Biological and Medical Physics, Biomedical Engineering Saverio E. Spagnolie Editor Complex Fluids in Biological Systems Experiment, Theory, and Computation Complex Fluids in Biological Systems BIOLOGICAL AND MEDICAL PHYSICS, BIOMEDICAL ENGINEERING The fields of biological and medical physics and biomedical engineering are broad, multidisciplinary and dynamic. Theylie atthe crossroadsof frontierresearchinphysics, biology, chemistry, andmedicine. The BiologicalandMedicalPhysics,BiomedicalEngineeringSeriesisintendedtobecomprehensive,coveringa broadrangeoftopicsimportanttothestudyofthephysical,chemicalandbiologicalsciences.Itsgoalisto providescientistsandengineerswithtextbooks,monographs,andreferenceworkstoaddressthegrowingneed forinformation. Booksintheseriesemphasizeestablishedandemergentareasofscienceincludingmolecular,membrane, and mathematical biophysics; photosynthetic energy harvesting and conversion; information processing; physicalprinciplesof genetics;sensorycommunications; automata networks, neuralnetworks, andcellular automata. Equally important will be coverage of applied aspects of biological and medical physics and biomedicalengineeringsuchasmolecularelectroniccomponentsanddevices,biosensors,medicine,imaging, physical principles of renewable energy production, advanced prostheses, and environmental control and engineering. Editor-in-Chief: EliasGreenbaum,OakRidgeNationalLaboratory,OakRidge,Tennessee,USA EditorialBoard: MasuoAizawa,DepartmentofBioengineering, JudithHerzfeld,DepartmentofChemistry, TokyoInstituteofTechnology,Yokohama,Japan BrandeisUniversity,Waltham,Massachusetts,USA OlafS.Andersen,DepartmentofPhysiology, MarkS.Humayun,DohenyEyeInstitute, Biophysics&MolecularMedicine, LosAngeles,California,USA CornellUniversity,NewYork,USA PierreJoliot,InstitutedeBiologie RobertH.Austin,DepartmentofPhysics, Physico-Chimique,FondationEdmond PrincetonUniversity,Princeton,NewJersey,USA deRothschild,Paris,France JamesBarber,DepartmentofBiochemistry, LajosKeszthelyi,InstituteofBiophysics,Hungarian ImperialCollegeofScience,Technology AcademyofSciences,Szeged,Hungary andMedicine,London,England RobertS.Knox,DepartmentofPhysics HowardC.Berg,DepartmentofMolecular andAstronomy,UniversityofRochester,Rochester, andCellularBiology,HarvardUniversity, NewYork,USA Cambridge,Massachusetts,USA AaronLewis,DepartmentofAppliedPhysics, VictorBloomfield,DepartmentofBiochemistry, HebrewUniversity,Jerusalem,Israel UniversityofMinnesota,St.Paul,Minnesota,USA StuartM.Lindsay,DepartmentofPhysics RobertCallender,DepartmentofBiochemistry, andAstronomy,ArizonaStateUniversity, AlbertEinsteinCollegeofMedicine, Tempe,Arizona,USA Bronx,NewYork,USA DavidMauzerall,RockefellerUniversity, BrittonChance,UniversityofPennsylvania NewYork,NewYork,USA DepartmentofBiochemistry/Biophysics EugenieV.Mielczarek,DepartmentofPhysics Philadelphia,USA andAstronomy,GeorgeMasonUniversity,Fairfax, StevenChu,LawrenceBerkeleyNational Virginia,USA Laboratory,Berkeley,California,USA MarkolfNiemz,MedicalFacultyMannheim, LouisJ.DeFelice,DepartmentofPharmacology, UniversityofHeidelberg,Mannheim,Germany VanderbiltUniversity,Nashville,Tennessee,USA V.AdrianParsegian,PhysicalScienceLaboratory, JohannDeisenhofer,HowardHughesMedical NationalInstitutesofHealth,Bethesda, Institute,TheUniversityofTexas,Dallas, Maryland,USA Texas,USA LindaS.Powers,UniversityofArizona, GeorgeFeher,DepartmentofPhysics, Tucson,Arizona,USA UniversityofCalifornia,SanDiego,LaJolla, EarlW.Prohofsky,DepartmentofPhysics, California,USA PurdueUniversity,WestLafayette,Indiana,USA HansFrauenfelder, AndrewRubin,DepartmentofBiophysics,Moscow LosAlamosNationalLaboratory, StateUniversity,Moscow,Russia LosAlamos,NewMexico,USA MichaelSeibert,NationalRenewableEnergy IvarGiaever,RensselaerPolytechnicInstitute, Laboratory,Golden,Colorado,USA Troy,NewYork,USA DavidThomas,DepartmentofBiochemistry, SolM.Gruner,CornellUniversity, UniversityofMinnesotaMedicalSchool, Ithaca,NewYork,USA Minneapolis,Minnesota,USA Moreinformationaboutthisseriesathttp://www.springer.com/series/3740 Saverio E. Spagnolie Editor Complex Fluids in Biological Systems Experiment, Theory, and Computation 123 Editor SaverioE.Spagnolie DepartmentofMathematics UniversityofWisconsin-Madison Madison,WI,USA ISSN1618-7210 ISSN2197-5647(electronic) ISBN978-1-4939-2064-8 ISBN978-1-4939-2065-5(eBook) DOI10.1007/978-1-4939-2065-5 SpringerNewYorkHeidelbergDordrechtLondon LibraryofCongressControlNumber:2014953309 ©SpringerScience+BusinessMediaNewYork2015 Thisworkissubjecttocopyright.AllrightsarereservedbythePublisher,whetherthewholeorpartof thematerialisconcerned,specificallytherightsoftranslation,reprinting,reuseofillustrations,recitation, broadcasting,reproductiononmicrofilmsorinanyotherphysicalway,andtransmissionorinformation storageandretrieval,electronicadaptation,computersoftware,orbysimilarordissimilarmethodology nowknownorhereafterdeveloped.Exemptedfromthislegalreservationarebriefexcerptsinconnection with reviews or scholarly analysis or material supplied specifically for the purpose of being entered and executed on a computer system, for exclusive use by the purchaser of the work. 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Printedonacid-freepaper SpringerispartofSpringerScience+BusinessMedia(www.springer.com) To life,inallitswondrous andstupefyingcomplexity Preface The complexity of biological systems, even on the smallest length scales, is staggering.Biologicalsystems are replete with active functionality,heterogeneity, memory, and interconnectedness on a vast spectrum of length and time scales. With our ever-advancing abilities to observe nature in vivo at the microscale, and with continuing developments of mathematical and numerical machinery for understanding multiscale physical systems, the fields of complex fluids and biological systems are ripe for fruitful cross-pollination.There have already been manysuccessfulscientificadvancesalongtheselines, aswillbemadeclearinthe chaptersthatfollow.Theaimofthisbookistointroducethereadertomanyofthe exciting directions that this research is taking and to provide a valuable reference onfundamentalphenomena,models,andanalysisofcomplexfluidsinavarietyof biologicalsystems. The bookis organizedinto four parts. In PartI, Newtonian andcomplexfluids areintroduced,alongwith theterminologyandmodelsthatwillappearfrequently throughout the book. The first chapter provides the mathematical framework of continuummechanicsandpresentscommonconstitutivelawsusedtodescribefluids with such properties as shear-dependent viscosity and viscoelasticity. Classical rheologicalflowsfrequentlyusedinexperimentsareintroduced.Thesecondchapter lays the foundationsfor the topics to be coveredin the book and explorescritical functionalrolesplayedbycomplexfluidsinafamiliarbiologicalsystem,thehuman body. Using mucus as an illustrative example, a multidisciplinary approach to studyingandmodelingsoft,complexbiologicalmatterisemphasized. InPartII,themeasurementofbiologicalmaterialproperties,orrheology,takes center stage. The first chapter is devoted to microrheology, wherein the behavior ofsmallimmersedparticlesisused toinfermaterialpropertiesofthesurrounding environment.Bothpassivemicrorheologyandactivemicrorheologyarediscussed, beginningwiththefamedStokes-Einsteinrelationandmarchingthroughahistory of the field towards a “nonequilibrium equation of state.” The following two chaptersreturntospecificbiologicalstructures,namelythecellmembraneandcell cytoskeleton. Microrheology is revisited as a means of studying the viscoelastic propertiesofmolecularlythinshells,andtheintricatebiopolymernetworkinternal vii viii Preface toindividualcellsisintroduced.Afinalchapterinthissectionexploresavarietyof challengesfacedbyexperimentalistsinthe studyofcomplexbiologicalfluidsand shows how a misinterpretationof data can suggest complexfluid propertieswhen therearenoneandviceversa. PartIIIfocusesonthelocomotionofmicroorganismsthroughcomplexbiological fluids,asdescribedfromexperimental,analytical,andnumericalperspectives.The firstchapterreviewstherecentexperimentalstudiesofbiolocomotioninviscousand viscoelasticfluidsandthenturnstointriguingexperimentalresultsonthepropulsion ofamodelorganism,theroundwormC.elegans.Thissetsthestageforthefollowing chapter, which covers a detailed mathematical theory of locomotion in complex fluids, and connections between microrheology and biolocomotion are described. Theinteractionofswimmingorganismsincomplexfluidsisalsodiscussed,which leadsnaturallyintothefinalchapterofthepart.Inthelastchapter,thefocusturnsto amodeloflargecollectionsofsuchswimmingorganisms,oranactivesuspension, which can exhibit large-scale correlated motions, pattern formation, and complex fluid propertiesincluding normal stress differences. The model is extended to the studyofothersystems,includingtheinteractionofmicrotubulesandtranslocating motorproteinsasfoundinindividualcells. Finally, Part IV covers methods for computing fluid flows with intricate immersedboundaries.Commonnumericalapproachesaremadeconsiderablymore challenging when the fluid is highly elastic. The first chapter describes many of thesechallenges,includingthecatastrophichigh-Weissenbergnumberproblem,and offerssolutions.Theimmersedboundarymethodisintroduced,andthelocomotion of C. elegansin viscoelastic fluids is revisited as a test problemfrom a numerical perspective.The final chapterof the book presentsa cell-levelnumericalstudy of bloodflow,wheretheshapesanddynamicsofindividualcellsandtheirinteractions are captured in a boundary integral formulation of the problem. The numerical methodisusedtounderstandphysicaleffectswellknowntophysiologistssuchas the Fåhræus effect, Fåhræus-Lindqvist effect, and the margination of leukocytes andplatelets. Thechapterscontainedhereinwillprovidethereaderwithanoverviewaswellas adetailedinspectionofthechallengesandopportunitiesthatawaitusinthecoming decades of research in complex biological flows, and the observations, methods, and tools available for their study. Active areas of exploration are presented by manyoftheworld’sforemostexpertsintheirrespectivefields.Consequently,each chapter both provides a substantial review of the literature and delivers the very cutting edge of our current knowledge. The book was developed with advanced undergraduate and early graduate students in the engineering, biological, and mathematicalsciencesinmind,butitwillappealtoanyoneinterestedintheintricate andbeautifulnatureofcomplexfluidsinthecontextoflivingsystems. Numerousacknowledgementsareinorder.Ithasbeenagreatpleasuretowork with the many authors of this book, who continue to forge new paths in their respective fields and to inspire with their creativity and remarkably hard work. It is immensely gratifying to toil as a member of an extended scientific family that knowsnogeographicalborders.IamparticularlyindebtedtoHarveySegur,Michael Preface ix Shelley, Eric Lauga, Thomas Powers, and Jean-Luc Thiffeault, and I would like to thank Gwynn Elfring for dependableconsultationon this project. Finally, I am forever grateful to my wife Elena for her love and support, and to my daughter Carinaforjoiningtheadventure. Madison,WI,USA SaverioE.Spagnolie July,2014