This page intentionally left blankLight and Photosynthesis in Aquatic EcosystemsThirdeditionBeginning systematically with the fundamentals, the fully updated third edition ofthis popular graduate textbook provides an understanding of all the essentialelements of marine optics. It explains the key role of light as a major factor indetermining the operation and biological composition of aquatic ecosystems, andits scope ranges from the physics of lighttransmission within water, through thebiochemistry and physiology of aquatic photosynthesis, to the ecologicalrelationships that depend on the underwater light climate. This book also providesa valuable introductionto the remote sensing of the ocean from space, which isnow recognized to be of great environmentalsignificance due to its directrelevance to global warming.An important resource for graduate courses on marine optics, aquaticphotosynthesis, or ocean remote sensing; and for aquatic scientists, bothoceanographers and limnologists.j ohnt. o. ki rkbegan his research into ocean optics in the early 1970s in theDivision of Plant Industry of the Commonwealth Scientific & Industrial ResearchOrganization (CSIRO),Canberra, Australia, where he was a chief researchscientist, and continued it from 1997 in Kirk Marine Optics. He was awarded theAustralian Society for Limnology Medal (1981), and besides the two successfulprevious editions of this book, has also co-authored The Plastids: Their Chemistry,Structure, Growth and Inheritance (Elsevier, 1978), which became the standard textin its field.Beyond his own scientific research interests, he has always been interested in thebroader implications of science for human existence, and has published a book onthis and other issues, Science and Certainty (CSIRO Publishing, 2007).Light and Photosynthesisin Aquatic EcosystemsThird editionJOHNT. O. KIRKKirk Marine OpticsCAMBRI DGEUNI VERSI TYPRESSCambridge, New York, Melbourne, Madrid, Cape Town, Singapore,Sa o Paulo, Delhi, Dubai, Tokyo, Mexico CityCambridge UniversityPressTheEdinburgh Building,Cambridge CB2 8RU, UKPublished in the United States of America by Cambridge University Press, New Yorkwww.cambridge.orgInformation on this title:www.cambridge.org/9780521151757#John T. O. Kirk 2011This publicationis in copyright. Subjectto statutory exceptionand to the provisions of relevant collectivelicensing agreements,no reproduction of any part may takeplace withoutthe written permission of Cambridge UniversityPress.First published 1983Second edition1994Printedin the United Kingdom at the UniversityPress, CambridgeA catalogue record for this publication is available from the British LibraryLibrary of Congress Cataloging-in-Publication DataKirk, John T. O. (John Thomas Osmond), 1935Light and photosynthesisin aquatic ecosystems/ John T. O. Kirk. 3rd ed.p. cm.Includes bibliographicalreferences and indexes.ISBN 978-0-521-15175-7 (Hardback)1. Photosynthesis. 2. PlantsEffectof underwater light on. 3. AquaticplantsEcophysiology. 4. Underwaterlight. I. Title.QK882.K53 20105720.46dc222010028677ISBN978-0-521-15175-7 HardbackCambridge University Presshas no responsibility for the persistence oraccuracy of URLs for external or third-party internet websites referred toin this publication,and does not guarantee that any content on suchwebsites is,or will remain, accurate or appropriate.ContentsPreface to the third edition pageixPART I THE UNDERWATER LIGHT FIELD 11 Concepts of hydrologic optics 31.1 Introduction 31.2 The nature of light 31.3 The propertiesdefining the radiationfield 61.4 The inherent optical properties 141.5 Apparent and quasi-inherentopticalproperties 211.6 Opticaldepth 241.7 Radiative transfer theory 242 Incident solar radiation 282.1 Solarradiationoutside the atmosphere 282.2 Transmissionof solarradiationthroughthe Earths atmosphere 302.3 Diurnal variationof solarirradiance 382.4 Variationof solarirradianceand insolationwithlatitudeand timeof year 422.5 Transmissionacross the airwater interface 443 Absorption of light within the aquatic medium 503.1 The absorptionprocess 503.2 The measurementof lightabsorption 533.3 The majorlight-absorbingcomponentsof the aquatic system 61v3.4 Optical classificationof natural waters 923.5 Contribution of the differentcomponentsof the aquatic mediumto absorptionof PAR 954 Scattering of light within the aquatic medium 984.1 Thescattering process 984.2 Measurement of scattering 1044.3 Thescattering propertiesof natural waters 1164.4 Thescattering propertiesof phytoplankton 1285 Characterizing the underwater light field 1335.1 Irradiance 1335.2 Scalar irradiance 1435.3 Spectraldistribution of irradiance 1445.4 Radiance distribution 1475.5 Modellingthe underwater lightfield 1496 The nature of the underwater light field 1536.1 Downward irradiance monochromatic 1536.2 Spectraldistribution of downward irradiance 1596.3 Downward irradiance PAR 1596.4 Upward irradianceand radiance 1686.5 Scalar irradiance 1786.6 Angular distribution of the underwaterlightfield 1816.7 Dependence of propertiesof the fieldon optical properties of the medium 1886.8 Partial vertical attenuationcoefficients 1977 Remote sensing of the aquatic environment 1997.1 The upward flux and its measurement 2007.2 The emergent flux 2157.3 Correction for atmospheric scatteringand solar elevation 2187.4 Relation betweenremotely sensedreflectanceand the scattering/absorption ratio 2257.5 Relation betweenremotely sensedreflectancesand watercomposition 228vi ContentsPART II PHOTOSYNTHESIS IN THEAQUATICENVIRONMENT 2638 The photosynthetic apparatus of aquatic plants 2658.1 Chloroplasts 2658.2 Membranes and particles 2688.3 Photosyntheticpigment composition 2758.4 Reactioncentres and energy transfer 2988.5 The overall photosyntheticprocess 3009 Light capture by aquatic plants 3089.1 Absorption spectra of photosynthetic systems 3089.2 The package effect 3119.3 Effectsof variationin cell/colony sizeand shape 3149.4 Rate of lightabsorption by aquatic plants 3199.5 Effectof aquatic plantson the underwaterlightfield 32510 Photosynthesis as a function of the incident light 33010.1 Measurement of photosyntheticrate in aquaticecosystems 33010.2 Photosynthesisand lightintensity 33910.3 Efficiencyof utilizationof incidentlightenergy 36010.4 Photosynthesisand wavelength of incidentlight 38011 Photosynthesis in the aquatic environment 38811.1 Circulation and depth 38811.2 Optical characteristics of the water 39711.3 Otherlimiting factors 40011.4 Temporalvariationin photosynthesis 43011.5 Photosyntheticyield per unit area 44012 Ecological strategies 45312.1 Aquatic plantdistribution in relationto lightquality 45312.2 Ontogenetic adaptation intensity 46912.3 Ontogenetic adaptation spectralquality 47912.4 Ontogenetic adaptation depth 48812.5 Significance of ontogenetic adaptationof thephotosynthetic system 50312.6 Rapid adaptationof the photosyntheticsystem 514Contents vii12.7 The microphytobenthos 52812.8 Highlyproductive aquatic ecosystems 532References and author index 539Index to symbols 626Index to organisms 628Index to water bodies 632Subject index 638Thecolourplatesappearbetween pages 212 and 213.viii ContentsPreface to the third editionFourthingsarerequiredforplant growth: energyintheformof solarradiation; inorganic carbon in the form of carbon dioxide or bicarbonateions;mineralnutrients;andwater.Thoseplantswhich,inthecourseofevolution, have remained in, or have returned to, the aquatic environmenthave one major advantage over their terrestrial counterparts: namely,thatwaterlackofwhichsooftenlimitsproductivityintheterrestrialbiosphere is for them present in abundance; but for this a price must bepaid.Themediumairinwhichterrestrialplantscarryoutphotosyn-thesis offers, withinthe sort of depththat plant canopies occupy, nosignificantobstacletothepenetrationoflight.Themediumwaterinwhichaquaticplantsoccur,incontrast,bothabsorbsandscatterslight.Forthephytoplanktonandthemacrophytesinlakesandrivers,coastalandoceanicwaters, boththeintensityandspectral qualityof thelightvarymarkedlywithdepth. Inall buttheshallowestwaters, lightavail-abilityisalimitingfactorforprimaryproductionbytheaquaticecosys-tem.Theaquaticplantsmustcompeteforsolarradiationnotonlywitheach other (as terrestrial plants must also do), but also with all the otherlight-absorbingcomponentsoftheaquaticmedium.Thishasled,inthecourseof evolution, totheacquisitionbyeachof themajorgroupsofalgae of characteristic arrays of light-harvesting pigments that are of greatbiochemical interest, and also of major significance for an understandingbothoftheadaptationofthealgaetotheirecological nicheandofthephylogenyandtaxonomyofthedifferentalgal groups. Nevertheless, inspiteoftheevolutionofspecializedlight-harvestingsystems,theaquaticmediumremovessomuchoftheincidentlightthataquaticecosystemsare, broadlyspeaking, lessproductive than terrestrial ones.Thus, the nature of the light climate is amajor difference betweenthe terrestrial and the aquatic regions of the biosphere. Within theixunderwater environment, light availability is of major importance indetermininghowmuchplantgrowththereis, whichkindsofplantpre-dominateand,indeed, whichkindsofplantshaveevolved. Itisnotthewhole story biotic factors, availability of inorganic carbon and mineralnutrients, and temperature, all make their contribution but it is a largepart of that story. This book is a study of light in the underwater environ-ment fromthe point of viewof photosynthesis. It sets out tobringtogetherthephysicsoflighttransmissionthroughthemediumandcap-turebytheplants, thebiochemistryof photosyntheticlight-harvestingsystems,thephysiologyofthephotosyntheticresponseofaquaticplantstodifferent kinds of light field, andthe ecological relationships thatdependonthelight climate. Thebookdoesnot attempt toprovideascompleteanaccountof thephysical aspectsofunderwaterlight asthemajor works by Jerlov (1976), Preisendorfer (1976) and Mobley (1994); itis aimed at the limnologist and marine biologist rather than the physicist,although physical oceanographers should findit of interest. Its intentionis to communicate a broad understanding of the significance of light as amajor factor determiningtheoperationandbiological compositionofaquatic ecosystems. It is hopedthat it will be of value topractisingaquaticscientists, touniversityteacherswhogivecoursesinlimnologyor marine science, and to postgraduate and honours students in these andrelateddisciplines.Certain features of the organization of the book merit comment.Althoughinsomecasesauthorsanddatesarereferredtoexplicitly, tominimizeinterruptionstothetext, referencestopublishedworkareinmost cases indicated by the corresponding numbers in the completealphabetical referencelist at theendof thebook. Accompanyingeachentry in the reference list is (are) the page number(s) where that paper orbook is referred to in the text. Although coverage of the field is, I believe,representative, it is not intended to be encyclopaedic. The papers referredto have been selected,notonlyonthegrounds oftheirscientificimport-ance, but inlarge part onthe basis of their usefulness as illustrativeexamples for particular points that need to be made. Inevitably, therefore,many equally important and relevant papers have had to be omitted fromconsideration, especially in the very broad field of aquatic ecology. I havetherefore, where necessary, referred the reader to more specialized worksinwhich more comprehensive treatments of particular topics canbefound. Becauseitscontributiontototal aquaticprimaryproductionisusually small I have not attempted to deal with bacterial photosynthesis,complex and fascinating though it is.x Preface to the third editionThebehaviour of sunlight inwater, andtherolethat light plays incontrollingtheproductivity,andinfluencingthebiologicalcomposition,ofaquaticecosystemshavebeenimportantareasofscientificstudyformorethanacentury, andit wastomeet theperceivedneedforatextbringingtogetherthephysicalandbiologicalaspectsofthesubject,thatthefirst,andthensecond,editionsof Lightand Photosynthesis in AquaticEcosystemswerewritten. Thebookwaswell received, andisinusenotonlybyresearchworkersbutalsoinuniversitycourses. Inthe27yearssince the first edition, interest in the topic has become even greater than itwas before. This may be partly attributed to concern about globalwarming, andtherealizationthattounderstandtheimportantroletheoceanplays intheglobal carboncycle, weneedtoimprovebothourunderstanding and our quantitative assessment of marine primaryproduction.Anadditional, but related, reasonisthegreat interest that hasbeenaroused in the feasibility of remote sensing of oceanic primary productiv-ityfromspace. Thepotentialitieswerejustbecomingapparentwiththeearly Coastal Zone Color Scanner (CZCS) pictures when the first editionwas written. The continuing stream of further remote sensing informationin the ensuing years, as space agencies around the world have put new andimprovedoceanscanners intoorbit, enormouslyenlargingour under-standing of oceanic phytoplankton distribution, have made this a particu-larly active and exciting field within oceanography. But the light flux thatisreceivedfromtheoceanbythesatellite-borneradiometers,andwhichcarries with it information about the composition of the water, originates infact as apart of the upwellinglight fluxwithinthe ocean, whichhasescapedthroughthesurfaceintotheatmosphere. Tointerpret thedatawethereforeneedtounderstandtheunderwaterlightfield, andhowitscharacteristics are controlled by what is present within the aquatic medium.Inconsequenceof this sustained, evenintensified, interest inunder-water light, thereis acontinuedneedfor asuitabletext, not onlyforresearchers, but also for use in university teaching. It is for this reason, thefirst andsecondeditions being out of print, that I have preparedacompletely revisedversion. Since marine bio-optics has beensuchanactivefield,avastamountofliteraturehadtobedigested,butasintheearlier editions, I have tended to select specific papers mainly on the basisof their usefulness as illustrative examples, and many other equally valu-able papers have had to be omittedfrom consideration.In the 16 years since the second edition of this book appeared, interestin this subject has, if anything, increased. While there has been anPreface to the third edition xiacceleration, ratherthanaslackeningintherateofpublicationofnewresearchitmustbesaidthatthishasbeenmuchmoreevidentincertainareas than in others. Remote sensing of ocean colour, and its use to arriveatinferencesaboutthecompositionandoptical propertiesof, andpri-maryproductiongoingonwithin, oceanwatershasbeenthestandoutexample of a very active field. A variety of new instruments for measuringtheoptical propertiesofthewater, andtheunderwaterlightfield, havebeen developed, and a number of these are described. So far as photosyn-thesisitselfisconcerned,themostnotablechangehasbeenthedevelop-ment of instrumentation, together with the necessary accompanyingtheoretical understanding, for in situ measurement of photosynthetic rate,usingchlorophyll afluorescence. Agreatdeal moreisalsonowknownabout carbonconcentrating mechanisms inaquatic plants, andthesetopics arediscussed. Thepresumptiveroleof ironas alimitingfactorforprimaryproductioninlargeareasoftheoceanhasreceivedagreatdealofattentioninrecentyears,andcurrentunderstandingissummar-ized. Nevertheless, quiteapartfromthesespecificareas, therehasbeenacross-the-boardprogressinallpartsofthesubject,nochapterremainsunchanged, and the reference list has increased in length by about 50%.IwouldliketothankDrSusanBlackburn,ProfessorD.Branton,DrM. Bristow, Mr S. Craig, Dr W. A. Hovis, Mr Ian Jameson, Dr S. Jeffrey,Dr D. Kiefer, Professor V. Klemas, Professor L. Legendre, Dr Y. Lipkin,ProfessorW.Nultsch,Mr D.Price,ProfessorR.C.Smith,DrM. Vesk;Biospherical Instruments Inc., who have provided original copies offigures for reproductioninthis work; andMr F. X. DuninandDrP.A.Tylerforunpublisheddata.IwouldliketothankMrK.LyonofOrbitalSciencesCorporationforprovidingillustrationsoftheSeaWiFSscanner and spacecraft, and the SeaWiFS Project NASA/Goddard SpaceFlight Center, for remote sensing images of the ocean.John KirkCanberraApril 2010xii Preface to the third editionPARTIThe underwater light field1Concepts of hydrologic optics1.1 IntroductionThepurposeofthefirstpartofthisbookistodescribeandexplainthebehaviour of light in natural waters. The word light in common parlancerefers toradiationinthat segment of the electromagnetic spectrumabout 400to700 mmtowhichthe humaneye is sensitive. Our primeconcernisnot withvisionbut withphotosynthesis. Nevertheless, byaconvenient coincidence, the waveband within which plants can photosyn-thesizecorresponds approximatelytothat of humanvisionandsowemay legitimately refer to the particular kind of solar radiation with whichwe are concernedsimply as light.Optics is that part of physics which deals with light. Since the behaviourof light is greatly affected by the nature of the medium through which it ispassing, there are different branches of optics dealing with different kindsofphysicalsystems. Therelationsbetweenthedifferentbranchesofthesubject andof opticstofundamental physical theoryareoutlineddia-grammatically in Fig. 1.1. Hydrologic optics is concerned with the behavi-our of lightin aquatic media. It can be subdivided intolimnologicalandoceanographic optics according to whether fresh, inland or salty, marinewatersareunderconsideration. Hydrologicopticshas, however, uptonow been mainly oceanographic in its orientation.1.2 The nature of lightElectromagneticenergyoccursinindivisibleunitsreferredtoasquantaor photons. Thusabeamofsunlight inairconsistsofa continualstreamof photons travellingat 3 108ms1. The actual numbers of quanta3involvedareverylarge. Infull summer sunlight. for example, 1 m2ofhorizontalsurfacereceivesabout1021quantaofvisiblelightpersecond.Despite its particulate nature, electromagnetic radiation behaves in somecircumstances as though it has a wave nature. Every photon has awavelength, l, and a frequency, n. These are relatedin accordancewithl cv 1.1wherecisthespeedoflight.Sincecisconstantinagivenmedium,thegreater the wavelength the lower the frequency. If c is expressed in ms1andnincycles s1, thenthewavelength, l, isexpressedinmetres. Forconvenience, however, wavelength is more commonly expressed in nano-metres, ananometre (nm) beingequal to109m. The energy, , inaphotonvarieswith the frequency, and therefore inverselywiththe wave-length, the relationbeinge hv hcl 1.2where h is Plancks constant and has the value of 6.63 1034J s. Thus, aphotonof wavelength700 nmfromtheredendof thephotosyntheticspectrumcontainsonly57%asmuchenergyasaphotonofwavelength400 nm from the blue end of the spectrum. The actual energy in a photonof wavelength l nm is givenby the relationELECTROMAGNETIC THEORYINTERACTION PRINCIPLEGENERAL RADIATIVETRANSFER THEORYGEOPHYSICALOPTICSASTROPHYSICALOPTICSPLANETARYOPTICSMETEOROLOGICALOPTICSHYDROLOGICOPTICSOCEANOGRAPHICOPTICSLIMNOLOGICALOPTICSFig.1.1 Therelationshipbetweenhydrologicopticsandotherbranchesofoptics (after Preisendorfer, 1976).4 Concepts of hydrologic opticse 1988l 1019J 1.3A monochromatic radiation flux expressed in quanta s1can thus readilybeconvertedtoJ s1,i.e. towatts(W). Conversely, aradiationflux, F,expressedin W,can be converted to quanta s1usingthe relationquantas1 5.03 Fl 10151.4Inthe case of radiationcoveringabroadspectral band, suchas forexample the photosynthetic waveband, a simple conversion fromquanta s1toW, or viceversa, cannot becarriedout accuratelysincethe value of l varies across the spectral band. If the distribution of quantaorenergyacrossthespectrumisknown,thenconversioncanbecarriedout for aseries of relativelynarrowwavebands coveringthe spectralregion of interest and the results summed for the whole waveband.Alternatively, an approximate conversion factor, which takes intoaccount thespectral distributionof energythat islikelytooccur, maybe used. For solar radiation in the 400 to 700 nmband above thewater surface, Morel and Smith (1974) found that the factor (Q/W)requiredtoconvert Wtoquanta s1was2.77 1018quanta s1W1toanaccuracyofplusorminusafewpercent,regardlessofthemeteoro-logicalconditions.As we shall discuss at length ina later section (}6.2) the spectraldistribution of solar radiation under water changes markedly with depth.Nevertheless, Morel andSmithfoundthat forawiderangeof marinewatersthevalueofQ:Wvariedbynomorethan 10%fromameanof2.5 1018quanta s1W1. As expected fromeqn 1.4, the greater theproportionoflong-wavelength(red)lightpresent, thegreaterthevalueof Q:W. For yellow inland waters with more of the underwater light in the550to700 nmregion(see }6.2),byextrapolatingthedataofMorelandSmith we arrive at a value of approximately 2.9 1018quanta s1W1forthe valueof Q:W.In any medium, light travels more slowly than it does in a vacuum. Thevelocity of light in a medium is equal to the velocity of light in a vacuum,divided by the refractive index of the medium. The refractive index of airis 1.00028, which for our purposes is not significantly different from thatof a vacuum (exactly 1.0, by definition), and so we may take the velocityoflightinairtobeequal tothatinavacuum. Therefractiveindexofwater,althoughitvariessomewhatwithtemperature,saltconcentrationandwavelengthof light, maywithsufficient accuracyhe regardedasequal to1.33forall natural waters. Assumingthatthevelocityoflight1.2 The nature of light 5inavacuumis 3 108ms1, the velocityinwater is therefore about2.25 108ms1The frequency of the radiation remains the same in waterbutthewavelengthdiminishesinproportiontothedecreaseinvelocity.Whenreferringtomonochromatic radiation, the wavelengthwe shallattributetoitisthatwhichithasinavacuum.Becausecand lchangeinparallel, eqns 1.2, 1.3and1.4areas trueinwater as theyareinavacuum:furthermore,whenusingeqns1.3and1.4.itisthevalueofthewavelength in a vacuum which is applicable, even when the calculation iscarriedout for underwaterlight.1.3 The properties defining the radiation fieldIf we are tounderstandthe ways inwhichthe prevailing light fieldchangeswithdepthinawaterbody, thenwemust first considerwhatare the essential attributes of alight fieldinwhichchanges might beanticipated.Thedefinitionsof theseattributes,in part, followthereportoftheWorkingGroupssetupbytheInternational AssociationforthePhysical Sciences of the Ocean (1979), but are also influenced by the morefundamental analyses given by Preisendorfer (1976). Amore recentaccountofthedefinitionsandconceptsusedinhydrologicopticsisthatby Mobley(1994).We shall generally express direction within the light field in terms of thezenith angle, y (theanglebetweena givenlightpencil, i.e.athinparallelbeam, andthe upwardvertical), andthe azimuth angle, f(the anglebetweentheverticalplaneincorporatingthelightpencilandsomeotherspecifiedverticalplanesuch as theverticalplaneof the Sun). In the caseof the upwelling light stream it will sometimes be convenient to express adirectionintermsofthenadirangle, yn(theanglebetweenagivenlightpencil and the downward vertical). These angular relations are illustratedin Fig.1.2.Radiant flux,F, isthetimerateofflowofradiantenergy. Itmaybeexpressed in W (J s1) or quanta s1.Radiant intensity, I, is a measure of the radiant flux per unit solid angleina specifieddirection. The radiant intensity of a source ina givendirectionistheradiantfluxemittedbyapointsource,orbyanelementof anextended source, inaninfinitesimal cone containing the givendirection, dividedbythatelementofsolidangle. Wecanalsospeakofradiant intensity at a point in space. This, the field radiant intensity, is theradiantfluxatthatpoint ina specifieddirectionin aninfinitesimal cone6 Concepts of hydrologic opticscontainingthegivendirection, dividedbythat element of solidangle.I has the unitsW (or quanta s1) steradian1.I ddoIfweconsidertheradiantfluxnotonlyperunitsolidanglebutalsoperunit area of a plane at right angles to the direction of flow, then we arriveattheevenmoreuseful conceptofradiance, L. Radianceatapoint inspaceistheradiantfluxatthatpointinagivendirectionperunitsolidangleperunitareaatrightanglestothedirectionofpropagation. ThemeaningofthisfieldradianceisillustratedinFigs. 1.3aandb. Thereisalso surface radiance, which is the radiant flux emitted in a given directionper unit solid angle per unit projected area (apparent unit area, seen fromthe viewingdirection) of asurface: this is illustratedinFig. 1.3c. Toindicatethatitisafunctionofdirection,i.e.ofbothzenithandazimuthangle, radiance is commonly written as L(y, f ). The angular structure of alight field is expressed in terms of the variation of radiance with y and f.Radiancehas the units W (or quanta s1) m2steradian1.horizontalyxqqnfFig. 1.2 The angles defining direction within a light field. The figure shows adownwardandanupwardpencil oflight,both,forsimplicity, inthesamevertical plane. Thedownwardpencil haszenithangle y;theupwardpencilhas nadir angleyn, whichis equivalent toazenithangle of (180

yn).Assumingthexyplaneisthevertical planeoftheSun, orotherreferencevertical plane, then c is the azimuth angle for both light pencils.1.3 The properties defining the radiation field 7L0. f d2FdS cos 0doIrradiance(atapointofasurface),E,istheradiantfluxincidentonaninfinitesimal elementofasurface, containingthepointunderconsider-ation, dividedbytheareaof that element. Less rigorously, it maybedefinedastheradiant fluxperunit areaof asurface.*It hastheunitsWm2or quanta (or photons) s1m2, or mol quanta (or photons)s1m2, where 1.0 mol photons is 6.02 1023(Avogadros number)photons. Onemoleof photonsissometimesreferredtoasaneinstein,but this term is nowrarelyused.(a) (b) (c)DdwdAPdA dwL =d2FdS cosq dwL (q, f) =d2FdwdSqfdS cosqdwdSfqdS cosqFig.1.3 Definitionofradiance. (a)Fieldradianceatapointinspace.ThefieldradianceatPinthedirectionDistheradiantfluxinthesmall solidangle surrounding D, passing through the infinitesimal element of area dA atrightanglestoDdividedbytheelementofsolidangleandtheelementofarea. (b) Fieldradiance at apoint inasurface. It is oftennecessarytoconsider radiance at a point on a surface, from a specified direction relativetothatsurface. dSistheareaofasmall elementofsurface. L(y, c)istheradiance incident ondSat zenithangley(relative tothe normal tothesurface) andazimuthanglec: its valueis determinedbytheradiant fluxdirected at dS within the small solid angle, do, centred on the line defined byy and c. The flux passes perpendicularly across the area dS cos y, which is theprojectedareaof theelement ofsurface, dS, seenfromthedirectiony, c.Thus theradianceonapoint inasurface, fromagivendirection, is theradiantfluxinthespecifieddirectionperunitsolidangleper unit projectedareaofthesurface.(c)Surfaceradiance.Inthecaseofasurfacethatemitsradiation the intensity of the flux leaving the surface in a specified direction isexpressed in terms of the surface radiance, which is defined in the same way asthe fieldradiance at a point ina surface except that the radiationis consideredtoflow away from, rather than on to, the surface.* Terms such as fluence rate or photon fluence rate, sometimes to be found in the plantphysiological literature,are superfluous and should not be used.8 Concepts of hydrologic opticsE dFdSDownward irradiance, Ed, and upward irradiance, Eu, are the values of theirradianceon the upper and the lowerfaces, respectively, of a horizontalplane. Thus, Ed is the irradiance due to the downwelling light stream andEu isthat due to the upwelling lightstream.Therelationbetweenirradianceandradiancecanbeunderstoodwiththe help of Fig. 1.3b. The radiance in the direction defined by y and f is L(y,f)W(orquanta s1)perunitprojectedareapersteradian(sr). Theprojected area of the element of surface is dS cos y and the correspondingelementofsolidangleisdo. ThereforetheradiantfluxontheelementofsurfacewithinthesolidangledoisL(y,f)dScosydo. Theareaofthe element of surface is dS and so the irradiance at that point inthesurfacewheretheelementislocated,duetoradiantfluxwithindo,isL(y, f)cos ydo. Thetotal downwardirradianceatthatpointinthesurface is obtained by integrating with respect to solid angle overthe whole upper hemisphereEd 2pL0. f cos 0do 1.5Thetotal upwardirradianceisrelatedtoradianceinasimilarmannerexcept that allowance must be made for the fact that cos y is negative forvalues of y between90 and 180

Eu 2pL0. f cos 0do 1.6Alternatively the cosine of the nadir angle, yn (see Fig. 1.2), rather than ofthe zenith angle, maybe usedEu 2pL0n. f cos 0ndo 1.7The 2p subscript is simply to indicate that the integration is carried outover the 2p sr solid angle in the lower hemisphere.Thenet downwardirradiance,

E, isthedifferencebetweenthedown-ward and the upward irradiance

E Ed Eu1.8It is relatedto radiance by the eqn1.3 The properties defining the radiation field 9

E 4pL0. f cos 0do 1.9which integrates the product of radiance and cos y over all directions: thefact that cos y is negative between 90 and 180

ensures that the contribu-tion of upward irradiance is negative in accordance with eqn 1.8. The netdownwardirradianceisameasureofthenetrateoftransferofenergydownwardsat that point inthemedium, andasweshall seelaterisaconceptthat can be used to arriveat somevaluable conclusions.The scalar irradiance, E0, is the integral of the radiance distribution at apoint over all directionsabout the pointEo 4pL0. fdo 1.10Scalarirradianceisthusameasureof theradiant intensityat apoint,whichtreatsradiationfromall directionsequally. Inthecaseofirradi-ance, on the other hand, the contribution of the radiation flux at differentanglesvariesinproportiontothecosineofthezenithangleofincidenceof theradiation: aphenomenonbasedonpurelygeometrical relations(Fig. 1.3, eqn1.5), andsometimesreferredtoastheCosineLaw. It isuseful todividethescalarirradianceintoadownwardandanupwardcomponent. The downwardscalarirradiance, E0d, istheintegral oftheradiance distribution over the upper hemisphereE0d 2pL0. fdo 1.11The upward scalar irradiance is defined in a similar manner for the lowerhemisphereE0u 2pL0. fdo 1.12Scalar irradiance (total, upward, downward) has the same units asirradiance.It is always thecaseinreal-liferadiationfields that irradiance andscalar irradiancevarymarkedlywithwavelengthacross thephotosyn-theticrange. Thisvariationhasaconsiderablebearingontheextenttowhich the radiation field can be used for photosynthesis. It is expressed intermsofthevariationinirradianceorscalarirradianceperunitspectraldistance(inunitsofwavelengthorfrequency,asappropriate)acrossthespectrum. Typicalunits would be W (orquanta s1) m2nm1.10 Concepts of hydrologic opticsIf weknowtheradiancedistributionover all angles at aparticularpoint in a medium then we have a complete description of theangular structure of the light field. Acomplete radiance distribution,however, coveringall zenithandazimuthangles at reasonablynarrowintervals, represents a large amount of data: with 5

angular intervals, forexample, thedistributionwill consist of 1369separateradiancevalues.A simpler, but still very useful, way of specifying the angular structure ofa light field is in the form of the three average cosines for downwelling,upwellingand total light and the irradiancereflectance.Theaveragecosinefordownwellinglight, jd,ataparticularpointintheradiationfield, mayberegardedastheaveragevalue, inaninfini-tesimally small volume element at that point in the field, of the cosine ofthe zenith angle of all the downwelling photons in the volume element. Itcanbecalculatedbysumming(i.e. integrating)forall elementsofsolidangle (do) comprising the upper hemisphere, the product of the radianceinthatelementofsolidangleandthevalueofcos y(i.e.L(y, f)cos y),andthendividingbythetotal radianceoriginatinginthat hemisphere.By inspectionof eqns 1.5 and 1.11it can be seenthatjd EdE0d1.13i.e. theaveragecosinefordownwellinglight isequal tothedownwardirradiance divided by the downward scalar irradiance. The average cosinefor upwelling light, ju, may be regarded as the average value of the cosineof the nadir angle of all the upwelling photons at a particular point in thefield. By a similar chain of reasoning to the above, we conclude that juisequal to the upward irradiancedivided by the upward scalar irradianceju EuE0u1.14Inthecaseofthedownwellinglightstreamitisoftenuseful todeal intermsofthereciprocal oftheaveragedownwardcosine, referredtobyPreisendorfer (1961) as the distribution function for downwelling light, Dd,whichcanbeshown712tobeequal tothemeanpathlengthperverticalmetre traversed, of the downward flux of photons per unit horizontal areapersecond.ThusDd 1jd.Thereis,ofcourse,ananalogousdistribu-tion function for the upwellinglightstream,defined by Du 1ju.The average cosine, j, for the total light at a particular point in the fieldmay be regarded as the average value,in an infinitesimally small volumeelement at that point in the field, of the cosine of the zenith angle of all thephotonsinthevolumeelement. Itmaybeevaluatedbyintegratingtheproduct of radiance and cos y over all directions and dividing by the total1.3 The properties defining the radiation field 11radiance from all directions. By inspection of eqns 1.8, 1.9 and 1.10, it canbe seenthat the average cosine for the total light is equal tothe netdownwardirradiancedivided by the scalar irradiancej

EE0 Ed EuE01.15ThatEd Eushouldbeinvolved(ratherthan,say,EdEu)followsfromthe fact that the cosine of the zenith angle is negative for all the upwellingphotons (90

70024080m23$14050OceanicpicoplanktonCoralSea,OctNov42410m$27344818100m72245NETropicalAtlanticOceanPhytoplanktonEutrophicsite15016050MesotrophicsiteNearsurface$240Mid-pointeuphotic150160Table10.1(cont.)Irradiance,mmolquanta(PAR)m2s1SpeciesorplanttypeLocation,seasonTemperature

CAtsaturationAtonsetofsaturationEkAtcompensationpointReferenceOligotrophicsiteNearsurface$400Mid-pointeuphotic$320Bottomofeuphotic$60NorthAtlanticOceanAzoresFront,$34

N829Surface$25206Deepchlorophyllmaximum($100m)$1728ContinentalshelfphytoplanktonBransfieldStrait,Antarctica,DecMarch0150180.51.0581,915Coastalphytoplankton(110m)NovaScotia,Canada,allyear015$300105(av.)4(av.)1063Coastalphytoplankton(0m)Baltic,Denmark12983Feb140020015July17120050031Oct12800300CoastalphytoplanktonS.CaliforniaBight,USA12521m1625432m1242SurfzonephytoplanktonAlgoaBay,SthAfrica1522.57001000300450 198EstuarinephytoplanktonChesapeakeBay,USA.June525Prorocentrummariae-lebouriaeSurfacemixedlayer(0.5m)24412Subpycnocline(15m)2167IntertidalbenthicdiatomsCapeCod,USA.Summer27571349Sea-icealgae(pennatediatoms)CanadianArctic.Spring13250.54.30.18258Sea-icealgae(pennatediatoms)McMurdoSound,Antarctica.Summer2255.41033PlateleticediatomsBenthicdiatoms(26m)McMurdoSound,Antarctica.November22 5.912.61.34.5 1139SubtidalmicrophytobenthosPortPhillipBay,Australia.Werribeesite,10mdepth811July(winter)12.2March(earlyautumn)$320SeagrassesCymodoceanodosaHalophilastipulaceaPosidoniaoceanicaMalta252517 15883108178 17323PhyllospadixtorreyiZosteramarinaCalif.,USA1515 1492082125323ZosteraangustifoliaScotland1013312323Halophilaovalismeadow,1416mdepthSouthSulawesi,Indonesia$40033367Table10.1(cont.)Irradiance,mmolquanta(PAR)m2s1SpeciesorplanttypeLocation,seasonTemperature

CAtsaturationAtonsetofsaturationEkAtcompensationpointReferenceMarinemacroalgaeChlorophytaEnteromorphaintestinalisW.Baltic.SpringSummerCalif.,USA102021450 245 566 15669129CladophoraglomerataAcrosiphoniacentralisUlothrixspeciosaW.Baltic.SummerSpringSpring201010700200700 8 7 6691MonostromagrevilleiN.Baltic51201430UlvalactucaWoodsHole,Mass.USA.Summer232501601101UlvalobataCalif.,USA16245761129Ulvarigida21412509Codiumfragile21346509Chaetomorphalinum214188210PhaeophytaFucusserratusLaminariasaccharinaScytosiphonlomentariaEctocarpusconfervoidesW.Baltic.Winter53505691Autumn1520012W.Baltic.Winter5254Autumn1570018W.Baltic.Spring107008W.Baltic.Spring102005LaminariasaccharinaNEGreenland,YoungSound.Newleafblades.June,10m,undericeAugust,openwater1.83521382.5mdepth01702210mdepth0174.2LaminariasolidungulaAlaskanHighArctic.Summer23846340DictyosiphonfoeniculaceusPilayellalittoralisN.BalticN.Baltic14144300200100 18201430MacrocystisintegrifoliaVancouverI.,BC,Canada.September1380501256M.pyriferaS.Calif.,USA.MarchAugust1621300140-300446NereocystisluetkeanaVancouverI.,BC,Canada.1463February9.522September1464Fucoid-dominatedmacroalgalcommunitySouthAustraliaSummerWinter1915642447214149348223RhodophytaDumontiaincrassataW.Baltic.Winter51005691Spring105008PhycodrysrubensW.Baltic.Spring102005Table10.1(cont.)Irradiance,mmolquanta(PAR)m2s1SpeciesorplanttypeLocation,seasonTemperature

CAtsaturationAtonsetofsaturationEkAtcompensationpointReferencePhycodrysrubensSummer2020014PolysiphonianigrescensW.Baltic.Spring104007Autumn1530024CeramiumtenuicorneRhodomelaconfervoidesN.BalticN.Baltic114,1010040 1430ChondruscrispusWoodsHole,Mass.,USA.Summer23120601101PorphyraumbilicalisWoodsHole,Mass.,USA.Summer2325090CoralStylophorapistillataSinai,Egypt378Highlightform286002000350Lowlightform2820040CoralreefalgalturfVirginIslands,CaribbeanSea.Jul,Oct,Nov,Dec2814001800780106060105209different Edvalues at intervals of only 10 to15s. ETRversus Edcurves obtainedin this way are often referred to as rapid light curves (RLC). Although an RLClooks very like a classical P versus Ed curve, it is not the same since the cellshavenot beenallowedtoadapt toeachactiniclight intensitybeforetheratemeasurement is taken. Hawes et al. (2003), usingPAMfluorometrytostudyphotosynthesis insubmergedmeadows of the quillwort, Isoetesalpinus, in Lake Wanaka, New Zealand, found that for plants at 7m depththe Ekvalue obtainedfromanRLC(117mmol photons m2s1) was markedlylower than that obtained (164 mmol photons m2s1) from leaves adapted tothe varying ambient irradiance during the day. Ralph and Gademann (2005)offer suggestions as to how RLCs may usefully be interpreted.Anumberofattemptshavebeenmadetofindmathematical expres-sionsthatgiveareasonablefittotheempirical curvesrelatingPtoEd.Since it is a fact of observation that for any given phytoplankton popula-tionthecurvewill exhibitafairlywell-definedinitial slopeandamax-imum, asymptoticallyapproached, valueof P, thevalues of aandPmbeingcharacteristicofthatpopulation, thenwemayreasonablyantici-pate that the relationship we are seeking will express P as a function of aand Pm, as well as Ed. Furthermore the relationship will be such that P f (a, Pm, Ed) reduces to P aEd as Ed tends to zero, and approaches P Pmas Edtends toinfinity. Jassby andPlatt (1976) testedeight differentexpressions that have at various times been proposed, against 188PversusEdcurvesmeasuredformarinephytoplanktonincoastalNovaScotia waters.Thetwo that fittedbestwereP PmEdP2m2E2d1=210:8originally (in a somewhat differentform) proposed by Smith (1936), andP Pm tanhEd=Pm 10:9proposedbyJassbyandPlatt(1976), thelatterexpressiongivingsome-what the better fit. These two expressions for P have been chosen simplyon the basis of goodness of fit to the observations: they are not based onany assumptionsabout the mechanisms of photosynthesis.There isa third, equally simple, equationP Pm1 eEdPm 10:10originallyproposedbyWebbet al. (1974)todescribephotosynthesisinthe tree species, Alnus rubra, and which Peterson et al. (1987) have found10.2 Photosynthesis and light intensity 351tosatisfactorilydescribePversus Edcurves inawiderangeof phyto-planktonsystemsthatcanbegivenaplausiblerationaleintermsofthemechanismof photosynthesis. Byapplicationof simplePoissondistri-bution statistics to the capture of photons by the photosynthetic unit perunit of timet, wheret is theturnover time, andassumingthat excessphotonsarenotutilized,itcanbeshownthattherateofphotosynthesisis proportional to(1em) wheremis themeannumber of incidentphotonscapturedbythephotosyntheticunitintimet.1050Sincemmustbeproportionaltotheincidentflux,Ed,itisclearthateqn10.10,oritsalternativeversionP Pm1 eEdEk 10:11(since Pm/a Ek), is in accordance with this simplemechanistic model.Equations10.8to10.11describethe variationof Pwith Ed onlyuptothe establishment of saturation; they do not encompass the decline in P athigher values of Ed. Platt et al. (1980) have obtained an empirical equationthatdescribesthephotosyntheticrateofphytoplanktonasasinglecon-tinuousfunctionofavailablelightfromtheinitiallinearresponseuptoand including photoinhibition.PhotoinhibitionTheinhibitionofphotosynthesisathighlightintensitiesmustbetakenintoaccount inecological studies, sincetheintensitiestypicallyexperi-encedinthesurfacelayerofnatural watersinsunnyweatherareintherangethat canproducephotoinhibition. Indeedif thedepthprofileofphytoplankton photosynthetic activity is measured by the suspendedbottle methodininlandor marine waters, anoticeable diminutioninthe specific photosynthetic rate or the rate per unit volume is commonly,althoughnot invariably, observednear thesurface. Figure l0.4showsexamples of this surface inhibition of photosynthesis in a coastaland an inland water. With increasing depth and diminishing lightintensity, photoinhibitionlessensandthemaximum, light-saturatedbutnot inhibited, photosyntheticrateisachieved. Withfurtherincreaseindepth, irradiance falls to the point at which light intensity becomeslimitingandfromhere onthe photosynthetic rate diminishes roughlyexponentially withdepth approximately in parallelwithirradiance.Many,butnotall,macrophytespeciesalsoshowinhibitionofphoto-synthesiswhenexposedtolightintensitiesintherangeoffull sunlight,352 Photosynthesis as a function of the incident lightandthisisespeciallythecaseforalgaetakenfromgreaterdepths.517,1162Ecologically,however,thisphenomenonisoflesssignificancesinceanygivenmacrophytespecies is generallytobefoundgrowingat adepthwherethelightintensityisonetowhichitiswelladapted(Chapter12),whereasphytoplanktonarecirculatedwithinarangeofdepthsbywatermovement. Some photoinhibition nevertheless sometimes occurs inmacrophytesinshallowwatersinthemiddlepartoftheday.517Marinemacrophytic algae of the intertidal zone are intermittently exposedto very high light intensities. At irradiance values equivalent to fullsunlight some of these species show no inhibition, but others arepartiallyinhibited.691Inthecoral, Stylophorapistillata, intheGulf ofAqaba(RedSea), Winterset al. (2003)usinginsituPAMfluorescenceFig. 10.4 Depth profiles of phytoplankton photosynthetic rate per unitvolumeof water. Thecurves arefor aninlandwater (LakeWindermere,England; plotted fromdata of Belay, 1981, assuming a photosyntheticquotientof1.15),andacoastalwater(BedfordBasin,NS,Canada;plottedfrom data of Marra, 1978).10.2 Photosynthesis and light intensity 353measurements, foundamarkedmiddaydepression(63%) of effectivequantum yield in coral growing at 2 m depth, but only an 8% depressionin coral growingat 11 m.Inhibitionof photosynthesis by highlight intensities takes time todevelop. InthecaseofphytoplanktonpopulationsfromLakeOntario,Canada,thedeclineinphotosyntheticactivitybeganafterabout10 minexposure.537Measurements of the time course of photosynthesis by popu-lations of the diatom Asterionella in bottles suspended at the surface of aWelshlakeindicatedthattheinhibitoryeffectwassmallduringthefirsthour but becamesignificant duringthesecondhour.91Thehigher thetemperature at a given light intensity, the more rapidly inhibitionensues.537Inthe case of laboratorycultures of Asterionella grownat18

C and 200mmol photons m2s1, exposure to 2000mmol photons m2s1($fullsunlight)for1 hat18

and25

Creducedthesubsequentlymeas-ured photosynthetic rateby about 10 and 50%, respectively.92Phytoplankton can recover from the inhibitory effects of intense lightif they are transferred to a lower light intensity.470The longer theexposuretobright light, thelongertherecoverytakes. InthecaseofAsterionella populations from a Welsh lake, recovery from 2 h exposuretobrightsunlightwascompleteafter4 hinlowlightintensity:after6 hbright sunlight, whichreducedphotosyntheticrateby70%, recoverytook20 h.91Themechanismofphotoinhibitionhasbeenstudiedinmostdetail inhigherplants. JonesandKok(1966) measuredtheactionspectrumofphotoinhibitionofelectrontransportinspinachchloroplasts. Thespec-trum showed its main activity in the ultraviolet (UV) region with a peak at250to260 nm. Photoinhibitionalsooccurredinthevisibleregionbutwith a very much lower quantum efficiency. Between 400 and 700 nm, theactionspectrumfollowedthe absorptionspectrumof chloroplast pig-ments, withadistinct chlorophyll peakat 670to680 nm. The lesionappearsprimarilyto affectthe lightreactionsof photosynthesis bydam-aging the reaction centre of photosystem II.265,266,230The shape of the actionspectruminthe UVregion suggests thatplastoquinoneorsomeotherquinonefunctional inthereactioncentremaybethesensitivemoleculesofarasUVinhibitionisconcerned.Theprimary site of damage to the photosynthetic system by UVB appears tobephotosystemII,suggestingthatitisQA,thequinonoidprimaryelec-tron acceptor of photosystem II that is the crucial target. The shape of theactionspectruminthe visible regionindicates that at veryhighlightintensitiessomeoftheenergyabsorbedbythephotosyntheticpigments354 Photosynthesis as a function of the incident lightthemselves is transferred to a sensitive site not necessarily the same siteas that affectedby UV where it causesdamage.Although detailed studies on the basis of photoinhibition of algalphotosynthesis have not been carried out, the most plausible and econom-ical hypothesis is that the mechanism is the same as in higher plants. Foroceanicphytoplankton,theobservedphotoinhibitionwasfoundtovarylinearly with the daily biological dose calculated using the Jones and Kokaction spectrum.1247In the surface layer of clear ocean waters, 50% of thephotoinhibitorydoseisatwavelengthslessthan390 nm; inmoderatelyproductivewaters(0.5 mg chl a m3)at 10 mdepth, 50%ofthephoto-inhibitorydoseisatwavelengthslessthan430 nm.1243Thus,foroceanicwaterswemayattributeabout50%ofthephotoinhibitiontoUVandabout50%tovisiblelight.FieldmeasurementsbySmithetal.(1992)intheBellingshausenSeaintheaustral springof1990indicatedthatpri-mary production in the Antarctic marginal ice zone was 6 to 12%inhibited by the increased UVflux resulting fromozone depletion.Inthegiant kelp, Macrocystispyrifera, Clendennenet al. (1996) foundthat doses of UV that reduced photosynthesis by 50% caused a substan-tial reduction in the number of functional photosystemII centres,and impaired energy transfer fromantenna pigments (fucoxanthin,chlorophyll a, chlorophyll c) to photosystemII, but had no effectonphotosystemI,indicatingthatinthisphaeophytespecies,asinspin-ach, photosystem II is the primary site of damage. The 32 kDa D1 proteinof photosystemII, whichcontains the QBplastoquinone-bindingsite,undergoes continuous rapid turnover in the light, at a rate which increaseswith light intensity. Greenberg et al. (1989) found that the quantum yieldfor degradation was highestin the UVB region of the spectrum, suggest-ingthat enhancedbreakdownof this proteinmaybe involvedinthesensitivity of photosystemII to UV.Glacial lakes at higher latitudes, whichwere formedfollowing theretreatoftheglaciersattheendofthelastIceAge, $10 700yearsago,didnot acquiretreecoverintheircatchmentsformanycenturies, andconsequently lacked the supply of dissolved organic matter, with itsassociatedcolour,whichtreeleavesprovide.Onthebasisofpalaeoeco-logical analysis (fossil algal pigments, organic matter content) of thesediments of lakes inBritishColumbia, Canada, Leavitt et al. (2003)concludedthatalgalabundancewasdepressedten-foldbyUVradiationin the first millenniumof lake existence.Over the course of evolution, some aquatic plants have acquiredadegree of protection against UV in the form of the mycosporine-like amino10.2 Photosynthesis and light intensity 355acids(MAAs, Chapter 3),compounds thatabsorbin the UVwithpeaksinthe300to360 nmregion.Theirdistributioninmarineorganismshasbeen reviewed by Shick and Dunlap (2002). They occur in both prokaryo-tic and eukaryotic phytoplankton, but not all species possess them.Bloom-formingdinoflagellateshaveaparticularlyhighcapacitytoformMAAs, and the cellular concentration is many-fold greater in cells grownat high light than in low light.978Some diatom species do not accumulatethese compounds. Five species of Antarctic diatomincultureshowedlittle or no ability to synthesize MAAs, even when exposed to highlevelsofUV, incontrasttotheAntarcticprymnesiophyte, Phaeocystis,which does formthese compounds.281The marine cyanobacterium,Trichodesmium, whichforms extensive surface blooms inoligotrophictropical and subtropical seas, and which is consequently exposed tointense solar radiation, contains particularly high levels of MAAs, amongthehighestknownforfree-livingphytoplankton.1319Amongthemacro-phytes,MAAsynthesisiscommonamongtheRhodophytes,butlesssoamongChlorophytes. Somedeep-water redalgal species, whichwouldnot normally encounter UVB, lack the ability to make MAAs.590Phaeo-phytesdonotsynthesizeMAAs,butmaynotneedtosincebrownalgaecontain UV-absorbing phenolic compounds: in the intertidal brown alga,Cystoseiratamariscifolia, insouthernSpain, Abdala-Diaz et al. (2006)foundthelevel ofphenoliccompoundsinthethallustoincreaseaboutfour-fold as daily integrated irradiance increased from February to June,and then to decrease by nearly 50% as irradiance decreased from June toNovember. In those algae that can make MAAs, there is a generaltendency for the amounts formed to increase with UV exposure. In coralreefs the concentrationof MAAs withinthe coral colonies decreaseswithdepth.337AquaticyellowsubstancesabsorbstronglyintheUV.Wemaythere-fore expect photoinhibitiontobe less apparent inthe more colouredwaters: this has been observed to be the case in highly productive tropicaloceanicwaterswithhighlevelsofgilvin.735Bythesametokenitseemslikely that photoinhibition in the more highly coloured (i.e. most inland)waters iscausedmainlybythevisible(400700 nm) component of thesolar radiation.In addition to that photoinhibition which is due to direct damage to thereactioncentres,andwhichtakessomehourstorepair,thereisanotherkind which comes into operation very quickly in intense light, andwhichisreversedrelativelyquickly(inamatterofminutesratherthanhours) inthedark. This process, whichinvolves reversiblechanges in356 Photosynthesis as a function of the incident lightthecarotenoidcompositionofphotosystemII,referredtoasthexantho-phyll cycle,1482,303,1021canberegardedasauseful adaptiveresponseofthe photosynthetic system to excessively intense light rather than a symp-tomof internal damage. Inhigher plants andmost members of theChlorophyta,andinthePhaeophyta,oneoftheantennapigmentsfeed-ing energy tothe reactioncentre of photosystemII is the diepoxidecarotenoid, violaxanthin. Whenthe photosystems are absorbing lightenergy at a rate approaching the maximum at which the photochemicallygenerated electrons can be used for CO2 reduction, the internal pH of thethylakoidlumenfallsmarkedly.Thisactivatestheenzyme,violaxanthinde-epoxidase,whichremovesfirstoneoftheepoxyOatoms,togivethemonoepoxide, antheraxanthin, andthenremoves theother togivethenon-epoxidecarotenoid, zeaxanthin. Energyabsorbedbyzeaxanthinisnot transferredtothe photosystemII reactioncentre andis, instead,dissipatedasheat.Whenthecellsaretransferredtothedark,theintra-lumenal pHrisesandadifferentenzyme, anepoxidase, isbroughtintoplay,whichbringsabout the oxidation ofzeaxanthin,bythe addition oftwoepoxyOatoms,reconvertingittoviolaxanthin.Innon-greenalgae,xanthophyll cycles that make use of other carotenoids occur. Forexample, inthe Bacillariophyceae, Chrysophyceae, Haptophyceae andEuglenophyta, interconversiontakes place betweenthe monoepoxide,diadinoxanthin(Fig.8.12f ), and the non-epoxide,diatoxanthin.In the algae generally, both phytoplankton and benthic, the proportionof total xanthophyll existinginthe photosyntheticallynon-functional,photoprotectiveform,suchaszeaxanthin,increaseswiththelightinten-sity in their environment, and changes with ambient irradiance during theday.Inthecaseofthefloatingpelagicphaeophyte,Sargassumnatans,inthegulfofMexico, Schofieldet al. (1998)foundthattheviolaxanthin:zeaxanthinratiofellfrom $4at04:00 hto $1atmidday,andthenroseagain to $6 by 22:00 h. The microphytobenthos of tidal mudflats adjuststhe state of its xanthophyll pool when it becomes exposed to full sunlightat low tide. In the mudflats of the estuary of the River Barrow (Ireland),wherethemicrophytobenthiccommunityisdominatedbydiatoms,VanLeeuweet al. (2008) foundthat whereas diatoxanthincouldhardlybedetectedat09:00himmediatelyafteremersion,thediatoxanthin/(diato-xanthin diadinoxanthin) ratio had risen to $0.2 at 10:00 h, and reachedits maximum value of just over 0.3 at midday. In phytoplankton popula-tions fromalargenumber of stations intheArabianSeaandcoastalwatersaroundVancouverIsland(Canada), Stuartet al. (1998)foundastrong inverse relationship between the proportion of non-photosynthetic10.2 Photosynthesis and light intensity 357carotenoids, suchaszeaxanthinanddiatoxanthin, andthechlorophyllconcentration, suggestingthat thesmall cells that arecharacteristicofoligotrophic waters have a higher proportion of photoprotective xantho-phyll pigments. Inphytoplanktonsampledfromdepthsbetween5and75 mintheNWAtlanticOceannearthecontinentalshelfbreak, Prietoetal.(2008)foundasignificantpositivecorrelationbetweenthepropor-tionofphotoprotectivecarotenoidsandtheirradianceofPARtowhichthe cells were exposedat the timeof collection.Depth profiles of phytoplankton photosynthesis, such as those inFig.10.4,determinedbythesuspendedbottlemethod,tendtooveresti-mate the extent towhichphotoinhibitiondiminishes primaryproduc-tion.537,867,855Innaturethephytoplanktonarenotforcedtoremainatthe samedepth for prolongedperiods. Some, such as dinoflagellates andblue-green algae, can migrate to a depth where the light intensity is moresuitable(see}12.6). Eventhenon-motilealgaewill onlyremainat thesame depthfor extended periods under rather still conditions. Windblowingacross awater surface induces circulatorycurrents knownasLangmuir cells, after the eminent physical chemist, Irving Langmuir,who first studied them.765Langmuir cells are horizontal tubes (roll vorti-ces) of rotatingwater, theiraxesalignedapproximatelyparallel tothewind direction (Fig. 10.5). Adjacent tubes rotate in opposite direc-tions andtubes of varyingdiameter canbepresent at thesametime.The simultaneous occurrence of both wind and waves is necessaryfor thegenerationof theseroll vortices,386but evenalight windoversmall-amplitude waves canset themgoing. Cells canhave diametersrangingfromafewcentimetresto hundredsofmetres:withawindspeedof 5 ms1, a typical cell might have a diameter of 10m and a surface speedof1.5 cms1.371MeasurementsbyWelleret al. (1985)fromtheresearchplatformFLIP,driftingoffthecoastofsouthernCalifornia,showedthatwithquitemoderatewindspeeds(mainly18 ms1), downwellingflowstypically between 0.05 and 0.1 ms1were generated. The mixed layer abovethe seasonal thermocline was at the time about 50m deep, and the strongestdownwelling flows were observed between 10 and 35m depth, correspond-ing to the middle region of the mixed layer. Above and below that region,downwelling flows were generally less than 0.05ms1), and there appearedto be no downwelling flow in or below the seasonal thermocline.Thus it will very commonly be the case that phytoplankton are not heldin the intensely illuminated surface layer but are slowly circulatingthroughout themixedlayer. HarrisandPiccinin(1977) point out thatontheGreatLakesofNorthAmericatheaveragemonthlywindspeed358 Photosynthesis as a function of the incident lightthroughout all the winter, and most of the summer period, is sufficient togenerate Langmuir cells, and that the residence time at the surface undersuchconditions will not belongenoughfor photoinhibitiontoset in.Within any given month of course, although the average wind speed maybeenoughtoensureLangmuircirculation,therewillbecalmperiodsinwhichit does not occur. Phytoplankton sampledinwinter fromthewaters of Vineyard Sound (Massachusetts, USA) showed marked photo-inhibitionin bottles heldat surface lightintensities, butwere infact welladapted to the average light intensity that they would actually encounterin this well mixed shallow coastal water.462Photoinhibition of phytoplankton is only likely to be of frequent signifi-canceinwaterbodiesinwhichhighsolarirradiancecommonlyoccursFig. 10.5 Wind-induced circulatory currents (Langmuir cells) in a water body.10.2 Photosynthesis and light intensity 359togetherwithweakwindactivity, leadingtotheformationoftransientshallowtemperature/densitygradients inthesurfacelayer that impedemixingandthustrapphytoplanktonforpart of thedayintheintensenear-surfacelightfield. Awell-documentedexampleisthehigh-altitude(3803 m), low-latitude (16

S) Lake Titicaca (PeruBolivia). Vincent, Nealeand Richerson (1984) found the typical pattern of thermal behaviour to bethat anear-surfacethermoclinebegantoformeachmorning, persistedduring the middle part of the day, and was then dissipated by wind mixingand convective cooling towards evening and through the night. While thenear-surface stratification persisted, phytoplankton photosynthesis in theupper layer was strongly depressed. That this was not an artifact resultingfrom phytoplankton immobilization in bottles was shown by the observa-tionthat the cellular fluorescence capacity(believedtocorrelate withthe number of functional photosystemII complexes) of phytoplank-ton samples taken from the water was also greatly reduced. Neale (1987)estimated the diminution of total water column photosynthesis inL. Titicaca on such days to be at least 20%. Elser and Kimmel (1985) havealsousedmeasurementsofcellularfluorescencecapacityto showthatinreservoirs in temperate regions (southeastern USA) photoinhibition doesoccur in the surface layer under calm sunny conditions.On balance we may reasonably conclude that photoinhibition ofphotosynthesisinthesurfacelayer,althoughitexists,isnotasfrequenta phenomenon as was originally thought. It can significantly reduce arealphotosynthesis under sunny, still conditions, but is likely to be of small ornosignificancewhenthereisevenalight wind. Underestimatesofpri-mary production resulting from the use of stationary bottles are likely tobemoreseriousinoligotrophicwatersrequiringlongincubationtimesthaninproductivewaters.Itshouldbenoted,however,thatcirculationdoesnotbyanymeansalwaysincreaseprimaryproduction:asweshalldiscussmorefullyinthenext chapter, circulationthroughtoogreat adepthcandiminishtotal photosynthesisbykeepingthecellsforsignifi-cant periods in lightintensities too low forphotosynthesis.10.3 Efficiency of utilization of incident light energyOf the light energy incident on the water surface, only a small fraction isconvertedtochemical energyintheformofaquaticplantbiomass.Weshall nowconsider the reasonswhy this isso.360 Photosynthesis as a function of the incident lightThe first mode by which energy is lost is reflection at the surface. As wesawearlier (}2.5, Table2.1), however, suchlosses aresmall. For thatrangeof solarangles at whichmost aquaticprimaryproductiontakesplace, only 2 to 6% of the incident light is lost by surface reflection. Thusthe main causes of inefficiency of light utilization are to be found beneaththe watersurface.In shallow water bodies (very shallow in coloured and/or turbid waters;moderately shallow in clear waters) substantial amounts of light reach thebottom.Someisabsorbed,somereflected,theproportiondependingonthe optical characteristics of the substrate. Of the bottom-reflected light, afractionwillsucceedinpassingupthroughthewatercolumnagainandescaping through the surface. Thus in shallow waters, bottom absorptionandbottomreflection,followedbysurfaceescape, aremechanismspre-ventingutilizationofsomeofthelightinphotosynthesis. Thelightlostcan be anything from a trivial proportion up to nearly 100% in, say, veryshallowclearwateroverawhitesandybottom.Ourmainconcernhere,however, is with optically deep waters in which the fraction of the incidentlightthatpenetratestothebottomisnegligible.Insuchwaters,mostofthe light that penetrates the surface is absorbed within the aquaticmedium. A fraction of the light, however, usually small, is back-scatteredupwardswithinthewater(see }6.4) andsomeofthissucceedsinpassingupto, andoutthrough, thesurface. Combiningdatafortheirradiancereflectance just beneath the surface (}6.4) with the fact that about half theupwellingfluxisreflecteddownagainatthewaterairboundary,41wemayconcludethattheamountofincidentPARlostinthiswayis1to2.5%in oceanic waters, 1 to 10%in inland waters of lowto highturbidityandaslittleas0.1to0.6%inwaterswithintensecolourbutlow scattering.Proportion of incident light captured by phytoplanktonA major factor limiting conversion of solar energy to chemical energy byphytoplanktonis,aswaspointedoutbyClarke(1939),thecompetitionfor radiant energy by all the non-living components of the water. We sawinChapter 3that the different components of the aquatic mediumwater, solublecolour, triptonandphytoplanktoneachaccount foraproportionofthetotal lightabsorbedbythewaterbody. WealsosawthattoobtainanaccurateestimateoftheamountofPARcapturedbyeachcomponentseparately,calculationsshouldbecarriedoutusingtheabsorptioncoefficients for aseries of narrowwavebands followedby10.3 Efficiency of utilization of incident light energy 361summation across the photosynthetic spectrum. A useful approximation,however, is tofirst consider thetotal PARandthenassumethat therelative rates of absorption of light by the different components oftheaquaticmediumareinproportiontotheirindividual contributionstothetotal vertical attenuationcoefficient fordownwardirradianceofPAR,in accordancewitheqn 9.10KdPAR KwKGKTRKPHFormany, perhapsmost, watersofinteresttolimnologistsandmarinebiologists, thisassumptionwill not beunacceptablyfarfromthetruthbut it does presuppose that absorption rather than scattering is thedominant contributortoeachofthepartial attenuationcoefficientsonthe right-handside of eqn9.10. For Kw(water), KG(gilvin) andKPH(phytoplankton) this will be true, and when the tripton fraction isstronglycoloured(e.g. byinsolublehumicmaterial)itwill alsobetruefor KTR. If,however,the tripton fraction ishighin concentrationsothatKTRishigh, but consistsof mineral particleslowinintrinsiccoloursothatKTRismadeupmainlyofthescatteringcontribution(see } 6.8,eqn6.31), thentheassumptionthatrelativeratesofabsorptionarepropor-tional tothepartial vertical attenuationcoefficientswill beseriouslyinerror.Nevertheless, for waters other than the kind we have just described, thefraction of the total absorbed light that is captured by the phytoplanktonis, with thisapproximate treatment,given byKPHKdPARChlkcKdPARChlkcKWKG KTR ChlkcChlkcKNPChlkc10:12whereKNP(whichisequaltoKw KG KTR)istheverticalattenuationcoefficient due to all non-phytoplankton components, [Chl ] is the phyto-planktonconcentration(mgchl am3) andkcis the specific verticalattenuationcoefficient perunitphytoplanktonconcentration. Thustheextent to which the phytoplankton succeed in competing with othercomponents of the mediumfor the available quanta depends ontherelative size of [Chl ]kcandKNP. The range of possibilities is limitlessbut we shall consider a few specific examples. We shall take0.014 m2mg1asatypical mid-rangevalueofkc(seeTable9.1). Table10.2listssomevaluesfortheproportionofabsorbedPARcapturedbyphytoplanktoninanumber of hypothetical (but typical) water bodiesrangingfromverypureoceanicwaterwithKNPnotmuchgreaterthanthat due to pure water (KW0.03 0.06 m1), to a quite highly coloured,362 Photosynthesis as a function of the incident lightbut productive, inlandwater. Veryapproximatethoughthese calcula-tionsare, theydoshowthattheshareoftheavailablequantacollectedby the phytoplankton can vary from a few per cent in the less productivewaters, to well over 40%in highly productive systems. They alsoemphasize the point that quite dilute algal populations cancollect asubstantial proportionofthequanta, providedthebackgroundabsorp-tionislow.Somecalculationsof thistypehavebeencarriedout forreal waterbodies. DubinskyandBerman(1981) estimatedthat intheeutrophicLakeKinneret(SeaofGalilee)theproportionoftheabsorbedquantacapturedbyphytoplankton(mainlythedinoflagellateCeratium)variedfromabout4to60%asthealgal concentrationrosefromabout 5to100 mg chl a m3. For the eutrophic, blue-green-algal-dominatedHalstedBay, LakeMinnetonka, USA, Megardet al. (1979)calculatedTable10.2Proportion of total absorbed PAR captured by phytoplanktonin idealized water bodies of different types. Calculations carried out usingeqn 10.12 and assuming kc0.014 m2mg chl a1. KNP is the verticalattenuation coefficient due to all non-phytoplankton material.Type ofwater bodyKNP(m1)Phytoplankton(mg chl a m3)Proportion ofabsorbed PARcaptured byphytoplankton(%)Proportion ofabsorbed PARcaptured bynon-phytoplanktonmaterial (%)Clear oceanic 0.08 0.2 3.4 96.60.5 8.0 92.01.0 14.9 85.1Coastal 0.15 1.0 8.5 91.52.0 15.7 84.34.0 27.2 72.8Clear lake,limestonecatchment0.4 4.08.012.012.321.929.687.778.170.4Productivelake,colouredwater1.0 8.016.032.064.010.118.330.947.389.981.769.152.7Oligotrophiclake,colouredwater2.0 1.02.04.00.71.42.799.398.697.310.3 Efficiency of utilization of incident light energy 363thattheproportionofabsorbedPARcollectedbythealgaerosefromabout 8to80%as the phytoplanktonconcentrationincreasedfromabout 3 to100 mg chl a m3. Fromthe data of Talling (1960) theseworkersestimatedthatforLakeWindermere(Asterionella-dominated),England, whichhasrelativelylowbackgroundabsorption, thepropor-tionofabsorbedPARcollectedbythealgaerosefromabout5to25%over the population density range of 1 to 7 mg chl a m3. For theeutrophic, shallow(andthereforeturbid) LoughNeagh, Ireland, Jew-son(1977)estimatedthatphytoplanktonaccountedforabout20%ofthe absorbedlight at the lowest populationlevel (26.5 mg chl a m3)and50%at thehighest (92 mg chl a m3). InmesotrophicLakeCon-stance(Germany), Tilzer (1983) calculatedfractional light absorptionbyphytoplanktontovarybetweenabout 4and70%overatwo-yearperiod in which chlorophyll a levels varied between about 1 and30 mg m3(Fig. 11.8).Aswesawinthepreviouschapter, inthesea, wherethewatersaredeepandusuallywithlittledissolvedyellowcolour,andthelightfieldwithincreasingdepthbecomesincreasinglyconfinedtotheblue-green(400550 nm) spectral region, thespecificeffectiveabsorptioncoeffi-cient of the phytoplankton for PAR, " afz (}9.4 and below), alsoincreases withdepth. Where, as is normally the case inthe ocean,there is alayer of increasedphytoplanktonconcentration(the deepchlorophyll maximum, }11.1) near thebottomof theeuphoticzone,the combination of increased pigment concentration and enhancedlight-harvestingefficiencyleadstoagreat increaseintheproportionofthetotal lightabsorptionthatiscarriedoutbythephytoplankton.Inthe Pacific Ocean, off southeasternJapan, Kishinoet al. (1986)foundthe fractional light absorption by phytoplanktontoincreasefrom1.7%at the surfaceto40% in themiddle of the deep chlorophyllmaximumat75 m.As we have just discussed, the usefulness of agivenlight fieldforphotosynthesis is not simplyafunctionof thetotal intensityof PAR,butisverymuch determinedbyhowwellthespectral distributionofthePARmatches theabsorptionspectrumof thephytoplanktonor otheraquaticplants.Morel(1978,1991)hasintroducedtheconceptofphoto-syntheticallyusableradiation, or PUR, whichmaybe thought of as amodified PAR obtained by weighting the actual PAR across its spectrumforabsorbabilitybythephytoplankton. Thiscanbeachievedbymulti-plyingthePARineachnarrowwavebandbysomedimensionlessquan-tityproportional tophytoplanktonabsorptioninthat waveband, and364 Photosynthesis as a function of the incident lightthen summing across the spectrum. As a suitable dimensionless quantity,Morel in fact chose the ratio of the phytoplankton absorption coefficientin any given waveband to the maximum absorption coefficient which iscommonlythevalueit hasat about 440 nm. Photosyntheticallyusableradiationcan thus be defined byPURz 700400E0l;zapl;zaplmax;zdl 10:13whereap(l, z) andap(lmax, z) aretheabsorptioncoefficients at wave-lengths l and lmax (wavelength of maximum phytoplankton absorption),respectively,ofthephytoplanktonpopulationexistingatdepthz m,andE0(l, z) is the scalar irradiance per unit bandwidth (nm1) at wavelength land depth z m. From the definition of the effective absorption coefficient," ap(z), of the phytoplankton for the whole PAR waveband (eqn 10.16, seebelow)it followsthatwe can also writePURz PARz" apzaplmax;z10:14Efficiency of conversion of absorbed lightOnce the light energyis absorbedbythe chloroplast pigments of thephytoplankton or aquatic macrophytes it is used, by means of the photo-synthetic fixation of CO2, to generate useful chemical energy in the formofcarbohydrate.Weshallnowconsidertheefficiencyofthisconversionof excitation energyto chemical energy.Anupper limit tothe efficiency is imposedby the nature of thephysical andchemical processesthatgoonwithinphotosynthesis. WesawinChapter8thatthetransferofeachhydrogenatomfromwaterdown the electron transport chain to NADP requires two photons, eachdrivingadistinct photochemical step. Thereductionof onemoleculeof CO2tothe level of carbohydrate uses four hydrogenatoms (2 NADPH2) andsorequires eight photons. Puttingit another way, toconvertonemoleofCO2toitscarbohydrateequivalent(onesixthofamoleof aglucoseunit incorporatedinstarch) requires not less thaneight molar equivalents, i.e. 8 moles of photons. The energy in a photonvaries with wavelength (e hc/l) and so we shall obtain an average valueby takingadvantage of the observationbyMorel andSmith(1974)that forawiderangeof watertypes2.5 1018quantaof underwater10.3 Efficiency of utilization of incident light energy 365PAR1 J, with an accuracy of better than 10%. We may thus regard typicalunderwaterlight ascontaining0.24MJ(megajoules) of energyper molephotonsandso8molesofphotonsisequivalentto1.92 MJ.Theincreaseinchemical energy associatedwiththe photosynthetic conversionof one moleof CO2to its starch equivalent is 0.472 MJ. Thus, of the light energy absorbedanddeliveredtothereactioncentres,about25%isconvertedtochemicalenergy as carbohydrate and this is the maximum possible efficiency.To equate the plant biomass to carbohydrate is an oversimplification, sincethe aquatic plants also contain protein, lipids and nucleic acids, none of whichconformcloselyintheiroverallcompositiontoCH2O.Thebiosynthesisofthesesubstancesrequiresadditional photosyntheticallygeneratedreducingpower andchemical energy inthe formof NADPH2andATP, andsorequiresadditional light quanta per CO2 incorporated. The true minimum quantumrequirement per CO2for growing cells is likely tobe about 10 to12 rather than8,1099which brings the maximumefficiency down to 16 to 20%. Thus the bestefficiencywecanhopeforintheconversionof absorbedlight energytochemical energy in the form of new aquatic plant biomass is about 18%.The conversionefficiencyor quantumyieldactually achievedbyagivenphytoplanktonpopulationormacrophytecanbedeterminedfrommeasurements of thephotosynthetic rateandtheirradiance, providedthat information on the light absorption properties of the plant material isavailable. Usingtheabsorptionspectrum, 400to700 nm, ratesoflightabsorption for a series of wavebands can be calculated and summed. Forexample, the rate of absorption of PARby phytoplankton per unitvolume of mediumat any givendepth, z, isdpzdv700400apl;z E0lz dl 10:15whereap(l, z)istheabsorptioncoefficientatwavelength lofthephyto-planktonpopulationexisting at depthz m, andE0(l, z) is the scalarirradianceper unit bandwidth(nm1) at wavelength l and depth z m.Auseful concept here is that of the effective absorptioncoefficientof the phytoplankton forthe whole PAR waveband. Thisis defined by" apz 700400apl;z E0l;z dl700400E0l;z dl10:16and as an alternativeto eqn 10.15 wecan thereforewrite366 Photosynthesis as a function of the incident lightdpzdv " apz E0PAR;z 10:17The specific absorption coefficient of the phytoplankton for PAR," af*(z),isdefinedbysubstitutingaf*(l,z)forap(l,z)ineqn10.16:also" ap(z) [Chl] " af*(z)so thatdpzdvChl" afz E0PAR;z 10:18In any attempt to calculate the rate of energy absorption by phytoplank-ton(and, byimplication, quantumyieldseebelow) witheqn10.18,using estimatedvalues of " af*(z) the fact that, as we sawearlier, theeffectivespecificabsorptioncoefficient of thephytoplanktonfor PARcan vary markedly withdepth must be takeninto account.It is often more convenient to work in termsof downward,rather thanscalar, irradiance, but E0 is always greater than Ed (see Fig. 6.10, }6.5) by afactor that depends on the angular structure of the light field at that particu-lar depth. Following Morel (1991) we shall indicate this geometrical cor-rectionfactorbyg. Thiscorrectionisnottrivial: forwavelengthsinthephotosynthetically important 400 to 570 nm region, and for phytoplanktonconcentrations in the 0.1 to 1.0 mgchl a m3range, Morel (1991) calculatedvalues of g varyingbetween 1.1and1.5. Using thegeometrical correctionfactorwecannowwriteanotherexpressionfortherateofabsorptionofPAR by phytoplankton per unit volume of medium at depth z m, namelydpzdv700400apl;z Edlz gl;z dl 10:19whereEd(l, z)isthedownwardirradianceperunitbandwidth(nm1)atwavelength l and depth z m.An alternative approach starts from the fact that the rate of absorptionof radiantenergy per unitvolumeat depth z m is givenbydzdvKE~Ez 10:20where~Ez isthenet downwardirradianceat depthz mandKEisthevertical attenuation coefficient for net downward irradiance. From this itcan readily be shown thatdzdvKdEdz 1 RzKuKd %KdEdz1 Rz 10:2110.3 Efficiency of utilization of incident light energy 367where Ku is the vertical attenuation coefficient for upward irradiance and(asisusuallythecase)Ku %Kd,andR(z)isirradiancereflectance(Eu[z]/Ed[z]).Ifwechoosetoignorethecontributionoftheupwellingfluxareasonable approximation in most marine waters, with reflectance valuesof only a few per cent, but not in turbid waters then we can writedzdv%KdEdz 10:22for the total rate of absorption of energy per unit volume, as a function ofdownwardirradiance. Tocalculatetherateofabsorptionofenergybyphytoplanktonwemakeuseofthefactthatinanygivenwavebandtheproportion of the absorbed energy that is captured by the phytoplanktonisap(l, z)/at(l, z), theratioof theabsorptioncoefficient duetophyto-plankton to the total absorption coefficient, at that wavelength. The rateof absorption of PAR by phytoplankton per unit volume of medium, as afunctionof downward irradianceis therefore givenbydpzdv700400apl;z=atl;z Kdl;z Edl;z dl 10:23where Kd(l, z) is the vertical attenuation coefficient for downward irradi-anceatwavelength landdepthz m. Ineqns10.15, 10.16and10.19wecan,ofcourse,replaceap(l,z)with[Chl ](z)af*(l,z),theproductofthephytoplanktonconcentration(mg chla m3)andthespecificabsorptioncoefficient(m2mg chla1)atwavelength l,ofthephytoplanktonpopu-lationpresentat depth z m.Toarriveat anaccuratedeterminationof photosyntheticefficiency,thespectral variationbothof thelight fieldandof absorptionbythebiomassshouldbetakenintoaccount, alongthelinesindicatedabove,andnumerousworkershavesoughttodothis.111,244,376,727,728,778,940,1190Useful informationcan, however, still beobtainedfromphotosynthesismeasurementscombinedwithbroad-bandirradiancedata. Since, aswesaw earlier, the fraction of the total absorbed PAR that is captured by thephytoplanktonisapproximately[Chl ]kc/Kd(PAR), thenfromeqn10.22we can writedpzdv%ChlkcEdPAR;z 10:24for the rate of absorptionof light energybyphytoplanktonper unitvolume,atdepthz m.Estimatesofenergyabsorptionbyphytoplankton(andconsequentlyofquantumyieldseebelow) madewitheqn10.24368 Photosynthesis as a function of the incident lightcan, however, be grossly inaccurate if the variation of kc with the type ofphytoplankton present, the background colour of the water and thedepth(kcvaryingwithdepthinasimilarmannerto" af) arenot takeninto account.ItisusefulindealingwiththepresenttopictohaveaspecificsymbolfortherateofabsorptionofPARbyphytoplanktonperunitvolumeofmediumat a givendepth.We hereintroduce the symbol w, defined byz dpzdz10:25where w(z) can have the units Wm3, or MJ m3h1, or quanta (or mmolesphotons) m3s1.Wecan,inaddition,define w*(z)tobethespecificrateof absorptionof PARbyphytoplanktonperunit volumeat depthz m,i.e. therateperunitphytoplanktonconcentration, expressedintermsofmgchl a m3. Thus w(z) [Chl ] w*(z), and w*(z) has the units Wmg chl a1,or quanta (or mmoles photons) s1mgchl a1. For any given aquaticsystem, w(z) is determinedbyusingoneor other of eqns 10.15, 10.17,10.23 and 10.24, or some equivalent procedure.Toobtaintheenergyconversionefficiencyatagivendepthwedividethe rate of accumulation of chemical energy per unit volume at that depthby the rate of absorptionof light energy by phytoplanktonper unitvolume. Given a specific photosynthetic rate of P* (CO2) moles CO2 fixedmg chl a1h1, and an increase in chemical energy of 0.472 MJ associatedwiththefixationofeachmoleofCO2,thentherateofaccumulationofchemical energyperunit volumeis0.472[Chl ] P*(CO2) MJm3h1.Dividingby w(z) we obtainthe conversion efficiencyec0:472ChlPCO2wz0:472 PCO2wz10:26w(z) beingexpressedinMJ m3h1(quantameasurementscanbecon-vertedusing2.5 1024quanta 1 MJ, seeabove). Alternatively, ifP*isexpressed in terms of mg carbon fixed mg chl a1h1, P* (C), then, sincethereisanincreaseinchemicalenergyof3.93 105MJassociatedwiththe fixation of 1 mg C, the conversion efficiency is givenbyec3:93 105ChlPCwz3:93 105PCwz10:27Another way of expressing the efficiency of conversion of absorbedlightenergy to chemical energy by aquatic plants is the quantum yield, f. Thisis definedtobe the number of CO2molecules fixedinbiomass per10.3 Efficiency of utilization of incident light energy 369quantum of light absorbed by the plant. Given the quantum requirementper CO2 fixed, imposed by the mechanism of photosynthesis (see above),it follows that the quantumyieldcouldnever be greater than0.125,andforgrowingcells,evenunderidealconditions, isunlikelytoexceedabout 0.1. Quantumyieldandper cent conversionefficiency are, ofcourse, linearly related. Allowing 0.472 MJ chemical energy per CO2 fixedand 0.24 MJ per mole photons of underwaterPAR,we arrive atec 1:97f 10:28Equations corresponding to 10.26 and 10.27 can be written for the calcula-tion of quantum yield from w(z) or w*(z) and specific photosynthetic ratefChlPCO2wzPCO2wz10:29fChlPC12 000: wzPC12 000 : wz10:30w(z) in theseequations has the units moles photons m3hl.Thequantumyieldattainedbyanaquaticplant isafunctionof thelight intensity to which it is exposed. That this is so is apparent from thevariation of specific photosynthetic rate with irradiance (Fig. 10.3).Ignoringforthemoment anychangesinchloroplast shapeorpositionwith light intensity, we may assume that the rate of absorption of quantais proportional tothe incident irradiance. Thus, at any point inthephotosynthesisversusirradiancecurvethevalueofP/Ed(seeFig. 10.3)is proportionalto the quantum yield.For aplant tobe able tomake efficient use of light quantabeingabsorbed at a given rate, the activity of the electron transfer componentsinthethylakoidmembranesandoftheenzymesofCO2fixationinthestromamust bothbehighenoughtoensurethat theexcitationenergycollected by the light-harvesting pigments is utilized as fast as it arrives atthereactioncentres. Ifthissituationexists, thenamoderateincreaseinlightintensity, causingaproportionateincreaseinquantumabsorptionrate, leadstoacorrespondingincreaseinthespecificrateofphotosyn-thesis. In the initial, linear, region of the P versus Ed curve this is what ishappening. Over this range of intensity, P/Edis constant andhas itshighestvalue,indicatingthattheplantsareachievingtheirhighestcon-version efficiency and quantum yield. If the absorption characteristics oftheplant areknown, thenthismaximumvalueof P/Edcanbeusedtocalculate fm, the maximum quantumyield.370 Photosynthesis as a function of the incident lightAstheincidentlightintensityisfurtherincreased,therateofabsorp-tionof quantareaches thepoint at whichexcitationenergybegins toarriveat thereactioncentresfasterthanit canbemadeuseof bytheelectrontransfercomponentsand/ortheCO2fixationenzymes. Atthisstagesomeoftheadditionalabsorbedquanta(overandabovethosethesystemcanreadilyhandle)areutilizedforphotosynthesis,andsomearenot,theenergyofthelatterbeingeventuallydissipated, mainlyasheat.For this reason, inthis range of light intensity, increments inEdareaccompaniedbylessthancommensurateincreasesinP,i.e.theslopeofthe curve progressively diminishes, until eventually the point is reached atwhichDP/DEdbecomes zero. Inthis light-saturatedstate, theelectrontransfer and/or CO2 fixation enzymes (most likely, the latter) are workingas fast as they are capable, and so any additional absorbed quanta are notused for photosynthesis at all. From the end of the linear region throughtothelight-saturatedregion,sincephotosyntheticratedoesnotincreaseinproportiontoirradiance(P/EdsteadilyfallsFig.10.3)thequantumyieldandconversionefficiencynecessarilyundergoaprogressivefall invalue. This is accentuated further if, at even higher light intensities,photoinhibitionsetsin.Ifthecellscontainphotoprotectivecarotenoids,inwhichabsorbedlight energyis dissipatedas heat rather thanbeingtransferred to the reaction centre, then to the extent that these capture theincident light, the quantum yield must be proportionately reduced at anylightintensity.The characteristic manner in which P varies with Edcan, as wesaw earlier, be represented mathematically in a number of different ways(eqns 10.8, 10.9, 10.10, 10.11). Since quantum yield and P/Ed are linearlyrelated, thenforeachparticularformof thefunction, P f (Ed), therewill be a corresponding expression for quantum yield as a function of Ed,i.e. f Constant.Ed1. f (Ed). Usingthetanhform(eqn10.9) Bidigareet al. (1992) arrivedatffmEkEPAR;ztanhEPAR;zEk 10:31and using the exponentialform (eqn 10.11) we obtainffmEkEPAR;z1 eEdPAR; zEk 10:32The consequence in natural water bodies of the decrease in quantum yieldwith increasing light intensity is that quantumyield and conversionefficiency vary markedly with depth, the general tendency being, as might10.3 Efficiency of utilization of incident light energy 371be expected, for f and ec to increase with depth.330,940Quantum yields inthe surface layer in the middle period of the day, when irradiancevaluesaregenerallyabovetherangecorrespondingtothelinearpartofthe P versus Ed, curve, are usuallybelow fm.Morel (1978)calculatedthequantumyieldataseriesofdepthsfrom14CO2 fixation, chlorophyll and light data for a variety of oceanic watersfromthehighlyoligotrophicSargassoSeatotheproductivewaters oftheMauritanianupwellingarea. Inmostcasesfincreasedwithdepth,i.e. with decreasing irradiance. On average, the f values for greeneutrophicwaterswerehigher thanthoseobservedinblueoligotrophicwaters. In the surface layers the f values were mainly in the range 0.003 to0.012 (equivalent to ec values of 0.62.4%). Kishino et al. (1986) found, inthePacificOceansoutheastofJapan,thatquantumyieldsofphotosyn-thesis were0.005to0.013at thesurface, 0.013to0.033at that depth(1020 m) where photosynthesis reachedits maximum ratein the surfacemixed layer, and 0.033 to 0.094 in the deep chlorophyll maximum($70 m).If,astheseauthorssuggest, wereduceallthesevaluesby20%,asanapproximatecorrectionfactorforthefactthattheyarebasedonmeasured irradiance, rather than scalar irradiance, values then we obtainquantumyields of 0.004 to0.01, 0.01 to 0.026, and 0.026 to 0.075,respectively.In oligotrophic Lake Superior, Fahnenstiel et al. (1984) found quantumyieldstobeverylow, $0.003,at thesurface,andtoincrease with depth,reachingmaximumvaluesof0.031to0.052(correctedforscalarirradi-ance)at15to25 m.DubinskyandBerman(1981)estimatedthatduringthespringPeridiniumbloominLakeKinneret (Seaof Galilee), ecrosefromabout 5%at thesurfaceto8.5%at 3 m. Inlatesummer, withamuchlower populationof different (green) algae, ecwas 2.5%at thesurfacebut roseto about 12% at 5 to 7 m.The maximumquantumyieldthat aphytoplanktonpopulation, oraquatic macrophyte, can exhibit, fm, is a parameter of considerabletheoretical andecological interest. Ontheassumption(seeabove) thatin the linear region of the Pversus Ecurve the cells are achievingtheirmaximumefficiency, estimatesoffmarenormallyobtainedfromthe observed slope, P/E, commonly referred to as a, in this regionof the curve.From the equations for f it follows that fm should be proportional toa. For example, if E is E0, then from eqns 10.29, 10.25 and 10.18 it followsthat fm a/" af*. If Eis Ed, thenfromeqns 10.29, 10.25and10.24itfollows that fma/kc. The photosynthetic process imposes by its372 Photosynthesis as a function of the incident lightessentialnatureamaximumvaluefor fmof $0.1,forallphotosyntheticsystems. Onthebasisofacritical analysisofliteraturedata, Bannisterand Weidemann (1984) have concluded that published values of in situ fminexcessof0.10arealmostcertainlyinerror. Thefactthata fmvalue$0.1isonewhichanyplantspeciesmightinprincipleachieve,andalsothat aislinearlyrelatedto fm(since a " af*fmorkc fm), hasarousedexpectations that ashouldnot vary markedly for a givenspecies indifferent environments, or fromone species toanother. Suchexpect-ations, however, ignoretheextent towhichtheproportionalityfactor," af* or kc, can vary. We saw earlier (Chapter 9) how markedly" af* varieswith the size and shape of the cells or colonies, for example decreasing asthe absorbing units become largeror more intensely pigmented. Taguchi(1976),fromstudiesonsevenspeciesofmarinediatom,found,asmightbe predicted, that a decreased with increasing size of the cells. Also, since" af* andkcare expressedper unit chlorophyll a, thenthey canvarymarkedlyinvalueinaccordancewithvariationinthetypeofaccessoryphotosyntheticpigmentspresent,andtheirratiotochlorophylla(} 9.5):the resulting changes in shape of the absorption spectrummarkedlyinfluencetherateofenergycapturefromthewhitelightfieldsnormallyusedinthedeterminationof a.WelschmeyerandLorenzen(1981),inacomparison of six species of marine phytoplankton growing exponentiallyunder identical conditions, foundthat therewerenosignificant differ-ences in f, but there were significant differences in a: these they attributedto differences in the lightabsorptionefficiency per unit of chlorophyll.Anotherprobleminthedeterminationofavalues, particularlywhenwe wish to compare different data sets from the literature, is that there isnogenerallyacceptedstandardfor the light source tobe usedinitsmeasurement. Someworkersusenatural sunlight, othersusetungstenhalogenlamps, whilesomewill uselamps fittedwithbluefilters. Thespectral distribution of the incident lightwill be quite markedly differentin all three cases, with the result that for any given phytoplanktonpopulation, withagivenabsorptionspectrum, awill have adifferentvalue foreach lightsourcebecausethe effective specificabsorption coef-ficient, " af*, forthe incident PAR will be differentfor each lightsource.Thus, even if we did not expect fm to vary dramatically with species orenvironment,weshouldnotexpectthesameconstancyof a,becauseofthe variability of" af* and kc. Unfortunately this variability in" af* and kc,andtheconsequentuncertaintyintheirvalues,makesthedeterminationof fminnatural populations, froma, difficult. Thebest estimates areundoubtedly those based on full spectral data for phytoplankton10.3 Efficiency of utilization of incident light energy 373absorption and the underwater light field, and combining eqn 10.29 withw(z) values fromeqns 10.15, 10.19 or 10.23.Sometypical values of afor natural phytoplanktonpopulations, inthe units mg Cmg chl a1h1(mmoles photons m2s1)1, are: 0.05(range 0.0070.15) for NovaScotiacoastal waters,10630.06for nano-plankton(50

S 1.95 32Global oceanCZCS data 4550 826SeaWiFS data 5255 126111.5 Photosynthetic yield per unit area 451and the impossibility of deep circulation of the phytoplankton (below thecriticaldepth)arealsolikelytocontributetotheenhancedproductivity.Inoneof theworlds oceans theArctic total primaryproductionappears tobeincreasing, becauseof theincreasedareaof openwaterresultingfrom globalwarming.1029Inthecaseof inlandwaters, oligotrophic(nutrient-poor) lakeshavephytoplankton primary productivities usually in the 4 to 25 g C m2yr1rangewhereas eutrophic(nutrient-rich) lakes typicallyfix75to700gCm2yr1,520,1143although,forthesalineRedRockTarninAustralia,anannual productionof 2200gCm2hasbeenreported.520Hammerpresentsanextensivecompilationofproductivitydataforinlandwatersin the 1980 IBP report.781Brylinskys survey of a large number of lakes allover the world for the IBP report indicated that phytoplankton product-ivity is negatively correlated with latitude. This can reasonably beexplained in terms of the diminution of annual solar radiation input withincreasing latitude.We have notedearlier that, by bringing about the transfer of thegreenhouse gas, carbon dioxide, fromthe atmosphere to the deepocean(thebiological pump), marinephytoplanktonproductivityplaysa major role in the regulation of global climate. There is another import-ant mechanism of climate control in which phytoplankton mayplay a role, namely, cloud formation. Many classes of unicellular marinealgaeprymnesiophytes, dinophytes, prasinophytes, somediatomsandchrysophytes854producelargeamountsofdimethylsulfoniopropionate(DMSP),whichactsasanosmolyte.Thisisreleasedintothesea,eitherpassively by leakage, or actively by zooplankton grazing or viral lysis, andis then broken down to dimethyl sulfide (DMS) by microbial action. TheDMS escapes from the ocean, and is the main biogenic source of reducedsulfurtotheatmosphere,77whereitisoxidizedtosulfateintheformofsubmicronaerosol particles, whichactascondensationnuclei forwatervapour, thuspromotingcloudformation. ItwassuggestedbyCha