenotherS.fuscicollissubspecies,whichmeansthat,ifS.tripar
9
titusisconsideredasadistinctspecies,other,perhapsallothers,subspeciesofS.fuscicollis
shouldbetreatedasspeciesaswell(Heymann,2000).
AnotherpointofdiscussionwithintheS.fuscicolliscomplexisthetaxonomicstatusofS.f.
melanoleucus which is distributed between the Rio Jurua and Rio Tarauacu in Brazil. First
CoimbraFilho(1990)listedS.melanoleucusasadistinctspecies,withS.f.acrensisandS.f.
crandalliassubspeciesofS.melanoleucus.IntheheadwaterregionoftheRioJuruathereis
hybridizationwithS.f.fuscicollis,whichleadtointermediategenoandphenotypesonthe
leftbankoftheheadwaterstream(Peres,1996).Peresalsoassumethattheacrensispelage
aswellasthecrandallipelagecouldrepresentonlycolormorphsofS.melanoleucus,which,
thus,wouldbeamonotypicspecies.Thecrandallimorphcouldalsobetheresultofhybridi
zationbetweenS.melanoleucusandS.f.fuscicollis(Rylandsetal.,2000).
TheblackmantletamarinislistedbyHershkovitz(1977)asonespeciesS.nigricolliswiththe
threesubspeciesS.n.nigricollis,S.n.hernandezi,andS.n.graellsi.Thestatusofthelatteris
subjecttodiscussionswhetheritshouldbeelevatedtofullspeciesrank.Thisassumptionis
basedontheassertionofS.graellsilivingsympatricwithS.nigricollisinsouthernColombia
(regionofPuertoLeguizamo)(HernandezCamachoandCooper,1976).S.graellsiisfeatured
asadistinctspeciesbyRylandsetal(2000)andGroves(2001).IngeneticstudiesS.f.fuscus
showedmoresimilaritieswithS.nigricollisthanwithotherS.fuscicollissubspecies(Croppet
al.,1999).MooreandCheverud(1992)suggestedtheelevationofthissubspeciestofullspe
ciesrank,duetodifferencesinfacialmorphology.
Insummary,thestatusofS.fuscicollisandS.nigricollisasmonophyleticspeciescanbecon
sideredasquitequestionable.
1.3 GeographicoriginanddispersalofSaguinus
The radiation and dispersal of the Callitrichinae throughout the Amazon basin remains a
pointofgreatdiscussionandisstillquiteenigmatic.InthisperspectiveSaguinusappearsto
beoneofthemostcomplicatedgenera(NatoriandHanihara,1988).Littlefossilevidenceis
availableforcallitrichineprimates(Croppetal.,1999),ThefewfossilsassignedtotheCallitri
chinaearehighlydisputed,suchastheoftenhighlightedLagonimicofromtheLaVentafor
10
mationinColombia(MiddleMiocene),describedasgianttamarinbyKay(1994),butcon
sidered as pithecine by Rosenberger (2002). Another fossil from La Venta, Mohanamico, is
considered as callimiconin callitrichine (Rosenberger et al., 1990). So theories for the bio
geographichistory of Saguinus mainly dependon morphological, molecularand behavioral
evidence. To understand the biogeography of this genus, different approaches, amongst
whichistheuseofmolecularanddivergenceageestimates,shouldbecombinedwithavail
ablemorphologicalandbehavioralinformationandwithgeneralmodelsofspeciationproc
essesinAmazoniaandthegeologicalhistoryoftheregion.
Sofar,therearebasicallytwodifferenttheoriesforthephylogeographicoriginofthegenus
Saguinus, and how they dispersed across their current range. One is given by Hershkovitz
(1977),theotherbyFerrari(1993).BotharebasedontheassumptionofPleistocenerefugias
as origins of dispersal. The problem with these two models is that they argue in complete
contrary directions. Hershkovitz` theory of the Saguinus radiation is based on the current
distributionofSaguinusandthetheoryofmetachromism.Heregardsalargerbodysizeasa
derivedcharacter.Accordingtothat,theancestraltamarinwasarathersmallanimalwithan
agoutipelage.Duetothis,heconsiderstherecentS.nigricollisasthemostbasaloftheliving
tamarins, with the agouticolored S. n. graellsi as a relict near to the ancestral type
(Hershkovitz,1977).SoHershkovitzpostulatestherangeoftheancestraltamarinwithinthe
rangeoftheS.nigricollisspeciesgroupinthewesternAmazonbasin.Theoriginoftamarin
dispersalwouldstartinsouthernPeruandnorthernBoliviaalongtheeasternAndeanbase.
FromtheserefugiaHershkovitzsuggeststwodispersalroutes,onenorthwardsleadingtothe
S. inustus and S. oedipus species groups and another northeastern route, leading to the S.
bicolorandS.midasspeciesgroups.
Ferrari(1993)contradictsHershkovitz`theorybyrecurringtothephyleticdwarfismhypothe
sis(Ford,1980)toexplainthecallitrichidradiation.Thekeywordsinthishypothesisarebody
sizeandecology.Hedescribestheancestralcallitrichidasarelativelargemonkey,notvery
specialized in its ecology and especially feeding habits. Thus, the smallbodied forms (i.e.
Cebuella)wouldbethemostderived,andnotthemostprimitiveasHershkovitzargues.Also,
the gumfeeding specialization in marmosets is seen as a highly derived character. Within
SaguinushedescribesthesmallbodiedandhighlygumfeedingS.fuscicollisasthemostde
rivedformandthelargerbodiedandprobablyleastgummivorusS.midasasthemostprimi
11
tive one (Ferrari, 1993). So Ferrari claims that the initialradiation of the tamarins is repre
sentedbytheS.midas/S.bicolorgroup.Thesecondtamarinradiationcouldhavebeenthe
mustachedtamarinsandthethirdthesaddlebacktamarins.Smallsize,increasedgummivory
and specialized foraging behavior of the saddleback tamarins (S. fuscicollis) could be ex
plainedbytheselectivepressureexertedbymembersofthemustachedgroup,livingsym
patricwithS.fuscicollisinmostpartsoftheirrange.Ferrariproposestheoriginofthegenus
withinthecurrentdistributionofS.midasinthenortheastoftheAmazonbasin.Fromthis
regionnorthoftheAmazonriverandeastoftheRioNegrohesuggestsdifferentdispersal
routeinalldirections,withonesouthwesternroutewhichleadtotheS.mystaxandS.nigri
collisspeciesgroups.
Onlyfewstudieshavebeenpublishedtocontributetothisdiscussion.However,theradiation
ofSaguinusisstillfarfromsolvedandalsothemechanismsofspeciationprocessesremain
ingquiteambiguous.Onlyfewmoleculargeneticstudiesinthepastwereconcernedwiththe
taxonomyandbiogeographyofthetamarins.Mostofthemwerebasedonmuseumspeci
mens and captive animals, which often cannot be assigned to a certain geographic origin.
This is the first comprehensive molecular assessment of tamarin taxonomy and phylogeny
usinggeoreferencedsamplesfromwildtamarinpopulations.
12
1.4 Specificquestions
Thecurrentstudywasdesignedtoreexaminetamarinevolution,taxonomyandbiogeogra
phy.WeconductedtwocomprehensivefieldexpeditionsthroughoutthePeruvianAmazonof
intotal10month.Forthegeneticanalysiswecollectedover100samplesofwildtamarins
from 29 locations covering 12 of 13 taxa, described for the country. Furthermore we col
lecteddataondistributionareas,barriersorpossiblesympatry.Interviewswithlocalhunter
usingpicturesanddrawingsprovidedreliableinformationonthelocalprimatefauna.
PhylogeneticrelationshipswithinthegenusSaguinus:
WhatisthepositionofSaguinuswithintheCallitrichinae?
Howarethephylogeneticrelationshipsamongthedifferenttamarinspeciesgroups?
WastheancestraltamarinmoresimilartotheS.nigricollisortotheS.midasspecies
grouporhasanothermodeltobedeveloped?
Whichtaxonomicimplicationscanbemadeonthegenusandsubgenuslevel?
PhylogenyoftheS.nigricollisspeciesgroup:
AreS.fuscicollisandS.nigricollismonophyleticspecies?
CanwedelimitatespecieswithinthediverseS.nigricollisgroup?
WhatisthetaxonomicstatusoftheproposedspeciesS.graellsi,S.tripartitusandS.
melanoleucus,andtheirrelationshiptotheremainingtamarintaxa?
CanwedetectanysympatrybetweentaxaoftheS.nigricollisgroup?
BiogeographyofSaguinus:
WhatisthegeographicoriginanddirectionoftheSaguinusradiation?
Canwefindeventualcoincidencewithpalaeogeographichistoryofthe Amazonba
sin?
Did they cross the main Amazon channel or was it more or less a parallel dispersal
northandsouthoftheAmazon?
13
These questions are addressed in the current study. The structure of the study comprises
threemainparts.
The first part (chapter 2) starts with a broader perspective, illuminating the phylogenetic
relationshipswithintheCallitrichinaeonabroaderscale,includingnearlyallgeneraandspe
ciesgroups.SpecialemphasisinthispartisgiventhepositionofthedifferentSaguinusspe
cies groups within the callitrichine tree and the comparison of divergence ages between
marmosetsandtamarins.Thereforethesequencedataofwholemitochondrialgenomesis
used.
The second part (chapter 3) goes more into detail by focusing on the S. nigricollis species
group,whichisthemostdiversegroupandwithitsnumeroustaxa,subspeciesand/orcolor
variants and cryptic distribution areas surely one of the most complicate genera of New
World primates. More variable markers and samples from 100 wild tamarins with known
originareusedtodefineclustersandlineages,whichprovideabasisforspeciesdelimitations
andataxonomicrevisionofthespeciesgroup.
Thethirdpart(chapter4)isbringingtogethertheinformationondistributionareas,distribu
tionlimitsandsympatryofcertaintaxaoftheS.nigricollisgroup,obtainedduringourextant
fieldsurveysinthePeruvianAmazon,withtheevidenceofotherfieldresearchersandthe
current knowledge provided by museum specimens and historic reports. This provides a
comprehensive overview over the distribution areas and possible sympatry of at least four
tamarintaxa,whicharecrucialtounderstandthetaxonomyofthisspeciesgroup.
14
2 Completemitochondrialgenomedatarevealthephy
logenyofcallitrichineprimatesandalateMiocenedi
vergenceoftamarinspeciesgroups
ChristianMatauschek1,EckhardW.Heymann1,KnutFinstermeier2&ChristianRoos3
Unit of Behavioral Ecology and Sociobiology, German Primate Center, Kellnerweg 4, D
37077Gttingen,Germany
2
MaxPlanckInstituteforEvolutionaryAnthropology,IndependentJuniorResearchGroupof
MolecularEcology,DeutscherPlatz6,D04103Leipzig,Germany
3
GeneBankofPrimatesandPrimateGeneticsLaboratory,GermanPrimateCenter,Kellner
weg4,D37077Gttingen,Germany
Correspondingauthor:ChristianMatauschek,BehavioralEcologyandSociobiologyUnit,GermanPrimateCen
ter, Kellnerweg 4, D37077 Gttingen, Germany, Tel.: +495513851468, email: christian.matauschek@t
online.de
Forsubmissionto:PLosONE
15
2.PhylogenyoftheCallitrichinae
Abstract
TheCallitrichinaearesmallbodiedNewWorldprimates,includingtwoofthemostdiverse
groups of primates, the marmosets (genera Callithrix and Mico) and tamarins (genus Sa
guinus).Thephylogeneticrelationshipswithinthissubfamilyandinparticularthephylogeny
ofthesixspeciesgroupsoftamarins(Saguinus)andtheirpositionwithintheCallitrichinaeis
disputed. To further address these issues, we sequenced 13 complete mitochondrial ge
nomesofallcallitrichinegeneraandnearlyallSaguinusspeciesgroups.Basedon ourphy
logeneticreconstructions,SaguinusbranchedofffirstamongCallitrichinae,followedbyLeon
topithecus. Among the remaining genera, Callimico is basal, and Mico and Cebuella form
sistergeneratotheexclusionofCallithrix.ThegenusSaguinusisfurtherdividedintovarious,
unexpectedly old lineages. We found much older and deeper phylogenetic splits between
differentspeciesgroupsofSaguinusthanbetweenthedifferentgeneraofmarmosets.TheS.
nigricollisgroupsplitofffromothertamarinsinthelateMiocenearound9.5mya.Theother
speciesgroupsdivergedbetween7.5and5.3mya.Thetaxonomicnomenclatureofthedif
ferentspeciesgroupsshouldberevisedandwerecommendanelevationtogenericlevelfor
atleasttheS.nigricollisspeciesgroup.Webringourdatatogetherwiththecurrentstandard
of knowledge of Amazonian geology. Our data support a WestAmazonian origin and an
eastwarddispersalofthegenusSaguinus.
16
2.1 Introduction
guinus). Rosenberger (1981) grouped them as subfamily Callitrichinae into the family Ce
bidae together with the subfamily Cebinae. Rylands and Mittermeier (2009) keep them as
familyCallitrichidae,ratherthansubfamilyCallitrichinae.Sevengeneraarecurrentlyrecog
nized:Goeldi`smonkey(Callimico),dwarfmarmosets(CebuellaandCallibella),Atlanticmar
mosets(Callithrix),Amazonianmarmosets(Mico),tamarins(Saguinus)andliontamarins(Le
ontopithecus)(RylandsandMittermeier,2009).
InthelasttwodecadesanalysesofDNAsequencedatahavesignificantlyincreasedourun
derstandingofthephylogeneticrelationshipsamongNewWorldprimates.Thephylogenetic
relationships within the Callitrichinae on the genus level have been addressed in several
studiesandarequitegoodresolvedongenericlevel.OnlythepositionofLeontopithecusand
Saguinushasnotbeenfullyresolvedsofar;differentstudiesrevealdifferentarrangements,
witheitherSaguinusorLeontopithecusasbasalcallitrichines(seeCortsOrtiz,2009).Mean
while the longtime debate about the position of the monotypic genus Callimico is almost
completed.MoleculardatastronglysupportasisterrelationshipbetweenCallimicoandthe
marmosets(CroninandSarich,1975;Seuanezetal.,1989;Schneideretal.,1993;Pastoriniet
al.,1998;Chavesetal.,1999;Canavezetal.,1999).
The internal phylogeny of the marmosets is less clearly resolved. A number of studies
showedacloserphylogeneticrelationshipbetweenCebuellaandtheAmazonianmarmosets
thanbetweenAmazonianandAtlanticmarmosets,andthereforesupportanowngenusfor
the Amazonian marmosets (Mico) (Rosenberger, 1981; Barroso et al., 1997; Porter et al.,
1997;Tagliaroetal.,1997).Groves(2001,2005)listsCebuella,CallibellaandMicoassubgen
eraofCallithrix.
Incontrasttothemarmosets,thephylogenyofthetamarinshasbeenwidelyneglected.The
currentclassificationofthegenusSaguinusismainlybasedonstudiesofHershkovitz(1977)
whoidentified33taxa,groupedintosixspeciesgroups.Hedividedthespeciesgroupsinto
three sections: hairyfaced (S. nigricollis group, S. mystax group), mottlefaced (S. inustus)
andbarefacedtamarins(S.midasgroup,S.oedipusgroup,S.bicolorgroup).Thefewgenetic
17
studiesthathavebeenconductedtoclarifytheinterspecificrelationshipofSaguinusdonot
supportasplitintohairyfacedandbarefacedtamarins(Croppetal.,1999;Canavezetal.,
1999; Tagliaro et al., 2005). They rather support a division of Saguinus into two clades, no
matter of hairy or barefaced: a smallbodied and a largebodied clade. The smallbodied
clade consists only of the S. nigricollis group,while all other speciesform the largebodied
clade(Croppetal.,1999).With1617taxatheS.nigricollisspeciesgroupisthemostdiverse
ofallSaguinusspeciesgroups(Hershkovitz,1977).
Hershkovitz(1977)proposedthesmallbodiedS.nigricollisgroupasthemostprimitiveone
andconcludedthattheoriginoftheentiregenusliesinwesternAmazoniawithinthecurrent
distributionareaofthisspeciesgroup.Incontrast,Ferrari(1993)regardedthemasmostde
rived and recognized the relatively largebodied S. midas group as the ancestral tamarins
withanortheasternAmazonianorigin.
MostofthedescribedspeciesgroupsofSaguinusareconfirmedintheirmonophyly,buttheir
phylogeneticrelationshipsarenotfullyresolvedandalsoseriousestimationsofdivergence
agesarestilllacking.ThisstudyincludesallgeneraandsubgeneraoftheCallitrichinae(ex
ceptforthedwarfmarmosetCallibella),andnearlyallspeciesgroupsofSaguinus(exceptS.
inustus). The use of whole mitochondrial genomes provides a solid basis for phylogenetic
reconstructions and in particular (1) illuminating the phylogenetic relationships between
differentSaguinusspeciesgroups,(2)examiningtheirphylogeneticage,alsoincomparison
withthedifferentgeneraofmarmosetsand(3)reconstructingthebiogeographichistoryof
thegenusSaguinus.
2.2 Methods
2.2.1 Laboratorymethods
Blood,tissueorfecalsamplesfromrepresentativesofsixcallitrichinegeneraaswellasfrom
severaloutgrouptaxawereobtainedfromspecimenskeptinzoosorbreedingfacilities,or
collected in the field (Table 2.1). Sample collection was conducted according to relevant
Germanandinternationalguidelines,includingcountrieswherewecollectedsamples.Fae
calsampleswerecollectedinanoninvasivewaywithoutdisturbing,threateningorharming
theanimals.Bloodsamplesweretakenbyveterinariansfordiagnosticreasonstocheckthe
18
healthstatusoftherespectiveindividuals,andtissuesampleswereobtainedonlyfromde
ceased specimens. Total genomic DNA was extracted with the DNeasy Blood & Tissue or
QIAamp DNA Stool Mini kits from Qiagen. Extractions followed standard protocols as rec
ommended by the supplier, with the exception that the DNA was diluted in HPLC quality
waterandstoredat20Cbeforefurtherprocessing.
Toreducethelikelihoodofamplifyingnuclearpseudogenes(numts),completemitochondrial
genomes from 13 species (Saguinus fuscicollis weddelli, Saguinus nigricollis nigricollis, Sa
guinus midas, Saguinus bicolor, Saguinus oedipus, Saguinus labiatus labiatus, Mico argen
tatus,Callithrixgeoffroyi,Callimicogoeldii,Cebuellapygmaea,Leontopithecusrosalia,Aotus
azarae,Saimiriboliviensis)weregeneratedfollowinganapproachinwhichoverlappingfrag
mentswereamplifiedvialongrangePCR(Sterneretal.,2006).Forhighqualitymaterial,we
performedtwolongrangePCRs,eachwithalengthof10kblong,whileforDNAextracted
fromfeces,uptofour5kblongfragmentsweregenerated.
AlllongrangePCRswereperformedwiththeSuperTaqPluspolymerasefromAmbionfollow
ingprotocolsofthesupplier.LongrangePCRampliconswereseparatedon1%agarosegels,
excised from the gel, purified with the Qiagen Gel Extraction kit and used as template for
nested PCRs. PCR conditions for all nested PCR amplifications (for primers and amplified
fragments see Supplementary Table 2.1 and Supplementary Figure 2.1) were identical and
comprisedapredenaturationstepat94Cfor2min,followedby30cycleseachwithdenatu
rationat94Cfor1min,annealingat60Cfor1min,andextensionat72Cfor1.5min.At
theend,afinalextensionstepat72Cfor5minwasadded.NestedPCRproducts(8001,200
bp in length) were cleaned with the Qiagen PCR Purification kit and sequenced on an ABI
3130xl sequencer using the BigDyeTMTerminator v1.1 Cycle Sequencing Kit (Applied Biosys
tems). The results of the PCR amplifications were checked by running an aliquot on a 1 %
agarose gel, stained with ethidium bromide. PCR products were purified using Mon
tageTMPCRCentrifugalFilterDevices(Millipore)followingthedeliveredinstructions.Forone
of the fragments in Callimico goeldii, the PCR product was cloned into a pGEM vector
(pGEMTMT Easy Vector System I, Promega), averaging 24 clones. Both strands of the PCR
productsweresequenced,usingtherespectiveprimerpairusedforamplificationandstan
dardvectorprimersM13FandM13Rfortheclonedproducts.Topreventcrossspeciescon
tamination, we followed standard methods as described in Roos et al. (2008). Direct se
19
quencingrevealednomultiplepeaksorinconsistentpositionsinoverlappingfragmentsand,
thus,numtsaremostlikelynotincludedinourdataset.Moreover,allproteincodingregions
were correctly transcribed. Newly generated sequences will be deposited at GenBank and
availableunderaccessionnumbersXXXX(Table2.1).
Table2.1OriginofthesamplesandGenBankaccessionnumbersofcompletemitochondrialgenomesequences
fromstudiedcallitrichineandotherprimates.
Taxon
Callimicogoeldii
Callithrixgeoffroyi
Micoargentatus
Cebuellapygmaea
Saguinusoedipus
Saguinusbicolor
Saguinusmidas
Saguinuslabiatuslabiatus
Saguinusnigricollisnigricollis
Saguinusfuscicollisweddelli
Leontopithecusrosalia
Aotusazarae
Saimiriboliviensis
Cebusalbifrons
Atelesbelzebuth
Callicebusdonacophilus
Papiohamadryas
Theropithecusgelada
Macacafascicularis
Pantroglodytes
Homosapiens
Origin/GenBankaccessionno.
MulhouseZoo,France
DresdenZoo,Germany
RomagneZoo,France
MulhouseZoo,France
GermanPrimateCenter
MulhouseZoo,France
MulhouseZoo,France
PandoDept.,Bolivia
Peru,RioApayacu
Peru,RioTambopata
KrefeldZoo,Germany
RomagneZoo,France
NurembergZoo,Germany
AJ309866
FJ785422
FJ85423
NC_001992
FJ785426
FJ906803
CHPMTB
AF346963
2.2.2 Phylogeneticanalysis
Sequences were assembled and manually edited using GENEIOUS 4.8 (Drummond et al.,
2009). For statistical analysis, additional sequences deposited in GenBank were included in
ourdataset.ThesecomprisedtheplatyrrhinesCebusalbifrons,AtelesbelzebuthandCallice
busdonacophilusandthecatarrhinesMacacafascicularis,Papiohamadryas,Theropithecus
gelada,PantroglodytesandHomosapienswhichwereusedasoutgroup.Thefinalalignment
comprised21completemitochondrialgenomesequences.Alignmentswereconductedwith
ClustalW as implemented in GENEIOUS 4.8 and corrected by eye. Poorly aligned positions
and indels were eliminated using GBLOCKS 0.91b (Castresana, 2000). Therefore, a relaxed
20
selectionofblockswasused(TalaveraandCastresana,2007).Aftertheeliminationofthese
sites and also of the control region, the original alignment with a length of 16,752 bp was
reducedto14,263bp(datasetmt1).Allanalyseswereconductedalsowithaseconddata
set,includingonlyproteincodinggenesoftheheavystrand(datasetmt2).Thefinalalign
mentlengthofthisdatasetwas10,810bp.Phylogenetictreeswerecalculatedforalldata
sets with a maximumlikelihood (ML) and a Bayesian approach. For both analyses, the
GTR+I+GmodelwasselectedastheoptimalnucleotidesubstitutionmodelwithjMODELTEST
0.1.1(Posada,2008)usingtheAkaikeInformationCriterion(AIC).MLtreeswereconstructed
with GARLI 0.96.win23 (Zwickl, 2006). 500 pseudoreplications were conducted to estimate
MLbootstrappercentages.A50%consensustreewascalculatedinPAUP4.0b10(Swofford,
2002).BayesiananalyseswerecarriedoutinMrBAYESv3.1.2(Hulsenbecketal.,2001;Ron
quistandHulsenbeck,2003).Ineachanalysis,fourMonteCarloMarkovchains(MCMC)with
adefaulttemperatureof0.2andachainlengthof10,000,000generationswereperformed.
Trees and parameters were sampled every 1,000 generations. 2,500 of the sampled trees
werediscardedasburnin.ObtainedphylogenetictreeswerevisualizedandeditedusingFig
Treev1.3.1(Rambaut,2006).
2.2.3 Estimationsofdivergenceages
CalculationsofdivergenceageswerecarriedoutusingaBayesianapproachimplementedin
the programme BEAST (Drummond and Rambaut, 2007). We used a GTR model with a
gammadistributedratevariationbetweensitesandinvariantsitesasoptimalnucleotidesub
stitutionmodel.ThemodelwaschosenbyjMODELTEST2.2usingAkaikeInformationCrite
rion(AIC)(Posada,2008).Fortheanalysis,weusedarelaxedlognormalclockmodelofline
age variation, and for branching rates, a Yule process as prior was assumed. Since the
estimationofphylogeneticrelationshipswasnotthemainaimofthisanalysis,weusedana
priorifixedtreetopologyasobtainedfromphylogeneticreconstructionsandpublisheddata
fortaxaotherthanSaguinus(Osterholzetal.,2009).Analyseswererunfor25,000,000gen
erations,withtreeandparametersamplingevery1,000generations,ofwhich10%weredis
cardedasburnin.Theadequacyofa10%burningandconvergenceofallparameterswere
assessed by visual inspection of the trace of the parameters across generations using the
21
software TRACER v1.3 (Rambaut and Drummond, 2005). Subsequently,the sampling distri
butionsofmultipleindependentreplicateswerecombinedusingthesoftwareLogCombiner
v1.4.6 and then summarized and visualized using the software TreeAnnotator v1.4.6. Both
programsarepartoftheBeastpackage(Drummond,2007).FortheBayesianMCMCmethod
weusedarelaxedlognormalclockmodeloflineagevariationandforbranchingratesweas
sumedaYuleProcessasprior.
Fourcalibrationpointsbasedonwelldocumentedfossilswereused.ThesplitbetweenPan
andHomowasdatedabout67myaago(Brunetetal.,2002,Vignaudetal.,2002)andbe
tweenTheropithecusandPapioatabout3.54.5myaago(Leakey,1993;Delsonetal.,2000).
FortheinitialsplitbetweenplatyrrhinesandcatarrhinesPouxetal.(2006)givearangefrom
about3440mya.Withinplatyrrhines,thefossilrecordisratherscarce.Forafourthcalibra
tionpointwithintheplatyrrhinelineageweusedthesplitbetweenSaimiriandCebus,which
wasdatedbyLavergneetal.(2010)atabout16mya,withaupperlimitof20mya,markedby
Dolichocebus (Szalay & Delson, 1979) and a lower limit of about 12 mya, resulting from
Neosaimiri,datedbyStirton(1951).
Instead of hardbound calibration points, we used published dates as a normal distribution
prior for the respective node. For C1 (HomoPan) this translates into a normal distribution
withameanof6.5myaandastandarddeviation(SD)of0.31,forC2(TheropithecusPapio)
intoameanof4myaandaSDof0.31,forC3(CatarrhiniPlatyrrhini)intoameanof37mya
andaSDof1.8andforC4(SaimiriCebus)ameanof16myaandaSDof2.0.
2.3 Results
Wesuccessfullysequencedmitochondrialgenomesfrom13cebidprimates(Saguinusfusci
collis,S.nigricollis,S.midas,S.labiatus,S.oedipus,S.bicolor,Callithrixgeoffroyi,Micoargen
tatus,Cebuellapygmaea,Callimicogoeldii,Leontopithecusrosalia,Saimiriboliviensis,Aotus
azarae). All of them show the typical organization of mammalian mitochondrial genomes,
including13proteincodinggenes,tworRNAgenes,22tRNAsandthecontrolregion.
22
2.3.1 Phylogeneticreconstructions
MaximumlikelihoodandBayesianreconstructionsrevealidenticaltreetopologies(Fig.2.1).
AllsplitswithintheCallitrichinaeareverywellsupportedbystrongbootstrapvaluesandpos
terior probabilities for all nodes in both data sets. The only exception is the split between
Leontopithecus and the marmoset/Callimico clade, which is only weekly supported by ML
bootstrapvalues(Fig.2.1).WithintheplatyrrhinesCallicebusasrepresentativeofthePithe
ciidae family branches off first, followed by Ateles as representative of the Atelidae family.
AmongCebidae,CebusandSaimiriclustertogethertotheexclusionofAotus.TheCallitrichi
naeformamonophyleticgroupwithabasalpositionofSaguinusandLeontopithecusbranch
ingoffassecondlineage.Callimico,Cebuella,CallithrixandMicoshowacloserelationship.
Within the marmosets, Cebuella is related with the Amazonian marmosets of the genus
Mico.WithinSaguinuswefindawellsupporteddeepinitialsplitbetweenthesmallbodied
S.fuscicollisandS.nigricollisontheonehandandallotherlargerbodiedrepresentativesof
the S. mystax, S. bicolor, S. midas and S. oedipus group on the other hand. Within the
largebodied clade we find a separation of South Amazonian (S. mystax group) and North
Amazonian(S.bicolor,S.midasandS.oedipusgroup)lineages.S.labiatus(representingthe
S.mystaxgroup)branchesofffirst,whileS.midasandS.bicolorformacladetotheexclusion
ofS.oedipus.
23
Fig.2.1Phylogrambasedonthe21mitochondrialgenomes,asrevealedbyBayesiananalysis.Bootstrapvalues
forMLareindicatedtogetherwithposteriorprobabilitiesfortheBayesianapproach(ML/Bayesian)fordataset
mt1abovebranchesandfordatasetmt2belowbranches(*:100/1).
24
2.3.2 Estimatesofdivergenceages
Accordingtodivergenceageestimations(Fig.2.2,Table2.2),thesplitbetweenplatyrrhines
andcatarrhinesisdatedat37.4mya(C1)(for95%credibilityintervalsseeTable2.2),thesplit
betweenHomoandPanat6.39mya(C2)andbetweenTheropithecusandPapioat4.0mya
(C3). Among platyrrhines, the initial split separating Callicebus from the other platyrrhines
occurred 20.24 mya (N3). Cebus + Saimiri split 14.4 mya (C4). Within the Callitrichinae Sa
guinus branched off first, around 13.29 mya (N7). The initial division within Saguinus oc
curred9.2mya(N12).ThisdivisionseparatedallmembersoftheS.nigricollisgroupfromthe
largebodied tamarins. S. nigricollis and S. fuscicollis, here represented by S. f. weddelli di
verged 2.86 mya (N13). Among the largebodied tamarins, the mustached tamarin species
group (S. labiatus) split from S. oedipus, S. midas and S. bicolor shortly after the initial Sa
guinusdivision7.3mya(N14).TheseparationbetweenS.oedipusandtheS.midas/S.bicolor
cladeoccurred5.32mya(N15)andthesplitbetweenthelattertwoaround2.87mya(N16).
Table2.2Bayesiandivergenceageestimatesinmya*.
Node
mean
95%credibility
interval
C1CatarrhiniPlatyrrhini
N1Hominoidea(Homo+Pan)Cercopithecoidea(Macaca+ Papio
C2HomoPan
N2MacacaTheropithecus+Papio
C3TheropithecusPapio
N3PitheciidaeCebidae+Atelidae
N4AtelidaeCebidae
N5CallitrichinaeCebus+Saimiri+Aotus
N6AotusCebus+Saimiri
C4SaimiriCebus
N7 Saguinus Leontopithecus + Callimico + Callithrix + Mico +
N8LeontopithecusCallimico+Callithrix+Mico+Cebuella
N9CallimicoCallithrix+Mico+Cebuella
N10CallithrixMico+Cebuella
N11MicoCebuella
N12Saguinus
N13S.nigricollisS.fuscicollis
N14S.labiatusS.oedipus+S.midas+S.bicolor
N15S.oedipusS.midas+S.bicolor
N16S.midasS.bicolor
25
37
24.59
6.39
10.11
4.0
19.97
18.11
16.58
15.9
14.4
13.29
12.49
10.63
5.3
4.0
9.2
2.86
7.3
5.32
2.87
34.1440.63
19.5530.12
5.796.98
7.612.82
3.544.66
16.8723.52
15.2921.1
14.0819.32
13.4518.59
11.9716.88
11.1415.65
10.3514.76
8.5812.87
3.817.01
2.725.53
7.4411.17
1.814.03
5.739
3.996.76
1.953.89
Fig.2.2Ultrametrictreeshowingdivergenceagesamongplatyrrhineprimates.Nodesofinterestarearbitrarily
numbered(N215).C4referstoanodeusedforcalibrationpurposes.NodesN1andC13arenotshowninthe
tree.FulldetailsofageestimatesarepresentedinTable2.2.
2.4 Discussion
We sequenced complete mitochondrial genomes from at least one representative of each
speciesgroupofSaguinus.FortheS.mystaxspeciesgroup,weincludedS.labiatuslabiatus,
since previous studies clearly showed that all members of this species group, S. mystax, S.
labiatusandS.imperatorformamonophyleticgroup(Croppetal.,1999;Araripeetal.,2008;
Matauscheketal.,inpress).TheS.oedipusspeciesgroup,includingS.oedipus,S.geoffroyi
andS.leucopusisrepresentedbyS.oedipus.FurthermoreweincludedwithS.bicolorandS.
midas as representatives of the correspondent species groups. From the highly diverse S.
nigricollis species group the mitochondrial genomes from the two species proposed by
26
Hershkovitz(1977)S.fuscicollisweddelliandS.nigricollisnigricollisweresequenced.Tocom
pletethepictureofthepositionoftheseSaguinusspeciesgroupsonemitochondrialgenome
ofeachcallitrichinegenus(exceptCallibella)weregenerated.
2.4.1 PhylogeneticrelationshipswithintheCallitrichinae
In contrast to previous studies, we found a basal position of Saguinus, instead of, A sister
groupingofSaguinusandLeontopithecus,assuggestedbyseveralauthorsisnotsupported
byourdata.CroninandSarich(1975)argueforabasalpositionofLeontopithecusbasedon
immunological evidence. An analysis of ALU insertions rather supports a basal position of
Saguinus(Osterholzetal.2009),whichisalsoindicatedbynuclearsequencedata(Canavez
etal.,1999;Chavesetal.,1999;Opazoetal.,2006;Borgesetal.,2008).Allotherdepicted
relationshipsamongcallitrichinegenera,e.g.thecloserelationshipofCallimicotothemar
mosetsareinagreementwithearlierstudies(CroninandSarich,1975;Seuanezetal.,1989;
Schneideretal.,1993;Pastorinietal.,1998;Chavesetal.,1999;Canavezetal.,1999).
Our data show a close relationship of the Amazonian marmosets (Mico) with the dwarf
marmoset (Cebuella) to the exclusion of the Atlantic marmosets (Callithrix). This phyloge
neticarrangementiswidelyacceptedtodayandalsoconfirmedonthebasisofchromosome
studiesandnumbers(Barrosoetal.,1997;Canavezetal.,1999;Porteretal.,1997;Tagliaro
et al., 1997). The blackcrowned dwarf marmoset was described as new species within the
genusCallithrixbyvanRoosmalenetal.(1998)andwasplacedlateroninitsowngenusCal
libellabyvanRoosmalenandvanRoosmalen(2003).TheexactphylogeneticpositionofCal
libellaisnotaddressedinthisstudy,assamplesfromtheseanimalsarenotavailable.
2.4.2 PhylogeneticrelationshipswithinthegenusSaguinus
ThedifferentspeciesgroupsofthegenusSaguinuswereneverincludedasdistinctentitiesin
phylogenetic studies of callitrichine phylogeny. Our data show that the genus Saguinus is
dividedintodifferent,unexpectedlyoldlineages.
The two main lineages within the tamarins separated already during the late Miocene,
around9.2mya.Theydifferconsiderablyfromeachother.ThelineageleadingtotheS.nigri
27
collisgroupconsistsofsmallbodiedtamarins.Theyunderwentarapidradiationaround23
myawhichleadtothecurrentdiversityof17describedtaxa(Matauscheketal.,inpress).
Within the largebodied tamarins the first major split occurred between the mustached
tamarins (S. mystax species group) south of the Amazon river and the NorthAmazonian
tamarinsalreadyduringtheoutgoingMiocenearound7.3mya.Themonophylyofthemus
tached tamarins (S. mystax, S. imperator, S. labiatus), which was described already by
Hershkovitz(1977),couldbeconfirmedbyseveralstudies(Cropp,1999;Araripeetal.,2008;
Matauscheketal.,inpress).Itisalsotheonlyspeciesgroupwhichlivessympatricallywith
anothertamarinspeciesgroup,theS.nigricollisgroup,throughoutitsrangeandevenforms
stablemixedspeciesassociationwiththem(Heymann,1997;HeymannandBuchananSmith
2000).
ThenextlineageleadstotheS.oedipusgroup,thenorthernmostrepresentativesoftheCal
litrichinae. S. oedipus and S. geoffroyi, which are considered as subspecies by Hershkovitz
(1977), areassigned to this group. The position of S. leucopus, which geographically repre
sents the link between the S. oedipus group and the Amazonian tamarins, is not clear yet.
Hershkovitz (1977) positioned it in the S .oedipus species group. In a molecular study by
Araripe et al. (2008), it formed a distinct lineage. Given that samples from this species are
difficulttoobtainandthatitisverydifficulttogeneratewholemitochondrialgenomesoutof
museummaterial,thisspeciescouldnotbeincludedinthisstudy.TheinclusionofS.leuco
pus in future studies is desirable. The same applies to the mottlefaced tamarin S. inustus,
whichisevenlessknownthanS.leucopusandwhichwasplacedintoitsownspeciesgroup
byHershkovitz(1977).
TheresultofourphylogeneticreconstructionsisacloserelationshipbetweenS.midasandS.
bicolor. This is in concordance with the findings of Cropp et al. (1999) and Araripe et al.
(2008).Rylandsetal.(1993)evenproposedthatS.midasandS.bicolorshouldformadistinct
group.Thetwospeciesdivergedaround2.9mya.Rylandsetal.(1993)approveagroupingof
these taxa into one group. They share the morphology of the P2 premetacristid exclusively
andotherdentalfeatures,likethelossofaseparateinferiorpetrosalsinusforamenandthe
derivedstatesofentoconidreductiononM1withtheS.oedipusgroup(Groves2001).
28
2.4.3 TaxonomicimplicationsforthedifferentSaguinusspeciesgroups
Inatimebasedphylogeneticclassification,asproposedbyGoodmanetal.(1998),taxawith
a divergence time of more than 6 mya should be treated as separate genera. Although an
onlytimedependentconceptofgenericnomenclatureisproposed,wethinkthatalsoother
factors, like morphology, ecology or behavior should be taken into account to confirm
whetheragroupofanimalsreallyformsadistinctevolutionarylineageorbelongstooneand
thesameradiation.Consideringthatdivergencetimeestimationsarehighlydependentfrom
thechoiceofcalibrationpointsandgenerallyshowhighvariances,webelievethattherela
tionsbetweenthedivergenceagesbetweendifferentgeneraorgroupsshouldbemorecon
sideredthantheabsolutevalues.Forinstance,wefindmuchdeepersplitswithinthegenus
Saguinusthanwithinthemarmosets(theS.nigricollisgroupsplittingofat9.5mya).Diver
genceagesforotherNewWorldprimategeneraaresimilartothesplitswithintheCallitri
chinae(CacajaoChiropotes:67mya;LagothrixBrachyteles:1011mya;CebusSaimiri:1619
mya)(Opazoetal.,2006).
In summary it can be concluded, that the different species groups of Saguinus are in most
casesconsiderablyolderthanthedifferentmarmosetgenera.Theycanalsobeidentifiedas
distinctmonophyleticentitiesbymolecularandmorphologicalindications(Tab.2.3).There
forearearrangementoftheirtaxonomicdesignationshouldbeconsidered.Keepingthefour
generaofmarmosets,likeRylandsetal.(2000),then,inconsequence,thedifferentspecies
groups of tamarins have to be elevated genera as well. Groves (2001, 2005) lists Cebuella,
Callibella and Mico as subgenera of Callithrix,which is inconcordance with the concept of
Goodman et al. (1998) and confirmed by our data, showing divergence ages between the
differentmarmosetlineagesbetween4and5.3mya.Thus,werathersupportthetaxonomic
arrangementofGroves(2001)withonegenusCallithrixcomprisingthesubgeneraCallithrix,
Mico,CebuellaandCallibella.
In Saguinus at least the differences between the S. nigricollis lineage and the remaining
tamarinsandtheirdivergencetimeofabout9.5mya,inouropinion,shouldbereflectedin
thetaxonomicnomenclature.Theyalsodifferconsiderablymorphologicallyandinmanyas
pectsoftheirecologyandbehavior(e.g.foragingstrategiesanddiet;microhabitatuseand
locomotion;olfactorycommunication;[Garber,1988,1991,1993;HeymannandBuchannan
29
Smith,2000;Heymann,2001]).Consideringthedivergencetimeandtheirecological,behav
ioralandmorphologicaldistinctiveness,weclearlysupportagenericstatusoftheS.nigricol
lisspeciesgroup.AgenericstatusoftheS.mystaxgroupwithanageof7.3myacanbedis
cussed, but maybe more comparative data on behavior and ecology should be added to
furtherdeterminetheirdistinctivenessfromtheotherlargebodiedtamarins.TheS.oedipus
andS.midas/bicolorgroupliewith5.3myaslightlybelowthis6myathreshold.Considering
thelowresolution,whichsuchdivergenceageestimationsnaturallyunderlie,wewouldsup
portasubgenericstatusforthelatterthreespeciesgroups(Tab.2.3).
Table2.3Tamarinspeciesgroupswithcharacteristicmorphologicalfeatures,estimateddivergenceagesandthe
proposedgenusorsubgenusname,respectively.
Speciesgroup
Morphologicalcharacters
Divergence
time[mya]
Proposedgenus/subgenus
name
S.nigricollis
Lowerbodysize
9,2
GenusLeontocebus,
Wagner1840
S.mystax
I2onlylittlewiderthanlong
7,3
SubgenusMystax,
Gray1870
S.oedipus
Narrowmaxilla
5,32
SubgenusOedipus,
Lesson1870
S.midas/bicolor
DerivedformofpremetacristidonP2
5,32
SubgenusSaguinus,
Hoffmannsegg1807
2.4.4 Biogeographicimplications
Molecular phylogenetic studies on various Amazonian organisms indicate major diversifica
tions during the late Miocene or Pliocene with the uplift of the Eastern Cordilleras of the
northernandcentralAndes(GregoryWodzicki,2000;Garzioneetal.,2008).Thedivisionof
the Callitrichinae in the major lineages occurred in the middle Miocene, the initial split
withintheSaguinuslineageinthelateMiocene.
Duringthattime,~10mya,westernAmazoniawasmainlyinfluencedbytheformationofthe
Acre megawetland, a large fluviotidal landscape covering most of the area in central and
westernAmazoniaandtheestablishmentofthemaintranscontinentaldrainagesystem(Fi
30
gueiredo et al., 2009). Thus, the great Acre wetland could account for the first initial split
within Saguinus, which separated the ancestors of the S. nigricollis species group from the
Saguinus stem, which led to the largerbodied tamarins. Within the largebodied tamarin
lineageourdataindicateawesternoriginwiththemustachedlineagebranchingofffirstwith
asubsequentnorthwarddispersalaround7myaformingtheS.oedipusgroupintodaysCo
lombiaandPanamaandaconsecutivemovementnorthoftheAmazonmaincoursetothe
eastleadingtotheS.midasandS.bicolorspeciesgroups.ThissplitintoaSouthAmazonian
andaNorthAmazonianlineageisroughlyconformwiththeonsetoftheAmazondrainage
systemandthecourseoftheAmazonasweseeittoday,whichisdatedaroundsevento10
mya (Figueiredo et al., 2009). Thus, our data clearly support an eastward dispersal with a
WestAmazonianoriginassuggestedbyHershkovitz(1977)ratherthananeasternoriginof
SaguinuswithawestwarddispersalasproposedbyFerrari(1993).
TheradiationwithintheS.nigricollisgroupoccurredmuchlater,~3mya(Matauscheketal.,
inpress).ThisradiationmaycoincidewiththedeclineoftheAcrewetlandandthefollowing
formationoftheAmazonianriversystem(Wesselinghetal.,2010).Theexpansionoftropical
rainforestacrosstheformerwetlandareaenabledasubsequentdispersaloftheancestralS.
nigricollis stock. The emerging rivers formed barriers to the dispersing tamarins and en
hancedtheirdiversificationandbroughtthembackintocontactwiththeS.mystaxgroup.
IfwecomparethishypothesiswithotherNeotropicalprimates,wedetectparallelswiththe
biogeography and dispersal patterns on a similar timescale in squirrel monkeys (Saimiri)
(Lavergne et al., 2010). The disappearance of the great Acre megawetland and the subse
quent formation of the Amazonian fluvial system could have enhanced speciation in both
groups.
Amazoniasextremelyrichbiodiversity,whichweseetoday,surelyevolvednotduringbya
single,shorttermevent(Wesselinghetal.,2010).Asrecentmolecularstudiesondifferent
groupsoforganismssuggest,thediversificationoflifeinAmazoniawasamorecontinuous
processthattookplacethroughouttheCenozoic.Forsomegroups,asortofaccelerationof
thisprocessisindicatedduringtheMiocene(seeRull,2008).Ofcourse,weshouldbeaware
that correlating geological and putative speciation events might be oversimplified, as the
documentationforbothisoftenincompleteandthatmolecularmethodscanonlyreflectthe
31
situationfoundinmodernbiota(Lundbergetal.,1998;Wesselinghetal.,2010).Neverthe
less, combining molecular studies on the evolution of widespread and diverse groups of
animals,suchasthetamarins,cansurelybeausefultooltouncoverthebiogeographichis
toryofoneofthemostspeciesrichtrerrestrialecosystemsoftheworld.
Acknowledgements
WethankthefieldassistantManuelShahuanoTelloforexcellentworkduringthefieldsurveys,StephanBehl
andPeterGottleuberfortheirhelpandassistanceinthefield,andChristinaOberdieckandMarionSeilerfor
helpandsupportinthelab.WearefurthergratefultoPierreMoissonandthestaffofMulhouseZoo,France,
JanVermeerfromValledesSinges,RomagneandSandraSuarezforprovidingsamplesfromBolivia.Wethank
INRENA in Lima for authorizing this study (1062007INRENAIFFSDCB) and to the dean of the Forestry De
partmentoftheUniversidadNacionaldelaAmazonaPeruanainIquitosforadministrativesupport.Thisstudy
wasfinanciallysupportedbytheGermanPrimateCenter,theBiodiversittsPaktoftheWissenschaftsgemein
schaftGottfriedWilhelmLeibniz,andtheMargotMarshBiodiversityFoundation.
32
3 MitochondrialPhylogenyofTamarins(Saguinus,Hoff
mannsegg1807)withTaxonomicandBiogeographicIm
plicationsfortheS.nigricollisSpeciesGroup
ChristianMatauschek1,ChristianRoos2&EckhardW.Heymann1
UnitofBehavioralEcologyandSociobiology,GermanPrimateCenter,D37077Gttingen,
Germany
2
GeneBankofPrimatesandPrimateGeneticsLaboratory,GermanPrimateCenter,D37077
Gttingen,Germany
Corresponding author: Christian Matauschek, Unit of Behavioral Ecology and Sociobiology, German Primate
Center, Kellnerweg 4, D37077 Gttingen, Germany, Tel.: +495513851468, email: christian.matauschek@t
online.de
AmericanJournalofPhysicalAnthropology
Received:17June2010/Accepted:27September2010
33
3.PhylogenyofSaguinus
Abstract
TamarinsofthegenusSaguinus,subfamilyCallitrichinae,representoneofthemostdiverse
primate radiations. So far, about 35 taxa have been described, but detailed information
about their taxonomy and phylogeny is still lacking. To further elucidate the phylogenetic
relationships and the biogeographic history within the genus, and to contribute to a more
reliable classification of its taxa, we sequenced the complete mitochondrial cytochrome b
geneandthehypervariableregionIoftheDloop.Therefore,wemainlyusedfecalsamples
fromwildtamarinscollectedduringtwoexpeditionstothePeruvianAmazon,anareaofhigh
tamarindiversity.OurdatasuggestthatthenumeroustaxaoftheS.nigricollisspeciesgroup
arederivedfromacommonancestorthatseparatedfromtheotherrepresentativesofthe
genus ~10 mya. Most taxa of the S. nigricollis group form monophyletic clusters, which
mainlyoriginatedinasinglerapidradiation~2.9mya.S.fuscicollisandS.nigricollisappearas
polyphyletic taxa, but we could identify various clusters, which are mainly consistent with
differencesincoatcoloration.Wecouldconfirmmostoftheexistingtaxaasdistinctentities
andsuggestspeciesstatusforfuscicollis,illigeri,lagonotus,leucogenys,nigricollis,nigrifrons,
tripartitusandweddelli.Ourgeneticdatadonotsupportaseparatestatusformelanoleucus
and graellsi, but due to differences in fur coloration, we give them subspecies status. The
speciesgroupmostlikelyoriginatedinwesternAmazoniaanddiversifiedduringthedecline
oftheAcrewetlandandtheformationoftheAmazonianriversystem.
Keywords:Saguinus,cytochromeb,Dloop,evolution,Peru
34
3.1 Introduction
TamarinsaresmallbodiedNeotropicalprimates,whichtogetherwithmarmosets(Callithrix
andMico),pygmymarmosets(CebuellaandCallibella),Goeldi`smonkey(Callimico)andlion
tamarins (Leontopithecus) constitute the New World monkey subfamily Callitrichinae
(Groves, 2001; Osterholz et al., 2009). Despite their wide distribution and their relatively
high abundance throughout Amazonia and Central America, still little is known about the
actualdiversityandphylogeneticrelationshipsofthegenusSaguinus.Thisisexemplifiedby
therecentdiscoveryofanewtamarinformBrazil(Rheetal.,2009).Today,about35tama
rintaxaarerecognized,thusmakingtamarinsoneofthemostdiverseprimategenera.
Tamarin taxa can be distinguished by a variety of morphological characters, mainly differ
encesinpelagecoloration(Groves,2001).Hershkovitz(1977)identified33taxa,whichwere
grouped into 10 species and three species groups (hairyfaced, mottlefaced, barefaced
tamarins).Thefewgeneticstudiesthathavebeenconductedtoclarifytheinterspecificrela
tionship of Saguinus do not support this split (Cropp et al., 1999; Canavez et al., 1999;
Tagliaroetal.,2005).Instead,thesestudiessupportadivisionofthegenusintosmallbodied
and largebodied clades; both of which include individuals with hairy and bare faces. The
smallbodiedcladeconsistsonlyoftheS.nigricollisgroup.Allotherspeciesformthelarge
bodiedclade(Croppetal.,1999).
With16to17taxa,theS.nigricollisspeciesgroupisthemostdiverseofallSaguinusspecies
groups(Hershkovitz,1977).ItisdistributedthroughoutwesternAmazonia,whereitseems
tohavedifferentiatedwithinthelargeinterfluvialareasbetweenthemajortributariesofthe
Amazon River (Fig. 3.1). The highest diversity of this species group is found in Peru
(Herhskovitz, 1977). According to Hershkovitz (1977), the S. nigricollis group includes the
blackmantled tamarin S. nigricollis with three subspecies and the saddleback tamarin S.
fuscicollis with 14 subspecies, including the goldenmantled tamarin S. f. tripartitus. This
classicaltamarintaxonomywasreviewedandchangedseveraltimes(CoimbraFilho,1990;
Rylandsetal.,1993;Rylandsetal.,2000;Groves,2001).Someofthesesubspeciesmayrep
resentonlycolormorphsorhybridpopulations(Peresetal.,1996).Proposedsympatrybe
tweenS.fuscicollisandS.nigricollisishighlydisputed(e.g.Heymann,1997)andspeciesor
subspecies descriptions are often based on single museum specimens. Molecular studies
indicatethatsomesubspeciesofS.fuscicollisaremorecloselyrelatedtoS.nigricollis,sothat
35
the status of these two species as monophyletic entities remains doubtful (Cropp et al.,
1999). The taxon with the greatest variety of subspecies and color patterns is the saddle
backtamarinS.fuscicollis(CheverudandMoore,1990).Hershkovitz(1977)mentions14sub
species,whichdifferfromeachotherincolorpatternanddistribution.Thetaxonomicstatus
ofseveralofthesetaxaisfairlycontroversial.Somesubspecies,S.f.tripartitus,S.f.graellsi
andS.f.melanoleucus,havebeengivenfullspeciesrank,sothattherearenowuptofive
differentspecieswithinthisspeciesgroup(HernandezCamachoandCooper,1976;Thoring
ton,1988;CoimbraFilho,1990;Groves,2001).WefollowheretheclassificationofGroves
(2001)andrecognizefivespecieswithintheS.nigricollisgroup.
MostrecentstudiesonSaguinustaxonomyarebasedonthecomparisonofmorphological
characterslikepelagecoloration(e.g.Hershkovitz,1977)oronmorphometricalanalysesof
theskullordentition(Natori,1988;NatoriandHanihara,1988).Molecularapproacheshave
beenappliedonlytoalimitedsampleoftamarintaxa(Jacobsetal.,1995;Peresetal.,1996;
Croppetal.,1999;Canavezetal.,1999;Tagliaroetal.,2005;Vallinotoetal.,2006).Nearly
all of these studies relysolely on museum material or captive animals for which the exact
geographicoriginisoftenunknown.
Duetotheseuncertainties,wesetupamoleculargeneticstudytoexamine(i)thestatusof
S.fuscicollisandS.nigricollisasmonophyleticspecies,(ii)thetaxonomicstatusofthepro
posedspeciesS.graellsi,S.tripartitusandS.melanoleucus,and(iii)theirrelationshiptothe
remainingPeruviantamarintaxa.
3.2 Methods
3.2.1 Samplingsitesandsamplecollection
Toobtainfecalsamplesfromwildtamarinpopulations,twofieldtripstoPeruvianAmazonia
were conducted between June and October 2007 and 2008. Samples were collected at 29
locations(Fig.3.1,SupplementaryTable1).Samplinglocationswereselectedtoincludeall
majorinterfluvialareasinthePeruvianAmazonaccordingtothedistributionpatternaspro
posedbyHershkovitz(1977)andAquinoandEncarnacin(1994).Themainfocuswasonthe
membersoftheS.nigricollisspeciesgroup,butwheneverpossible,weadditionallysampled
the sympatric taxa S. mystax mystax (AGC, PIJ,RBR, EBQB)and S. imperatorsubgrisescens
36
(LAM). Taxa were identified by their putative distributions (Hershkovitz, 1977; Aquino and
Encarnacin,1994)andfurcolorationasdescribedinHershkovitz(1977).Ateachsampling
site,wetriedtoobtainsamplesfromseveraltamaringroups.Coordinatesofeachsampling
locationwererecordedwithaGarminGPSMAP76CSx(SupplementaryTable1).Onlyfresh
droppings were collected. Additionally, samples of animals kept as pets by local villagers
weretaken,butonlyifinformationofexactgeographicoriginwastraceable.Wefurtherin
cluded fecal samples from the Estacin Biolgica Quebrada Blanco (EBQB), the Estacin
Biolgica Cahuana (CA) and the Estacin Biolgica Tahuamanu, Bolivia (BOL), which were
kindly provided by other researchers. All samples were stored in plastic tubes (5 ml) filled
withethanol(90%).Complementarytothefecalsamples,amusclesampleofS.melanoleu
cusmelanoleucustakenfromaspecimenpreservedinethanolandstoredattheZoological
StateCollection Munich (ZSM) wasincluded. Although theorigin of this specimenwas not
available,theindividualcouldbeclearlyidentifiedasS.m.melanoleucusbasedonitsoverall
whitish coloration as described in Hershkovitz (1977). Blood samples from S. oedipus and
CallithrixgeoffroyiwereobtainedfromtheGermanPrimateCenter(DPZ)andDresdenzoo,
Germany,respectively.Intotal,weanalyzed101tamarinindividuals.
37
Fig.3.1MapofPeruwithallsamplinglocationsofthetwofieldsurveysanddistributionmapoftheS.nigricollis
group.(Abbreviations:P:Pantoja,RioNapo;V:Vencedores,RioNapo;CS:CampoSerio,RioNapo;QH:Que
bradaHuiririma,RioNapo;SL:SergentoLores,RioNapo;TP:Tutapishcu,RioNapo;AP:RioApayacu,Amazonas;
PV:Pevas,Amazonas;NA:DiamanteAzul,RioNanay;PC:PadreCocha,RioNanay;PW:Pilpintuwasi,RioNanay;
IT: Rio Itaya; NY: Nueva York, Rio Tigre; MF: Miraflores, Rio Maraon; EBQB: Estacin Biologica Quebrada
Blanco;CA:Cahuana;RBR:RioBlanco,rightbank;TAPL:RioTapiche,leftbank;TAPR:RioTapiche,rightbank;
AGC:AguasCalientes,RioUcayali;PIJ:Pijuyal,RioUcayali;PL:PuebloLibre;MOY:Moyobamba;RP:RumiPata;
TAR:Tarapoto;BEL:Bellavista;PA:BiologicalStationPanguana,RioPachitea;LAM:BiologicalStationLosAmi
gos,RioMadredeDios;TAM:RioTambopata).
38
3.2.2 Laboratorymethods
FortheDNAextractionfromfecalandmuseumsamples,theQIAGENQIAampStoolKitand
QIAGEN QIAamp Tissue Kit was used. Extractions followed standard protocols as recom
mendedbythesupplier,withtheexceptionthattheDNAwasdilutedinHPLCqualitywater
and stored at 20 C before further processing. From the mitochondrial genome, we se
quencedthecompletecytochromebgene(cytb)anda546bpfragmentoftheDloop,in
cluding theHVI region. Amplifications were carried out in30l reactions containing a final
concentrationof0.33Mofeachprimer,3mMMgCl2,0.166mMdNTPs,1xamplification
buffer and 1U Taq DNA polymerase (Biotherm, Genecraft). Primer sequences are listed in
Table3.1.Forallamplifications,waxmediatedhotstartPCRswereperformed.Theprogram
forallamplificationscomprised40cycles,eachwitha1mindenaturationstepat92C,1min
annealing(forannealingtemperaturesseeTable3.1)andextensionat72Cfor1min,witha
finalextensionat72Cfor5min.TheresultsofthePCRamplificationswerecheckedbyrun
ning an aliquot on a 1 % agarose gel, stained with ethidium bromide. PCR products were
purified using MontageTMPCR Centrifugal Filter Devices (Millipore) following the delivered
instructions.PCRproductsweresequencedinbothdirectionswithrespectiveamplification
primers on an ABI PRISMTM3130xL Genetic Analyzer (Applied Biosystems) using the
BigDyeTMTerminatorv3.1CycleSequencingKit(AppliedBiosystems).Topreventcrosstaxon
contamination,wefollowedstandardmethodsasdescribedinRoosetal.(2008).Theampli
fication of nuclear pseudogenes (numts) was reduced by using mainly faecal and museum
material in which nuclear DNA is highly degraded (Hofreiter et al., 2003; Thalmann et al.,
2004),byapplyingSaguinusspecificprimerswhichweredesignedinourlaboratory,andby
direct sequencing of PCR products. Sequencing revealed no multiple peaks or inconsistent
positionsinoverlappingfragmentsandnoprematurestopcodonsweredetectedinthecytb
sequences.NewlygeneratedsequencesweredepositedatGenBankandareavailableunder
accessionnumbersHM367879HM368078(SupplementaryTable3.1).
39
Table3.1Primersusedinthisstudy.Givenarelocus,primersequence,referenceandannealingtemperature
(AT)inC.
Locus
Primersequence(5`3`)
Reference
AT
cytb
AATGATATGAAAAACCATCGTTGTA
Thisstudy
58
TTTCAGCTTTGGGTGTTGATG
Thisstudy
58
cytb+HVI
CCYTAAACACCCCTCCCC
Thisstudy
60
CCATCGTGATGTCTTATTTAAG
Thisstudy
60
ATTGATATGAAAARYCATCGTTG
Thisstudy
60
GGAATGTTATGCTTTGTTGTTTG
Thisstudy
60
HVI
AACATTAAAGTACTTTACAAGTACATA
Hucketal.2007
60
CTGGCAAAACACAGTCAGGCG
Hucketal.2007
60
CTACCATCAACACCCAAAGC
Thisstudy
60
CCTCCCGGCAATGCTGAT
Thisstudy
60
3.2.3 Statisticalmethods
SequenceswereassembledandmanuallyeditedusingSEQUENCHER4.7(GeneCodesCor
poration,AnnArbor,MI,USA).Asoutgroup,weusedanorthologoussequencefromC.geof
froyi. Alignments were conducted with ClustalW as implemented in GENEIOUS 4.8 (Rozen
andSkaletsky,2000)andcorrectedbyeye.Forfurtherstudies,identicaltamarinhaplotypes
wereremoved.IndelpositionsintheHVIalignmentwereeliminatedusingGBLOCKS0.91b
(Castresana, 2000). Therefore, a relaxed selection of blocks was applied. For phylogenetic
treereconstructions,thecytbandHVIdatasetswereconcatenated.Treeswerecalculated
with maximumparsimony (MP), maximumlikelihood (ML) and Bayesian approaches. MP
reconstructionswereperformedinPAUP 4.0b10with10,000bootstrapreplications(Swof
ford, 2002). Therefore, all characters were treated as unordered and equally weighted
throughout. A heuristic search was performed with the maximum number of trees set to
100.Forbothdatasets,theGTR+I+Gmodelwasselectedastheoptimalnucleotidesubstitu
tion model with jMODELTEST 0.1.1 (Posada, 2008) using the Akaike Information Criterion
(AIC).MLtreeswereconstructedwithGARLI0.96.win23(Zwickl,2006).500pseudoreplica
tionswereconductedtoestimateMLbootstrappercentagesanda50%consensustreewas
40
calculatedinPAUP.BayesiananalyseswerecarriedoutinMrBAYESv3.1.2(Hulsenbecketal.,
2001; Ronquist and Hulsenbeck, 2003). The dataset was partitioned into cyt b and HVI re
gions.Intheanalysis,fourMonteCarloMarkovchains(MCMC)withadefaulttemperature
of0.2andachainlengthof10,000,000generationswerecarriedout.Treesandparameters
weresampledevery1,000generations.2,500ofthesampledtreeswerediscardedasburn
in. Obtained phylogenetic trees were visualized and edited using FigTree v1.3.1 (Rambaut,
2006).
CalculationsofdivergenceageswerecarriedoutusingaBayesianapproachimplementedin
theprogrammeBEAST(DrummondandRambaut,2007). Duetothehighmutationrateof
theHV1region,divergenceageestimationswerebasedonlyonthecytbalignment.Inthe
finaldataset,weincluded20tamarinsequences,whichrepresentatleastonehaplotypeper
major clade. For calibration purposes, additional sequences of other platyrrhines (C. geof
froyi, Cebus albifrons, Saimiri boliviensis, Aotus nancymaae, Callicebus torquatus, Cacajao
calvus, Pithecia monachus, Alouatta seniculus) and outgroup taxa (Macaca mulatta, Papio
hamadryas,Pantroglodytes,Homosapiens)weretakenfromGenBank(SupplementaryTa
ble1).Thus,thefinalalignmentcomprised32sequences.DuetoatripletdeletioninCebus,
PitheciaandCacajao,thealignmentlengthfortheBEASTcalculationswasreducedto1,137
bp.WeusedaHKYmodelwithagammadistributedratevariationbetweensitesandinvari
antsitesasoptimalnucleotidesubstitutionmodel.ThemodelwaschosenbyjMODELTEST
2.2usingtheBayesianinformationcriterion(BIC)(Posada,2008).Fortheanalysis,weuseda
relaxedlognormalclockmodeloflineagevariation,andforbranchingrates,aYuleprocess
aspriorwasassumed.Sincetheestimationofphylogeneticrelationshipswasnotthemain
aimofthisanalysis,weusedanapriorifixedtreetopologyasobtainedfromphylogenetic
reconstructions(Fig.3.2)andpublisheddatafortaxaotherthanSaguinus(Osterholzetal.,
2009). Analyses were run for 25,000,000 generations, with tree and parameter sampling
occurringevery1,000generations,ofwhich10%werediscardedasburnin.Theadequacyof
a 10% burnin and convergence of all parameters was assessed by visual inspection of the
traceoftheparametersacrossgenerationsusingthesoftwareTRACERv1.3(Rambautand
Drummond,2005).Subsequently,thesamplingdistributionsofmultipleindependentrepli
cates were combined using the software LogCombiner v1.4.6, and then summarized and
41
visualized using the software TreeAnnotator v1.4.6. Both programs are part of the BEAST
package(DrummondandRambaut,2007).
Ascalibrationpoints,weselectedfourwelldocumentedfossils.First,thesplitbetweenPan
and Homo is dated 67 million years ago (mya) (Brunet et al., 2002; Vignaud et al., 2002;
Steiper and Young, 2006) and between Macaca and Papio 78 mya (Delson et al., 2000;
SteiperandYoung,2006).Fortheinitialsplitbetweenplatyrrhinesandcatarrhines,Pouxet
al.(2006)givearangeof3440mya.Ascalibrationpointamongplatyrrhines,weusedthe
splitbetweenSaimiriandCebus,whichwasdatedbyLavergneetal.(2010)at~16mya.They
set the upper limit to 20 mya, marked by Dolichocebus, which most likely is the crown
Saimiri(SzalayandDelson,1979),andthelowerlimitto12mya,resultingfromNeosaimiri,
datedbyStirton(1951).Insteadofhardboundedcalibrationpoints,weusedthepublished
datesasanormaldistributionpriorfortherespectivenode.ForC1(CatarrhiniPlatyrrhini),
this translates into a normal distribution with a mean of 37 mya and a standard deviation
(SD) of 3.0 mya, for C2 (Homo/Pan) into a mean of 6.5 mya and a SD of 0.5 mya, for C3
(MacacaPapio)intoameanof7.5myaandaSDof0.5myaandforC4(SaimiriCebus)
intoameanof16myaandaSDof4.0mya.
3.3 Results
We successfully sequenced the complete cyt b gene and the HVI region from 99 Saguinus
individuals from 29 localities in the Peruvian Amazon and Bolivia, and each one individual
from captivity (S. oedipus) and museum collections (S. m. melanoleucus). The combined
alignment had a length of 1,487 bp, of which 483 sites were variable and 345 parsimony
informative.Amongallstudiedindividuals,weobserved66haplotypesintheHVIregion,58
inthecytbgeneand72inthecombineddataset.
Allphylogeneticreconstructionsasobtainedfromvariousalgorithmsrevealedidenticaltree
topologies and similar support values. Accordingly, Saguinus initially diverged into a clade
consistingofS.oedipusandthemustachedtamaringroupmembers,S.mystax,S.imperator
and S. labiatus, and a clade including all the members of the S. nigricollis group (Fig. 3.2).
AlthoughthesistergroupingofthemustachedtamaringroupandS.oedipusisonlyweakly
supported, at least species group monophylies are well supported. Within the mustached
42
tamaringroup,S.imperatorbranchedofffirst,beforefinallyS.mystaxdivergedfromS.labi
atus.
WithintheS.nigricollisgroup,wedetectedfourwellsupportedmajorclades,buttheirphy
logeneticrelationshipsareonlyweaklysupportedandthereforeremainunresolved.Within
clade1,wefoundtwosubclades,ofwhichoneincludedallS.f.illigeriindividualsfromthe
EstacinBiolgicaCahuana(CA)andfromtheleftbankoftheRioTapiche(TAPL),andthe
other,allS.f.illigerifromAguasCalientes/Contamana(AGC),eastoftheUcayaliriver,andall
haplotypesofS.f.leucogenyscollectedintheDepartamentoSanMartn(TAR,MOY,RP,BEL,
PL) in the northern part of the proposed distribution area of this subspecies (Hershkovitz,
1977).Clade2couldbedividedintofourwellsupportedsubclades,whichrefertoindividu
alsidentifiedasS.f.weddelli+S.m.melanoleucus,S.f.fuscicollis,S.f.nigrifronsandS.f.
leucogenysfromPanguana(PA),southoftheRioPachitea.Allreconstructionssuggesteda
closerelationshipbetweenS.f.fuscicollisandsouthernS.f.leucogenys,andbetweentheS.
m. melanoleucus specimen and S. f. weddelli. Clade 3 consisted of S. n. nigricollis and S.
graellsihaplotypes.Interestingly,S.graellsiformedamonophyleticcladenestedwithinS.n.
nigricollis, which appeared as paraphyletic taxon. Clade 4 comprised all individuals of S. f.
lagonotusandS.tripartitus,whichbothformedreciprocalmonophyleticclades.
43
Fig.3.2Phylogramofthe72haplotypesinthecombineddataset(cytbandHVI)asrevealedbyBayesiananaly
sis.OutgrouprootedwithC.geoffroyi.BootstrapvaluesforMPandMLareindicatedabovebranchestogether
withposteriorprobabilitiesfortheBayesianapproach(MP/ML/Bayesian).
44
Accordingtodivergenceageestimations(Fig.3.3,Table2.2),thesplitbetweenplatyrrhines
andcatarrhineswasdatedat42.51mya(C1)(for95%credibilityintervalsseeTable2.2),the
splitbetweenHomoandPanat6.55mya(C2)andbetweenMacacaandPapioat7.67mya
(C3).Amongplatyrrhines,theinitialsplitseparatingPitheciidaeincludingCallicebus,Pithecia
andCacajaofromtheotherplatyrrhinesoccurred21.1mya(N2).Afterwards,Atelidaerep
resentedbyAlouatta,branchedofffromCebidae19.87mya(N5).Amongthelatter,Saimiri,
Cebus and Aotus diverged from Callithrichinae 18.36 mya (N6). Aotus separated from the
Cebus+Saimiriclade17.62mya(N7),andlattertwosplit14.46mya(C4).Thesplitbetween
SaguinusandCallithrixwasdated14.23mya(N8),whiletheinitialdivisionwithinSaguinus
occurred10.07mya(N9).ThisdivisionseparatedallmembersoftheS.nigricollisgroupfrom
the largerbodied tamarins. Among the latter, the moustached tamarin species group split
from S. oedipus shortly after the initial Saguinus division 9.07 mya (N10). S. imperator di
vergedfromS.labiatusandS.mystax6.03mya(N11),whilethesplitbetweenlattertwowas
dated at 1.15 mya (N12). The initial differentiation of major clades within the S. nigricollis
group (clades 14) was dated 2.91 mya (N13). Further splitting events within the species
group into recognized taxa occurred 2.580.07 mya (N1420). For detailed information see
Table3.2.
45
Fig. 3.3 Ultrametric tree showing divergence ages among platyrrhine primates based on complete cyt b se
quencedata.For individualcodes see Figs. 1, 2 and Supplementary Table 1. Nodes of interestarearbitrarily
numbered(N220).C4referstoanodeusedforcalibrationpurposes.NodesN1andC13arenotshowninthe
tree.FulldetailsofageestimatesarepresentedinTable2.
46
Table3.2Bayesiandivergenceageestimatesinmya*.
Node
mean
95%credibility
interval
C1CatarrhiniPlatyrrhini
42.51
37.3747.92
N1 Hominoidea (Homo + Pan) Cercopithecoidea (Macaca + 25.45

Papio)
22.6627.14
C2HomoPan
6.55
5.937.10
C3MacacaPapio
7.67
6.638.66
N2PitheciidaeCebidae+Atelidae
21.10
16.6427.07
N3CallicebusPithecia+Cacajao
16.89
11.8122.75
N4PitheciaCacajao
11.23
5.2213.16
N5AtelidaeCebidae
19.87
15.6924.64
N6CallitrichinaeCebus+Saimiri+Aotus
18.36
15.1223.77
N7AotusCebus+Saimiri
17.62
13.8322.00
C4SaimiriCebus
14.46
12.4319.28
N8CallithrixSaguinus
14.23
10.6717.96
N9Saguinus
10.07
7.0612.40
N10S.oedipusS.mystaxgroup
9.07
6.2911.11
N11S.imperatorS.mystax+S.labiatus
6.03
2.916.61
N12S.labiatusS.mystax
1.15
1.013.01
N13S.nigricollisgroup
2.91
1.823.64
N14S.tripartitusS.f.lagonotus
1.92
1.042.57
N15S.graellsi+S.n.nigricollisS.f.fuscicollis+S.f.leucogenys 2.58
(South)+S.f.weddelli+S.m.melanoleucus+S.f.nigrifrons
1.382.86
N16S.f.nigrifronsS.f.weddelli+S.melanoleucus+S.f.fusci
collis+S.f.leucogenys(South)
1.55
0.701.72
N17 S. f. weddelli + S. m. melanoleucus S. f. fuscicollis + S. f. 1.40

leucogenys(South)
0.601.52
N18S.n.nigricollisS.graellsi
0.26
0.070.48
N19S.f.fuscicollisS.f.leucogenys(South)
0.52
0.160.68
N20S.f.weddelliS.m.melanoleucus
0.07
0.020.28
*seealsoFig.3.3.NodesC1C3andN1arenotshowninFig.3.3.
47
3.4 Discussion
ThisstudyissofarthemostcompleteassessmentofthehighlydiverseS.nigricollisspecies
complex using almost exclusively samples from wild tamarin populations with confirmed
samplinglocalities.OurresultsallowaclearidentificationofdistinctclusterswithinSaguinus
thatmainlycoincidewithdescribedtaxa.
Thephylogeneticrelationshipsbetweenthethreespeciesbelongingtothemustachedtama
rin (or S. mystax) species group are well resolved and in agreement with Araripe et al.
(2008).Asinourstudy,Araripeetal.(2008),usingmitochondrial16SrRNAsequencedata,
revealedabasalpositionofS.imperatorandasistergroupingofS.labiatusandS.mystax.
Whilethebranchingpatterninthelatterspeciesgroupiswellresolved,relationshipsamong
taxawithinthehighlydiversesmallbodiedtamarinclade,theS.nigricollisspeciesgroup,are
disputed.ConcordantwithCroppetal.(1999),ourdatashowthatmosttaxaoftheS.nigri
collisgroupformmonophyleticgroups,butnotallbranchingpatternsamongthedifferent
lineageswithinthespeciesgrouparewellresolved.Thus,mosttaxa,whichdiffermainlyin
coatcoloration,seemtohaveevolvedduringasinglerapidradiation,mostlikely~2.9mya.
3.4.1 ThestatusofS.tripartitus
The goldenmantled tamarin, S. tripartitus, considered as a subspecies of S. fuscicollis by
Hershkovitz(1977),wasgivenfullspeciesrankbyThorington(1988)duetosupposedsym
patrywithS.f.lagonotusontherightbankoftheRioNapo.However,neitherAquinoand
Encarnacin(1994)norHeymannetal.(2002)foundevidenceforasympatricoccurrenceof
both taxa and the Rio Curaray might be a natural border between them (Heymann et al.,
2002;Rylandsetal.,inpress).Moreover,itwasassumedthatonlytamarintaxaareableto
live sympatrically, which differ sufficiently in bodysize and ecology, which is not the case
betweenthetaxaoftheS.nigricollisgroup(Heymann,1997;HeymannandBuchananSmith,
2000).Duringourfieldsurvey,wefoundnoevidenceofsympatryalongtheRioNapo.Mor
phologically and ecologically, S. tripartitus and S. f. lagonotus do not seem to differ more
thanotherS.fuscicollissubspecies(Hershkovitz,1977;Heymann,2000).IncontrasttoCropp
etal.(1999),ourphylogeneticdataclearlysupportacloserelationshipbetweenS.tripartitus
andS.f.lagonotus.
48
3.4.2 ThestatusofS.melanoleucus
AnotherdisputedissueisthetaxonomicstatusofS.melanoleucus,whichisdistributedbe
tweentheRioJuruaandRioTarauacuinBrazil.CoimbraFilho(1990)listedS.melanoleucus
as a distinct species, with acrensis and crandalli as subspecies. There is no uninterrupted
chainofintermediateforms,whichleadsfromS.fuscicollistotheentirelywhiteS.melano
leucus in the sense of Hershkovitz theory of metachromism (Rylands et al., 1993; Groves,
2001). Hybridization with S. f. fuscicollis occurs in the headwater region of the Rio Jurua,
whichleadtointermediatephenotypesontheleftbankoftheheadwaterstream(Pereset
al.,1996).TheacrensisandcrandallipelagemightrepresentonlycolormorphsofS.melano
leucus,whichthuswouldbeamonotypicspecies(Groves,2001).Thecrandallimorphcould
alsobetheresultofhybridizationbetweenS.melanoleucusandS.f.fuscicollis(Rylandset
al.,2000).Inourdata,thesingleS.melanoleucusindividualrepresentsasisterlineagetothe
S.f.weddelliclade,withanestimateddivergenceageofonly0.07mya.Acloserelationship
betweenbothtaxawasalsosuggestedbyTagliaroetal.(2005).Hence,inviewoftheclose
geneticaffiliationtoS.f.weddelli,thespecificstatusofS.melanoleucusremainsdoubtful.
3.4.3 ThestatusofS.fuscicollissubspecies
ThereisanincongruitybetweenthedescribedsubspeciesS.f.leucogenysanditsdistribution
area with our observations in the field and the genetic data. We observed intergradation
betweenthedarkbrownmantledS.f.illigeritypeandthemoreorlessblackmantledS.f.
leucogenystype.EspeciallyatthelocationsinSanMartnintheareaofMoyobamba(MOY,
RP) and further north in the Rio Mayo valley (PL), tamarins showed more the S. f. illigeri
phenotype,likeanimalswefoundalongtheRioUcayali(AGC)andattheRioTapiche(TAPL),
andobservedbyHeymann(1990)attheRioPacaya(CA).Hershkovitz(1977)madeasimilar
observationonmuseumspecimensfromMoyobamba,whichwereindistinguishablefromS.
f. illigeri individuals. But according to their origin, which lies inside the range of S. f. leu
cogenys,heassignedthemtoS.f.leucogenys.Theseobservationsonthephenotypereflect
verywellourmitochondrialdata,whereallindividualssampledinthenorthernpartofthe
proposedrangeofS.f.leucogenys(BEL,MOY,TAR,PL)formawellsupportedcladewithall
S.f.illigeriindividuals,whileallanimalsfromtheonlysouthernsamplingpoint(PA),southof
theRioPachitea,clearlyfallintothecladewithalleastern/southeasterntaxa,S.f.weddelli,
49
S.f.fuscicollis,S.f.nigrifronsandS.melanoleucus.Thesesouthernindividualsalsoshowthe
very darkmantled phenotype, as described for S. f. leucogenys. Morphological and mito
chondrialevidencesuggestsarangelimitforS.f.leucogenysfarmoresouthwardsthande
scribed by Hershkovitz (1977) and an inclusion of the northern populations of S. f. leu
cogenysintoS.f.illigeri.Forthedeterminationoftheexactborderbetweenthesetwotaxa,
ifthereisone,furtherresearchisneeded.
3.4.4 ThestatusofS.n.nigricollisandS.graellsi
Theblackmantledtamarin,S.nigricollis,islistedbyHershkovitz(1977)asspecieswiththe
threesubspecies,S.n.nigricollis,S.n.hernandeziandS.n.graellsi.Thestatusofthelatteris
subjecttodiscussionwhetheritshouldbeelevatedtofullspeciesrankornot.Thisassump
tionisbasedontheputativesympatryofS.graellsiwithS.n.nigricollisinsouthernColombia
(regionofPuertoLeguizamo)(HernandezCamachoandCooper,1976).Thisclaim,however,
may have been due to a mislabeled museum specimen (Hershkovitz, 1977). Nevertheless,
graellsiisfeaturedasadistinctspeciesbyRylandsetal.(2000)andGroves(2001).
Inourstudy,S.graellsiformsamonophyleticclade,butisnestedwithintheS.n.nigricollis
clade.Thus,S.n.nigricollisappearsparaphyletic.Moreover,thecladeconsistingofallS.n.
nigricollisandS.graellsiindividuals(clade3)isnestedinS.fuscicollis.Alsoduringthefield
survey,wecouldnotdetectanyclearbarrierorgeographicaldelimitationbetweenthetwo
taxa. The northwestern part of the interfluvium between the Rios Putumayo and Napo
AmazonasseemstobetherangeofS.graellsi,thesoutheasternparttherangeofS.n.ni
gricollis.Sincethereisnomajorgeographicbarrierinthisinterfluvium,itismorelikelythata
zoneofintergradationexists,perhapswithintermediatephenotypes,insteadofaclearbar
rier.Despitetheunresolvedgeneticrelationshipsandtherelativelyrecentdivergencetime
(0.26mya),thecolorationofgraellsiiswelldefined(Hershkovitz1977)andcanbeverifiedin
the field as well as in museum specimens. Taking this into account, we favor subspecific
status for graellsi as previously suggested by Hershkovitz (1977) and Rylands and Mitter
meier(2009).
Questionable is also the status of S. f. fuscus. Moore and Cheverud (1992) suggested the
elevationofthissubspeciestofullspeciesrankduetodifferencesinfacialmorphology.In
previous genetic studies, S. f. fuscus showed more similarities with S. nigricollis than with
50
otherS.fuscicollissubspecies(Croppetal.,1999).Forfurtherresearch,theinclusionofS.f.
fuscusandS.n.hernandeziwouldbedesirabletofullyresolvethecomplexphylogenyand
taxonomyoftheS.nigricolliscomplexinnorthernPeru,ColombiaandEcuador.
3.4.5 Speciesconceptsandgeneraltaxonomicimplications
Our data show that all taxa of the S. nigricollis group derived from a common ancestor,
which separated early from the lineage leading to all larger bodied tamarins. Despite this
earlyseparationfromothertamarins,thetaxaoftheS.nigricollisgroupevolved relatively
recentlyduringarapidradiation~2.9mya.
Basedonourdata,S.fuscicolliscanbeconsideredaspolyphyleticandthetaxonomicstatus
ofthenumeroussubspeciesneedstobereconsidered.Thetaxanigricollis,graellsi,triparti
tus and melanoleucus, lately featured as distinct species, are included in the S. fuscicollis
clade and evolved during the same radiation. Sympatry between S. nigricollis, S. fuscicollis
andS.tripartitushasyettobeprovenandislackingsolidevidence.Ifweacceptthetaxo
nomic status of S. tripartitus, S. melanoleucus and S. nigricollis/graellsi as distinct species,
thestatusofothertaxa,especiallythedifferentsubspeciesofS.fuscicollis,hastoberevised
aswell,asalreadysuggestedbyseveralauthors(e.g.Heymann,2000;RylandsandMitter
meier,2009).Dependingontheappliedspeciesconcept,onecandiscussthetaxonomyof
theS.nigricollisspeciesgroupintwodirections.Eitheralltaxaarecollapsedassubspeciesof
asingle,widespreadanddiversespeciesortheyareallupgradedtofullspecies.
From a more conservative point of view, we could consider the taxa of the S. nigricollis
group, included in this study, as members of one widespread superspecies. Accordingly,
nigricollis, graellsi, tripartitus, lagonotus, nigrifrons, fuscicollis, weddelli and melanoleucus
wouldbeincludedaslocalsubspeciesintothesuperspeciesS.nigricollis.Forthenorthern
leucogenys/illigeri clade and southern leucogenys clade, further research will be necessary
toresolvetheirtaxonomicstatus.
Recently,anotherconceptofspeciesdelimitationprevailedinprimatetaxonomy.Theappli
cation of the socalled phylogenetic species concept, as it was suggested for example by
Groves(2001),whichdefinesaspeciesasthesmallestclusterofindividualorganismswithin
there is a parental pattern of ancestry and descent and that is diagnosably distinct from
othersuchclustersbyauniquecombinationoffixedcharacterstates(Cracraft,1983).The
51
consequenceisadramaticincreaseinprimatespeciesnumbers.Nevertheless,atpresentit
iswidelyusedandappliedinmostrecentstudiesonprimatetaxonomy.Inplatyrrhinepri
mates,almostallformersubspeciesoftitimonkeys(Callicebus)(vanRoosmalen,2002)and
marmosets (Callithrix and Mico) (see Groves, 2001) have been elevated to full species. So
far,ithasbeenappliedtothetamarinsonlyonalimitedscale.
MostoftheS.nigricollisspeciesgroupmembersemergedduringatimeinwhichspeciation
eventsoccurredalsoinotherplatyrrhines.Forexample,Lavergneetal.(2010)founddiver
gencetimesbetweenspeciesofsquirrelmonkeys(Saimiri)1.74.3mya,andCortsOrtizet
al. (2003) estimated the split between some howler monkey (Alouatta) species at 2.34.0
mya. Within Saguinus, S. labiatus and S. mystax diverged 1.15 mya, which is significantly
more recent than the splits between most of the taxa of the S. nigricollis group, although
bothtaxaarewidelyrecognizedasdistinctspecies.AmongtheS.nigricollisgroup,terminal
cladescanbedirectlyassignedtoataxonwithdistinctcoatcoloration.Theonlyexception
hereofisS.f.leucogenysandS.n.nigricollis.Byapplyingthephylogeneticspeciesconcept
onthehereinexaminedtamarintaxa,wecanidentifylagonotus,tripartitus,nigrifrons,wed
delliandfuscicollismorphologicallyandgeneticallyasdistinctandwelldefinedentitiesand,
thus,wewouldrecommendfullspeciesstatusforthesetaxa.Forgraellsi,asubspecificrank
shouldbereconsideredaspreviouslysuggestedbyHershkovitz(1977).Forfinalconclusions
concerning melanoleucus, which is genetically closely related to S. f. weddelli, despite its
striking distinctiveness in fur coloration, more individuals and also individuals from the in
termediatemorphs,crandalliandacrensis,shouldbeexamined.Duetoitsclosegeneticaf
filiation, we do not support the specific status as introduced by Rylands et al. (1993), but
consideringitsdistinctivecoloration,werecommendmelanoleucusassubspeciesofS.wed
delli. More complicated is the situation for S. f. illigeri and S. f. leucogenys, where we can
observeanincongruitybetweenthegeneticdataandthedescribeddataonfurcoloration
and distribution. To further examine the distinctiveness, especially of the southern leu
cogenys clade, data from more locations from the southern parts of the distribution area
andinparticularfromtheareabetweenournorthernsamplingpointsinSanMartnandthe
northbankoftheRioPachiteawouldbenecessary.Furthermore,adetailedrevisionofthe
availablemuseummaterialandtheapplicationofadditionalgeneticmarkers(nuclearloci)to
detect possible hybridization are recommended. Provisionally, we include tamarins of the
52
northernpartsoftheleucogenysrangeintoS.illigeriandkeepthenameS.leucogenysfor
thesouthernpopulations.Forthedeterminationofexactdistributionareas,furtherresearch
andsamplingisrequired.Asummaryofthetaxonomicimplicationderivedfromourdatais
giveninTable3.3.
Table3.3Classificationoftamarinsexaminedinthisstudy,followingHershkovitz(1977)andGroves(2001)com
paredwiththehereinproposedclassification*.
Hershkovitz1977
Groves2001
Proposedclassification
S.nigricollisgraellsi
S.graellsi
S.nigricollisgraellsi+
S.fuscicollis
S.illigeri(includingnorthernleucogenys)
S.leucogenys
S.nigrifrons
S.lagonotus
S.weddelliweddelli
S.fuscicollismelanoleucus
S.melanoleucusmelanoleucus S.weddellimelanoleucus+
S.fuscicollistripartitus
S.tripartitus
S.tripartitus
+
*Speciessplittingsaremarkedwithdoublelines. Differencesinfurcoloration
3.4.6 Biogeographicimplications
MolecularphylogeneticstudiesonvariousAmazonianorganismsindicatemajordiversifica
tionsduringthelateMioceneorPliocenewhentheEasternCordillierasofthenorthernand
centralAndesuplifted(GregoryWodzicki,2000;Garzioneetal.,2008).Duringthattime,~11
mya,westernAmazoniawasmainlyinfluencedbytheformationoftheAcremegawetland,
alargefluviotidallandscapecoveringmostoftheareaincentralandwesternAmazoniaand
the establishment of the main transcontinental drainage system (Figueiredo et al., 2009).
Thus,thegreatAcrewetlandcouldhaveseparatedtheancestorsoftheS.nigricollisspecies
groupfromtheSaguinusstem,whichledtothelargerbodiedtamarins.Theradiationwithin
theS.nigricollisgroupoccurredmuchlater,accordingtoourdataset~3mya,whichcould
coincidentwiththedeclineoftheAcrewetlandandthefollowingformationoftheAmazo
nianriversystem(Wesselinghetal.,2010). Theexpansionoftropicalrainforestacrossthe
53
formerwetlandareaenabledasubsequentdispersaloftheancestralS.nigricollisstock.The
emerging rivers formed barriers to the dispersing tamarins and enhanced their diversifica
tion.
IfwecomparethishypothesiswithotherNeotropicalprimates,wedetectparallelswiththe
biogeography and dispersal pattern in Saimiri. Lavergne et al. (2010) proposed a western
AmazonianoriginofthegenusandinitialspeciationduringthePlio/Pleistocene.Thedisap
pearanceofthegreatAcremegawetlandandthesubsequentformationoftheAmazonian
fluvialsystemcouldhaveenhancedspeciationinbothgroups.However,sincethephyloge
neticrelationshipsamongthedifferentcladeswithintheS.nigricollisgrouparenotsignifi
cantlyresolvedwecannotdetermineadirectionofdispersal.
Amazoniasextremelyrichbiodiversity,whichweseetoday,surelyevolvednotduringbya
single,shorttermevent(Wesselinghetal.,2010).Asrecentmolecularstudiesondifferent
groupsoforganismssuggest,thediversificationoflifeinAmazoniawasamorecontinuous
process,whichtookplacethroughouttheCenozoic.Forsomegroups,asortofacceleration
of this process is indicated during the Miocene (see Rull, 2008). Unfortunately, molecular
methods can only reflect the situation, we find in modern biota (Wesselingh et al., 2010).
We should be aware that correlating geological and putative speciation events might be
oversimplified,asthedocumentationforbothisoftenincomplete(Lundbergetal.,1998).
Thestudyshowsthatmitochondrialmarkersareusefultoidentifydistinctlineagesintama
rins.Futureresearchisneeded,especiallytheexaminationoftheBrazilian,Ecuadorianand
Colombiantaxa,tocompletethepictureofthetaxonomyofoneofthemostdiversegenera
ofNewWorldprimates.
Acknowledgements
WethankthefieldassistantManuelShahuanoTelloforexcellentworkduringthefieldsurveys,StephanBehl
andPeterGottleuberfortheirhelpandassistanceinthefield,andChristinaOberdieckforhelpandsupportin
the lab. We are further grateful to Sandra Suarez for providing samples from Bolivia. Thanks also to Richard
Kraft and Juliane Diller for giving us the possibility to collect samples from the Zoological State Collection in
MunichandattheBiologicalFieldStationPanguana,Peru.WethankINRENAinLimaforauthorizingthisstudy
(1062007INRENAIFFSDCB) and to the dean of the Forestry Department of the Universidad Nacional de la
Amazona Peruana in Iquitos for administrative support.This study was financially supportedbythe German
Primate Center, the BiodiversittsPakt of the Wissenschaftsgemeinschaft GottfriedWilhelm Leibniz, and the
MargotMarshBiodiversityFoundation.
54
4 TheRangeoftheGoldenmantleTamarinSaguinustri
partitus(MilneEdwards,1878):DistributionsandSym
patryofFourTamarinsinSouthernColombia,Ecuador
andNorthernPeru
Anthony B. Rylands1, Christian Matauschek2, Rolando Aquino3, Filomeno Encarnacin4,

EckhardW.Heymann2,StelladelaTorre5&RussellA.Mittermeier1
ConservationInternational,2011CrystalDrive,Arlington,VA22202,USA
UnitofBehavioralEcologyandSociobiology,GermanPrimateCenter,D37077Gttingen,
Germany
3
C. I. Instituto Veterinario de Investigaciones Tropicales y de Altura, Universidad Nacional
Mayor,Apartado575,Iquitos,Loreto,Per
4
EcologayVegetacinAmaznica,Jr.Tacna620,Iquitos,Per
Universidad San Francisco de Quito, College of Life Sciences, Av. Interocenica, Quito,
Ecuador
Correspondingauthor:AnthonyB.Rylands,ConservationInternational,2011CrystalDrive,Suite500,Arling
ton,VA22202,USA,Tel:+17033412421,Email:a.rylands@conservation.org
Primates
Received:17June2010/Accepted:5August2010
DOI10.1007/s1032901002173
55
4.DistributionsandSympatry
Abstract
A detailed understanding of the range of the goldenmantle tamarin, Saguinus tripartitus
(MilneEdwards,1878),inAmazonianPeruandEcuadorisofparticularrelevance,notonly
because it is poorly known but also because it was on the basis of its supposed sympatry
withthesaddlebacktamarin(Saguinusfuscicollislagonotus)thatThorington(Am.J.Prima
tol.15:367371,1988)arguedthatitisadistinctspeciesratherthanasaddlebacktamarin
subspecies,aswasbelievedbyHershkovitz(LivingNewWorldMonkeys,Vol.I.TheUniver
sityofChicagoPress,Chicago,1977).Anumberofsurveyshavebeencarriedoutsince1988
inthesupposedrangeofSaguinustripartitus,inbothEcuadorandPeru.Herewesummarize
and discuss these, and provide a new suggestion for the geographic range of this species;
that is, between the ros Napo and Curaray in Peru, extending east into Ecuador. We also
review current evidence for the distributions of Spixs blackmantle tamarin (S. nigricollis
nigricollis),Graellsblackmantletamarin(S.n.graellsi)andthesaddlebacktamarin(S.fusci
collis lagonotus), which are also poorly known, and examine the evidence regarding sym
patrybetweenthem.Weconcludethatdespitetheexistenceofanumberofspecimenswith
collectinglocalitieswhichindicateoverlapintheirgeographicranges,thefactthatthefour
tamarins are of similar size and undoubtedly very similar in their feeding habits militates
stronglyagainsttheoccurrenceofsympatryamongthem.
Keywords: Callitrichidae, tamarin, Saguinus, Taxonomy, Distribution, Sympatry, northwest

ernAmazon
56
4.1 Introduction
Thegoldenmantletamarin,Saguinustripartitus(MilneEdwards,1878),ofthewesternAma
zon, was one of the fourteen subspecies of saddleback tamarin, Saguinus fuscicollis (Spix,
1823),proposedinthetaxonomyofHershkovitz(1977).Thorington(1988)showedthatthat
theinformationconcerningitsgeographicdistributionwasscarceandconfusedbut,follow
ingareappraisaloftheevidence,hearguedthatitwasinfactafullspeciesduetoitssym
patrywiththeredmantlesaddlebacktamarin,S.fuscicollislagonotus.Sincethispublication,
anumberofsurveyshavebeencarriedoutinEcuador(Albuja,1994;delaTorre,1996),and
Peru(Encarnacinetal.,1990;AquinoandEncarnacin,1996;Heymann,2000;Heymannet
al.,2002;Aquinoetal.,2005;Matauschek,inprep.;Aquino,unpubl.data).Herewesumma
rize the information obtained in these surveys and propose new boundaries for the geo
graphicrangeofthisspecies.WealsoexaminetheevidenceregardingsympatrywithS.fus
cicollis,aswellaswithGraellsblackmantletamarin(Saguinusnigricollisgraellsi)andSpixs
blackmantletamarin(Saguinusnigricollisnigricollis).
4.2 TheDistributionofSaguinustripartitus
ThedistributionofSaguinustripartitushasbeenindoubtformanydecades.ThetypeofMi
dastripartitusMilneEdwards,1878isaskinofafemaleintheMuseumNationaldHistoire
NaturelleinParis(No.122(653[633A.1877562]),andthetypelocalityisRoNapo,Oriente,
Ecuador(Hershkovitz,1977;Groves,2001).vilaPires(1974)proposedthatthespeciesoc
cursalongthenorthbankoftheRoAmazonasrightuptothemouthoftheRoPutumayo
I in Brazil. Apparently supporting this, HernndezCamacho and Cooper (1976, p.39; see
also HernndezCamacho and Defler 1985) reported that S. fuscicollis is not known in the
immediateregionofLeticia(ontheRoAmazonas,northbank,intheColombiantrapezium),
butthattheyhadexaminedspecimensreferabletoS.fuscicollistripartitusinLeticia,which
werereportedlyfromtheColombianbankoftheRoAmazonas;PuertoNariobytheQue
brada Pichuna Yac, upstream of Leticia (Fig. 4.1). Neville et al. (1976) and Freese et al.
(1982) reported that they found only S. nigricollis during surveys along the Ro Ampiyacu,
north of the Ro Amazonas, near to Colombia, in Peru (Fig. 4.1). Hershkovitz (1977) con
cluded that S. tripartitus occurred between theRos Putumayo (right bank) and Napo (left
57
bank),westtotheAndesinPeruandEcuador,andeasttobeyondtheconfluenceoftheRo
NapowiththeRoAmazonas.
Fig.4.1ThewesternAmazon,includingsouthernColombia,northeasternPeruandBrazil.Locality90isPuerto
Indiana, cited as the north bank Ro Maraon and a locality for Saguinus tripartitus and Saguinus fuscicollis
lagonotusbyHershkovitz(1977).SeeTable4.1.MapKelleeKoenig/ConservationInternational.
Defler(1994,2004)mentionedthattheoccurrenceofS.tripartitusbetweentheRosPutu
mayoandAmazonasinColombiahadstilltobeconfirmed.Inmorerecentsurveys,Monte
negroandEscobedo(2004),likeNevilleetal.(1976),foundonlyS.nigricollis(presumedby
themtobeS.n.nigricollis)atsurveysitesalongtherosAmpiyacuandApayacu(alittleto
thewestofAmpiyacu),butrecordedS.nigricollisandasaddlebacktamarin(S.fuscicollis)at
sitesalittleeastontheRoYaguas(Fig4.1).TheymadenomentionofS.tripartitus,andone
couldsupposethatthesaddlebacktamarintheysawisanundescribedsubspecies(S.f.fus
cusoccurstothenorthofthePutumayoandS.f.nigrifronstothesouthoftheRoAmazonas
[AquinoandEncarnacin,1994;Defler,2004]).S.tripartitushasneverbeenrecordedinBra
zil.
58
Hershkovitzs(1977)beliefthatitoccurrednorthoftheRoNapoeastasfarastheRoAma
zonasinPeruwasbasedonspecimenscollectedbyCarlosOlallaandhissonsin1926and
labelledPuertoIndiana,atownontheleftbankoftheRoAmazonas,approximately40km
northofIquitos.Hershkovitz(1977)placedPuertoIndiananorthoftheRoMaraon(Ama
zonas)justdownstreamofthemouthoftheRoNapo(Fig.4.1,Table4.1)but,aspointedout
byThoringtonJr.(1988),PuertoIndianaisinfactontheleftbankoftheRioAmazonasup
streamofthemouthoftheRoNapo(Fig.4.1).PuertoIndianaisalsoalocalityforS.f.lago
notus(seeTable4.1),andforthisreasonThorington(1988)concludedthat1)S.tripartitus
occursontherightbankofthelowerRoNapoatitsmouth(nottheleftbankasarguedby
Hershkovitz[1977]),and2)that,occurringontherightbank,itissympatricwithS.f.lagono
tus,andthereforemustbeconsideredadistinctspecies.ThoringtonJr.(1988)alsobelieved
thatafurthertwolocalitiesidentifiedbyHershkovitz(1977)themouthoftheCuraray(south
of the Napo, locality 80, gazetteer p.928, Fig XIII.4 on page 916 in Hershkovitz [1977]; see
Table4.1andFig4.1),andSanFrancisco(northoftheNapo,locality66,gazetteerp.927,Fig
XIII.4onpage916inHershkovitz[1977];seeTable4.1andFig.4.2)confirmedsympatrybe
tweenthesaddlebacktamarinstripartitusandlagonotus(Table4.1).
ThisconfusionstimulatedAquinoandEncarnacin(1996)toinvestigatetheNapobasinspe
cificallytoclarifythedistributionsofS.tripartitusandS.f.lagonotus.Theresultsweresur
prising.TheywereunabletofindanyevidenceatallfortheoccurrenceofS.tripartitusalong
either bank of the lower Ro Napo. Their survey included Puerto Indiana, the localities of
FranciscodeOrellanaandMaznnearby,aswellastheleftbanktributariesoftheRoAma
zonaswestofPuertoIndiana,theRosAmpiyacu,Apayacu,Peruat,andAtacuar,andtribu
tariesontheleft(RoYanayacu)andright(RoTacshaCuraray)banksofthelowerRoNapo
(Fig.4.1).InnoneoftheseareasweretheyabletolocateS.tripartitusorfindanyevidence
ofitsoccurrencethere.OntheRoMazn,atributaryenteringtheRoAmazonasupstream
(west)oftheRoNapo(Fig4.1),theyfoundonlyS.f.lagonotusandS.n.graellsi.Theycon
sidered,anddiscarded,thepossibilitythatS.tripartitushadbecomeextinctinthearea,and
wereforcedtotheconclusionthatthelocalityattributedbytheOlallaBros.(PuertoIndiana)
was not where the type had been collected. On the same expedition (1925/1926) that in
cludedPuertoIndiana,theOlallaBros.alsocollectedandpurchasedanimalsandspecimens
alongandfromtheRo Curaray,anupstreamtributaryoftheRoNapo(Table4.1),where
59
theoccurrenceofS.tripartituswasconfirmedbyAquinoandEncarnacin(1994,1996),and
laterbyHeymann(2000;Heymannetal.,2002)andAquinoetal.(2005).
Table4.1ThefivelocalitiesofSaguinusfuscicollistripartituslistedbyHershkovitz(1977).
Hershkovitz(1977)
66
SanFrancisco,RoNapo,leftbank,030'S,7622'W.
Saguinusfuscicollistripartitus
P.Hershkovitz,FebruaryMarch1936,onleftbankat
200meters.
Saguinusnigricollisgraellsi
P. Hershkovitz, FebruaryMarch 1936, on right bank
at200meters.
67a
LagartoCocha,mouth,039'S,7516'W
Saguinusnigricollisgraellsi
OlallaBros.,January1926.
OlallaBros.,January1926.
67b
Aguarico(Ro),059'S,7511'W
OlallaBros.,January1924,December1925.
Notes
NorthoftheRioNapo.Theproximityofthelocalityof
Coca (also Francisco de Orellana) that is the type
locality of S. f. lagonotus indicated sympatry, and
comprised part of the argument of Thorington Jr.
(1988)thattripartitusshouldbeconsideredadistinct
species.
SeeFigure2.
NorthoftheRoNapo.TheLagartocochaistributary
of the Ro Aguarico which enters the Ro Napo from
thenorth.
SeeFigure2.
North of the Ro Napo. Napier (1976) lists the two

specimensasfollows:
1. 1934 .9.10.23. Male adult, skin, skull. Oriente,
neartheR.Napo,20003000ft.January1924.
2. 1934.9.10.24. Male adult, skin, skull, slide of hair.
Oriente, near Aguarico [0, 7620'W], 2000 ft. De
cember1925.
SeeFigure2.
SouthoftheRoNapo.TheRoCurarayisarightbank
tributaryofthelowerRoNapo.ThoringtonJr.(1988)
inferredthatS.f.lagonotusandS.f.tripartituswere
sympatricatthislocality.
SeeFigure2.
80
Curaray(Ro)(mouth),222'S,7405'W,140meters.
OlallaBros.,OctoberDecember1925.
Saguinusfuscicollislagonotus
OlallaBros.,May1926
Saguinusfuscicollisgraellsi
OlallaBros.,1925.
90
SouthoftheRoNapo.AspointedoutbyThorington
PuertoIndiana,RoMaraon,north
Jr.(1988),PuertoIndianaisinfactontheleftbankof
bank,320'S,7240'W,100meters.
theRoMaraon(Amazonas)abovethemouthofthe
RoNapo.Theapparentsympatryofthetwosubspe
OlallaBros.,May,June,July1926.
ciescomprisedpartoftheargumentofThoringtonJr.
Saguinusfuscicollislagonotus
(1988)thattripartitusshouldbeconsideredadistinct
OlallaBros.,August1926.
species.
SeeFigure1.
Numbers inthelefthandcolumnarethoseusedbyHershkovitz(1977;pp.927928,andmapp.916).SeeFig
ures1and2.
FromthesurveysofAquinoandEncarnacin(1996),Heymann(2000;Heymannetal.,2002)
Aquinoetal.(2005)andAquino(thispaper),itisnowevidentthatinPeruS.tripartitusoc
60
cursontherightbankoftheRoNapoonlywestfromthemouthoftheRoCuraray(Fig.2).
Aquino et al. (2005) registered 14 groups in three localities in the basin of the Ro Aushiri
(mainstreamandtributaryRioSanJos)(Fig.4.2).Basedonasightingofonegrouponthe
south (right) bank of the lower Ro Yuvineto (Encarnacin et al., 1990), Aquino and Encar
nacin(1996)concludedthatthedistributionofS.tripartitusextendstotheleftbankofthe
RoNapoonlyalongtheupperreachesoftheRoSantaMaria,anorthern(leftbank)tribu
taryoftheNapo,andfromtherenorthtotheRoPutumayoontheColombianborder,and
inthewestasfarastherightbankoftheRoGeppiandleftbankoftheRoLagartococha
(Fig.4.2).However,C.Matauschek(inprep.)wasunablefindS.tripartitusontheleft(north)
bankoftheNapoalongitsentirecourseinPeru.Interviewsofsettlersatdifferentlocations
alongthecourseoftheNaposhowedthattheydidnotknowofS.tripartitusnorthofthe
Napo,confirmingitspresenceonlysouthoftheNapo.
Fig. 4.2 The western Amazon, including eastern Ecuador, southern Colombia, and northeastern Peru. For an
explanationoflocalities66,67a,67band80,seeTable4.1.MapKelleeKoenig/ConservationInternational.
61
ThenorthernlimittothedistributioninPerucouldbetheRoPutumayo,buttheevidence
deniesitsoccurrencenorthoftheRoNapoinEcuador.There,Albuja(1994)reportedthatit
isrestrictedtotheleftbankoftheRoCuraray,northtoandnotbeyondthelowerreachesof
theRoNapoinEcuador,butlimitedtotheRoTiputini(arightbanktributaryoftheNapo)
furtherwest.Hershkovitz(1977),ontheotherhand,reporteditfromtheleft(north)bankof
theRoNapoatthelocalityofSanFrancisco(twospecimensintheUniversityofMichigan
MuseumofZoology,collectedbyHershkovitzin1936[locality66,Table4.1,Fig4.2]).Olalla
alsosupposedlycollectedS.tripartitusfromthemouthoftheRoAguarico,anorthern(left
bank)tributaryoftheRoNapoontheborderofEcuadorandPeru(specimenintheBritish
MuseumofNaturalHistory,seeTable4.1),aswellasthemouthoftheRoLagartococha,a
northern(rightbank)tributaryoftheRoAguaricoinEcuador(twospecimensintheAmeri
canMuseumofNaturalHistory).ThiswouldindicatethatatleastneartothePeruvianbor
der,S.tripartitusextendstothenorthoftheRoAguarico,northoftheRoNapo.However,
de la Torre et al. (1995a) recorded only S. n. graellsi from the Ro Cuyabeno (a left bank
tributaryoftheRoAguaricowestoftheRoLagartococha).Oversevenyearsduringherre
searchintheCuyabenoFaunalReserve,StelladelaTorretravelledfrequentlyalongtheRo
LagartocochainEcuadorandwasunablefindanyevidenceindicatingthatS.tripartitusoc
cursthere(oneitherbank).DelaTorre(1996)statedthatthereisnoevidenceofitspres
encenorthoftheRoNapo,noralongtheRosAguarico,CuyabenoandLagartococha(p.88).
There is a possibility that the Lagarto Cocha [sic] locality of Olalla (January 1926) listed by
Hershkovitz(1977,p.927)infactreferstoalakeofthesamenamesouthoftheRoNapo.
Thisbeingthecase,evidenceforitsoccurrencetothenorthoftheNapoinEcuadorwould
berestrictedtoHershkovitzslocalityofSanFrancisco,andtheRoAguaricolocalityofOlalla,
theprovenanceofwhichisgivenbyHershkovitz(1977)onpage927asAguarico(Ro),and
onpage658asnearAguarico,RoNapo,andismappedonpage916atthemouthoftheRo
Aguarico.Napier(1976)listedthetwoOlallaspecimensintheBritishMuseumwithlocalities
(labels) which are difficult to interpret (Table 4.1). We were unable to locate Oriente, and
thealtitudes2000to3000feetcannotrefertothemouthofAguarico(seenotesin Table
4.1). It might be that Hershkovitz (1977) interpreted the localities from the travels of the
OlallaBros.andthepossibilityremainsthatbothspecimenswerereallycollectedfromthe
62
southbankoftheNapo,oppositethemouthoftheRoAguaricoor,aswouldbeindicatedby
AquinoandEncarnacin(1996),fromthePeruvian,rightbankoftheRoAguarico.
TheSanFranciscolocalityofHershkovitz(66,seeTable4.1,Fig.4.2)remainsamystery.We
wereunabletolocateSanFranciscoonmapsofEcuador,butthelocality,asheplottediton
his map on page 916 in Hershkovitz (1977), is in or near to the Limoncocha Biological Re
serve (north bank of the Napo), and near (opposite) the mouth of the Ro Indillama.
Hershkovitz (1977, 1982) also collected a specimen of S. n. graellsi from San Francisco, on
therightbankoftheNapo(locality66,p.927).Despitethis,weconclude(seebelow)thatit
isunlikelythatthisspeciesoccurssouthoftheNapo.DelaTorre(1996)recordedS.f.lago
notusbetweentheRoIndillamaandtheRoNapo,andhasinterviewed,indifferentplaces
andtimes,sixoldSecoyamenwholivedintheareaoftherosSantaMaraandPutumayo,
andalloftheminformedthattheyhadneverseenS.tripartitusinthatarea,onlyS.nigricol
lis.
ThelackofevidencetodayfortheoccurrenceofS.tripartitusontherightbankoftheRo
Lagartococha,markingtheEcuadorianfrontierwithPeru,indicatesthatitsrangeinthein
terfluvium of the Ros Napo and Putumayo in Peru is limited to the east (left bank) of the
river,asindicatedbyAquinoandEncarnacin(1996)orevenfurtherrestrictedasindicated
above.
DelaTorre(1996,2000)andKostrub(1997)haveobservedgoldenmantledtamarinsinthe
Yasun National Park, between the ros Yasun and Indillama, and de la Torre (1996) con
firmedtheoccurrenceofS.tripartitusbetweenthesouthernbankoftheRoTiputiniandthe
northernbankoftheRoYasun.Kostrub(1997)reportedthatinEcuadormost,ifnotall,of
therangeofgoldenmantletamarinlieswithintheboundariesoftheParqueNacionalYasun
andtheReservaIndgenaHuaorani(p.102).
ThewesternlimitstotherangeofS.tripartitusinEcuadorarenotclearlydefinedbutAlbuja
(1994)extendeditasfarasthemiddlereachesoftherosTiputiniandCuraray(S.f.lagono
tus occurs at the headwaters of the Ro Curaray), the upper Ro Cononaco, and the entire
basinsoftheRosYasunandNashio(Fig.4.3).
ConcerningtheinformationonS.tripartitusnorthoftheNapoinPeru,wealsocontemplate
thepossibilitythatthisisanewtaxonthatisphenotypicallysimilarto,butdistinctfrom,S.
tripartitus.
63
Fig.4.3HypotheticaldistributionofSaguinustripartitus(shaded).Itsoccurrenceintheshadedareanorthof
theRoNapoisdoubtful.MapKelleeKoenig/ConservationInternational.
4.3 Sympatry
ThequestionofsympatryiscentraltounderstandingthetaxonomicstatusofS.tripartitus.
Therearethreetamarinsintheregionwhich,intheliterature,havebeenconsideredtobe
partiallysympatric.
4.3.1 Saguinusfuscicollislagonotus(JimnezdelaEspada,1870)
InPeru,thissaddlebacktamarinoccurssouthoftherosNapoandCuraray,easttotheRo
Amazonas, and north of the Ro Maran (Aquino and Encarnacin, 1994). Hershkovitz
(1977)andTirira(2007)indicatedthatthewesternlimittoitsrangewastheRoSantiago,a
north (left) bank tributary of the Maran. In their text, Aquino and Encarnacin (1994,
p.14) indicated its occurrence further west and south to the Ro Chinchipe, although their
map(p.108)takesitonlyasfarwestasthebasinoftheRoCenepa(bothalsonorth(left)
banktributariesoftheMaran)(Fig.4.4).ThePeruvianrangeisquitewelldocumentedin
64
termsofcollectinglocalities,withHershkovitz(1977)listingspecimensfromtheRosNanay,
Tigre,PastazaandupperSantiago.Significantly,Hershkovitz(1977)givesnolocalitiesnorth
oftheRoCuraray(oneatthemouthoftheCuraraywascollectedbytheOlallaBros.1926
andpresumablyfromthesouth[rightbank]oftheriver[Heymann,2000]).Itstypelocalityis
based on syntypes from the three localities; two in Ecuador: La Coca, Ro Napo and Hu
muyacu, Ro Napo, nearby (both plotted as locality 63, Fig. XIII.4, p.916, in Hershkovitz
[1977])andTarapotoinPeru,atributaryoftheleftbankoftheNaponearandontheoppo
sitebankofthemouthoftheCuraray(locality79,Fig.XIII.4,p.916,inHershkovitz[1977]).
Taropoto is also a locality for S. n. graellsi as is the Ro Curaray, and the reason why
Hershkovitz(1982)indicatedsympatrybetweenS.n.graellsiandS.f.lagonotus.Ifwefollow
theassertionofdelaTorre(1996),itdoesnotoccurineasternEcuadorbetweentheRos
CurarayandTiputini,whereS.tripartitusispresent.Albuja(1994),ontheotherhand,said
thatS.f.lagonotusandS.tripartituswerebothpresentintheTiputiniandTambocochalo
calities he reported (see Table 4.2). The range map of S. f. lagonotus provided by Tirira
(2007)coverstheentirerangeofS.tripartitusinEcuador,andTirirastated(p.119),without
explanationorreference,thatthetwotamarinsaresympatricinthenorthoftherangeof
tripartitusneartheRoNapo(Fig.4.5).
65
Fig.4.4HypotheticaldistributionsoffourtamarinsinthenortheasternAmazon:Saguinusnigricollisnigricollis,
S.n.graellsi,S.tripartitus,andS.fuscicollislagonotus.MapKelleeKoenig/ConservationInternational.
Table4.2LocalitiesforSaguinustripartitusinEcuadorandPeru
Ecuador
Tambococha,RoTambococha,
tributary of the Ro Jatuncocha,
right
bankoftheRoNapo,5kmsouthof
themouthoftheRoTiputini
RoTivacuno,mouthof,southbank
tributaryofthemiddleRoTiputini
Coordinates
7535'58"W,
0054'12"S,
alt.187m
Notes
Reference
Nov. 1991, obs. (6 groups). S. Albuja(1994)
fuscicollis lagonotus also re
ported
YasunResearchStation,Yasun
NationalPark,northofRoYasuni
PompeyaSurRoIrohighway,
betweenRoIndillama(RoTiputini)
andRoYasun
YasunNationalPark,Proyecto
PrimatesStudySite
Mar.1994,obs.(3
groups). S. fuscicollis lagonotus
alsoreported
Observationof4groups
Observation
Near
7633W,
048S
7620'W,
040'S
Observation
TiputiniBiodiversityStation
(UniversidadSanFrancisco),north
bankofRoTiputini,northofYasuni
NationalPark
Observation
66
R.Muoz,inAlbuja
(1994)
delaTorre(1996)
de la Torre (1996),
Kostrub
(1997)
Kostrub(1997)
Kostrub(1997)
Peru
Bellavista, Ro Yuvineto, south of
RoPutumayo
Puerto Elvira, south bank of Ro
Napo
7433'W,
0202'S
Aug.1978,obs.(2groups)
7432'W,
0202'S
SanRafael,northbankofRo
Curaray,nearmouth
7408'W,
0222'S
Correviento,northbankofRo
Curaray
Soledad,northbankofRoCuraray
7332'W,
0215'S
Jan. 1983, obs. (1 group), Nov.

1989(2groups);Aug.1992(1
group)+1specimencollected
Feb. 1983, obs. (3 groups), 1
specimencollected
Feb.1983.obs.(1group)
7425'W,
0217'S
Feb.1983,obs.(2groups)
Aushiri,RoAushiri,southbankof
RoNapo
7444'W,
0214'S
Dec. 1983, obs (1 group), 1

specimencollected
Tempestad,southbankofRoNapo
7452'W,
0115'S
7411'W,
0208'S
Dec.1989,obs.(1group)
Dec.1991, obs. (2 groups), 1

specimencollected(petinfant
male)
Aug.1992,1specimencollected Aquino & Encar
nacin(1996)
Sep.1999,obs.(1group)
Heymann(2000),
Heymann et al.
(2002)
Sep.1999,obs.(1group)
Heymann(2000),
Heymann et al.
(2002)
Jun.2007,obs.(5groups)
Matauschek
(in
prep.)
Jun.2007,obs.(1group,1pet)
Matauschek
(in
prep.)
Ingano,southbankofRoNapo
PuertoArica,northbankofRo
Curaray
Playa,RoCuraray,north(left)bank
7512'W,
0128'S
7453'W,
0202'S
Soledad,RoCuraray,north(left)
bank
Vencedores,RoNapo,rightbank
7426'W,
0216'S
CampoSerio,RoNapo,rightbank
7502W
0112S
7470W
0180S
Aquino & Encar

nacin
(1996)
Aquino & Encar
nacin
(1996)
Aquino & Encar
nacin
(1996)
Aquino & Encar
nacin
(1996)
Aquino & Encar
nacin
(1996)
Aquino & Encar
nacin
(1996)
Aquino & Encar

nacin(1996)
Aquino & Encar
nacin(1996)
ItwasonthebasisofsupposedsympatrywithS.f.lagonotus(throughapparentlycoincident
collectinglocalities)thatThorington(1988)arguedthatS.tripartitusshouldbeconsidereda
species.ThekeylocalityforThoringtonsargumentofsympatry,however,wasPuertoIndi
anaatthemouthoftheNapo,but,asdiscussedabove,AquinoandEncarnacin(1996)have
failed to find any evidence that S. tripartitus ever occurred there. Albuja (1994), however,
notingthatS.f.lagonotuswaspresentatthetwolocalitiesherecordedforS.tripartitus(see
Table 4.2), supported Thoringtons (1988) thesis that S. tripartitus should be considered a
distinctspecies.DeLaTorre(1996),Kostrub(1997)andHeymannetal.(2002),ontheother
hand,foundnoevidenceofsympatry.InEcuador,theywouldapparentlybesympatricsouth
of the Ro Napo, but de la Torre (1996) stated that to date, there are no reports of sites
67
whereanytwoofthe(Ecuadorian)tamarinspeciesliveinsympatry(p.88).SheobservedS.f.
lagonotus south of the Ro Napo in areas close to the Jatun Sacha Research Station, the
AangocochaLakeandalongthePompeyaSurRoIrohighwayasfarsouthas,butnotsouth
of,theRoIndillama,asouthbanktributaryoftheNapo.S.tripartitusoccurssouthoftheRo
IndillamatotheRoCuraray.Heymannetal.(2002)recordedaclearseparationofS.triparti
tus (left bank of the Ro Curaray) and S. f. lagonotus (right bank), and concluded that the
ecologicalsimilarity[ofS.tripartitus]withSaguinusfuscicollisandthelackofhardevidence
forsympatryargueagainstitbeingaseparatespecies(p.198).TheyagreedwithThorington
(1988),however,inindicatingthatifS.tripartitusshouldbemaintainedasadistinctspecies,
otherS.fuscicollissubspeciesshouldalsobeconsideredfullspecies.
AlthoughAquinoandEncarnacin(1994)indicatedthatS.n.graellsioccurredsouthofthe
lowerNapototheRoNanay,webelievethatitisimprobable(seebelow).Webelievethat
thegeographicrangesofS.f.lagonotusandS.n.graellsidonotoverlap.Duringasurveyin
2007, Matauschek (in prep.) encountered only S. f. lagonotus at all locations he visited on
therightbankoftheNapo,southoftheCurarayinPeru.Hesawbothwildanimalsandpets
(inthreedifferentvillages).Also,localpeopleclearlyidentifiedtheresidenttamarinsonthe
pictures shown to them. There was no evidence for S. f. lagonotus occurring on the right
bankoftheNapoabovethemouthoftheCuraray.
4.3.2 Saguinusnigricollisnigricollis(Spix,1823)
InformationonthedistributionofSpixsblackmantledtamarin,S.n.nigricollis,isconfused
and conflicting. Its type locality is the north bank of the Ro Solimes, near So Paulo de
Olivena, Amazonas, Brazil, and Hershkovitz (1977, 1982) placed it between the Ros
SolimesAmazonasandIPutumayo,atleastasfarwestasthemouthoftheRoNapo.
Encarnacinetal.(1990)andAquinoandEncarnacin(1996)suggesteditsoccurrencewest
fromtherealongtheleft(north)bankoftheRoNapoinPeru,upstreamtotherosLagarto
cochaandGeppiontheborderwithEcuador,whereaccordingtoHershkovitz(1982)itis
replacedbyS.nigricollisgraellsi.InarecentexplorationalongtheRoNapo,C.Matauschek
(inprep.)encounteredS.n.nigricollisonthenorthbankoftheNapooppositeSanFelipe,a
village270kmdowntheRioNapofromtheEcuadorianborder,andfromtherefurthereast
on different locations north of the Napo and the Amazon(for example, the ros Ampiyacu
68
andApayacu,seeFig.4.2).MontenegroandEscobedo(2004)sawblackmantledtamarins,
whichtheypresumedwereS.n.nigricollisnotgraellsi,betweentherosAmazonasandPu
tumayoinPeru,innumerouslocalitiestheysurveyedinthebasinsoftheRoYaguas,asouth
(rightbank)tributaryofthePutumayo,andtherosApayacuandAmpiyacu,both(leftbank)
tributariesoftheAmazonas(seeFig.4.1).
InColombia,HernndezCamachoandCooper(1976)andDefler(1994)reportedthatitoc
cursnorthoftheRoPutumayototheRoCaquet,andeasttotheBrazilianborder,indicat
ing its, as yet undocumented, presence between the ros Japur and Ia in Brazil
(Hershkovitz,1977,1982).EvidenceforitsoccurrencenorthoftheRoPutumayoinColom
biaissparse,however.AsdiscussedindetailbyDefler(2003,2004),theoccurrenceofS.n.
nigricollis in Puerto Leguzamo (Fig. 4.2) was based on a specimen in the collection of the
InstitutodeCienciasNaturales(ICN),registeredasfromtheQuebradaElHacha,aleft(north)
bankaffluentofthePutumayo(collectorsH.GranadosandH.Arvalo).Anumberofspeci
mensinthesamecollectionarelabeledasfrombetweentherosCaquetaandPutumayo.
HernndezCamacho and Cooper (1976) noted, however, that the population of the upper
Putumayo River has a dull and brownish cast to the lower back and hind limbs, as well as
somegrizzledyellowandblackinthesaddleandconcludedthatThispopulationisthusmore
reminiscentofS.fuscicollisthanisthelowerPutumayoandLeticiapopulation,whichhasa
richferruginouscasttothelowerbackandhindlimbsandnoyellowishtonesinthesaddle
area(pp.3739).Evaluatingthis,Defler(2003,2004)concludedthatthetamarinsthoughtto
beS.n.nigricollistothenorthoftheRoPutumayoareinfactdullspecimensofS.fucicollis
fuscus, and recorded that Philip Hershkovitz, in a personal communication to Defler, be
lievedthesame.
SouthoftheRoPutumayotherangeofS.n.nigricollisperhapsoverlapswithS.tripartitus
betweentherosYuvinetoandGeppi,asarguedbyEncarnacinetal.(1990)andAquino
andEncarnacin(1996).BravoandBorman(2008)carriedoutmammalsurveysatfivesites
betweentherosNapoandPutumayoinEcuadorandPeru:westofthemiddleRoLagarto
cocha(Garzacocha),onthesouth(right)bankoftheupperRoGeppi(Geppicillo)(bothin
theCuyabenoFaunalProductionReserveinEcuador),ontheright(east)bankoftheRoLa
gartacocha (Redondococha) in the proposed Airo Pai Communal Reserve (Peru), the south
(right)bankoftheRoGeppiintheproposedGepiNationalPark(Peru),andontheupper
69
reachesoftheRoPeneya(AguasNegras),arightbanktributaryofthePutumayo(Peru)(see
Fig. 4.2). Bravo and Borman (2008) reported S. nigricollis in all these sites. They made no
mentionofsubspecies,butpublishedaphotographofaninfant/juvenile(theirFig.8A)that
appearstobeS.n.nigricollisnotgraellsi.TheymadenomentionofS.tripartitus.
Fig.4.5Graellsblackmantletamarin(Saguinusnigricollisgraellsi),Spixsblackmantletamarin(Saguinusnigri
collis nigricollis), redmantle saddleback tamarin (Saguinus fuscicollis lagonotus), and the goldenmantle sad
dlebacktamarin(Saguinustripartitus).StephenD.NashConservationInternational.
4.3.3 Saguinusnigricollisgraellsi(JimnezdelaEspada,1870)
Graells blackmantle tamarin occurs in the upper Amazon, in southern Colombia, eastern
EcuadorandnortheasternPeru.Itsrangeisnotwellknown,however,andourinterpretation
of the current evidence indicates that it is probably more restricted than is indicated by
70
Hershkovitz(1977,1982).ThetypelocalityisbanksofRoNaponearTarapoto,andDesta
camento, near confluence with the Maran, Loreto, Peru (Hershkovitz, 1977). Cabrera
(1958)restrictedittoTarapoto,andHershkovitz(1977)restricteditfurthertorightbankRo
Napo,oppositeTarapotoandabovethemouthoftheRoCuraray(locality79,p.629).Desta
camentoisplottedbyHershkovitzasontherightbankoftheRoNapo,justaboveitsmouth
(locality91,map,p.626).TheRoTarapotoisaleftbank(north)tributaryoftheRoNapo.
HernndezCamacho and Cooper (1976) wrote that in Colombia it occurs south from the
right (south) bank of the upper Ro Caquet to the Ros Sucumbos and Putumayo on the
border with Ecuador. They recorded that it could also be found in the neighborhood of
PuertoAssontheupperPutumayo,easttothevicinityofPuertoLeguzamo,northbankof
theRoPutumayo.AsdiscussedaboveforS.n.nigricollis,theseauthorsindicatedaprobabil
itythattheformgraellsiissympatricwithS.n.nigricollisintheregionofPuertoLeguzamo,
andHernndezCamachoandCooper(1976)andDefler(1989,1994)listedgraellsiasafull
speciesasresult.TheconclusionofDefler(2003,2004)andHershkovitz(pers.comm.toDe
fler2003,2004),however,wasthatthespecimensconsideredtobeS.n.nigricolliswerein
factjustdullcolouredS.fuscicollisfuscus.InhismostrecentassessmentDefler(2003,2004)
listed graellsi as a subspecies of S. nigricollis. Genetic data (Matauschek et al., submitted)
supportthisassessment.Groves(2001,2005)maintainedgraellsiasafullspeciesbasedon
HernndezCamachoandCoopers(1976)suppositionofitssympatrywithnigricollis.
Hershkovitz(1982)arguedthatthereisnodefiniteevidenceforS.n.graellsioccurringnorth
of Ecuador, and suggested that blackmantled tamarins reported by HernndezCamacho
andCooper(1976)maybeeitherS.n.nigricollisorS.n.hernandezi.Herestricteditsnorth
ern limit to the Ros Putumayo and Sucumbos (Ro San Miguel), indicating as such that it
doesnotoccurinColombiaatall.
AccordingtoHershkovitz(1982),inEcuadorS.n.graellsiextendsthroughoutalargepartof
theAmazonregion,southfromtheRosPutumayoandSanMiguel,westtothefoothillsof
theAndes.Thealtitudinalrangeisbetween100mand1000m(Hershkovitz,1982).Saguinus
n.graellsiissupposedtooccurnorthoftheRoNapoinEcuador,andtoextendeastonlyas
fartherosGepiandLagartocochaonthefrontierwithPeru(Hershkovitz,1982),whereit
shouldbereplacedbyS.n.nigricollis(seeHershkovitz,1982;AquinoandEncarnacin,1996).
However,inPeru,Matauschek(inprep.)encounteredtamarinsnorthoftheNapobetween
71
Pantoja and Torres Causana that phenotypically matched S. n. graellsi exclusively. Conse
quentlytheborderbetweenS.n.graellsiandS.n.nigricollismustliefurthersoutheastin
Peru.TheonlylargerriverinthisareaistheRoTamboryacu.Theriveritselfseemsunlikely
toformabarrierforthetamarinsbecauseofitscourse,whichismoreorlessparalleltothe
RoNapo,leavingmuchspacefordispersalbetweenthePutumayoandtheTamboryacu.It
seemsmorelikelythatthelargeareaoflow,seasonalfloodedvrzeaforestsurroundingthe
vast streamnetwork of the Tamboryacu could form a barrier for the tamarins, which are
scarceandrarelyseeninthistypeofforest.Theapproximateareaismarkedinwhitewitha
questionmarkinFigure4.4.
IthasbeenrecordedrecentlyinanumberoflocalitiesinnorthernEcuadorbetweentheRos
NapoandPutumayo,includingthebasinsoftherosAguarico,CuyabenoandPacuyacu(S.
de la Torre, in litt. 1996). Borman (2002) recorded S. nigricollis (presumably graellsi) at Si
nangoeontheRoCofanes(aleftbanktributaryoftheupperAguarico),andfromtheupper
RoBermejo(arightbanktributaryofthePutumayo)inEcuador.Howeverithasnotbeen
foundintheYasunNationalPark,coveringthebasinoftheRoYasun,whereitwouldseem
thatonlyS.tripartitusand,accordingtoAlbuja(1994),butnotdelaTorre(pers.obs.1996),
S.fuscicollislagonotusoccur.
Hershkovitz(1977)suggestedthattherangeinEcuadormayextendasfarsouthastheright
bankoftheupperRoSantiago,althoughinhislaterpublication(1982)hewasmoreconser
vative,givingthenorth(right)bankoftheRoPastazaasthelimit.Thespecimensfromthe
ros Pastaza and Tigre are from their uppermost reaches in Ecuador. Hershkovitz (1982)
showedthefourlocalities,numbers1922,onhisFigure3(p.653),andlistedthemasfol
lows:
(19)YanaRumi(Ro),mouthofRoPindoYacu,138'S,7659'W.R.Olalla,December,1934,
February,1935;
(20)PindoYacu(Ro),joinsRoCunambo,upperRoTigreat237908'S,7604'W.R.Olalla,
October,1934,abovejunctionwithRoCunamboat250m;
(21)Pastaza(Ro),205'S,500m.C.S.Webb;and
(22)CapahuaraorCapihuara(Ro),mouthatRoPastaza,203'S,7651'W.R.Olalla,Novem
ber1934,abovemouthat300m.
72
These are the only records south of the Ro Napo in Ecuador, and the reason why
Hershkovitz(1982)tentativelyextendedtherangetotheentirelowlandAmazonianregion
ofPerubetweentherosNapoandPastazatotherosAmazonasandMaran.Bothdela
Torre(1996)andTirira(2007)restrictS.n.graellsitothenorthoftheNapoinEcuador.Tirira
(2007)discountedthePastazaandTigrerecordsforthisspecieslistedbyHershkovitz(1982)
saying only that: The validity of certain populations to the south of the Ro Napo, in the
provincesofOrellanaandPastaza,ismotiveforcontroversy(p.118).
AquinoandEncarnacin(1994)reported,however,thatS.n.graellsihasneverbeenfound
alongtherosTigreandPastazadespiteanumberofprimatologicalsurveysalongtheseriv
ersbetween1981and1986.TheyindicatedthatS.n.graellsiextendseastwardsfromEcua
dorintoPerualongtheright(south)bankoftheRoNapoandthattherangeinPeruisre
stricted to the region between the ros Nanay and NapoCuraray. Matauschek (in prep.)
could not find any evidence for S. n. graellsi along the Ro Nanay (Santa Mara, Diamante
Azul)in2007and2008.Aquinoetal.(2005)surveyedtheRoAushiri(rightbankaffluentof
theNapo)in2005andintheareabetweentherosCurarayandNashio(leftbankaffluent
oftheCuraray)in2007and2008.TheydidnotfindanyevidenceforthepresenceofS.n.
graellsi,encounteringonlyS.tripartitus.
Hershkovitz(1982)gavejustthreelocalitiesforS.n.graellsiinPeru.Twoofthemaretype
localities quite distant from each other. The third is Curaray (Ro), boca (= mouth) at Ro
NapocollectedbyOlallaandSonsin1925.Heymanns(2000;Heymannetal.,2002)finding
thatS.n.graellsidoesnotoccuralongeitherbankoftheRoCurarayputstheTarapotoand
mouth of the Curaray localities (both number 4, p.655) in doubt. Likewise, Hershkovitz
(1977,p.629)givesthe(type)localityofDestacamentoasnearconfluencewithMaran
butmappeditattheconfluenceoftheRoNapo.ThethirdPeruvianlocalityofHershkovitz
(1982) is listed as Destacamento (=Francisco Orellana), Ro Napo, at the junctionwith Ro
Amazonas (Hershkovitz, 1977, locality 91, p.626; 1982, locality 5, p.652). There is another
Francisco de Orellana (Puerto), which is at the mouth of the Ro Coca, an affluent of the
Napo, in Ecuador (Fig. 4.2), a region where itwould seem that S. n. graellsi certainly does
occur,andwhich,suggestively,isalsonearorat(thesamelocalityas)thetypelocalityofS.
f.lagonotus,alsodescribedbyJimnezdelaEspada.FranciscodeOrellanaatthemouthof
theRoCocaisalsoknownasCoca.
73
IfweacceptthatS.n.graellsiislimitedtothenorthoftheRoNapoinEcuador,anddoes
notoccurbetweentherosCurarayandNapoinEcuadororPeru,anddoesnotoccuralong
therightbankoftheCurarayinPeru,itisverydifficulttoacceptthatitoccursbetweenthe
lowerRoNapoandRoNanayinPeru.Thissuppositioniseitherbasedonerroneouslocali
ties(eitherincorrectlabelsorincorrectinterpretationofthem),or,iftamarinsconsideredto
begraellsihavebeenseenthere,thattheyareinfactasimilarbutdistincttaxon.
Saguinusn.graellsiislargelyrestrictedtoEcuadornorthoftheRoNapoincludingthebasin
oftheRoCuyabeno,and,probablyoccurringinPerubetweentherosNapoandPutumayo
westpossiblyasfartheupperreachesoftheRoTamboryacu.Evidenceforitspresencein
ColombiaisbasedonapreservedspecimenfromtheComisaraofPutumayo,andanumber
ofreliablesightings(forexample,ontherightbankoftheRoGuamus,reportedinMoyni
han[1976],whosaidthattheirappearanceconformedtothedescriptionS.n.graellsipro
videdbyHershkovitz(1966);butnospecimenswereobtained),andcaptivespecimensfrom
Puerto Ass, east to the vicinity of Puerto Leguzamo (HernndezCamacho and Cooper
1976).
ThedistributionofS.n.graellsihasyettobeclearlydefined.HernndezCamachoandCoo
per(1976)informedthat,inColombiabetweentheupperreachesoftherosPutumayoand
Caquet,S.graellsiisundoubtedlysympatricwithS.fuscicollisfuscusthroughoutitsrange
(p.39)andthisisconfirmedbyDefler(2003,2004).ItdoesnotoccurbetweentheRosCura
rayandNapoinPeruandEcuador,andisnot,therefore,sympatricwithS.tripartitus.
4.4 Sympatry,BodySizeandEcologicalNiches
Inordertosharethesamehabitat,organismsmustdifferinsomedimensionoftheirreal
izedecologicalniche(Putman,1994).Thisistrueindependentofwhethernichedifferences
arebroughtaboutthroughinterspecificcompetition,predationorotherbioticinteractions,
or whether differences result from inherently diverging fundamental niches (Keddy, 1989;
Putman, 1994). In the context of examining the geographic distribution of different taxa
fromthegenusSaguinus,itisappropriatetoaddressthequestionoftheirnichedifferentia
tionandtheimplicationsforpossiblesympatricoccurrenceorexclusion.
Body size is an important lifehistory parameter with direct implications for the ecological
nicheoccupiedbyanorganism.Ecologicaltheoryconsidersbodysizeasanimportantfactor
74
forstructuringcommunities(Schoener,1984,1988).ItisastructuringfactorforNeotropical
primate communities through its implications for diet, foraging strategies, 447 predator
avoidance,locomotion, andmetabolicneeds(Terborgh,1983).Saguinusspecieswhichun
doubtedlyliveinsympatry(SaguinusfuscicolliswithSaguinusimperator,orSaguinuslabia
tus,orSaguinusmystax)differinbodymassby21%49%,andinheadbodylengthby8%
17%(Heymann,1997).Thisdifferenceislinkedtodifferencesinlocomotorstyle,substrate
use, vertical space use and perhaps more important to different strategies of foraging for
animalprey(BiccaMarques,1999;BuchananSmith,1990,1999;Garber,1991,1993;Nickle
and Heymann, 1996; Nyakatura and Heymann, 2010; Peres, 1992; Pook and Pook, 1982;
Terborgh, 1983; Yoneda, 1981). Different prey foraging strategies in turn result in a larger
divergence in the animal component of the diet between sympatric tamarin species com
paredtotheplantcomponent(Heymannetal.,2000;NickleandHeymann,1996).Thishas
beensuggestedasamechanismwhichallowsnotonlyforsympatriccoexistencebutalsofor
the formation of stable mixedspecies groups in tamarin monkeys (Heymann, 1997; Hey
mannandBuchananSmith,2000).IncontrasttothebodysizedifferencesinsympatricSa
guinusspecies,differencesbetweendoubtfulsympatrictaxa(Saguinusfuscicollislagonotus
Saguinustripartitus;SaguinusfuscicollisfuscusSaguinusnigricollisnigricollis)amountfor
only14%inheadbodylength(Heymann,1997).Headbodylengthissimilaroridenticalfor
other taxa of the Saguinus fuscicollis/nigricollis clade with debated sympatry (Table 4.3).
Unfortunately, no body mass data from wild animals areavailable for these taxa for more
detailedanalyses.
Table 4.3 Headbody length of taxa from the Saguinus fuscicollis/nigricollisclade with debated sympatry
(source:Hershkovitz1977;Appendix.Table1)
Species
Measurements
Saguinusn.graellsi
223mm(n=5)
Saguinusn.nigricollis
223mm(n=2)
Saguinusf.fuscus
226mm(n=16)
Saguinustripartitus
229mm(n=2)
Saguinusf.lagonotus
232mm(n=11)
When organisms occur in sympatrythey may differ inmorphological, physiological or eco

logical parameters more strongly than if they occur allopatrically, a phenomenon called
75
character displacement (Schoener, 1988). It can therefore be asked whether the observed
differencesbetweensympatricSaguinusspeciesresultfromsuchcharacterdisplacementor
whethertheyarepartofthefundamentalecologicalniche.Onlyonekindofdataisavailable
forsuchacomparison,namelythepatternsofverticalspaceuse.Theuseofverticalspace
has been compared between Saguinus fuscicollis subspecies living sympatrically and allo
patrically with another Saguinus species by BuchananSmith (1999) and Heymann (2000).
ThestronglysimilartoalmostidenticalpatternsofverticalspaceuseofS.fuscicollisweddelli
atsiteswhereitlivessympatricallywitheitherS.labiatusorS.imperatorcomparedtosites
whereitoccursalone,andofS.fuscicollisnigrifrons(sympatricwithS.mystax)andS.fusci
collisilligeri(nosympatriccongener)suggeststhatthisispartofthefundamentalnicheand
notinfluencedbythepresenceofacongenericspecies.Examinationofthefewdataavail
able on vertical space use by other members of the smallbodied Saguinus clade (sensu
Croppetal.[1999];thatisS.n.nigricollis,S.n.graellsi,S.n.hernandezi,S.tripartitus)also
revealssimilaroridenticalpatternsofverticalspaceuse.Thesetaxaperformmostoftheir
activitiesatlowerstrataoftheforest,likeSaguinusfuscicollis(delaTorreetal.,1995;Hey
mann,2000;UlloaVaca,1988;VargasTovar,1994).Qualitativeandquantitativedescriptions
ofthepatternsofforagingalsosuggestthatthedifferentsubspeciesofS.fuscicollisandS.
nigricollis,andS.tripartitusarealsoverysimilaroridenticalinthisaspect(Heymann,2000;
Izawa, 1978; Peres, 1993; Soini, 1982). In summary, we can say that (1) all taxa of the Sa
guinus fuscicollis/nigricollisclade for which information is available, be they sympatric or
allopatricwithanotherSaguinusspecies,showsimilaroridenticalpatternsofverticalspace
use;(2)Saguinusspecieswhichcertainlyaresympatric,evenformingmixedspeciesgroups,
clearlydifferinbodysize,whileallopatricordoubtfullysympatrictaxahaveaverysimilarto
identicalbodysize(Table4.3).
GiventhesimilarityinverticalspaceuseandbodysizeofthetaxaoftheSaguinusfuscicol
lis/nigricollisclade, it is unlikely, and for theoretical reasons implausible, that they can co
existinthesameforests,eventhoughtheirgeographicdistributionsoverlap.
76
4.5 GeographicRanges,Sympatry,andtheTaxonomyofSaguinusnigricollisand
S.fuscicollis
The definitions of these tamarin species and their range limits are, of course, hypotheses.
The confusion concerning the geographic distributions of the northwestern Amazonian
tamarinsarisesnotonlyfromtherelativelyfewlocalityrecordsuponwhichtheyarebased
(HershkovitzwasabletousefiveforS.tripartitus)butalso,evenwhenprecise,theuncer
taintythatthelabelsattachedtomuseumspecimensaccuratelystatethelocationwherethe
specimens were actually obtained. As Hershkovitz (1977) fully recognized, knowing from
whichbankofariveraspecimenwasobtainedisfundamental,andsooftencanonlybein
ferred from other locations where the species has been recorded. The collector, receiving
thespecimenfromahunter,maynothaveknownorevencaredtoasktheexactprovenance
ofthespecimen,believingthatitoccurredeverywhereintheregionandthatthebasecamp
wasasufficientreference,eventhoughmanymilesaway.Manyplacenamesareconfused
or now difficult to identify or locate. These difficulties concerning interpretation are well
known,butwealsohavetheadditionalconfoundingfactorofthedefinitionofthespeciesin
question.Forexample,inacloselyrelatedgroupofcallitrichids,themarmosets,Hershkovitz
(1977)recognizedsixtaxainhisargentatagroup(twospecies,humeraliferandargentata,
eachwiththreesubspecies);todaywelist14withinthegeographicrangehecircumscribed
(Rylandsetal.,2008,2009).Withourunderstandingoftheimportanceofriversindemarcat
ingthegeographicdistributionsofsomanyoftheAmazonianprimates,itispossibletosup
pose that with further investigation, we would find that tamarins identified as tripartitus
northoftheNapoareinfactadistinctanddifferenttaxon.Lastly,wehavethesimpleprob
lemofassertionsofthepresenceofaspeciesbeingunknowntothereaderbasedmerelyon
theauthorityofadistributionmap;consideredafactratherthanahypothesis.Thenumer
oussourcesofinexactitudeshavecometogethertoconfoundourtrueunderstandingofthe
rangesofthesetamarins,andoursuppositionsarebasedtoalargeextentonsurveyswhich
failedtofindevidenceoftheoccurrenceofaspecieswhereitshouldbe,onourunderstand
ing of the ecology and patterns of sympatry of these small insectivore frugivores, and on
distributionpatternsfoundelsewhereintheAmazon,withgeographicrangesbeingdelim
itedevenbyminortributaries.
77
Here we conclude that S. tripartitus occurs between the Ros Napo and Curaray and that
therethereisnostrongevidencethatitoccursinsympatrywithS.f.lagonotus,S.n.nigricol
lisorS.n.graellsi.ThepopulationnorthoftheNapoaroundtheheadwatersoftheRoSanta
Mara and along the left (west) bank of the Ro Yuvineto (Encarnacinet al., 1990) means
that it is potentially sympatric with S. nigricollis, but only one group was seen and further
investigationisneeded.Itmaybeadistincttaxon,andwebelievethatsympatryisunlikely.
ConcurringwithotherauthorssuchasTirira(2007),wearguethattherangeofS.n.graellsi
ismuchsmallerthanwasindicatedbyHershkovitz(1977,1982)andlimitedtothenorthof
theNapoinEcuador.Thisimpliesconsiderableconfusioninthemuseumspecimenlocalities
forS.n.graellsiandtheinterpretationofthem,asisalsothecasefortripartitusandlagono
tus.SpecimenscitedbyHershkovitzfromtheupperrosTigreandPastazainEcuadorrequire
investigation(Tirira,2007).Saguinusn.graellsiextendsintoPeruperhapsasfarasthelow,
seasonalfloodedvrzeaforestsurroundingtheRoTamboryacu.Beyondthatwouldbethe
domain of S. n. nigricollis, which otherwise occurs in themiddle andlower interfluvium of
theAmazonasNapoandPutumayoI.
According to Defler (2004), S. n. graellsi also occurs between the upper ros Caquet and
Putumayo in Colombia. The middle and lower interfluvium of the ros Caquet and Putu
mayoisotherwiseoccupiedbyS.f.fuscus.Saguinusn.hernandeziextendsthroughareasto
the north of the Caquet, north to the upper Ro Guaviare, and east to the Ro Yari
(HernndezCamacho and Cooper, 1976; Hershkovitz, 1977; Defler, 2003, 2004). The re
moval of S. tripartitus from the NapoPutumayo interfluvium (except for the Ro Yuvineto
localityofEncarnacinetal.[1990])meansthatS.f.fuscusassuchisgeographicallyisolated
from other saddleback tamarins a reason to raise eyebrows and questions concerning its
taxonomic status and even perhaps the distinction of the blackmantled and saddleback
tamaringroups.ThegeographicalproximityofS.f.fuscusandS.nigricollisisconcordantwith
thephylogeneticaffinityfoundbyCroppetal.(1999),whosuggestedthatfuscusshouldbe
considered a separate species as a result; an argument also supported by Moore and
Cheverud(1992),whostudiedfacialmorphology.Notable,however,isthesightingofS.fus
cicollis on the Ro Yaguas (between the Putumayo and Amazonas in Peru) by Montenegro
andEscobedo(2004).
78
Cropp et al. (1999) were also concerned with their finding that S. tripartitus, considered a
distinctspeciesonthebasisofsympatrywithS.f.lagonotus,was,basedonmtDNAsequenc
ing,phylogeneticallysoveryclosetoit(sistertaxa).Itwouldseemthatthesympatryinthis
casecannotbethedeterminingfactorforconsideringS.tripartitustobeaspecies.Whether
itshouldbeconsideredagainasubspecies,however,isaquestionwhichrequiresareview
ofthetaxonomyoftheSaguinusnigricollisgroupofHershkovitz(1977),andfurtherresearch
onthegeographicdistributionsofthe17componenttaxa(Rylandsetal.,2008;Rheetal.,
2009).
Acknowledgements
Our sincere thanks to two people who reviewed this article, one anonymous, the other Colin P. Groves, for
theircommentsandwisdom.WearemostgratefultoKelleeKoenig,ConservationInternational,fordrawing
themaps,figures4.14.4,andtoStephenD.Nash,StonyBrookUniversityandConservationInternational,for
theillustrationsofthefourtamarins(figure4.5).
79
5.GeneralDiscussion
5 GeneralDiscussion
5.1 Summaryofresults
TamarinsofthegenusSaguinus,subfamilyCallitrichinae,representoneofthemostdiverse
primate radiations. So far, about 35 taxa have been described, but detailed information
about their taxonomy and phylogeny is still lacking. To further elucidate the phylogenetic
relationships and the biogeographic history within the genus, and to contribute to a more
reliableclassificationofitstaxa,wesequencedcompletemitochondrialgenomes,thecyto
chromebgeneandthehypervariableregionIoftheDloop.Therefore,wemainlyusedfecal
samples from wild tamarins collected during two expeditions to the Peruvian Amazon, an
areaofhightamarindiversity.
PhylogeneticrelationshipswithinthegenusSaguinus:
WhatisthepositionofSaguinuswithintheCallitrichinae?
SaguinusbranchedofffirstwithintheCallitrichinae.Theyseparatedaround13mya.Leon
topithecusbranchedoffsecondandformsasisterlineagetoCallimicoandthemarmosets.
Howarethephylogeneticrelationshipsamongthedifferenttamarinspeciesgroups?
WithinSaguinuswefindawellsupporteddeepinitialsplitbetweenthesmallbodiedS.fus
cicollis 1 andS.nigricollisontheonehandandallotherlargerbodiedrepresentativesofthe
S.mystax,S.bicolor,S.midasandS.oedipusspeciesgroupsontheotherhand.Withinthe
largebodied clade we find a separation of South Amazonian (S. mystax group) and North
Amazonian(S.bicolor,S.midasandS.oedipusgroup)lineages.S.labiatus(representingthe
S.mystaxgroup)branchesofffirst,whileS.midasandS.bicolorformacladetotheexclu
sionofS.oedipus.
AlthoughweproposethegenusnameLeontocebusfortheS.nigricollisspeciesgroup(seeChapter2),theold
genusnameSaguinusisprovisionallykeptuntilourresultsarepublishedanddiscussedbythescientificcom
munity.
80
5.GeneralDiscussion
WastheancestraltamarinmoresimilartotheS.nigricollisortotheS.midasspecies
group?
Within Saguinus the S. nigricollis group branched off first. Within the largebodied lineage
the S. midas and S. bicolor group are the most recent offshoots. Thus, the hypothesis of
phyleticdwarfismandabasalpositionofS.midasasproposedbyFerrari(1993)cannotbe
confirmed.
Whichtaxonomicimplicationscanbemadeongenusandsubgenuslevel?
We found much older and deeper phylogenetic splits between different species groups of
Saguinusthanbetweenthedifferentgeneraofmarmosets.TheS.nigricollisgroupsplitoff
fromothertamarinsinthelateMiocenearound9.2mya.Theotherspeciesgroupsdiverged
between 5.3 and 7.3 mya. The taxonomic nomenclature of the different species groups
should be revised. On a mainly timebased genus concept we recommend an elevation to
genericlevelforatleasttheS.nigricollisspeciesgroupandsubgenericstatusfortheS.mys
tax,S.oedipus,andtheS.bicolor/S.midasgroups.
PhylogenyoftheS.nigricollisspeciesgroup:
AreS.fuscicollisandS.nigricollismonophyleticspecies?
Wecouldshow,thatinthecurrentlyrecognizedtaxonomy,S.fuscicollisandS.nigricollisare
polyphyletic taxa. Taxa, which are currently recognized as species are closer related with
somesubspeciesofS.fuscicollisthanthesewitheachother.
CanwedelimitatespecieswithinthediverseS.nigricollisgroup
We could confirm most of the existing taxa as distinct entities and could identify various
clusters, which are mainly consistent with described differences in coat coloration. On the
basisofthephylogeneticspeciesconcept(PSC)wesuggestspeciesstatusforthefollowing
taxa:fuscicollis,illigeri,lagonotus,leucogenys,nigricollis,nigrifrons,tripartitusandweddelli.
WhatisthetaxonomicstatusoftheproposedspeciesS.graellsi,S.tripartitusandS.
melanoleucus,andtheirrelationshiptotheremainingPeruviantamarintaxa?
Ourgeneticdatadonotsupportaseparatestatusforthetaxamelanoleucusandgraellsi,as
theyaretoocloselyrelatedwithS.weddelliandS.nigricollis,respectively.Butduetoclearly
defineddifferencesinfurcoloration,wegivethemsubspeciesstatus.S.tripartitusisclearly
distinctincolorationandinthegeneticdata,andthereforedeservesspeciesstatus.
81
5.GeneralDiscussion
CanwedetectanysympatrybetweentaxaoftheS.nigricollisgroup?
Weconcludethatdespitetheexistenceofanumberofspecimenswithcollectinglocalities
whichindicateoverlapintheirgeographicranges,thefactthatthesetamarinsareofsimilar
sizeandalmostidenticalintheirfeedinghabitsandotheraspectsoftheirecologymilitates
strongly against the occurrence of sympatry among them. We also could not find any evi
denceforsympatrybetweendifferenttaxaoftheS.nigricollisgroupduringfieldsurveysin
Peru.
BiogeographyofSaguinus:
WhatisthegeographicoriginanddirectionoftheSaguinusradiation?
OurdatasuggestthatthenumeroustaxaoftheS.nigricollisspeciesgrouparederivedfrom
acommonancestorthatseparatedfromtheotherrepresentativesofthegenus~9.2mya.
MosttaxaoftheS.nigricollisgroupformmonophyleticclusters,whichmainlyoriginatedina
singlerapidradiation~2.9mya.ThespeciesgroupmostlikelyoriginatedinwesternAmazo
niaanddiversifiedduringthedeclineoftheAcrewetlandandtheformationoftheAmazo
nianriversystem.
CanwefindeventualcoincidencewithpalaeogeographichistoryoftheAmazonba
sin?
Our data clearly match geological events like the establishment of the Amazon channel
around seven to 10 mya (split of the southAmazonian S. mystax group from the north
Amazonianspeciesgroups),theestablishmentofthegreatAcremegawetland,whichcov
eredlargepartsofwesternAmazoniacouldhaveisolatedtheancestralS.nigricollisstockin
thewesternpartfrom.ThedeclineofthemegawetlandandtheformationoftheAmazo
nianriversystemenhancedtheradiationoftheS.nigricollisgroupandbroughtthemback
intocontactwiththeS.mystaxlineage.
DidSaguinuscrossthemainAmazonchannelorwasitmoreorlessaparalleldisper
salnorthandsouthoftheAmazon?
ThedevelopmentoftheAmazonriverchannelseemstohaveseparatedtheS.mystaxgroup
intheSouth.NorthoftheAmazonriverourdataindicateonedispersalrouteintothenorth,
leadingtotheS.oedipusgroupandanotherheadingtotheeast,leadingtothecloselyre
latedS.midasandS.bicolorgroups.
82
5.GeneralDiscussion
5.2 Theimportanceofextantfieldsamplingforphylogeneticstudies
Forappropriatephylogeneticstudies,especiallyofsuchawidespreadanddiversegroupas
thetamarins,anareawidedensesamplingisessential.Samplesofmuseumspecimensare
extremely difficult to analyze. Most of the museum material is treated with chemicals for
preservation.Thesechemicals,liketheoftenusedboraxandformalin,normallydestroythe
DNAandinhibitanysuccessfulextraction(Coombsetal.,1999).Inoldermaterial,whichis
nottreatedwithchemicals,onlydriedorsalted,theDNAisoftendegradedandhighlyfrag
mented (Wandeler et al., 2007). Another problem with museum specimens, that they are
oftenmislabeledortheoldnamesofthelocalitiescannotberecoveredtoday.However,for
accurate phylogenetic and biogeographic interpretations it is important to know the exact
provenanceofasample,forexamplewhichsideoftheriver,asrivers,especiallyintheAma
zon basin, often form barriers between different taxa or populations (Ayres and Clutton
Brock,1992).Sometimestheoldcollectorsboughttheskinsonlocalmarkets,wherehunters
oftensellanimalsfromvariouslocations.Oftenusedcaptiveorzooanimalstodayarenor
mallybredovergenerationsincaptivity.Theoriginofthefounderanimalsisinmostcases
notcomprehensible(Willis,1993).
Therefore, samples from wild animals with certain localities across their distribution range
arenecessarytoresolvethephylogeneticrelationshipsofsuchadiversegenuslikeSaguinus
andinparticulartheS.nigricollisspeciesgroup.Asmentionedabovethenumeroustaxaof
thisspeciesgrouparedistributedthroughoutthewesternAmazonregionofSouthAmerica,
avastareacoveredwithlowlandrainforestcontaininganetworkofriversandswamps.For
acomprehensivesampling,Peruofferstheuniquepossibilitytoencounter13differenttaxa
oftamarinswithinonecountry.TheareaofthePeruvianAmazonismainlynotdevelopedby
roadsorotherinfrastructure.Theonlypublictransportinthisareaislocalcargoboatswhich
travel the main rivers. To reach also smaller rivers and sidearms the only possibility is to
travelbysmallboatsorcanoes,whichmakesexpeditionsintheseareasextremelydifficult
and logistically extensive. Drug farming, gold mining and guerrilla activities bear consider
ablerisksforstrangers,whichmakessafetravellingandworkingforforeignresearchersex
tremelyriskyandinsomeareasimpossible.Theseareprobablyreasons,whycomprehensive
phylogeneticstudiesofmostNewWorldprimatesareveryscarceandoftenincomplete.This
studyissofarthemostcompleteassessmentofthehighlydiverseS.nigricollisspeciescom
83
5.GeneralDiscussion
plex using almost exclusively samples from wild tamarin populations with confirmed sam
plinglocalities.
5.3 Methodicalapproach:CanmitochondrialDNAserveasasuccessfultoolin
tamarintaxonomy?
The present study is based on mitochondrial DNA (mtDNA) sequence data. Mitochondrial
DNAisonlymaternallyinherited.Analysesonmitochondrialsequencedatathusonlyreflect
maternallineages.MtDNAfunctionsasasinglelocus.Thereforeitisdifficulttoruleoutsort
ing failures of ancestral polymorphisms (incomplete lineage sorting) (Funk and Omland,
2003).IngeneralmtDNAislikelytosortfasterthannuclearDNA(Avise,2004).Ourphylog
enyofcallitrichinegeneraandSaguinusspeciesgroupsseemstobeconfirmedextensively
byongoingnucleardataanalysesonthegenericlevel(Roos,pers.comm.).Theresultsofthe
present study clearly demonstrated that mtDNA provides sufficient information to identify
distinctclustersandlineageswithinthegenusSaguinusandinparticularthevarioustaxaof
the S. nigricollis species group. The mitochondrial lineages reflect in most cases the taxo
nomicarrangementsofHershkovitz(1977)basedonfurcoloration.Exceptionsareasmen
tionedabove,thewhitesaddlebacktamarinS.melanoleucus,whichiscloselyrelatedtoS.
weddelliandthenorthernAndeansaddlebacktamarins,whichwereoriginallydescribedas
leucogenysbutmatchgeneticallyandphenotypicallymoreilligeri.
Inrecentyearshybridizationhasbeenincreasinglyconsideredasanimportantfactorinspe
ciesevolution(ArnoldandMeyer,2006).ItwasforexampledescribedforAfricancichlidfish
(Egger et al., 2007). Meanwhile molecular genetic studies uncovered various examples for
hybridization as speciation factor also in primates. The recently described highland man
gabey(Rungwecebuskipunji)appearstobetheresultofanancienthybridizationbetween
baboons (Papio) and mangabeys (Lophocebus) (Burrell et al., 2009). Ancient hybridization
wasalsodetectedinAsianColobinemonkeys(Tingetal.,2008).Currently,stablehybridiza
tionzonesareknowninbaboons(Zinneretal.,2009;Kelleretal.,2010).Todetectsuchhy
bridizationevents,mitochondrialDNAisnotsufficient.ThereforeanalysesofnuclearandY
chromosomalmarkersarenecessary.Inthisperspective,tamarinfecalsamplesprovedtobe
difficulttoanalyze.HighqualityDNAfrombloodortissuewouldbemoresuitableforlabora
toryanalyses,butdifficulttoobtainfromthewildwithoutharmingtheanimals.Inthetama
84
5.GeneralDiscussion
rinsstudiedhere,thiswouldbeofspecialinterest,toexaminethesituationofthenorthern
leucogenys clade, which are mitochondrial closer related to illigeri than to the nominate
form of (southern) leucogenys and show an intermediate or even more illigerilike pheno
type.
5.4 Speciesconceptsandspeciesdelimitationsandtheireffectonconservation
issues
Foralltaxonomicstudiesthechoiceofthespeciesconceptisalwaysacrucialpointandone
of the most disputed questions in biology in general, as the traditional biological species
concept proposed by Ernst Mayr (1963) is proven to be insufficient (De Queiroz, 2007).
Meanwhile there are various other species concepts on the taxonomic market (Groves,
2004).Mostofthemaretheoreticalapproachestomeetthechallengeofputtingadynamic
systemintostaticcategories.Anewapproach,aconceptofspeciesaspopulationlevelline
ageseliminatesthediscussionaboutspeciesconcepts.Theonlynecessarypropertyofaspe
ciesisthepropertyasseparatelyevolvingmetapopulationlineages(DeQueiroz,2007).But
this will not solve the problems related to species delimitation in practice. We should not
confuse our understanding of the nature of a species with our criteria for detecting them
(Hey2006).
Recently, the application of the socalled phylogenetic species concept (PSC) prevailed in
primatetaxonomy.Itdefinesaspeciesasthesmallestclusterofindividualorganismswithin
there is a parental pattern of ancestry and descent and that is diagnosably distinct from
othersuchclustersbyauniquecombinationoffixedcharacterstates(Cracraft,1983).Itwas
adapted for example by Groves (2001, 2004) and addresses the morepractical part of the
species problem. The main advantage of the PSC is that the amount of difference is not
important,sothatitcanbeappliedonthebasisofanyavailabledataset,butdoesnotex
cludethecomprehensiveanddoubtlessaccurateapproachofDeQueiroz(2007).Theconse
quenceoftheapplicationofthePSCwasadramaticincreaseinprimatespeciesnumbers.
Nevertheless,atpresentitiswidelyusedandappliedinmostrecentstudiesonprimatetax
onomy. In platyrrhine primates, almost all former subspecies of titi monkeys (Callicebus)
(van Roosmalen, 2002) and marmosets (Callithrix and Mico) (see Groves, 2001) have been
elevatedtofullspecies.Especiallyinlemurs,a drasticincreaseinspeciesnumbers,forex
85
5.GeneralDiscussion
ampleinmouselemurs(Microcebus)orsportivelemurs(Lepilemur),canbeobservedinre
centyears(Tattersall,2007;Mittermeieretal.,2010).
Sofar,ithasbeenappliedtothetamarins,oneofthemostdiversegenera,onlyonalimited
scale.Inourstudies,weshowedthatthePSCwasproventobeadaptabletothetamarinsas
well,aswecoulddefinedistinctgeneticlineageswhichareinconcordancewithtaxa,previ
ouslydescribedonthebasisoffurcoloration.
The taxonomic term species is, despite all theoretical problems, the currency in biology,
whichisunderstoodbyscientistsandnonscientistsaswellandthebasisforallpoliticalde
cisionsconcerningconservation,animaltradeandwelfare,landscapeprotection,etc.Facing
the rapid decline of biodiversity and growing threats, it is necessary to find practical solu
tions to the species problem to provide a solid basis to deal with decision makers and
stakeholders,butalwaysbeingawareofadvancingtoapoliticalspeciesconcept.
Fortheevaluationtheconservationstatusespeciallyofsuchwidelydistributedgenera,like
these tamarins, it is highly important to know the taxonomic status and the phylogenetic
relationships between the different populations. The conservation status of a species can
changedramatically,ifitturnsout,thattherearealotofsmallpopulationswhicharedis
tinctevolutionaryunitsanddeserveahighertaxonomicstatus.InthecurrentIUCNredlist
onlyoneof15listedSaguinusspecies(S.oedipus)islistedascriticallyendangered,oneas
endangered(S.bicolor),andoneasvulnerable(S.niger).Allothersarelistedunderthecate
goryleastconcern,includingalltaxawhicharefeaturedassubspeciesofS.fuscicollisand
S.nigricollis(IUCN,2010).Thisissurelytrueifoneconsidersallthedifferenttaxaasonespe
cies.Butifthesingletaxaareconsideredasdistinctspecies,theirconservationstatushasto
berevisedaswell.Formostofthetaxathestatusleastconcernremainsappropriatefor
themoment,asthroughoutwesternAmazonialargeareasarestillcoveredwithrelativein
tactrainforest.Thecapabilityofthetamarinstocopewithdegradedhabitatsenablesthem
tosurviveinareaswithstronghumandisturbances(JohnsandSkorupa,1987).Butthepres
sureontheAmazonianrainforestsisgrowingrapidly.Thehumandemandsforoil,tropical
timber,andlandforagricultureandcattlefarmingiscausesrapiddeforestationandleadto
more and more fragmented habitats for forest animals (Strier, 2007). Already 72% of the
PeruvianAmazoniscoveredbyblocksforoilandgasexploration(Fineretal.,2009).Some
areas,likethedistrictSanMartninthelowerAndesontheedgeoftheAmazonianlowland,
86
5.GeneralDiscussion
arealreadynearlycompletelydeforested.Onlyinsomesteepareassmallforestpatchesare
left.Thesearetheareas,fromwherethesamplesofthenorthernleucogenysoriginated.The
tamarinssharetheselastrefugiaswiththeendemicAndeantitimonkey(Callicebusoenan
the),whichisoneofthemostendangeredPeruvianprimates.Thehighfragmentationofthe
habitatandtheisolationoftheremainingpopulationsareamajorthreatfortheirsurvival
(BvedaPenalba et al., 2009). As the tamarins in this area are faced with the same prob
lems,furtherresearchisneededtodetermine,ifthetamarinsthereareinfactleucogenys,
illigeriorevenformanownevolutionaryunit.
5.5 TherelevanceofmolecularstudiesfortheunderstandingofAmazoniasdi
versityandbiogeography
TheunderstandingoftheextremelyrichbiodiversityofAmazoniarequirestheinterdiscipli
narycollaborationofabroadrangeofscientificfields(Hoornetal.,2010).Withtheexami
nationoffossilrecordsandmolecularphylogeneticstudiesthefieldofbiologycanprovide
usefulevidenceforthegeologicalandevolutionaryhistoryofabioregion.Thecombination
ofvariousphylogeneticstudiesonabroadrangeoforganisms,forinstance,clearlyshowed
thatthemostoftenhighlightedPleistocenerefugia(e.g.Haffer,1969,1997)arerathersam
plingartifactsthanthemaindrivingmechanismfortheevolutionoftheAmazonianbiodiver
sity(Nelsonetal.,1990).Formostgroupsoforganismsthetimeofenhanceddiversification
clearlypredatesthePleistocene.Theyratherindicateanincreasedproliferationofbiodiver
sityduringmiddleandlateMiocene,whereanacceleratedAndeanupliftandthedrainingof
theAmazonbasinprovidedthebasisforacceleratedevolutionandspeciation(Hoornetal.,
2010).Thisisstronglyreflectedbyourdataontamarinevolution.Ourdataontamarinphy
logeny clearly match current findings of the geological history of the Amazon basin (Acre
megawetland,Amazonriverchannel).Thisshowsthatmolecularphylogeneticstudieswith
divergence time estimates, especially on diverse and widely distributed groups of animals
cancontributetotheunderstandingofthebiogeographyandbiodiversity.
87
5.GeneralDiscussion
5.6 Outlook
AnestablishmentofnuclearandYchromosomalmarkerstodetectancientandrecenthy
bridizationswouldbedesirable.Onthegenericlevel,thesestudiesarealreadyontheway
(Roos, pers. comm.) but they could also provide interesting insights on species group and
specieslevel,ifmarkerswithsufficientvariabilitycanbeidentified.Inparticularthiswould
beimportanttoclarifythesituationandrelationshipbetweenS.illigeri/S.leucogenysfrom
thesouthernandwesternPeruvianAmazon.TofurtherexaminethestatusofS.illigeriand
S.leucogenysinthenorthwesternpartoftheirdistributionareaadditionalsamplingwould
bedesirabletodetectdistributionlimits,possiblehybridzonesorzonesofphenotypicinter
gradations. This would also be highly necessary to examine the conservation status of the
tamarinsinthisthreatenedandstronglyfragmentedhabitat.
TocompletethepictureoftamarindiversitytheinclusionofsamplesfromEcuadorian(S.f.
fuscus, S. n. hernandezi) and Brazilian taxa, especially from the S. melanoleucus complex
(crandalli,acrensis)andpossiblehybridsofthemwithS.fuscicollisfromBrazilandthe
Peruvianborder(AltoPurus)wouldbeofgreatinterest.
Similar studies on other diverse and widespread New World primate taxa, could provide
invaluable information to find accordance and to detect patterns for primate evolution in
Amazonia.Acomparablestudyontitimonkeys(Callicebus),whichlivesympatricallywiththe
tamarinsandshowasimilardiversity,couldofferfurtheropportunitiestoconfirmourfind
ingsandtouncoverAmazoniasbiogeographichistory.
88
Summary
guinus).Sofar,about35tamarintaxahavebeendescribed.Thephylogeneticrelationships
within this subfamily and in particular the phylogeny of the six species groups of tamarins
(Saguinus)andtheirpositionwithintheCallitrichinaeisdisputed.
ThefirstpartofthisthesisilluminatesthephylogeneticrelationshipswithintheCallitrichinae
onabroaderscale.Wesequenced13completemitochondrialgenomesofnearlyallcallitri
chine genera and Saguinus species groups. Based on our phylogenetic reconstructions, Sa
guinus branched off first among Callitrichinae, followed by Leontopithecus. Among the re
maininggenera,Callimicoisbasal,andMicoandCebuellaformsistergeneratotheexclusion
of Callithrix. The genus Saguinus is further divided into various, unexpectedly old lineages.
We found much older and deeper phylogenetic splits between different species groups of
Saguinusthanbetweenthedifferentgeneraofmarmosets.TheS.nigricollisgroupsplitoff
fromothertamarinsinthelateMiocenearound9.2mya.Theotherspeciesgroupsdiverged
between 5.3 and 7.3 mya. The taxonomic nomenclature of the different species groups
shouldberevisedandwerecommendanelevationtogenericlevelforatleasttheS.nigricol
lis species group. We bring our data together with the current standard of knowledge of
Amazoniangeology.OurdatasupportaWestAmazonianoriginandaneastwarddispersalof
thegenusSaguinus.
ThesecondpartgoesmoreintodetailbyfocusingontheS.nigricollisspeciesgroup,whichis
the most diverse group and with its numerous taxa, subspecies and/or color variants and
crypticdistributionareassurelyoneofthemostcomplicategeneraofNewWorldprimates.
Tofurtherelucidatethephylogeneticrelationshipsandthebiogeographichistorywithinthis
species group, and to contribute to a more reliable classification of its taxa, we sequenced
thecompletemitochondrialcytochromebgeneandthehypervariableregionIoftheDloop.
Therefore,wemainlyusedfecalsamplesfromabout100wildtamarinscollectedduringtwo
expeditions to the Peruvian Amazon, an area of high tamarin diversity. Most taxa of the S.
nigricollisgroupformmonophyleticclusters,whichmainlyoriginatedinasinglerapidradia
tion ~2.9 mya. S. fuscicollis and S. nigricollis appear as polyphyletic taxa, but we could
89
identifyvariousclusters,whicharemainlyconsistentwithdifferencesincoatcoloration.We
couldconfirmmostoftheexistingtaxaasdistinctentitiesandsuggestspeciesstatusforfus
cicollis,illigeri,lagonotus,leucogenys,nigricollis,nigrifrons,tripartitusandweddelli.Ourge
neticdatadonotsupportaseparatestatusformelanoleucusandgraellsi,butduetodiffer
ences in fur coloration, we give them subspecies status. The species group most likely
originatedinwesternAmazoniaanddiversifiedduringthedeclineoftheAcrewetlandand
theformationoftheAmazonianriversystem.
Thethirdpartisbringingtogethertheinformationondistributionareas,distributionlimits
and sympatry, obtained during our extant field surveys in the Peruvian Amazon, with the
evidenceofotherfieldresearchersandthecurrentknowledgeprovidedbymuseumspeci
mens and historic reports. A detailed understanding of the range of the goldenmantle
tamarin,Saguinustripartitus,inAmazonianPeruandEcuadorisofparticularrelevance,not
only because it is poorly known but also because it was on the basis of its supposed sym
patrywiththesaddlebacktamarin(Saguinusfuscicollislagonotus).Anumberofsurveyshave
beencarriedoutsince1988inthesupposedrangeofSaguinustripartitus,inbothEcuador
andPeru.Herewesummarizeanddiscussthese,andprovideanewsuggestionforthegeo
graphicrangeofthisspecies;thatis,betweentherosNapoandCurarayinPeru,extending
east into Ecuador. We also review current evidence for the distributions of Spixs black
mantletamarin(S.nigricollisnigricollis),Graellsblackmantletamarin(S.n.graellsi)andthe
saddlebacktamarin(S.fuscicollislagonotus),whicharealsopoorlyknown,andexaminethe
evidence regarding sympatry between them. We conclude that despite the existence of a
number of specimens with collecting localities which indicate overlap in their geographic
ranges, the fact that the four tamarins are of similar size and undoubtedly very similar in
theirfeedinghabitsmilitatesstronglyagainsttheoccurrenceofsympatryamongthem.
90
Zusammenfassung
DieKrallenaffen(Callitrichinae)sindkleineNeuweltAffen.Zuihnenzhlenzweiderformen
reichstenPrimatengruppen,dieMarmosetten(CallithrixundMico)unddieTamarine(Sagui
nus). Bisher wurden etwa 35 verschiedene Tamarintaxa beschrieben. Die phylogenetischen
BeziehungeninnerhalbderUnterfamilieundinsbesonderezwischendensechsArtengruppen
der Tamarine und deren Position innerhalb der Krallenaffen ist weitgehend ungeklrt und
teilweiseumstritten.
DerersteTeildieserDissertationbefasstsichmitderPhylogenieinnerhalbderKrallenaffen.
Dazu sequenzierten wir insgesamt 13 komplette mitochondrielle Genome von Vertretern
aller Krallenaffengattungen und Tamarin Artengruppen. Nach unseren phylogenetischen
Rekonstruktionen spalteten sich die Tamarine als erstes innerhalb der Callitrichinae ab, ge
folgtvondenLwenaffen(Leontopithecus).UnterdenverbleibendenGattungenbildetCalli
mico eine Schwesterlinie basal zu den Marmosetten. Innerhalb der Marmosetten sind die
AmazonischenMarmosetten(Mico)nhermitdenZwergmarmosetten(Cebuella)verwandt,
alsmitdenAtlantischenFormen(Callithrix).DieGattungSaguinusteiltsichinmehrereun
erwartetalteLinien.WirfandeninnerhalbderTamarinetiefereundlterephylogenetische
AufspaltungenalszwischendenverschiedenenGattungenvonMarmosetten.DieS.nigricol
lisArtengruppespaltetesichbereitsimsptenMioznvoretwa9,2MillionenJahrenvonden
anderenTamarinenab.DieanderenArtengruppentrenntensichzwischen5.3und7.3Mil
lionen Jahren voneinander. Daher sollte die Nomenklatur der verschiedenen Artengruppen
berarbeitetwerdenundwirempfehlenGattungsrangzumindestfrdieS.nigricollisArten
gruppe. Die phylogenetischen Daten bringen wir weiterhin zusammen mit dem neuesten
KenntnisstandberdiegeologischeGeschichteAmazoniens.UnsereDatendeutenaufeinen
westamazonischenUrsprungderGattungSaguinusmiteinerstlichenAusbreitunghin.
DerzweiteTeilderArbeitbeschftigtsichdetailliertermitderformenreichstenGruppe,der
S. nigricollis Artengruppe, die mit ihren zahlreichen Taxa, Unterarten oder Farbvarianten,
sowieoftmalsunbekanntenVerbreitungsgebietensicherlichdiekompliziertesteGruppedar
stellen. Umdie Phylogenie und Biogeographiedieser Artengruppe aufzuklren, sequenzier
tenwirdaskompletteCytochrombGenunddiehypervariableRegiondesmitochondriellen
D
91
Zusammenfassung
Loops.DafrverwendetenwirfastausschlielichgeoreferenzierteKotprobenvonetwa100
freilebenden Tamarinen. Die Proben wurden whrend zwei Expeditionen im peruanischen
Amazonasgebiet gesammelt, einem Gebiet mit besonders hoher Tamarindiversitt. Unsere
Datenergaben,dasssichdiezahlreichenTaxadieserArtengruppeinnerhalbeinerschnellen
Radiation vor etwa 2,9 Millionen Jahren entstanden. Wir konnten klar abgegrenzte Kladen
definieren, die zumeist mit bereits anhand der Fellfrbungen beschriebenen Einteilungen
bereinstimmen. Deshalb schlagen wir Artstatus fr die Taxa fuscicollis, illigeri, lagonotus,
leucogenys,nigricollis,nigrifrons,tripartitusundweddellivor.DerArtstatusvonmelanoleu
cusundgraellsikonntevonunserengenetischenDatennichtbesttigtwerden.Aufgrundder
deutlichenUnterschiedeinderFellfrbungschlagenwirUnterartstatusfrdieseTaxavor.Die
Artgruppe entstand wahrscheinlich im westlichen Amazonasgebiet undverbreitetesich mit
demVerschwindeneinesausgedehntenSumpfgebietes(Acremegawetland)undderAusbil
dungdesheutigenamazonischenFlusssystems.
DerdritteTeilderArbeitgehtnochweiterinsDetailundbringtdieErkenntnisseausdenbei
den Expeditionen ins peruanische Amazonasgebiet ber Verbreitungsgebiete und grenzen
undSympatriemitdenErgebnissenandererFeldforscherunddemaktuellenKenntnisstand
ausMuseumssammlungenundhistorischenBerichtenzusammen.EindetailliertesVerstnd
nisdesVerbreitungsgebietsdesGoldmantelTamarins(S.tripartitus)imnrdlichenPeruund
inEcuadoristvonbesondererRelevanz,weilesdieGrundlagefrmglicheSympatriezwi
schenzweiTaxaausderS.nigricollisGruppe,nmlichzwischenS.tripartitusundS.fuscicollis
lagonotus, ist. Der Artstatus von S. tripartitus basiert auf dieser mglichen Sympatrie. Wir
fassen auch den aktuellen Kenntnisstand zu den weitgehend unbekannten Verbreitungsge
bietenvon S.n.nigricollis,S.n.graellsiundS.f.lagonotusundpotentiellerSympatriezwi
schendiesenTaxazusammen.Wirschlussfolgern,dass,trotzeinigerMuseumsexemplaremit
berlappendenHerkunftsorten,SympatriezwischendiesenTaxaunwahrscheinlichist,dasie
sichaufgrundgroerhnlichkeiteninGreundNahrungskologiegegenseitigausschlieen
wrden.
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100
Appendix
Supplementary Figure 2.1: Scheme of a mammalian mitochondrial genome. Genes are indicated in green.
Fragments,asamplifiedbyprimersusedinthisstudy,areindicatedinred.Forprimersequencesseesupple
mentarytable2.1.
101
Appendix
SuplementaryTable2.1:Primersusedinthisstudyfortheamplificationofthe21fragmentsofthemitochon
drialgenome.Givenarefragmentnumber(f:forward;r:reverse),taxon,primersequence,referenceandan
nealingtemperature(AT)inC.
Fragment
Taxon
Primersequence(53)
Reference
AT
1f
Callitrichinae
CAAGRCACTGAAAATGYCTAG
Thisstudy
58
1r
Callitrichinae
CTTACCATGTTACGACTTATC
Thisstudy
58
2f
S.bicolor
AAGGTGGATTTAGCAGTAAAC
Thisstudy
58
2f
Callitrichinae
ACGTTAGGTCAAGGTGCAG
Thisstudy
58
2r
S.bicolor
CAACTATGGTAGTTATATGGC
Thisstudy
58
2r
Callitrichinae
TGGCTGCTTTTARGCCAACT
Thisstudy
58
3f
Callitrichinae
AGCTGGTTGTCCAAGACAG
Thisstudy
58
3r
Callitrichinae
ATAGGATTGCGCTGTTATCC
Thisstudy
58
4f
Callitrichinae
GACGAGAAGACCCTATGGA
Thisstudy
58
4r
Callitrichinae
GRAGAGGAGTTGAACCTCTG
Thisstudy
58
5f
Callitrichinae
AATCCAGGTCGGTTTCTATC
Thisstudy
58
5r
Callitrichinae
AGCTTATTTAGCTGACCTTAC
Thisstudy
58
6f
Callimicogoeldii
ATACCTGTTCTAACATCCGG
Thisstudy
58
6f
S.fuscicollis
TTAGACCGGTAATATTTGGGT
Thisstudy
58
6f
Callitrichinae
CCMCAAACRTAAGAAATATGT
Thisstudy
58
6r
S.fuscicollis
TTATAGGAATCGAACCTATACA
Thisstudy
58
6r
Callitrichinae
GTGGRATTATGGGTATTATTC
Thisstudy
58
7f
S.fuscicollis
TAGCAGTACTGCTCTACAAC
Thisstudy
58
7f
S.fuscicollis
TAGCAGTACTGCTCTACAAC
Thisstudy
58
7f
Callitrichinae
CAAACMCAACTWCGMAAAATC
Thisstudy
58
7r
Callimicogoeldii
AGTAAGCATTAGACTGTAAATC
Thisstudy
58
7r
S.fuscicollis
CAGCTCTGAGGTGATTTATC
Thisstudy
58
7r
S.fuscicollis
CAGCTCTGAGGTGATTTATC
Thisstudy
58
7r
Callitrichinae
GCATTAGACTGTAAATCTAAA
Thisstudy
58
8f
S.labiatus
CTAATCAACTGGCTTCAATC
Thisstudy
58
8f
S.bicolor
AGCCCTTACTAGATCGATG
Thisstudy
58
8f
Mico
CTGGCTTCAATCTACTTCTC
Thisstudy
58
8f
S.nigricollis
CTGGCTTCAATCTACTTCTC
Thisstudy
58
8f
Leonotopithecus
ATGTGATAGTTCACCTCAGG
Thisstudy
58
8f
S.labiatus
CTAATCAACTGGCTTCAATC
Thisstudy
58
102
Appendix
8f
Callitrichinae
GGCTTCAATCTAMTTCTCCC
Thisstudy
58
8r
S.labiatus
CCGGTAGGAATAGCAATGA
Thisstudy
58
8r
S.bicolor
TGTGAGATTATTCCGAATCCT
Thisstudy
58
8r
Mico
CGGTAGAATGAGAATATACAC
Thisstudy
58
8r
S.nigricollis
GAGATTATTCCGAATCCTGG
Thisstudy
58
8r
Leonotopithecus
GTGCAGTGTGGCTAATCAG
Thisstudy
58
8r
S.labiatus
CCGGTAGGAATAGCAATGA
Thisstudy
58
8r
Callitrichinae
GCRATRATTATRGTRGCTGAT
Thisstudy
58
9f
S.fuscicollis
GTACATGGGAATAGTCTGAG
Thisstudy
58
9f
S.fuscicollis
GTACATGGGAATAGTCTGAG
Thisstudy
58
9f
Leonotopithecus
ATATCTATTGGTTTCCTAGGC
Thisstudy
58
9f
Callitrichinae
AGCYGCYGGAATTACAATAC
Thisstudy
58
9r
S.fuscicollis
ACTCCAGGTTGGTCGATAG
Thisstudy
58
9r
S.fuscicollis
GGTTGGTCGATAGTTGCTC
Thisstudy
58
9r
Callitrichinae
TGGCTTGAAACCAATTTTWGG
Thisstudy
58
10f
Callimicogoeldii
TCGAACAACTATCTACTAACC
Thisstudy
58
10f
Saguinus
AATRCCCCGACGATATTCAG
Thisstudy
58
10f
Callithrix
TGATTTGAGAAGCATTCTCCT
Thisstudy
58
10f
Mico
GATTTCAACCCACATCCTTC
Thisstudy
58
10f
Saguinus
AATRCCCCGACGATATTCAG
Thisstudy
58
10f
Callithrix
TGATTTGAGAAGCATTCTCCT
Thisstudy
58
10f
Callitrichinae
TRATYTGAGAAGCATTCTCYT
Thisstudy
58
10r
Callimicogoeldii
TATGTGGAATGTGAAACCAAG
Thisstudy
58
10r
Saguinus
TTTGGTTCATTTTAGATTTCAAG
Thisstudy
58
10r
Callithrix
TTGGTTCATTTTAGTTCTCAAG
Thisstudy
58
10r
Mico
ACTGGATGATGTAGAATAAGG
Thisstudy
58
10r
Saguinus
TTTGGTTCATTTTAGATTTCAAG
Thisstudy
58
10r
Callithrix
TTGGTTCATTTTAGTTCTCAAG
Thisstudy
58
10r
Callitrichinae
TTGGTTCATTTTAGTTCTCAA
Thisstudy
58
11f
Callitrichinae
GCATTAACCTTTTAAGTTAAA
Thisstudy
58
11r
Callitrichinae
ARGCRTGTGTTTGGTGTGTC
Thisstudy
58
12f
Callimicogoeldii
GCACTTATTCAAGCTTATGTG
Thisstudy
58
12f
S.fuscicollis
AATTATCATCGAAACAATCAGC
Thisstudy
58
12f
S.bicolor
CTAATACATCTACTTGGAGAC
Thisstudy
58
103
Appendix
12f
S.fuscicollis
AATTATCATCGAAACAATCAGC
Thisstudy
58
12f
Callitrichinae
TAATYATTATYGAAACAATYA
Thisstudy
58
12r
Callimicogoeldii
TACATGAAGACCGTGAAAGC
Thisstudy
58
12r
S.fuscicollis
CAGTCATACTACATCTACGAA
Thisstudy
58
12r
S.bicolor
TAATGACGTGAAGTCCGTG
Thisstudy
58
12r
S.fuscicollis
CAGTCATACTACATCTACGAA
Thisstudy
58
12r
Callitrichinae
TCTACRAARTGTCAGTATCAT
Thisstudy
58
13f
Callitrichinae
TTCTTTATRKCYACAGGYTTC
Thisstudy
58
13r
Callitrichinae
TGCRGCTTCRCATGCGGC
Thisstudy
58
14f
Callitrichinae
ACAAATGATTTCGACTCATTA
Thisstudy
58
14r
Callitrichinae
GTGATATTATCTGTTCATGATG
Thisstudy
59
15f
S.bicolor
TACCACCTAAGTAACTCAGG
Thisstudy
58
15f
S.fuscicollis
ACGCTTAAACGCTGGATCC
Thisstudy
58
15f
Callitrichinae
ATAGCCTTTATAGTHAAAATA
Thisstudy
58
15r
S.fuscicollis
TGGTAGCATGAGTTAGCAG
Thisstudy
58
15r
S.bicolor
TACTTGGAGTTGCACCAATG
Thisstudy
58
15r
Callitrichinae
TTRCTTTTATTTGGAGTTGCA
Thisstudy
58
16f
Saguinus
ATTAGATTGTGAATCTAATAATAG
Thisstudy
58
16f
S.labiatus
ACCATAGGATTAGTTCCCTG
Thisstudy
58
16f
Saguinus
ATTAGATTGTGAATCTAATAATAG
Thisstudy
58
16f
S.labiatus
ACCATAGGATTAGTTCCCTG
Thisstudy
58
16f
Callitrichinae
GATTGTGARTCTAATAAYAGA
Thisstudy
58
16r
S.labiatus
GATGCCAACTGTTACTATCAT
Thisstudy
58
16r
S.labiatus
GATGCCAACTGTTACTATCAT
Thisstudy
58
16r
Callitrichinae
CTARTTGGCTTGAGGTTGAG
Thisstudy
58
17f
S.fuscicollis
GACTCCCATCCGCCATAG
Thisstudy
58
17f
S.fuscicollis
GACTCCCATCCGCCATAG
Thisstudy
58
17f
Callitrichinae
CAGAHGCHAACACAGCAGC
Thisstudy
58
17r
S.fuscicollis
AATCAGAATAAGTCGAGTAGG
Thisstudy
58
17r
S.fuscicollis
AATCAGAATAAGTCGAGTAGG
Thisstudy
58
17r
Callitrichinae
RCCTAGYATRTTAGAGAAGTA
Thisstudy
58
18f
Callimicogoeldii
TCAAGTAACCATACCATATTAC
Thisstudy
58
18f
S.bicolor
TAAGCGTAACCATTATAGGAC
Thisstudy
58
18f
Callitrichinae
TTYGCYGGGTTTCTTATTTC
Thisstudy
58
104
Appendix
18r
S.bicolor
GTCATGGTTATAATCCATGTG
Thisstudy
58
18r
Callitrichinae
CTTATAGTTGAARTACAACRA
Thisstudy
58
19f
S.labiatus
ATCAATTGCTATAGCCGCAG
Thisstudy
58
19f
S.bicolor
ACGTAATCGCACAACCTACA
Thisstudy
58
19f
Mico
AGTAATAACACAACCTACAGC
Thisstudy
58
19f
S.nigricollis
AACGTAATAGCACAACCCAC
Thisstudy
58
19f
S.labiatus
ATCAATTGCTATAGCCGCAG
Thisstudy
58
19f
Callitrichinae
GCAGTRTARCCAAAAACMACC
Thisstudy
58
19r
Callimicogoeldii
TACTTGAGCCTGTTTCATGC
Thisstudy
58
19r
S.labiatus
CGTTAGGAGATCGGCTACT
Thisstudy
58
19r
S.bicolor
ATAGGGTTAGGCTTATCAGG
Thisstudy
58
19r
Mico
GAATATTAGTCCGAGGATATC
Thisstudy
58
19r
S.nigricollis
TGTCTGACGTGTAGTGTATG
Thisstudy
58
19r
S.labiatus
CGTTAGGAGATCGGCTACT
Thisstudy
58
20f
S.nigricollis
CACGATTCTTCACTTTCCAC
Thisstudy
58
20f
S.midas
TGCACCTCACATTAAACCAG
Thisstudy
58
20f
S.nigricollis
CACGATTCTTCACTTTCCAC
Thisstudy
58
20f
Callitrichinae
CACGATTCTTTACCTTCCAC
Thisstudy
58
20r
Callitrichinae
GGTCTCTTAATCTACCWACC
Thisstudy
58
21f
S.bicolor
CACACGACTACCAAGCATG
Thisstudy
58
21f
Callitrichinae
CCATCAACACCCAAAGCTG
Thisstudy
58
21r
S.bicolor
GGCTAGGACCAAACCTATG
Thisstudy
58
Supplementary Table 3.1: Sampling localities, locality IDs, coordinates and GenBank accession numbers of
cytochromebandDloopsequencesfromstudiedtamarinsandotherprimates.
Taxon
Samplinglocality
Locality Coordinates GenBanknr.cytb
GenBanknr.HVI
ID
S.graellsi
Pantoja,RioNapo,left
P
S094
P1:HM368029
P1:HM367929
W7519
P2:HM368030
P2:HM367930
bank
P3:HM368031
P3:HM367931
P4:HM368032
P4:HM367932
P5:HM368033
P5:HM367933
P6:HM368034
P6:HM367934
P7:HM367935
P7:HM368035
S.nigricollis
Tutapishcu,RioNapo,
TP
S311
TP1:HM368075
TP1:HM367975
W7314
nigricollis
leftbank
S.nigricollis
RioApayacu,Amazonas, AP
S327
AP1:HM367984
AP1:HM367884
W7218
AP2:HM367985
AP2:HM367885
nigricollis
leftbank
AP3:HM367986
AP3:HM367886
105
Appendix
S.nigricollis
nigricollis
S.tripartitus
PV
S.fuscicollis
lagonotus
S.fuscicollis
lagonotus
Pevas,Amazonas,left
bank
Vencedores,RioNapo,
rightbank
CampoSerio,RioNapo,
rightbank
SergentoLores,Rio
Napo,rightbank
QuebradaHuiririma,Rio
Napo,rightbank
S.fuscicollis
lagonotus
NuevaYork,RioTigre,
leftbank
NY
S432
W7429
S.fuscicollis
lagonotus
S.fuscicollis
lagonotus
Miraflores,RioMaraon, MF
leftbank
Pilpintuwasi,RioNanay, PW
leftbank
S448
W7408
S370
W7328
S.fuscicollis
lagonotus
S.fuscicollis
lagonotus
S.fuscicollis
lagonotus
S.fuscicollis
illigeri
PadreCocha,RioNanay,
leftbank
RioItaya,rightbank
PC
DiamanteAzul,Rio
Nanay,leftbank
Cahuana
NA
S368
W7328
S400
W7321
S353
W7347
S526
W7434
S.fuscicollis
illigeri
AguasCalientes,
Contamana,RioUcayali,
rightbank
RioTapiche,leftbank
AGC
S713
W7457
TAPL
S543
W7402
PuebloLibre
PL
RumiPata
RP
Moyobamba,EPS
MOY
Tarapoto
TAR
Bellavista
BEL
S552
W7708
S604
W7658
S604
W7658
S629
W7622
S701
W7636
S.tripartitus
S.fuscicollis
illigeri
S.fuscicollis
leucogenys
S.fuscicollis
leucogenys
S.fuscicollis
leucogenys
S.fuscicollis
leucogenys
S.fuscicollis
leucogenys
V
CS
SL
QH
IT
CA
S320
W7149
S112
W7502
S180
W7470
S248
W7370
S245
W7379
106
AP4:HM367987
AP5:HM367988
AP6:HM367989
AP7:HM367990
AP8:HM367991
AP9:HM367992
PV1:HM368046
AP4:HM367887
AP5:HM367888
AP6:HM367889
AP7:HM367890
AP8:HM367891
AP9:HM367892
PV1:HM367946
V1:HM368076
V2:HM368077
CS1:HM368006
V1:HM367976
V2:HM367977
CS1:HM367906
SL1:HM368059
SL1:HM367959
QH1:HM368050
QH2:HM368051
QH3:HM368052
NY1:HM368026
NY2:HM368027
NY3:HM368028
MF1:HM368021
QH1:HM367950
QH2:HM367951
QH3:HM367952
NY1:HM367926
NY2:HM367927
NY3:HM367928
MF1:HM367921
PW1:HM368047
PW2:HM368048
PW3:HM368049
PC1:HM368040
PW1:HM367947
PW2:HM367948
PW3:HM367949
PC1:HM367940
IT1:HM368013
IT1:HM367913
NA1:HM368024
NA2:HM368025
CA1:HM367999
CA2:HM368000
CA3:HM368001
CA4:HM368002
CA5:HM368003
CA6:HM368004
AGC1:HM367979
AGC2:HM367980
AGC3:HM367981
TAPL1:HM368066
TAPL2:HM368067
TAPL3:HM368068
TAPL4:HM368069
PL1:HM368045
NA1:HM367924
NA2:HM367925
CA1:HM367899
CA2:HM367900
CA3:HM367901
CA4:HM367902
CA5:HM367903
CA6:HM367904
AGC1:HM367879
AGC2:HM367880
AGC3:HM367881
TAPL1:HM367966
TAPL2:HM367967
TAPL3:HM367968
TAPL4:HM367969
PL1:HM367945
RP1:HM368058
RP1:HM367958
MOY1:HM368022
MOY2:HM368023
TAR1:HM368074
MOY1:HM367922
MOY2:HM367923
TAR1:HM367974
BEL1:HM367993
BEL2:HM367994
BEL3:HM367995
BEL1:HM367893
BEL2:HM367894
BEL3:HM367895
Appendix
S.fuscicollis
leucogenys
BiologicalStationPan
guana,RioPachitea
S.fuscicollis
weddelli
RioTambopata,leftbank TAM
S1257
W6930
S.fuscicollis
weddelli
BiologicalStationLos
Amigos,RioMadrede
Dios
LAM
S1234
W7006
S.fuscicollis
nigrifrons
RioBlanco,rightbank
RBR
S562
W7387
S.fuscicollis
nigrifrons
S.fuscicollis
fuscicollis
EstacinBiologicaQue
bradaBlanco
RioTapiche,rightbank
EBQB
S421
W7309
S552
W7400
S.mystaxmys
tax
Pijuyal,RioUcayali,right
bank
PIJ
S809
W7419
S.mystaxmys
tax
S.mystaxmys
tax
RioBlanco,rightbank
RBR
EstacinBiologicaQue
bradaBlanco
EBQB
S562
W7387
S421
W7309
S.mystaxmys
tax
S.mystaxmys
tax
RioTapiche,rightbank
TAPR
AguasCalientes,
Contamana,RioUcayali,
rightbank
BiologicalStationLos
Amigos,RioMadrede
Dios
ZoologischeStaats
sammlung,Munich
Bolivia,SanSebastian,
EstacinBiolgica
Tahuamanu
GermanPrimateCenter
(DPZ)
DresdenZoo
AGC
S.imperator
subgrisescens
S.melanoleucus
melanoleucus
S.labiatuslabia
tus
S.oedipus
Callithrixgeof
froyi
Cebusalbifrons
Saimiribolivien
sis
Aotusnancy
PA
TAPR
S937
W7456
S552
W7400
S713
W7457
PA1:HM368036
PA2:HM368037
PA3:HM368038
PA4:HM368039
TAM1:HM368060
TAM2:HM368061
TAM3:HM368062
TAM4:HM368063
TAM5:HM368064
TAM6:HM368065
LAM1:HM368014
LAM2:HM368015
LAM3:HM368016
LAM4:HM368017
LAM5:HM368018
RBR1:HM368053
RBR2:HM368054
RBR3:HM368055
RBR4:HM368056
EBQB1:HM368008
PA1:HM367936
PA2:HM367937
PA3:HM367938
PA4:HM367939
TAM1:HM367960
TAM2:HM367961
TAM3:HM367962
TAM4:HM367963
TAM5:HM367964
TAM6:HM367965
LAM1:HM367914
LAM2:HM367915
LAM3:HM367916
LAM4:HM367917
LAM5:HM367918
RBR1:HM367953
RBR2:HM367954
RBR3:HM367955
RBR4:HM367956
EBQB1:HM367908
TAPR1:HM368070
TAPR2:HM368071
TAPR3:HM368072
PIJ1:HM368041
PIJ2:HM368042
PIJ3:HM368043
PIJ4:HM368044
RBR5:HM368057
TAPR1:HM367970
TAPR2:HM367971
TAPR3:HM367972
PIJ1:HM367941
PIJ2:HM367942
PIJ3:HM367943
PIJ4:HM367944
RBR5:HM367957
EBQB2:HM368009
EBQB3:HM368010
EBQB4:HM368011
EBQB5:HM368012
TAPR4:HM368073
EBQB2:HM367909
EBQB3:HM367910
EBQB4:HM367911
EBQB5:HM367912
TAPR4:HM367973
AGC4:HM367982
AGC5:HM367983
AGC4:HM367882
AGC5:HM367883
LAM
S1234
W7006
LAM6:HM368019
LAM7:HM368020
LAM6:HM367919
LAM7:HM367920
ZSM
ZSM1:HM368078
ZSM1:HM367978
BOL
S1124
W6901
DPZ
BOL1:HM367996
BOL2:HM367997
BOL3:HM367998
DPZ:HM368007
BOL1:HM367896
BOL2:HM367897
BOL3:HM367898
DPZ:HM367907
CAL:HM367905
CAL:HM368005
GenBank
GenBank
AJ309866.1
AJ315389.1
GenBank
AJ489745.1
107
Appendix
maae
Cacajaocalvus
Pithecia
monachus
Callicebustor
quatus
Alouattasenicu
lus
Papiohama
dryas
Macacamulatta
Pantroglodytes
Homosapiens
GenBank
GenBank
FJ531656.1
FJ531668.1
GenBank
AF524890.2
GenBank
AJ489759.1
GenBank
Y18001.1
GenBank
GenBank
GenBank
U38272.1
X93335.1
DQ112959.2
108
Danksagung
Ichbedankemichbei
EckhardW.Heymann,frdieguteBetreuung,vieleAnregungenundeinstetsoffenesOhrfr
Fragen,
Christian Roos fr die Geduld bei vielen, vielen Fragen im Labor, bayrische Analysen und
unzhligeGrillfeiern,
Peter M. Kappeler fr die Mglichkeit diese Arbeit in seiner Abteilung durchzufhren und
allen Mitarbeitern der Abteilung Verhaltenskologie und Soziobiologie fr die gute Zusam
menarbeit,
ManuelShahuanoTello,meinemFeldassistenten,ohnedendiezahlreichenProbenmitsamt
demdazugehrigenDoktorandennichtheilvomAmazonasnachGttingengekommenw
ren,
StephanBehlundPeterGottleuberfrdieunvergesslicheZeitalsVagabundenimDschungel
undsomanchetapferdurchgestandenebrenzligeSituation,
Allen Helfern, Assistenten, Bootsfahrern, Brgermeistern, Gastgebern, aus zahllosen Dr
fernimperuanischenRegenwald,
ChristinaOberdieckfrdieHilfeundUntersttzungimLabor,
MarionSeilerfrdieUntersttzungunddievielenSequenzenundberstundenimLabor,
StephenD.NashfrdieschnenIllustrationen,
DirkMeyerfrdiegemeinsamdurchkmpfteZeitimbeschaulichenG,dieAbenteuerzwi
schen Zrich und New York, all die Feierabendbiere und diskussionen, und, und (Rock`n
Roll!), Sabine Hutschenreuther fr jede Menge Ruhe und Geduld und Hilfe im Endphasen
StressundbeilastminuteFormatierungen,YvanLledoFerrerfrdieschneundturbulente
Zeit im ChaosBro (un aventura mas!), Mojca StojanDolar und Vanessa Mass fr jede
Menge Motivation und zahlreiche Ausflge nach Neverland, Matthias Markolf, Susanne
SchlieheDieks,MarkusPort,Mr.ThinhvanNgocundallenanderenFreundenundKollegen,
diedieZeitinGttingenunvergesslichgemachthaben,MichaelPhlmann,BennoOrthuber,
MaxRennerundGertrudSprlfrdenstndigenDrahtzurAuenweltunddiezwischen
durchdringendnotwendigeErdung,
MeinenElternundGroeltern,ohnederenUntersttzungdieseArbeitnichtmglichgewe
senwre.
109
CurriculumVitae
ChristianMatauschek
Dateofbirth:17August1979inMunich,Germany
Burgstrasse37B
37073Gttingen
Tel:+495514920374
EMail:christian.matauschek@tonline.de
Since01/2007
GermanPrimateCentre(DPZ),Gttingen
Postgraduate
Subject:Taxonomy,PhylogenyandBiogeographyoftamarins(Genus
Saguinus)
Since01/2007
GeorgAugustUniversity,Gttingen
PhDprogramBiologicalDiversityandEcology
200406
Assistant at the Zoological Institute of the LudwigMaximilians

University,Munich
Controlandmaintenanceofplanktonculturesandaquaristicfacili
ties;Supervisionofuniversitycourses
10/2003
OsnabrckZoo
Internshipatthezoologicaldepartment
08/2003
BavarianStateResearchCentreforAgriculture,InstituteforFisher
ies,Starnberg
Internshipinaquacultureandfisheriesmanagement
10/199906/2005
Diploma degree in Biology at the LudwigMaximiliansUniversity,

Munich
Mainsubjects:Zoology,Ecology,Wildlifebiologyandmanagement,
Fisheriesmanagementandbiology
Diploma thesis in Aquatic Ecology: Interactions between phyto
andzooplanktondependingonmixingdepthsandconcentrationof
nutrients
110
ErklrungbereigeneLeistungen
Ichversichere,dassichdievorliegendeArbeitselbstndigverfasstundkeineanderenalsdie
angegebenen Hilfsmittel verwendet habe. Die Stellen die anderen Werken wrtlich oder
sinngementnommensind,sindalssolchekenntlichgemacht.EigeneBeitrgeimVerhlt
niszudenenvonKoautorenbeibereitspubliziertenoderzurPublikationeingereichtenTei
lendieserArbeitsindwiefolgt:
Kapitel2:SiebenmitochondrielleGenomewurdenvonChristianMatauschekzusammenmitMarionSeileram
DPZsequenziert.DieinderArbeitgenanntenspezifischenPrimerwurdenvonChristianMatauschekfrdiese
Studieangefertigt.FnfmitochondrielleGenomewurdenvonKnutFinstermeierbearbeitetundfrdieStudie
dankenswerterweisezurVerfgunggestellt.DieDatenauswertungunddasVerfassendesManuskriptswurden
vonChristianMatauschekdurchgefhrt.
Kapitel3:AlleTamarinprobenwurdenvonChristianMatauschekimPeruanischenAmazonasgebietgesammelt
undimLaborbearbeitet.DieDatenauswertungunddasVerfassendesManuskriptswurdenvonChristianMa
tauschekdurchgefhrt.
Kapitel4:DasManuskriptwurdeimWesentlichenvonAnthonyB.Rylandsverfasst.DatenzuVerbreitungsge
bietenundSympatriewurdenvonChristianMatauschekinPeruaufgenommen,ausgewertetundindasManu
skripteingearbeitet.
Ichversichereweiterhin,dassdieseArbeitingleicheroderhnlicherFormnochkeinerande
renPrfungsbehrdevorgelegenhat.
Gttingen,Dezember,2010
111

Matauschek2010 TaxonPhylogenDistribSaguinusPeru Thesis

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GttingerZentrum

The goldenmantle tamarin S. tripartitus, considered as a subspecies of S. fuscicollis by

Unit of Behavioral Ecology and Sociobiology, German Primate Center, Kellnerweg 4, D

N1 Hominoidea (Homo + Pan) Cercopithecoidea (Macaca + 25.45

N17 S. f. weddelli + S. m. melanoleucus S. f. fuscicollis + S. f. 1.40

Anthony B. Rylands1, Christian Matauschek2, Rolando Aquino3, Filomeno Encarnacin4,

C. I. Instituto Veterinario de Investigaciones Tropicales y de Altura, Universidad Nacional

Keywords: Callitrichidae, tamarin, Saguinus, Taxonomy, Distribution, Sympatry, northwest

North of the Ro Napo. Napier (1976) lists the two

Jan. 1983, obs. (1 group), Nov.

Dec. 1983, obs (1 group), 1

Dec.1991, obs. (2 groups), 1

Aquino & Encar

Aquino & Encar

When organisms occur in sympatrythey may differ inmorphological, physiological or eco

TingN,Tosi AJ,Li Y,Zhang YP,DisotellTR.2008.Phylogeneticincongruencebetweennuclearandmitochondrialmarkersin

Assistant at the Zoological Institute of the LudwigMaximilians

Diploma degree in Biology at the LudwigMaximiliansUniversity,

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