CREARE: A Course-Based Undergraduate Research Experience

Curriculum

DOI:https://doi.org/10.1128/jmbe.v22i1.2253C

CREARE:ACourse-BasedUndergraduateResearchExperiencetoStudythe

ResponsesoftheEndangeredCoral AcroporaCervicornis toa ChangingEnvironment†

JuanS.Ramírez-Lugo,a CarlosToledo-Hernández,b IvonneVélez-González,c andClaudiaP.Ruiz-Diazb,d aDepartmentofBiology,UniversityofPuertoRico,RíoPiedrasCampus,SanJuan,PuertoRico,USA00925 bSociedadAmbienteMarino,SanJuan,PuertoRico,USA cDepartmentofGraduateStudies,SchoolofEducation,UniversityofPuertoRico,RíoPiedrasCampus,SanJuan, PuertoRico,USA dDepartmentofEnvironmentalSciences,UniversityofPuertoRico,RíoPiedrasCampus,SanJuan, PuertoRico,USA

Thereismountingevidencetosupportthatstudentswhoparticipateinscientificresearchexperiencesare morelikelytocontinueontoadvanceddegreesandcareersinscience,technology,engineering,andmathematics(STEM).Tointroducemorestudentstothebenefitsofresearch,wehavedrawnonanongoing projectaimedatunderstandinghowtheCaribbeanstaghorncoral Acroporacervicornis respondstoenvironmental fluctuationstodevelopasemester-longcourse-basedundergraduateresearchexperience (CURE),entitledCREARE(CoralResponsetoEnvironmentAuthenticResearchExperience).Themain modeofinstructioninCREAREisthroughtopicmodules,andcourseevaluationisachievedthroughwritingassignments.StudentsinCREAREperformexperimentsinthelaboratorytomeasuretheabundance ofphoto-protectiveproteinsincoraltissuefromsamplescollectedatdifferentdepthsandatdifferent timesoftheyearandanalyzeenvironmentaldatausingtheRprogramminglanguage.CREAREparticipantshavecontributedtotheprogressoftheresearchprojectbygeneratingnoveldataandmaking improvementstoexperimentalprotocols.Furthermore,pre-andpost-courseassessmentofcontent knowledgerevealedthatstudentsperformsignificantlybetteronawrittenexamafterparticipatingin CREARE,whilealsodisplayingappreciableshiftsinattitudestowardscienceinstudentperceptionsurveys. Inaddition,throughqualitativeanalysisoffocusgroupinterviews,wegatheredevidencetosuggestthat mediatingvariablesthatpredictstudents’ persistenceinsciencearebolsteredthroughourapplicationof theCUREmodality.Overall,CREAREcanserveasamodelfordevelopingmoreresearch-basedcourses thatsuccessfullyengagestudentsinscientificresearch.

INTRODUCTION

Undergraduateresearchexperiences(UREs)havebeen prescribedbymanyasthemeanstoimprovestudentperformanceandincreasethelikelihoodofastudentpursuing advanceddegreesandacareerinSTEM(1–3).Thereported impactsattributedtoUREsdisproportionatelybenefitstudentsfromhistoricallyunderrepresentedgroupsinscience, asegmentofthepopulationwhoseenrollmentinSTEM programshasbeensteadilyincreasingoverthepastdecade

AddresscorrespondencetoDepartmentofBiology,Universityof PuertoRico,RíoPiedrasCampus,SanJuan,PuertoRico,USA 00925.Phone:787-764-0000,ext.88068. E-mail:juan.ramirez3@upr.edu.

Received:17August2020,Accepted:20February2021, Published:31March2021

butwhoalsoabandonSTEMdegreesatahigherratethan anyothergroup(4,5).Traditionally,theengagementof undergraduatestudentsinresearchhasbeenthroughoneon-oneapprenticeships,whicharelimitedintheirofferingdue toa finiteamountofresearchfaculty.Morerecently,higher inclusionofstudentsintoresearchhasbeenachievedthrough theintegrationofresearchintocoursesthroughthepracticeof course-basedUREs,orCUREs.Thismodalityprovidesopportunitiestoalargernumberofstudentsenrolledinacoursewho subsequentlyreportmanyofthesamebenefitsassociatedwith researchinternships,suchasincreasedself-efficacy,enhanced scientificidentity,andcareerclarification(6–9).

CUREsofferampleopportunitiesforlearningandskill development,therebyfosteringbeliefsinstudentsthatthey candowellandobtainapositiveoutcomeforengagingin researchandthereforecontinueacareerinscience(10–11). Thesebenefitsarepartlyexplainedbyself-efficacytheory,which positsthatanindividual’sbeliefsintheircapabilitiestoexecutea

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courseofactionandreachaspecificgoalarisefromparticipationinactivitieswheretheyviewthemselvestobeefficacious andinwhichtheyanticipatepositiveoutcomes(12–14).Inadditiontoresearchself-efficacy,scientificidentityandtheendorsementofvaluesassociatedwiththescientificcommunityhave beenshowntomediatetheintegrationofstudentsintoscience(3,4,15–18).Theconcatenationoftheparticipant’ s senseofbeliefinher/hiscapacitieswiththeiridentification withandinternalizationofthecollectivevaluesofacommunityhasbeentermedthetripartiteintegrationmodelofsocial integration(TIMSI)andhasbeensuccessfullyusedfordescribinghowstudentsbecomemoreengagedwithscience,particularlystudentsfromgroupshistoricallyunderrepresentedin STEM fields.AccordingtoTIMSI,whenastudentassumesthe identityofascientistandreportsfeelinglikeascientist,sheor heismorelikelytopursueacareerinscience(15).Hence, wesetouttodevelopaCUREwherestudentsarepresented withopportunitiestosuccessfullyengageinscientificresearch andtointernalizethevaluesofthescientificcommunity throughparticipationinaresearchprojectthatisbothlocally relevantandofglobalimportance.

Globalclimatechangeishavingaprofoundandpotentially devastatingeffectonmanymarineenvironments,including coralreefecosystems.Caribbeanreefcorals,includingthe once-commonscleractiniancoral Acroporacervicornis,havesufferedunprecedentedmortalityduetoclimatechange–related stressors,suchasincreasingseasurfacetemperature(SST) andsolarradiation(SR)(19,20).RisingSSTandincreasedSR arephysiologicalstressorstomarineorganisms,whichwhen severemightjeopardizevitalfunctionssuchasgrowth,reproduction,andthecapacityto fightdiseases.Since2006, A.cervicornis hasbeenlistedasathreatenedspeciesthroughoutallofitsrange (theCaribbeanSeaandtheAtlanticOceannearBahamasand Florida)undertheInternationalUnionforConservationsof Nature(IUCN)RedListandtheU.S.EndangeredSpeciesAct (ESA);thus,itsrecoveryhasbecomeamajorpriorityfortropical Atlanticnationsandconservationgroups(21,22).Coralsrelyon multipleresponsestothermalandirradiationstress,includingthe increasedsynthesisofphotoprotectivepigmentssuchas fluorescentproteins(FPs)andmelanin(23–26).Therefore,measuring theabundanceofFPsandtheactivityofenzymesinvolvedinthe synthesisofmelaninfromthetissueofcoralsgrowingunderdifferentenvironmentalconditionsservesasanindirectmeasurementofthestressenduredbyindividualcolonies.Furthermore, correlatingproxymeasuresofstresstolong-termenvironmental monitoringdataofSSTandSRwillprovideinsightsintounderstandinghow A.cervicornis coloniesarerespondingtoachanging environmenttoultimatelyhelpguidefuturecoralpropagation andrestockingefforts.

Inanefforttointroducemoreundergraduatestudents ataHispanic-servinginstitution(HSI)tothebenefitsof researchexperiences,wehavedrawnuponanongoing long-termresearchprojectaimedatunderstandinghowthe Caribbeanstaghorncoral A.cervicornis respondstoseasonal fluctuationsofSSTandSRtodevelopaCURE.ThesemesterlongcourseisentitledCREARE,anacronymforcoralresponse

toenvironmentauthenticresearchexperience,andalsobecause oftheLatinverbcreare,meaning “Icreate,make,produce,” whichreflectstheintentionofhavingstudentscreatenewknowledgetoaddressascientificallyrelevantquestionthroughparticipationinthecourse.Here,wedescribetheconsensusdesignof CREAREafterthreeiterationsandshareassessmentdatafor oneofthethreecohortsofstudentswhohaveparticipated.

INTENDEDAUDIENCEANDPREREQUISITESTUDENT KNOWLEDGE

CREAREisofferedasanelectivecourseforstudentsinthe CollegeofNaturalScienceswhohavecompletedatwo-course introductorysequenceinBiology,atwo-courseintroductory sequenceinChemistry,andanintroductorycourseinStatistics. Studentsareexpectedtohaveuniversity-levelknowledgeofbiodiversityanditsimportance,naturalselection,theimpactofbiotic andabioticfactorsonpopulations,structureandfunctionofmacromolecules,andenzymesandtheiractivity.Boththeintroductorybiologyandchemistrycoursesatourinstitutionhavealaboratorycomponent;therefore,studentsarealsoexpectedtohave experiencewiththeapplicationofthescientificmethod,handling biologicalspecimensandchemicalcompoundsandtheproper executionofprotocols.Inaddition,participantsareexpectedto knowhowtomakemeasurementsandobservationsaccurately, analyzeandsummarizequantitativedatausinggraphs,differentiatebetweendependentandindependentvariablesandusedescriptivestatisticssuchasmeasuresofcentraltendency.Mostof thestudentswhoparticipateinthecoursearesophomoresand juniorswithvaryinglevelsofexposuretoscientificresearchoutsideoflaboratorycourses,fromnopriorresearchexperienceto onefullyearofresearchexperience.

LEARNINGTIME

Allstudentsandfacultymeetformallyonceaweekfor3h duringa16-weeksemester(Table1).Afterthe firstintroductory meetingwherelaboratorysafetyguidelinesarediscussed (Appendix1),studentsareexpectedtoengageincourse-related activitiesforanadditional3hperweek.Theseactivitiesinclude additionaltimeinthelaboratorytoperformexperimentsandanalyzedata,reviewliterature,and/orworkonwritingassignments. Additionalmeetingtimesarecoordinatedwiththeinstructional staffbasedonavailability.

LEARNINGOBJECTIVES

Thelearningobjectivesandsupportingactivitiesare presentedinFig.1.UponcompletionofCREARE,students areexpectedto:

1.Describetherelationshipbetween fluctuationsin environmentalconditionsandchangesinthephysiologyof thestonycoral A.cervicornis

Timelineofactivitiesduringa16-weeksemester

1 Introduction

Assessment:Pre-coursesurveys+examinationofcontent

2 Biochemistrymodule

3

4

Writingassignment:Assignshortliteraturereview(Introduction)

DataanalysismoduleI

Writingdeliverable: Introduction

DataanalysismoduleII

Writingassignment:Discuss Introduction withinstructor

5 Fieldtrip(weatherpermitting)

Writingdeliverable:Revised Introduction + MaterialsandMethods 6 Sciencewritingmodule

Writingassignment:Discuss MaterialsandMethods

7 Labwork

Writingassignment:DiscussRevised Introduction and MaterialsandMethods

8 Labwork

Writingdeliverable: Figures forenvironmentaldataanalysis

9 Ecologymodule

WritingAssignment:Discuss Figures forenvironmentaldataanalysis 10 Labwork

Writingdeliverable: Results sectionofavailabledatawith Figures 11 Labwork

Writingassignment:Discuss Results 12 Labwork

Writingassignment:Revised Introduction,MaterialsandMethods and Results 13

Writingdeliverable: Discussion Presentation:PresentsketchofFinalPresentation 14

Writingassignment:Discuss discussion

Presentation:DiscussFinalPresentation 15

Finalpresentation

Writingassignment:Discuss FinalReport 16

Writingdeliverable: FinalReport Assessment:Post-CourseSurveys+ExaminationofContent

2.Developskillsandcompetenciestorecorddataand analyzeresults.

3.Demonstrate fluencyindataprocessingandanalysis oflargedatasetsanditsapplicationtouncoverrelationshipsinbiologicalsystems.

4.Effectivelycommunicatetheresultsofresearchto peersandmembersofthescientificcommunity,through writtenreportsandoralpresentations.

5.Reportincreasesinself-efficacy,enhancementsinscientificidentity,andclarificationofcareerintentions.

PROCEDURE

Theworkflowofexperimentsfromsamplecollection todataanalysisisprovidedinFig.2.Priortothebeginning

ofthecourse,membersofourresearchteamcollected coralsamplesfromcoralnurserieslocated3and12mof depthduringthespringandfall(Appendix2).Thestudysite isinPuntaSoldado,Culebra,PuertoRico(N18°16 0 50.7 W65°17 0 14.6)andismanagedbythelocalnonprofitorganizationSociedadAmbienteMarino.Collectedcoralfragmentsareplacedintubesandfrozeninliquidnitrogenimmediatelyuponretrieval,transportedtothelaboratory,and storedina 80°Cfreezeruntilfurtheranalyses.The DepartmentofNaturalandEnvironmentalResourcesof PuertoRicoapprovedthesamplingprotocolunderpermit numberDRNA:2016-IC-175issuedtoCTH.Smallgroups ofstudents(twotothreestudentspergroup)areassigned asetofcoralfragmentscollectedataspecificdatecoming fromoneoftwodepths(3and12m)foranalysis.Students areinstructedtoextracttissuefromfrozencoralfragments

FIGURE1.Learningobjectivesandsupportingactivities.The fivemainlearningobjectives(fourcirclesinthemiddleandtrapezoidon top)areachievedthroughengagedparticipationinlaboratory, fieldand insilico workandaresupportedbyTopicalModules(Ecology, Biochemistry,DataAnalysis,andScientificWriting),WritingAssignments,andaFinalPresentation.Arrowsfromsupportingactivities (bottomrow)toobjectives(middlerow)reflecthowtheseactivitiessupportthelearningobjectivesandultimatelystudent development(toprow).

(Appendix3)andusetheextractstoperformbiochemical assaystomeasuretheamountofphotoprotective fluorescentproteins(FPs)intheextractedtissue(Appendix4)and alsomeasuretheactivityoftheenzymephenoloxidase(PO), whichisinvolvedinthesynthesisofmelanin(Appendix5).In parallel,studentsperformstatisticalanalysisonenvironmentaldata(Appendix6)thatisprovidedbytheinstructors. ThesedataareforSSTandSRinthecollectionsitesinthe monthspriortosamplecollection.Finally,studentscompare thebiochemicalparametersbetweentheirsamplesatdifferentdepthsandseasonsandthecorrespondingenvironmental

FIGURE2.Experimentalwork fl ow,fromsamplecollectionto dataanalysis.

conditions.Togain fluencyandpracticeinthetechniques requiredtoperformalltheanalysesdescribedabove,studentsparticipateinaseriesofmodules.

Biochemistrymodule

Throughthebiochemistrymodule(Appendix7),studentswereintroducedtobasiccoralphysiologyandthe responsesoftheseorganismstotemperaturestressandsolarradiation.Themainfocuswasontheroleoftheenzyme POintheproductionofmelanin(25,26)andthephotoprotectivequalitiesof fluorescentpigmentsincorals(23,24). Herein,laboratoryruleswerediscussedandinstruction givenontheuseofbasiclaboratoryequipmentandhandling ofreagents.

Dataanalysismodule

Thtwo-partdataanalysismodule(Appendix8)providedguidedpracticeontheapplicationofstatisticstolarge datasetsofenvironmentaldatausing R:ALanguageand EnvironmentforStatisticalComputing (27).Inadditionto becomingfamiliarwiththeuseofRprogramminglanguage, themoduleincludedgeneraldiscussionontopicsofstatisticalanalysistechniquesusedinpopulationecologyandthe integrationofmathematicalandstatisticalanalysistobiologicalresearch.WithinR,studentslearnedaboutenvironmentsetup,basiccommands,scriptsyntax,uploadingand

reading fileswithdifferentextensions,performingdescriptive statisticalanalyseswithsmalldatasets,anddatavisualizations. Thismodulewasinitiallyofferedasasingle3-hsession.Based onstudentfeedbackfromthe firstiterationofthecourseand perceiveddifficultieswithR,wefounditnecessarytoextend themoduletotwo3-hsessionofferedinsuccessiveweeks.

Sciencewritingmodule

Thesciencewritingmodule’smainobjective(Appendix9) wastodevelopthetoolstocommunicatetheresultsobtained tostakeholdersoutsideoftheclassroom.Thesestakeholders arelocalcoralreefresearchers,membersofcommunity-based conservationgroups,andgovernmentagencies.Topicsdiscussedincludesentenceconstruction,organizationofideas withinaparagraph,scientificwordingandthefundamental partsofaresearchmanuscript.Themodulewascentered aroundanin-classactivitywherestudentswriteaparagraph usinggivenkeywordsfollowedbypeer-to-peercritiqueofanonymizedparagraphsproducedintheinitialexercise.

Ecologymodule

Theecologymodule(Appendix10)aimedtointroduce studentstothebasicecologyofcoralreefs,reef-building corals,associatedorganisms,andtheirimportanceto humankind.Themainfocuswasonthemajorstressors, bothhuman-derivedandnatural,thatarecurrentlythreateningtheexistenceofcoralreef.Themoduleisintendedto givestudentsabroadercontextoftheworkthattheyperformedthroughoutthesemester.Thisinformationiskey forsubsequentcommunicationofresearch findings.

STUDENTINSTRUCTIONS

Studentsareprovidedaccesstoafolderonacloudbasedsharingservicewiththerequiredreadingmaterial andalsoinstructedtodownloadandinstallR(Appendix8). Throughthesharedfolder,studentsreceiveexperimental protocolsandsubmitallcoursedeliverables.Studentswork togetherinsmallgroups(twotothreestudentspergroup). Collaborationandco-workingamongthegroups,especially fordataanalysis,arestronglyencouraged.

FACULTYINSTRUCTIONS

Duringthe firstmeetingwithstudents,projectobjectives werediscussed,bothintermsofeducationaloutcomesand researchobjectives.Duringthis firstmeeting,pre-coursesurveysandevaluations,laterusedtomeasurelearninggainsand shiftsinattitudestowardscience,areadministered.Duringthe secondweek,studentsbeginworkrelatedtotheproject throughparticipationinthe firstoffourtopicalmodules. Table1presentshowtopicalmodulesandothersupporting

activitiesaredistributedthroughoutthesemester.Thetopical modulesaredesignedtoexposestudentstotheunderlying theoreticalprinciplesoftheexperimentaldesignandtoreinforcefoundationalconceptsthatareimportantforsuccessful executionofexperimentsandinterpretationofdata(Fig.1 andAppendices7to10).Activelearningmethodologies,such aspeer-to-peerlearningandguidedinquiry,areusedinthe topicalmodulestoexplore,explain,andevaluatetopicsrangingfromoverarchingprinciplestospecificdetailsrelevantto theproject(28).Instructorsdevoteatleastanadditional6h perweekforcollectingsamples,preparinglaboratoryreagents, supervisingstudentexperiments,answeringstudentquestions, readingandprovidingfeedbacktostudentsonwritingassignments,andpreparingandanalyzingdatafromstudentassessment.Establishingadefinedtimeperiodduringtheweekto handletheseadditionaltaskswascriticaltominimizetheburden oninstructor’stime.

SUGGESTIONSFORDETERMININGSTUDENTLEARNING

Studentachievementoftheestablishedlearningobjectivesareevaluatedmostlythroughasemester-longprocess ofwritingandrevision,inwhichstudentsprogressivelyconstructareportmodeledafteraresearcharticle(Table2). Thisgradualcraftingofareportmirrorsthedeveloping engagementofthestudentsintheresearchproject:asstudentsbecomefamiliarwiththeresearchliterature,they writeanIntroduction;uponperformingexperiments,they writeMaterialsandMethods;astheygatherandinterpret data,theywriteaResultssection;andastheyinterpretand contextualizetheresults,theywritetheDiscussion.Upon completionofeachstageoftheprojectandwritingthecorrespondingsectionofthereport,studentsreceiveinputand recommendationsfrominstructorsoneachsection (WritingDeliverablesinTables1and2).Agradingrubric usedinotherlaboratorycoursesinourschoolisusedasa formativeassessmentandevaluationtool(seeAppendix11 andAppendix12forexamplesofstudentdata).

Inadditiontobeingusedasameansforstudentevaluation(Table3),writingassignmentsanddeliverablesfulfillthe criticalobjectiveofimprovingstudents’ abilitytoeffectively communicatetheresultsofresearchtopeers,thescientific community,andthepublic.Asecondwayofassessingstudent learningisthrough finaloralpresentationsthatarepresented toinstructors,peersandotherresearchersoncampus. Duringoneofthesemestersthatthecoursewasoffered,a localcoralreefsymposiumwasheldnearourcampus.Allstudentsenrolledinthecourseattendedthesymposiumandalso submittedanabstract,whichwasrequiredforevaluationasa writingdeliverableduringthatsemester.Agroupofthreestudentsgaveanoralpresentationtodescribetheprojecttoall symposiumparticipants(Appendix13).Toensurethatstudentsweresupportedinthedevelopmentoftheirscientific presentationskillsandwerepreparedforthepresentation,we providedopportunitiestopracticeinclassandoffered

TABLE2

Alignmentbetweenlearningobjectivesandcourseassessment

Describetherelationshipbetween fluctuationsinenvironmental conditionsandchangesinthephysiologyofthestonycoral A. cervicornis

Developskillsandcompetenciestorecorddataandanalyzeresults.

Demonstrate fluencyindataprocessingandanalysisoflargedatasets, anditsapplicationtouncoverrelationshipsinbiologicalsystems.

Effectivelycommunicatetheresultsofresearchtopeersandmembers ofthescientificcommunity,throughwrittenreportsandoral presentations.

Reflectincreasedself-efficacyinresearch,clarifycareergoalsand developtheirscientificidentity.

extendedcommentsonpresentations(Appendix14).Other coralreefresearchersandmembersofconservationgroups wereinattendanceforthispresentation.Althoughthiswasa uniquescenario,itclearlyevidencedthatstudentsfulfilledthe learningobjectiveofeffectivelycommunicatingtheresultsof researchtopeersandmembersofthescientificcommunity.

SAMPLEDATA

CREAREparticipantsengageindifferentaspectsofthe experimentalworkflowincludingtissueextraction,estimation ofproteinconcentrationsandenzymeassays.Participants alsoanalyzeenvironmentaldata,aswellasusestatisticalanalysistointerprettheresultsfrombiochemicalexperiments (Fig.2).Fig.3andAppendices12and13showsampledata generatedbystudentsandusedinwrittendeliverablesand presentations.

SAFETYCONCERNS

Studentsreceivedinstructiononlabsafetyonthe firstday ofthecourse(Appendix1)andwererequiredtocompletetwo

TABLE3

Gradingandevaluation

Writingdeliverable:Introduction

ContentExam

FinalReport

FinalPresentation

Writingdeliverable:Figuresforenvironmentaldataanalysis

Writingdeliverable: Figures forenvironmentaldataanalysis

Writingdeliverables

FinalReport

FinalPresentation

CUREsurvey

Focusgroupinterviews

onlinecoursespriortobeginningworkinthelaboratory,asixpart “OnlineEthicsResearchCourse” fromtheOfficeof ResearchIntegrityandalaboratorysafetycoursefromthecampusOfficeforEnvironmentalProtectionandOccupational Safety.Furthermore,studentsareinstructedabouttheproper useoflaboratoryequipmentandhandlingofchemicalreagents usedforexperiments.Noneofthereagentsusedforthe experimentsposeanyserioushealthandsafetyconcerns.

DISCUSSION

Fieldtesting

CREAREwasofferedasanelectivecourseforthree consecutivesemesters,fall2016,spring2017,andfall2017. ThreecohortsofsixtoninestudentsparticipatedinCREARE andsuccessfullyperformedbiochemicalexperimentsinthelaboratory,analyzedenvironmentaldatausingtheRsoftwareenvironment,anddisseminatedtheresultsofthisresearchproject thataddressestheeffectofclimatechangeonacriticallyendangeredreef-buildingcoral.Oncethecoursecontentandpracticeswereoptimizedwithinits firstiteration(cohort1),we gatheredassessmentandperceptiondatafromcohorts2and3. Weareonlypresentingresultsforcohort2sincethethirdsemesterthatthecoursewasofferedwasdisruptedbytwosuccessivecategory4hurricanes(HurricanesIrmaandMaría), whichresultedinmajordisruptionstoacademicactivitiesand researchefforts.

Evidenceofstudentlearning

Thegathereddataand fi guresgeneratedbystudents inCREAREserveasevidenceofstudentlearning(Table2).

FIGURE3.Sampleofstudent-generateddata.(Top)Fluorescenceemissionspectrafortissueextractsfromhealthylooking A.cervicornis samplescollectedfromPuntaSoldado,Culebra,PuertoRico(18°19 0 01N65°17 0 24W).Fluorescencebetweenandwithinsampleswas normalizedtototalproteinconcentration.SampleswerecollectedonNovember16,2016from3and12m.(Bottom)SST(°C)at3m and12matsamplingsite.DataweretakenusingaHoboPendanttemperature/lightdatalogger64k-UA-002-64(OnsetCompany)to threedecimalplaces.Datawerecollectedevery15minfortheperiodbetweenNovember19,2016,andApril11,2017.

Theseproductsdemonstrate fl uencyinrecording,analyzingandprocessingdatafromlargedatasetsofbiochemical andenvironmentaldata(Fig.3,Appendices12and13). Furthermore,thesestudent-generateddatahave

contributedtolargerdatasetsthatwillbeincludedina researchmanuscriptcurrentlyinpreparation.

TheimpactofCREAREonstudentlearninggainsand attitudestowardsciencewasmeasuredusingtheClassroom

FIGURE4.Studentperformanceoncontentexam(N =9).Studentperformanceon14-itemcontentexamadministeredpriorto participationinCREARE(PRE)andimmediatelyaftercompletingthecourse(POST).Shadedcirclesrepresenttheindividualscoresof eachstudent. P valueforapairedtwosample t testrevealedthestatisticalsignificanceofthedifferencebetweenaggregatedPREand POSTexamscores.

UndergraduateResearchExperienceSurvey(6).Students reportedthatparticipationinCREAREledtosignificantgains inreadinessfordemandingresearch,understandingthatscientificassertionsrequiresupportingevidenceandunderstandinghowknowledgeisconstructed.Furthermore,studentsreportedimprovedattitudestowardscienceand signifi cantperceivedincreasesintheirabilitiestocontributetoaresearchprojectandtocollect,analyze,andpresentdata(datanotshown).Studentself-reportingoften holdslittlecorrelationtomeasurablelearninggainsorthe mechanismsdescribingwhatmakesCUREseffectiveat in fl uencinglearninggainsorcareerchoicebehaviors(2,9, 29).Toverifythatclaimsoflearningcorrelatetoacquisitionofcontentknowledge,studentswhoparticipatedin CREAREduringspring2017(N =9)weregivena14-item examtoassesstheirknowledgeabouttheunderlyingconceptsrelatedtotheresearchprojectbeforeandafterparticipation(Appendix15).Collectively,scoreswerehigher afterCREARE[mean,7.78;standarddeviation(SD),1.86] comparedtoscoresatthebeginningoftheexperience (mean,6.89;SD,2.02)(Fig.4).Thisimprovementin

studentperformancewithregardtocontentisstatistically signifi cant(t 8 =2.28, P= 0.02)andvalidatesstudentclaims oflearninggainsafterparticipationinCREARE.

Severallinesofevidencesuggestthatthebenefi tsof CUREs,beyondcontentacquisitionandtechnicalmastery, aretheincreaseofself-ef fi cacy,clarifi cationofcareer goals,anddevelopmentofascientifi cidentity(14–16,30). Topeerdeeperintothemechanismsthatmediatethe changesinstudentperceptionregardingtheirabilitiesto performscienti fi cresearchandimprovetheirviewasscientists,afocusgroupinterviewwascarriedoutwiththe samespring2017studentcohorttosurveywhichelementsoftheCUREexperienceareconsideredbyparticipantstobethemostimportantfortheirdevelopment. Audiofrominterviewswasrecordedandtranscribedto identifyphraseswithinthetextthatrepresentedstatementsorre fl ectionsbystudentsregardinghowtheexperienceimpactedtheirpersonalandprofessionaldevelopment(Appendix16).Phraseswithinthetextthatmade mentionofwhatstudentsperceivedasopportunitiesfor developmentwereclassifi edandgroupedintofour

TABLE4

Focusgroupinterviewemergentcategoriesandquotes

EmergentcategoryRepresentativequote

Definitionofcareertrajectory

Self-efficacy

Opportunitiesfordevelopmentof researchskills

Opportunitiesfordevelopmentof interpersonalrelationships

“ youdonotknow,reallywhatcareeryouwanttogotountilyoustartpracticingit”

“IthoughtthatIcouldnotdowhatIamdoing,sothenextthingIwanttodo,probably IcanalsodoitifIputeffortaswell,asithappenednow.”

“Atthebeginningoftheinvestigation,youknowverylittleaboutwhatyouare investigating,andthen,intheend,yougo,youknowsomuch,andthenyoucontinue branchingout,andyouwanttoknowmoreaboutsomethingthathastodowithit.”

“Itchangesyourperspectiveabittoo,becausesometimesyouthinkthatprofessors arelike,like,someonelikebeyondhuman,theydonoteatoranything wespenda lotoftime,uh,withthemandyourealizethat,well,theyalsohavetheirdoubtsand thattheyalsolearnfromussomethingsaswell,buttheyalsolearnthingswithusand that,andthatthey,inreality,theyarebasicallythereforus.”

emergentcategoriesthatmostlyrelatedtothevaluation oftheexperienceasanopportunitytodevelopprofessionallyandtodefi neacareertrajectory(Table4).Asone studentputitsuccinctly: “Youdonotknow,reallywhatcareeryouwanttogotountilyoustartpracticingit.” Within thefourcategories,codesthatre fl ectedimprovementsin self-ef fi cacyandskilldevelopmentwereabundant,aswere thosethathighlightthevaluethatstudentsplaceonthe developmentofinterpersonalrelationshipsasafactorof highimpact.Withinthelattercategory,thereweremultiplementionsofmentoring,teamwork,andashiftintheir perceptionofpositionswithinascienti fi chierarchy (Table4andAppendix16).

Thecategoriesthatemergedfromouranalysisoffocus groupinterviewsmirrorthosedescribedintheTIMSImodelof socialintegration(15).Hence,wesearchedforphrasesassociatedwiththethreemodesoforientationdescribedinthe TIMSIframeworkandfoundahighfrequencyofcodesrelated toruleorientation(self-efficacy),roleorientation(scientific identity),andvalueorientation(internalizationofscientificcommunityvalues).Phrasesassociatedwiththedevelopmentofselfefficacyappearwiththehighestfrequencyamongallvariables associatedtoscientificintegration(Fig.5),reinforcingtheimportanceofthedevelopmentofself-efficacyasarobustmediator ofscientificintegration(14–16).Theseresults,takentogether withthevalidatedgainsinknowledge,demonstrated fluencyin dataanalysis,andimprovedcompetenceincommunicating results,inadditiontothehighvaluationoftheexperienceby participants,suggestthatCREAREiseffectiveinstrengthening perceptionsofsuccessandbelonging,whicharepredictiveof scientificintegrationbystudentsfromhistoricallyunderrepresentedgroupsinscience.

Possiblemodifications

Thesemester-longCUREdesignpresentedhere,with topicalmodulesasamainmodeofinstructionandwriting deliverablesforassessmentandevaluation,canbeadaptedasa

frameworkforintegratingresearchprojectsintocourses. OnlyoneoffourlearningobjectivesinCREAREisspecificto theresearchproject,anditcanalternativelybereplacedwith thespecificaimofotherresearchprojectsthatsurveythe impactoftheenvironmentonanorganism,frombehaviorto molecularbiology.Likewise,modulessuchastheData AnalysisModulecanbeusedasanindividualexercisetodevelopstudents’ fluencyinanalyzingenvironmentaldatawithin acourseoraCURE.Thiscanincludeinstanceswhereopen sourcedatasetsaccessibleviatheInternetareusedfordata analysisaswellascarryingouttheexercisesusingotherstatisticalprograms(seenotesaboutinstructioninAppendix8). Similarly,theScienceWritingmodule(Appendix9)canbe usedinanyothercoursewherescientificresultsmustbecommunicatedthroughwriting.

Itmeritsmentioningthatthemainstruggleforstudents inCREAREwasusingR,especiallywhenapplyingittoreal worldcircumstancesandlargedatasets.Spendingmore time(twomodulesratherthanone)tointroducestudents toRandstartingwithasmalldatasetforthemtowork withbeforehandlingtherealdatawereveryhelpful. Furthermore,keepingstudentsengagedaftersetbacksin experimentsand/ordataanalysisisalwaysachallenge.On occasion,wehadstudentsswitchtaskstoavoidexcessive frustration,specificallywithdataanalysisinR.

CONCLUSION

TheworkdonebystudentsinCREAREhasbeen instrumentaltotheprogressofourresearchproject,leadingtotherefinementofresearchprotocolsforfuture experimentsandthegenerationofscientificallyrelevant data.Theseoutcomes,togetherwithourassessment resultsindicatethatthroughourapplicationoftheCURE modalitystudentsshowappreciablegainsinknowledge, fluencyindatamanagement,andgainopportunitiestocommunicatetheresultsoftheirresearch.Takentogether,our

FIGURE5.FrequencyofcategoriesassociatedwithTIMSIframework.Focusgroupinterviewswerescoredforthefrequencyof mentionofcategoriesrelatedtothethreeorientingfactorsfortheintegrationofunderrepresentedminoritystudentsintoscienceof theTIMSI.Identityisred,self-efficacyisgreen,andvalueisblue.

workindevelopingandimplementingCREAREoffersfurthersupportoftheeffectivenessofCUREsinintegrating cutting-edgeresearchintocoursestherebybroadeningthe positivebenefitsofresearchexperiencestoamorediverse populationofstudents.

SUPPLEMENTALMATERIAL

Appendix1:Laboratorysafetyguidelines

Appendix2:Coralsamplingprotocol

Appendix3:Coraltissueextractionprotocol

Appendix4:BiochemicalexaminationofFPprotocol

Appendix5:BiochemicalexaminationofPOenzymatic activityprotocol

Appendix6:Environmentalmeasurementprotocol

Appendix7:Biochemistrymodule

Appendix8:Dataanalysismodule

Appendix9:Scientificwritingmodule

Appendix10:Ecologymodule

Appendix11:Rubrictoevaluatewrittenreports

Appendix12:Examplesofstudent-generateddataandreports

Appendix13:Studentpresentationatlocalcoralreef symposium

Appendix14:Exampleoffeedbackonstudentpresentation

Appendix15:14-itemcontentexam

Appendix16:Transcriptoffocusgroupinterview

ACKNOWLEDGMENTS

WethankallthestudentsthatparticipatedinCREARE fortheirpatienceandwillingnesstoconfrontthemany challengesthatwerefaced.Wearethankfulforthesupport providedbyDavidLopattoandLeslieJaworskifortheuseof theCUREsurvey.WeareforeverindebtedtoAbigailZoger andMollySchreyforsendingsolarequipmentthatkeptus workingafterHurricaneMaría.Financialsupportwasprovided bytheUniversityofPuertoRico,RioPiedrasCampusOfficeof Research,andGraduateStudiesInstitutionalResearchFund (FIPI)andNationalOceanicandAtmosphericAdministration’ s

(NOAA),NationalSeaGrantProgramGrantnumber NA14OAR4170068andProjectnumberR/105-02-16.The UniversityofPuertoRico,RioPiedrasInstitutionalCommittee fortheProtectionofHumanSubjectsinResearch(CIPSHI,IRB 00000944)approvedourprotocolwithnumber1617-089for workonthisproject.Theauthorshavenoconflictsofinterest todeclare.

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