Filling gaps in species distributions through the study of biological collections: 415 new distribution records for Neotropical Cryptinae (Hymenoptera, Ichneumonidae)

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RevistaBrasileiradeEntomologia62(2018)288–291

REVISTA

BRASILEIRA

DE

Entomologia

AJournalonInsectDiversityandEvolution

w w w . r b e n t o m o l o g i a . c o m

Biology,

Ecology

and

Diversity

Filling

gaps

in

species

distributions

through

the

study

of

biological

collections:

415 new

distribution

records

for

Neotropical

Cryptinae

(Hymenoptera,

Ichneumonidae)

Bernardo

F. Santos

a,∗

_,

_João

_Paulo

_M.

_Hoppe

b

a_National_Museum_of_Natural_History,_Department_of_Entomology,_Washington,_DC,_USA b_Universidade_Federal_do_Espírito_Santo,_Departamento_de_Ciências_Biológicas,_Vitória,_ES,_Brazil

a

r

t

i

c

l

e

i

n

f

o

Articlehistory: Received30June2018 Accepted1September2018 Availableonline28September2018 AssociateEditor:RodrigoGonc¸alves Keywords: AtlanticForest biodiversity Cryptini database parasitoidwasp

a

b

s

t

r

a

c

t

Fillinggapsinspeciesdistributionsisinstrumentaltoincreaseourunderstandingofnatural environ-mentsandunderpinefﬁcientconservationpolicies.Formanyhyperdiversegroups,thisknowledgeis hamperedbyinsufﬁcienttaxonomicinformation.Hereinweprovide415newdistributionrecordsfor theparasiticwaspsubfamilyCryptinae(Hymenoptera,Ichneumonidae)intheNeotropicalregion,based onexaminationofmaterialfrom20biologicalcollectionsworldwide.Recordsspanacross227sitesin24 countriesandterritories,andrepresent175speciesfrom53genera.Ofthese,102representnew coun-tryrecordsfor74species.Adistinct“roadpattern”wasdetectedintherecords,atleastwithinBrazil, where50.2%oftherecordsfallwithin10kmoffederalroads,anareathatoccupiesonly11.9%ofthe surfaceofthecountry.Theresultshelptoidentifypriorityareasthatremainpoorlysampledandshould betargetedforfuturecollectingefforts,andhighlighttheimportanceofbiologicalcollectionsinyielding newinformationaboutspeciesdistributionsthatisordersofmagnitudeabovewhatisprovidedinmost individualstudies.

Introduction

Ageneralcomprehensionofgeographicdistributionsofmajor taxa isessential tounderstandnatural environments,to recog-nizespeciesdiversitypatternsandtoplanconservationstrategies

(Gaston,2000;Myersetal.,2000;Lamoreuxetal.,2006).Aproper

understandingofspeciesdistributionsisalsoparamountto under-pinstudiesinevolutionarybiology,phylogeographyandtaxonomy

(Vamosietal.,2007,2009;Webbetal.,2002).

Becausecomprehensiverevisionaryworksarelessoften pro-ducedforhyperdiversegroups,updatesondistributionalrecords ofthesespeciesarecomparativelyrareandoftenpublisheddirectly incatalogues,withoutunambiguousreferencestoprimary (speci-men)records.Thus,itishardtodistinguishwhichrecordsproceed fromidentiﬁcations conﬁrmed by specialists, which affects the qualityofanydistributionalstudyasawhole,andconsequently anyanalysisbasedonsuchrecords.Thisproblemisparticularly evi-dentwhenonecomparestheavailabledataforvertebrateswiththe dearthofinformationforanyspecioseinvertebrategroup,inspite

∗ Correspondingauthor.

E-mail:santosbe@si.edu(B.F.Santos).

oftheirsigniﬁcantroleinecosystembalanceandrelativeamount ofbiomasstheyrepresent.Hence,ﬁllinggapsinourknowledgeof speciesdistributionsisparticularlyimportantforhyperdiverseand historicallyneglectedgroups,especiallyinthecontextofaglobal biodiversitycrisis(Myersetal.,2000;Soberónetal.,2000).

Cryptinewasps(Hymenoptera,Ichneumonidae,Cryptinae)are represented by 274 genera and over 2,800 described species

(Santos,2017).Theyareoneofthedominantcomponentsof

para-siticwaspdiversity,particularlyintropicalregions(Townes,1970;

see alsoVeijalainen et al., 2012).However, the group remains

poorlyunderstoodfromataxonomicand evolutionary perspec-tive.Recentadvanceshavebeenmadeinhigher-levelsystematics

(Santos, 2017), but species-level taxonomy still lags behind an

acceptablepace.Mostcryptinespeciesdescriptionsdatefrom1840 to1920,andfewrevisionaryworkshavebeenconductedsincethen. Hence,mostspeciesarestillrecordedonlyfromtheirtypelocality, oftenstatedvaguelyorimpreciselyintheoriginalworks.Atthe sametime,thelackoftaxonomicresourcesonthisgroupresultsin poorcuratorialstateofmostcollections,hinderingthecollection ofdistributiondata.

AseriesoftaxonomicrevisionsofNeotropicalgroupsstarted tochangethissituationinthepastdecade(e.g.AguiarandRamos,

2011;Aguiarand Santos,2015; Santosand Aguiar,2012, 2013,

https://doi.org/10.1016/j.rbe.2018.09.001

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B.F.Santos,J.P.Hoppe/RevistaBrasileiradeEntomologia62(2018)288–291 289

2015;ScherrerandAguiar,2012;TedescoandAguiar,2013).The

increased availability of reference work to accurately identify specimenstospecieslevelcanfosterasigniﬁcantincreaseinthe availabilityofdistributionrecords.Herein,weusedatagenerated fromloanedspecimens andvisitsby theﬁrstauthor toseveral collectionsworldwidetocontributetowardthatgoal,presenting 415newdistributionrecordsforNeotropicalCryptinae.

Materialandmethods

All data presented in this work proceed from specimens depositedin biological collections anddirectly observedbythe authors; noliterature data is included. Species were identified through comparison with determined species at the National Museum of Natural History (Washington, DC); by comparison withtypespeciesphotographedattherespectivecollections;or byconsultingtheoriginaldescriptionsandappropriate revision-aryworks (mostlyAguiarandRamos, 2011;Santosand Aguiar, 2013).Speciesof Cryptiniwerenotassignedtosubtribes,given thatpreviousresearchhasdemonstratedthatsuchaclassification islargely artificial(Laurenne et al.,2006; Santos,2017).Rather than providing a comprehensive compilationof specimen-level dataforCryptinae,ourgoalwastoprovidethemaximumamount ofnewgeographicalrecordsdrivenbyavailabilityofpreviously ornewlydeterminedspecimensincollections.Materialfrom20 institutionswasexamined,asfollows(curatorsinparentheses). AMNH,AmericanMuseumofNaturalHistory,NewYork,U.S.A.(J. Carpenter);APTA,AgênciaPaulistadeTecnologiados Agronegó-cios,RibeirãoPreto,Brazil(N.Perioto);BMNH,TheNaturalHistory Museum,London,U.K.(G.Broad);CASC,CaliforniaAcademyof Sci-ences,SanFrancisco,U.S.A.(R.Zuparko);CMNH,CarnegieMuseum ofNaturalHistory,Pittsburg,U.S.A.(JohnRawls);CNCI,Canadian NationalCollectionofInsects,ArachnidsandNematodes,Ottawa, Canada(A.Bennett);DCBU,DepartamentodeEcologiaeBiologia Evolutiva,UniversidadeFederaldeSãoCarlos,SãoCarlos,Brazil (A. Penteado-Dias); EMEC, Essig Museum of Entomology, Uni-versity of California Berkeley,U.S.A. (P.Oboyski); FSCA, Florida StateCollection ofArthropods, Gainesville,U.S.A. (K.Williams); IAVH, Institutode Investigaciónde RecursosBiológicos Alexan-dervonHumboldt,Bogotá,Colombia(C.Medina);MNHN,Muséum Nationald’HistoireNaturelle,Paris,France(C.Villemant);MUCR, UniversidaddeCostaRica,CostaRica(P.Hanson);MZUP,Museu deZoologiadaUniversidadedeSãoPaulo,SãoPaulo,Brazil(C.R.F. Brandão);UFES,UniversidadeFederaldo EspíritoSanto,Vitória, Brazil(M.T.Tavares);UNAM,UniversidadNacionalAutónomade México,MexicoCity,Mexico(A.Zaldívar-Riverón);UNESP, Univer-sidadeEstadualPaulistaJúliodeMesquitaFilho,SãoJosédoRio Preto,Brazil(F.Noll);USMC,UniversidadNacionalMayordeSan Marcos,Lima,Peru(G.Lamas);USNM,NationalMuseumofNatural History,Washington,U.S.A. (R.Kula);USUC, UtahState Univer-sity,Logan,U.S.A.(D.Wahl);ZSMC,ZoologischeStaatssammlung München,Munich,Germany(S.Schmidt).

Inearlystagesofthiswork,onlygeographicinformationwas collected,thoughlattereffortscompiledfulllabeldataforthe spec-imensexamined.Thelocalitydatacollectedwereverifiedagainst allpublishedrecordsforeachspeciesinordertopreciselyidentify new(i.e.unpublished)records.Inordertoavoidgivingnewrecord statustospecimenscollectedveryclosetoknownlocalities,records wereconsidered“new”whencollectedatleast60km(37.3miles) apartfromtheclosestknownrecords,orwhentheyrepresented newrecordsforanadministrativestate/province,regardlessof dis-tance.Whilethiscutoffissomewhatarbitrary,itavoidsartificial inflationof“newrecords”basedonrepeatedsamplingofthesame naturalarea,forexampledifferentpointswithinasamereserve orneighboringprivatelands.Duringthefilteringprocess,records

thatwerefoundtobepreviouslyknown,butnevergeoreferenced, wereincludedinaseparatetableinordertocomplementthenew localityinformation.

Geographic coordinates, when not present in the speci-menlabels, were obtainedfroma variety of sources, including GoogleEarthversion 7.3.1.4507 and the geoLoctool at

species-Link(http://splink.cria.org.br/geoloc).AmapinKMLformatwas

generated fromtheoriginal table(see supplementarymaterial) containingthefollowingfields:taxon(speciesname),coordinates indecimals,location(countrythrough locality),verbatim speci-menlabel,museumrepository,andspecialistswhoconductedthe identification(althoughallspecimens wereverifiedbythefirst author).Additionalinformation(recordnoveltystatus,referencing andidentificationremarks,etc.)isincludedintheoriginaltable, butwasnotimportedintotheKML.

Tests for a “road-based” pattern focused on records within Brazil,whereGISﬁlesforfederalroadsarereadilyavailable,andthe highnumberofindividualrecordsallowsforstatisticalanalyses. FollowingSoberónetal.(2000),thetestwasconductedbyplacing a10kmbufferoverexistinginter-statefederalroadsand calculat-ingtheproportionofrecordsthatfellwithinthebufferarea.The observedresultswerecomparedtoanexpectedproportion assum-ingrecordswererandomlydistributed,giventheareaoccupiedby thebufferusingaPearson’schi-squaredtest(Pateﬁeld,1981).

Results

Atotalof415newdistributionrecordswerecompiledfor175 speciesfrom53genera.Thecompiledresultsarepresentedwith fullinformationinAppendixS1(AppendixS2withthesamedatain DarwinCoreformat).Recordsencompass227sitesin24countries and territories,includingallcountriesin continentalSouth and CentralAmericaexceptSuriname(Fig.1,AppendixS3).Thenew recordsinclude102newcountryrecordsfor74species.Brazilwas thecountrywiththelargestnumberofrecords(175);not surpris-ingly,thevastmajorityoftheserecordswereconcentratedalong thecoastalportionoftheAtlanticForest,anareamoreextensively sampledthananyotherregioninthecountry.Infact,adistinct “roadpattern”wasdetectedintherecords,atleastwithinBrazil. Atotalof103outof205(50.2%)recordsand38outof85(44.7%) sitesforthecountry(includingnewrecordsandthosenewly geo-referencedherein)fallwithin10kmoffederalroads,anareathat occupiesonly11.9%ofthesurfaceofthecountry(2₌_51.138,_df₌_1,

P<0.00001;AppendixS4).IntheNeotropicalregionasawhole, areasthatremainpoorlysampledcomprisethecenterofSouth America,includingmostoftheAmazonbasin,centralArgentina andthearidregionofnorthernChileandsouthernPeruandBolivia.

Discussion

Approximatelyhalfthespeciestreatedhereinwerepreviously knownonly fromthetype locality, asretrieved fromliterature records compiled in Yu et al. (2012) and thorough review of morerecentliterature.ForseveralNeotropicalspeciesdescribed inthe19thcentury(e.g.intheextensiveworksofBrullé,1846;

Taschenberg,1876;Szépligeti,1916), speciﬁclocalitieswerenot

evenpresentedinthedescription,whichinsteadlistbroad geo-graphicregionsorcountries(e.g.“fromBrazil”).Forthesespecies, thenewrecordsprovidedhereinrepresenttheﬁrstgeoreferenced localityinformation.

Our resultshelp tohighlightpriorityareas for future samp-lingandopenthevenueformorecomprehensivecompilations. NewgeographicrecordsforIchneumonidaeasawholehavebeen advancedmoreorlessconsistentlyinthepastfewyears(e.g.C¸oruh

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290 B.F.Santos,J.P.Hoppe/RevistaBrasileiradeEntomologia62(2018)288–291 -100°0´ 3000 km 2000 1000 0 -40°0´ -20 °0´ -40 °0´ 0°0´ 20 °0´ -60°0´ -80°0´

Fig.1.HeatmapwithnewdistributionrecordsforNeotropicalCryptinae.Warmercolors(red)indicatehigherdensityofrecords,whilewhiterareasindicatesparserecords orlackthereof.

Riedel,2017;González-MorenoandBordera,2011;Martínezand

Torretta,2015;Meloetal.,2015;Vasetal.,2015),buttoour

knowl-edgenoneinthescaleorgeographicscopepresentedherein.Albeit extensive,outdatasetalsohelpstodemonstratethelimitationsof currentsamplingefforts,whichseemtobeforthemostpartlimited toareasofeasyaccess.Fordenselypopulatedorhighlythreatened areas,suchastheBrazilianAtlanticForest,havingrecords pub-lishedasstructureddata(i.e.Darwin-core)isparticularlyvaluable; asdataaccumulates,collectiondatescanbeanimportantvariable totestforpastversuspresentdistributionsandspeciesrichness. Atthesametime,whilethelogisticreasonsforsamplingaccessible areasareobvious,adeeperunderstandingofspeciesdistributions intheNeotropicalregionwillclearlydependonactivecollecting programsinmoreremoteareas.Additionalworkisneededinterms of compiling and geo-referencingliterature recordsin order to allowforsoundcomparativestudies.

Speedinguptheincreaseofknowledge

While it is widely acknowledged that biological collections are foundational for understanding biodiversity, including the effects of biological invasions and climatechange (Short et al.,

2018; Suarez and Tsutsui, 2004), the vast majority of reports

on new distribution records for insects comes from isolated surveys and ﬁeld expeditions (e.g. Aranda, 2017; da Silva,

2017; Duarte et al., 2018; Niemiller et al., 2017). Collections,

functioning as a repository from hundreds or thousands of individual collecting events, can yield new information about speciesdistributions that isordersof magnitudeabovewhat is provided in most studies. The endeavor of making this mas-sive stock of information available for researchers has been initiatedthroughsizableprojectsofspecimendigitization world-wide (e.g. Blagoderov and Smith, 2012; Soberón et al., 1996), and by special fundinginitiatives such asthe NationalScience Foundation’s“AdvancingDigitizationofBiodiversityCollections” program.

Inspiteofthetremendousadvancerepresentedbythese ini-tiatives,mostprojectsstillfaceakeylimitationinthatinalmost allcollectionsmanytaxaarestillinpoorcuratorialstate, partic-ularlywhenitcomestotheavailabilityofspecimensaccurately determinedtothespecieslevel–acrucialrequirementformany biodiversityapplications(FeeleyandSilman,2010;Goodwinetal., 2015).Theresultsobtainedinthisstudyshowthat,insomecases, anefﬁcient(oratleast,cost effective)approachmaybein situ curation followed by taxon-speciﬁcdigitization. A trained tax-onomistmayoftenidentifyhundredsorthousandsofspecimens indays. Specimen-leveldatacapturecanthenbeconductedby non-specialists,eitherinsituorthroughquickimagingof speci-menlabels(evenwithacellphone)followedbydigitizationand dataparsing.Thehundredsofnewdistributionrecordsgenerated

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B.F.Santos,J.P.Hoppe/RevistaBrasileiradeEntomologia62(2018)288–291 291 hereinserveasaproofofconceptthatitispossibletoreducethe

“taxonomicimpediment”thathassofarconstrainedtheadvance ofknowledgeonthedistributionofpoorlyknowngroups.

Authorcontribution

Conceivedanddesignedthestudy:BFS.Collecteddata:BFSand JPMH. Contributed specimens/materials/analysis tools: BFS and JPMH.Analyzedthedata:JPMH.Wrotethepaper:BFSandJPMH.

Conﬂictsofinterest

Theauthorsdeclarenoconﬂictsofinterest.

Acknowledgments

Allcuratorsmentionedinmaterialandmethodsreceivedthe firstauthorintheirinstitutionsand/orprovidedinvaluableloan ofCryptinaespecimens.AnaDalMolinkindlypreparedtheKML fileandreviewedanearlyversionofthemanuscript.Katja Selt-mann(UCSB)kindlyassistedtheauthorsinformattingallrecords toDarwinCorestandard.ThefirstauthorissupportedbyaPeter BuckPostdoctoralFellowshipattheNMNH.Thevisitstobiological collectionswerefundedbyaDoctoralDissertationImprovement GrantfromtheNationalScienceFoundation(award#1501802); a‘mini-ARTS’awardfromtheSocietyofSystematicBiologists;an AnnetteKadeGraduateStudentFellowshipandaTheodore Roo-seveltMemorialGrant,bothbytheAMNH;aJessupAwardbythe AcademyofNaturalSciencesof DrexelUniversity;and anEssig MuseumVisitingTaxonomistAwardbyUCBerkeley.Thesecond authorissupportedbyaCAPESscholarshipfunding.

AppendixA. Supplementarydata

Supplementarydataassociatedwiththisarticlecanbefoundin theonlineversionatdoi:10.1016/j.rbe.2018.09.001.

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