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Year: 2015

Sun-induced fluorescence - a new probe of photosynthesis: First maps from the imaging spectrometer HyPlant

Rascher, Uwe ; Alonso, L ; Burkart, Andreas ; Cilia, C ; Cogliati, S ; Colombo, R ; Damm, Alexander ; Drusch, Matthias ; Guanter, Luis ; Hanuš, Jan ; Hyvärinen, Timo ; Julitta, T ; Jussila, Jouni ; Kataja, Kari ; Kokkalis, P ; Kraft, S ; Kraska, Thorsten ; Matveeva, Maria ; Moreno, Jose ; Muller, Onno ; Panigada, C ; Pikl, M ; Pinto, Francisco ; Prey, L ; Pude, Ralf ; Rossini, Micol ; Schickling, Anke ; Schurr, U ; Schüttemeyer, D ; Verrelst, Jochem ; Zemek, F

Abstract: Variations in photosynthesis still cause substantial uncertainties in predicting photosynthetic CO2 uptake rates and monitoring plant stress. Changes in actual photosynthesis that are not related to greenness of vegetation are difficult to measure by reflectance based optical remote sensing techniques. Several activities are underway to evaluate the sun-induced fluorescence signal on the ground and on a coarse spatial scale using space-borne imaging spectrometers. Intermediate-scale observations using airborne-based imaging spectroscopy, which are critical to bridge the existing gap between small-scale field studies and global observations, are still insufficient. Here we present the first validated mapsof sun-induced fluorescence in that critical, intermediate spatial resolution, employing the novel airborne imaging spectrometer HyPlant. HyPlant has an unprecedented spectral resolution, which allows for the first time quantifying sun-induced fluorescence fluxes in physical units according to the Fraunhofer Line Depth Principle that exploits solar and atmospheric absorption bands. Maps of sun-induced fluorescence show a large spatial variability between different vegetation types, which complement classical remote sensing approaches. Different crop types largely differ in emitting fluorescence that additionally changes within the seasonal cycle and thus may be related to the seasonal activation and deactivation of the photosynthetic machinery. We argue that sun-induced fluorescence emission is related to two processes: (i) the total absorbed radiation by photosynthetically active chlorophyll and (ii) the functional status of actual photosynthesis and vegetation stress.

DOI: https://doi.org/10.1111/gcb.13017

Posted at the Zurich Open Repository and Archive, University of Zurich ZORA URL: https://doi.org/10.5167/uzh-117074 Journal Article Accepted Version

Originally published at: Rascher, Uwe; Alonso, L; Burkart, Andreas; Cilia, C; Cogliati, S; Colombo, R; Damm, Alexander; Drusch, Matthias; Guanter, Luis; Hanuš, Jan; Hyvärinen, Timo; Julitta, T; Jussila, Jouni; Kataja, Kari; Kokkalis, P; Kraft, S; Kraska, Thorsten; Matveeva, Maria; Moreno, Jose; Muller, Onno; Panigada, C; Pikl, M; Pinto, Francisco; Prey, L; Pude, Ralf; Rossini, Micol; Schickling, Anke; Schurr, U; Schüttemeyer, D; Verrelst, Jochem; Zemek, F (2015). Sun-induced fluorescence - a new probe of photosynthesis: First maps from the imaging spectrometer HyPlant. Global Change Biology, 21(12):4673-4684. DOI: https://doi.org/10.1111/gcb.13017

2 This article is protected by copyright. All rights reserved. This article isprotected rights by All copyright. reserved. 10.1111/gcb.13017 doi: as article this cite Please Record. of Version the and version this between differences to lead may which not process, has proofreading and but pagination review typesetting, peer copyediting, the full through undergone been and publication for accepted been has article This Accepted Date :26- Received :29-Nov-2014 Date U. Rascher spectrometefrommaps imaging the Sun Advances :Technical Article type M. Drusch Kokkalis M. Pikl Schüttemeyer [6] [5] [4] [3] [2] [1] +49-(0)2461-61fax. 2492 * [10] [9] [8] [7] Correspondence to: U. Rascher, e-mail [email protected], tel. +49-(0)2461-61 2638; [email protected],Rascher, Correspondence tel.+49-(0)2461-61 U. e-mail to:

Accepted Article

Institute for Space Sciences, Free University of Berlin, Carl-Heinrich-Becker- Berlin, of University Free Sciences, Space for Institute European (ESA), Keplerlaan ESTEC, Space Agency 1,2200AG Netherlands Noordwijk, Switzerland Studi degli Università Zurich, 8057 190, Winterthurerstrasse Zurich, of University Laboratories, SensingRemote DISAT, Lab, Dynamics ItalyMilano-Bicocca, Milano, Environmental of Sensing Remote 50, 46100Burjassot, Valencia, Spain Moliner, Dr Valencia, of University Thermodynamics, and Physics Earth of Department GermanyLeo-Brandt-Str., 52425Jülich, GmbH, Sciences,Institute Jülich Plant Bio-IBG-2: and Forschungszentrum of Geosciences, Klein-Altendorf 3, 53359 Rheinbach, Germany Klein-Altendorf Rheinbach, 3,53359 Germany LabField Agricultural Bonn, CampusKlein-Altendorf, Faculty,University of Observatory of Athens, Athens, 15236, Greece ObservatoryAthens, Athens, 15236,Greece of InstituteAstronomy,Astrophysics, for and Remote Sensing, Space Applications National ImagingSpecim, 90590Oulu, SpectralLtd., Finland Teknologiantie 18A, Global ChangeCentre Research A 12165 Berlin, Germany 12165 Berlin, Germany -induced fluorescence - a new probe of photosynthesis: First First probe ofphotosynthesis: new a fluorescence- -induced 7 , F.Pinto 9 , KraftS. 5 1, * , L.Guanter , L. Alonso, L. 5 , J.Verrelst 1 , L. Prey, L. May 5 , T. T. , Kraska -2015 -2015 6 2 , J.Hanus , A.Burkart 2 1 , F. Zemek , R.Pude 10 , M. Matveeva 7 S CR, 986/4a, 603 Republic Czech CR, S Bělidla 00 Brno, , HyvärinenT. 10 1 7 , C.Cilia , M. Rossini

1, 1 r , J.Moreno 3 , S. Cogliati, S. Hy 8 3 , T. Julitta, T. , A. Schickling Plant 2 , O.Muller

3 3 , R.Colombo , J.Jussila 1 , U. Schurr, 1 , C.Panigada 8 , K. Kataja 3 , A. Damm 1 Weg 6 Weg , D. – 8

, P. 10, 10, 3 , 4 , This article isprotected rights by All copyright. reserved. fluorescence Photosynthesis Keywords: photosynthetic COphotosynthetic cause substantialstill uncertainties predicting in photosynthesisVariations in Abstract monitoring machinery. We argues that and thus may be related to the seasonal activation and deactivationof the photosynthetic airborne-based imaging spectroscopy, which a spectroscopy,airborne-based which imaging spectrometers. using space-borne using observations Intermediate-scale imaging oncoarse a scale and the spatial on ground fluorescenceevaluate the sun-induced signal Severalare to remote activities underway techniques. reflectance sensing optical based that are are to vegetation measure not relatedphotosynthesis by difficult of to greenness (i) the total absorbed radiation (i) thetotal radiation absorbed largely differ in emittingfluorescence tha complement Differentclassical remotetypes, which crop approaches.types sensing between differenta large variability fluorescencesun-induced spatial show vegetation Depth Principle that exploits exploits Depth thatPrinciple physical fluorescence unitssun-induced in accordingFraunhofer tothefluxes the for first allows unprecedented an which timehas spectral quantifying resolution, employing resolution, novel airbornespatial the imaging spectrometer present the first validated maps of sun-induced fluorescence in that critical, in Here observations, and global studies we arebetween small-scaleinsufficient. still field Acceptedspatial patterns of photosynthesis. These spatio-temporal variations cannot to date be measured andefficiency machinery causegreat ofthe seasonal, diurnal, photosynthetic in variations lightdifferentatmosphere. andcanopy of absorption inthe due to structures Variations Terrestrial plant photosynthesis constitutes a major flux of carbon and water exchange with the Introduction and actualvegetation photosynthesis stress. status of functional Article – FLEX – sun-induced fluorescence 2 uptakemonitoring stress.rates actual plant in Changes and – imaging spectroscopy un so -induced fluorescence emission is related to two processes: by la r (ii)the and photosynthetically active chlorophyll and atmospheric absorption bands. Maps of of Maps atmospheric and bands. absorption – t remote sensing remote additionally changes additionally within the seasonal cycle – airborne measurements re critical to bridge the existing gap gap to bridgecritical the existing

–

HyPlant

– – chlorophyll vegetation vegetation HyPlant termediate Line . HyPlant

This article isprotected rights by All copyright. reserved. North, 2001, Garbulsky canopy structure (Barton & 2006) arechallenged bypigments thegreatleaf and contamination ofthe signal by various Photochemical(Asner ReflectanceIndex efficiency (PRI) toquantifyphotosynthetic and the Attempts touse thereflectance nm the amount ofchlorophyll. signal at531 photosynthesis directly, and remote sensing instruments on satellites only detect greenness and systemet measurethat can dedicated al.2009). satellite There available no iscurrently photosynthetic water carbon and and especially onthelocal exchange regional scale (Dolman directly, suffersand still modeling substantialuncertainties inestimating predicting and Greenhouse gasesGreenhouse(Frankenberg (GOSAT) Satellite Observing spectrometers.global mapsof fluorescence first from were the data The derived using usingspace-borne Fluorescence existing imagingcan retrievedon coarse resolution be spatial bands. high allowingsolar SNR fluorescence and absorption inthe atmospheric toretrieve spectralhigh fluorescence 0.2 nm anda witha spectral emission windowof resolution of spatial resolution the of300meters full globalrepeatedexploit coverage. andFLEX a will 2009, Meroni Fraunhofercombinationretrieval withtheLine (Malenovsky principleDepth (FLD) passively (Rascheratleaf tocanopylevel can thecores theFluorescence from be and apparatus photosynthetic detected isemitted of notablebe for used efficiency. potential asphotosynthetic of its to adirect indicator fluorescencesensingSun-inducedas remotemethod, anovel chlorophyll explored signal is 2009). scale o spatio-temporal variability of sun-induced fluorescence and plant photosynthesis on the spatial 2007, Guanter measure (670 ofsun-induced emission full spectrum fluorescence the The aims to FLEX candidateEXplorer) mission as missions. Explorer one Earth oftheir attempt byAgency this FLuorescence supported theFLEX (ESA) (FLEX: mission selecting Recently,sun-induced and themeasurement fluorescence theEuropean principle]. Space fluorescence track diurnal, fluorescence the demonstrated to potentialof have sun-induced Accepted Small-scalefocusing local sun-induced of quantification top-of-canopy studies onthe 2014). (GPP) in the high-production agricultural regions during main vegetation period (Guanter et al. grossused global demonstrateto primarygreatlyproductivity that modelsmay underestimate 10 days datamonthly These grid. fluorescence as were to averages 0.5° derived was onthe Article f 2°. Recently, Joinier et al (2013) also explored data from the GOME-2 satellite, andJoinier data theGOME-2 explored also et from al(2013)2°. Recently, et al. et al. , 2009). [S , 2012,Joiner ee supplementary information (S1) supplementaryfor on background information et al. , 2011), demonstrating onthe novel information et al. , 2009) using spectrometers, 2009) high-resolution in et al.

, 2011, Hall et al. 2008, Hilker et al. et al. , 2011,Guanter – 780nm)witha et al. et al. et al. , , , studies are available, which either recorded fluorescence in relative units (Rascher This article isprotected rights by All copyright. reserved. (Zarco-Tejada orempirical uselight-weighta spectrometers of onUAVs series requiring corrections intermediate meters i.e.coveringscale, spatialscale from tok the On the fluorescence structure-function relations. wererelatedchanges in signal that to cornin inthe showedrice dynamics fields,(2010) seasonal and etal. ina Rossini field. show et (2010) al. Damm of seasonal,adaptation photosynthesis. example, and For species-specific unprecedentedresolution dataspectral spectrally inthe red specificallyenable to region (http://www.itres.com/). Thisnew airborne instrument aim was toprovide designed withthe CASI or HySpex (http://www.opairs.aero/hyspex_en), (http://aviris.jpl.nasa.gov/), ofAVIRIS (http://www.apex-esa.org/), operationalairborne such as spectrometers, APEX HyPlant 2006, Schurr photosynthesissingle from (Rascher plant the thefield to of importancespatial utmost scale, incanopy tobetter however, understand is variability the retrievebandsfluorescence (Meroni inthe atmosphericabsorption imaging spectrometer the airbornecooperation Finnish company developed withthe (www.specim.fi) Specim ForschungszentrumTo scale, address intermittent (Germany) spatial Jülich ofan the lack in satellite-basedmeasurements. fluorescence vegetationcurrentas strategies carbon and well andfuture as water for validation fluxes greatlyproperties andour understanding facilitate rates predictionwould or photosynthetic of and(Dolman globalscale identifiedregional uncertainties asmost revealing the scaling the process models by to local flux modeling, this intermittent spatialscale modeling, referredintermittent as(also this flux to Formanaging varieties crop practices. todifferent related and performance management crop Accepted (Fignm 1c, d).and Asummary details thecharacteristics on of spectralwas for range and specifically designed fluorescence between 670and retrieval 780 2500 nm, and the second module has a high spectral resolution of 0.25 nm in the red and far- a single rack (Fig 1a, b). One module measures surface radiance in the spectral range of 380 to instrument is a push-broom imager consisting of two modules that are aligned and mounted on Article ed that sun-induced fluorescence improves forward modeling of diurnal courses of GPP GPP forwardfluorescence thatsun-induced modeling courses ofdiurnal improves of constitutes astate of imaging theart fleet existing complementing spectrometer the et al. et al. , 2006), which is a challenge for precision agricultur , 2013), , 2013), HyPlant et al. yet , which was vegetation specifically tomonitor and designed , 2009). Thus, direct measurements of functional vegetation , 2009).functional Thus,direct measurements of these maps still lackintermittent This a evaluation. proper mapsstill these et al.

01 ace Nedbal, & , 2011,Rascher HyPlant “ mesoscale ilo et al. meters, only a case few e and for measuring and , 2009). The , 2009). are given in Table 1. given are 1. inTable ” ) has been et al. , 2009) red radiativeMODTRAN-5 transfer (Berk model atmospheric detail.instrument in using the Highresolution irradiance simulated spectra, the spectral,flightandcharacterized radiometric we lines, ofthe performance spatial, ground,correspondingand a 3m,respectively. spatialresolution Based of1 to onselected maboveand flightrecorded were lines from 600and nominalflight altitudes, 1,780 two systematically (Guanter overestimated airborne fluorescence giving fluorescence in relative units (Panigadagiving fluorescence units inrelative procedure). studies have airbornethis fluorescence deliveredPrevious maps only singular, spectra descriptionwerefor of fine best Materials (see tuned for measured correlation with Parametersnominal characteristics the modeledfor sensor data of degrading the elements. This article isprotected rights by All copyright. reserved. fluorescenceretrieval. FWHM ϵ [1.0 to 20.0] nm;; and ii) a variable spectral shift (SS) ϵ [ Modeled spectra were convolved across trackpixels covering a area. homogeneous nm (at 760 nm). To avoid misinterpretations caused by spatial heterogeneity, we only analyzed sensor in flight operation. Additionally, we evaluated radiometric performance by sensor Additionally, inflightevaluated radiometric we operation. by performance correlation between modeled and measured spectra represent the spectral characteristics of the modeled with MODTRAN-5 (Berkmodeled withMODTRAN-5 signals absorption Theatmospheric pre-defined features. reference in signal radiance was The spectral performance of the Radiometric spectral characterization and of Methods Material and dedicated usingbands the of oxygen sun-induced inthe absorption spectrally narrow fluorescence spectroscopyfor retrievalof thefirstthe for high-resolution region inthepossibility red time distance interval for each FWHM (SSI = 0.5 nmfor thefluorescenceto 2.0] and module, a spectral and iii) fixed dual-channel sampling Acceptedquantificationon comparing was measured ( based oftheBoth detectorpositions array. parameters were investigated inpre-defined The within the detector array and the spectral band width (Full width at Half Maximum = FWHM). namelydescribing of theSpectralthe position Response Function (SRF) a spectral pixel, Article “ fluorescence module. fluorescence HyPlant was first operated in a series of campaigns atend the wasin aseries ofcampaigns 2012, firstoperated of HyPlant ” considering: i) a variable FWHM ϵ [0.1 to 0.4] nm and considering: FWHM ϵ [0.1 to variable i) a

et al. sensor was investigated by evaluating two parameters , 2004) in the highest spectral resolution, i.e. 0.0057 , 2004) inthe highest i.e. 0.0057 spectral resolution, × et al. FWHM). Parameters that resulted in the highest et al. HyPlant HyPlant , 2004), weredegradedgradually tothe , 2014,Rascher

) andreference modeled radiance et al. - 0.5 to 0.5] nm and SS ϵ [ , 2007). et al. , 2009) or have, 2009) HyPlant permits -2.0 Processing of effects, inTable 1. which are summarized This article isprotected rights by All copyright. reserved. investigating theoccurrence ofbad the signal- pixels, (

where spherical sun-induced and To decouple (F) albedo. fluorescence values radiance were from thenconverted numbers (mW·m to digital acquiredclosing Data of by thecamera theshutter after each line immediately acquisition. by was pixel The linearly using instrument's signal removed, frame a pixel image dark dark Image pre-processing camera.provided by theGPS/IMU Navigation of data for ofthe sensor each pixel using laboratory detailed calibration by themanufacturer of the the integration time during acquisition and using a radiometric calibration coefficient estimated diffuse arriving fluxes) thesurface, at between of thetwomodules (DEM)regioncorrectiongeometric used forof of the were theimages. overlapping Accurate reflectance ( canopy(Meroni The emitted chlorophyll fluorescenceadds theradiation to by signal reflected a vegetation Sun-inducedretrieval fluorescence batch mode. interface perform forgeo-rectification of interactively a single lineor group run a of themina steps were performed using the software CaliGeo Pro (Specim, Finland), which provides a user pre-processingcorrected.alignmentAll respectwas with of theGPS/IMU, bothmodules to λ

Accepted ) canas be expressed Article L p isthe path ofscattered radiance, ), radiance thesurface leaving ( HyPlant et al. , 2010), supplementaryLambertian 1).Assuming information surface

data, fluorescence sun-induced retrieval (F of HyPlant

(F was achieved was after wherea boresight calibration, the 760 τ↑ ) E is the upwelling and isthe transmittance, g isthe global (including irradiance direct and L ) measured by a sensor at a specific wavelength to HyPlant -noise ratio, radiometric and other

and a Elevation Digital Model and , at-sensor radiance, at-sensor -2 str 760 -1 ) nm -1 ) considering S isthe (eq. 1)

This article isprotected rights by All copyright. reserved. measurementsa target vegetation of ( inside required. Forairborne case, can the measurements as: be written such eachMODTRAN-5 using (Berk observation L

(2003, 2007). Thus, the system of equations (eq 2) contains only four unknowns: MODTRAN-interrogationin DammVerhoef etBach(2015) technique and al. or as described rgnl ruhfr ie et (L) prah Pack Gbil 17) alw to allows 1975), Gabriel, relate & linearly (Plascyk approach (FLD) Depth Line Fraunhofer original ρ n hs td, e xlie te rae O broader the exploited we study, this In absorption bands. sd h 3L mto (Maier method 3FLD the used rvd raoal acrc b big out gis sno nie (Damm noise sensor against robust being by accuracy reasonable provide Sun-induced fluorescenceat 760nm

o λ , which are values, and spectral reflectance inside fluorescence and of outside the Accepted Articleknown directly is the theterms measurement from and itself and with

R and F inside and outside of the O the of outside and inside F and

t al. et

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right O justified by(Alonsojustified and experiments simulations

Accepted Article relating factor the is 2 and -A band shoulders with with -A band shoulders

F i

and F , and and , ρ o (insideand the outside O i , and ,

ρ o and was derived from linear interpolation of interpolation linear from derived was and

760 emission (e.g., theupward toadjust soil) bare etal. 2 -A band)and was toavalue fixed of 0.8, (see (Damm 760 , 2008,Rascher signals(Damm

et al. , , 2014) for details on this et al. et al. , 2009). 2 -A band. ρ , 2011). We of the left and left the of (eq. 7). (eq. 6), (eq. B isthe This article isprotected rights by All copyright. reserved. nominal wavelengthas: spectral closest1997). the bandthatfrom calculated We to was a the NDVI narrow band Ripley, property &(Carlson canopy including leaf area,andcover, canopy architecture greenness,to canopynear-infrared The isacomposite NDVI wavelengths. which issensitive traditional, based multi-spectral onthedifference index atand reflectance incanopy red (NDVI)Index DifferenceTheto the oxygen-A line. NormalizedVegetation absorption isa The meteorological top-of conditions. canopy radiant intensity was extracted for 758 nm close wasatmospheric parameterized that using by transmission themeasured MODTRAN-5 the image, respectively by reflectanceTop-of-canopy (Fig calculated was 3a). modeling radiance bands of 695.54 nm, 708.26 nm, and 676.54 nm for the red, green, and blue channel of From pseudo-RGBreflectance composite top-of-canopy using a produced the we data, vegetation of Calculation products retrievals factor correction considering ofthe thesurface height. correction factor foreach vegetation target, a applied spatialinterpolation of we distinct methods generally provide a better estimate of chlorophyll content through using the full full the using through content chlorophyll of estimate better a provide generally methods Such available. are algorithms regression learning machine using methods advanced More R

Huete et al.1997 to according modified 9; (eq. sensor our for wavebands optimal the selected and MODIS of factors weighting the used We consideration. into waveband blue additional an taking by and (EVI) regions Index spectral the weighting Vegetation differently by Enhanced effects atmospheric the and structural for only, corrects wavebands two on relies NDVI the While where R x

Accepted denotesatreflectance for specific this wavelength. the Article NDVI (R = x denotes for the reflectance at this specific wavelength. reflectance wavelength. specific this at for denotes the ).

758

– R 670 ) /(R) 758

+ R + 670 ) (eq. 8) (eq. )

(eq. 9)(eq. This article isprotected rights by All copyright. reserved. estimate(Verrelst model during bands mean variable the with along pixel each spectralfor estimate uncertainty an provide and development the no of relevance relative making the spectra indicates reflectance statistics, which of regression combinations, non-linear probabilistic a fits Bayesian It distribution. data non-parametric the on processes assumptions on Gaussian based (2013). al. is et regression Verrelst to according on regression based processes algorithm retrieval Gaussian advanced an chose We signature. reflectance hyperspectral top-of-canopy fluorescence measurements. A highly significant relationship wastop-of-canopy established measurements.Afluorescence significant highly relationship HyPlant top-of-canopy fluorescence simultaneously measured on ground using established high high established (Meroni using spectrometers groundresolution on measured simultaneously fluorescence top-of-canopy with comparison a i) strategies: two includes values fluorescence retrieved of validation The of fluorescenceValidation maps representativethe most types cover showninFigure 4. of each for selected were algorithm SAM the for endmembers Spectral module. fluorescence physical units from airborne data with high spatial resolution (Figs. 2, 4 and 5 and 4 physical resolutionairborne (Figs. data with spatial high from 2, units the first time the quantification of sun-induced fluorescence at 760 nm (Fatthe first760 nm thequantification time fluorescence of sun-induced altitudes. flight contrasting two in but area same the over measured fluorescence between comparison os Fato (N) rnfrain acltd rm h 104 ad of bands 1,024 the from calculated transformation (MNF) Fraction Noise A Minimum the of bands approach. 10 first the to classification applied was algorithm supervised (SAM) Mapper Angle Spectral a through obtained was classification cover Land Accepted characteristicsThefluorescencemodule of spectral ofthe andradiometric Discussionand Results the validation measurements ground. on on details more for (S2) information supplementary See grassland). at (recorded value lower N, 50.863887 were the for E 6.451987 measurementsN, 50.869316 and beet) sugar at reference(recorded value high the for E ground6.450933 the of (position time) local (13:23 agl 1,780m and time) local magl (12:50 600 heights of inflight noon agricultural around site Article fluorescence maps showed good agreement with simultaneous ground andsimultaneous ground showed good with agreement fluorescencemaps HyPlant et al. aa sd o te aiain ee olce o 2 Ags 21 oe an over 2012 August 23 on collected were validation the for used data , 2012). , t al. et 21, Rossini 2011, ,

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foil-covered soil (A in Fig 3). (ii) Apple tree plantations (B (ii) foil-coveredApple and (A3 inFig tree plantations C 3). inFig soil bareclose including tozero athaverooftops, and orvery streets, fluorescence values values below just 1mW/m around 1.5 mW m around 1.5mW highest fluorescence values reaching 2 mW m highestreaching2 mW fluorescence values and(c). experimental plantations inFig.3) have (D consistently (iii)Sugar beet fields the s sih adtv ofe wee loecne aus band rm h hg fih are deviation this flight consider We high flight. low the the from from retrieved fluorescence obtained to compared values lower systematically fluorescence where offset additive slight a is UniversityF ismapped. In researchstructure-functionexperimental ofBonnFigure campus relationships. 3, the Maps of F of time theday. already this decreased during angle elevation sun the while flight, low the after min 40 roughly performed was flight close to the 1:1 line (R line 1:1 the to close both further height,flightthe Irrespectiveof 2b). (Figcovertypes land of set was extended anconfirmedusing ground above m 1,780 and 600 at flown maps fluorescence of agreement The may be reflected in high fluorescence values that maymay fluorescence that indicate reflected be inhigh values canopy. Also the perennial C canopy. Alsotheperennial commercially has late adense and autumn, fully photosynthetically harvestedactive in greendespite but thestill naturallycrop beet, a leaf-material. biannual Only sugar 2012)of August were ofobservationalready approaching the time (end senescence during Corn, apple annualcrops trees,andfluorescence other greenness. than just more measures sun-inducedThe that offluorescence highsuggests thesugar corn values beet fields and Mi This article isprotected rights by All copyright. reserved. 2a andbetweenground fluorescence fluxes C recentlyspace-borne dominatedagricultural byregions where derived from measurements, functionalfindings status ofphotosynthesis. Our thehypothesis are also agreement in with cannota canopy unravel finally denser the effects of thecontribution ofchanges from inthe firstdata basedgreen setphotosynthetic we However, in adense machinery onthis canopy. 4 ; Accepted have (Guanterrelative been the summer foundhighest toshow fluorescence late signal in Article scanthus sp. R HyPlant 2

= 0.97, RMSE =0.166 m 0.97, RMSE mW 760 from selected two clearly onplant agricultural information show sites novel fluorescence maps are only slightly affected by offsets, and selected values are values selected and offsets, by affected slightly only are maps fluorescence to and corn (E in Fig 3). (E and inFig corn 3). be realistic and related to a short time delay of data acquisitions. The high The acquisitions. data of delay time short a to related and realistic be -2 ·sr -1 2 ·nm 760 = 0.99, RMSE = 0.165 mW m mW 0.165 = RMSE 0.99, = showsseveral (i) note-worthy non-vegetated All surfaces features. 2 · -1 sr werefrom the ofthe also experimental observed plots C 4 grass ·nm. This fluorescence value remains low in commercial Thisfluorescence (b) in remains low value ·nm. Miscanthus -2

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760 and NDVI ea at oftime the ), the clearly visible around 750nm in the addition to the oxygen absorption lines. Despite their narrow nature, theseFraunhofer lines are the properties atmosphere Earth of 2013)and a may et the thus (Joiner valuable al. provide bewill further advantagenot influenced These solar thatthey lines the evaluated. are have by approaches fluorescencelines solar thatexploit absorption infilling (Fraunhofer inthe lines peaks etal. becomeavailable found 2015).Additionally, soon will inRossini (first results are TheF correlation of beet the summer remain (Fig. throughout high 6a). O (Sabaterwhole fluorescencesignal more advanced retrieval algorithms based on Spectral Fitting Methods that will reconstruct the taking the solar absorption lines around 755 nm into account dynamic resolution that also fluorescence can be retrieved in the oxygen-B band (at 687 nm) or iseasiest quantify,fluorescence to flux but This article isprotected rights by All copyright. reserved. asummer isassociated larger declineF with in This study clearly indicates that F This study indicates clearly to evaluate thatare retrieval different algorithms based absorption features. onthe In this paper, we only report sun-inducedIn fluorescence we onlyreportat paper, 760 nm this (Fig6b cornclusterwaswhich fromcorn, fillingthe already approachingin that of phase senescence distinguishingSugar this the fluorescencecorrelationfields beet had analysis. highest values, clearvariabilityclusterscropparameters. in However, types differentshowed between both transmittance in especiallyF photosynthetic incanopiesconversion (Damm light fluorescence emission in the far-red region. Because ofthe O fluorescence inthe wider far-redemission Because region. down-regulation in maize, while sugar beet still had maximum photosyntheticdown-regulation hadmaximum whilesugar still maize, rates in beet in chlorophyllsystem(Rascher fluorescence Leaffluorescence the well-established with PAM beet. level measurements insugar the activityis supported byvalues photosynthetic of ofthe This thehigh machinery. (Rossini selectively ofabsorbedmeasure theamount chlorophyll from light in (see also hypothesis 2

Accepted-B band (F Article ). et al.

760 687 , 2010)). Additionally,wesun-induced that propose to fluorescenceis related alsooriginates has foliage a highof from thecanopybecause deeper layers ) and thus quantify red fluorescence are way, under and data validated on both th is spectralF is region. Thus, 760 withthe remotelychlorophyll also high showed content quantified 760 et al. HyPlant measuresstructural of properties andfunctional , 2014). Studies thatalsoretrievefluorescenceat, 2014). Studies the et al. HyPlant data (Fig 1) and thus may provide a good test case 760 760 can be usedexcellent as indicatoran to , 2000) showed a physiological , whileF et al. data have spectral enough high and

, 2010). It, 2010). canassumed be that 760 (F values of perennial the sugar 687 ). In the future, we can expect (F 2 760 -A absorption band-A absorption this ) that corresponds to ) fluorescence better to may parameterize help absorption and light with conversion dynamics photosynthetic carbon sun-induced of Onthe rates. exchange process scale, topredict whichestimated thespatio-temporalglobal model, areour local, and regional, improveTherefore, to may help fundamentally ofsun-induced fluorescence measurements hours indicating blockfunctional ofactual the rates (Rossini photosynthetic This article isprotected rights by All copyright. reserved. year.the C Additionally, active, andchlorophyll ofsenescence nosigns breakdown or of time during the this happened still fullyperennial beet is photosynthesis plants September the in (Table sugar 2).Thus, canop and airborne measurements ofF and airborne measurements photosyntheticamount ofpigments leaving electron transport thetotal Ground untouched. photosynthesis demonstratedapplying was a recently by herbicide that blocks selectively stress regulating mechanisms are operational on photosystem II, thus functional regulation will photosystemsto these peaks, contribute are their but proportions different. Most physiological and F different causefromfunctionalclear deviation 1:1line a between asimple chlorophyll status differentsurpassingly simplyand speciesanbecause ofchlorophyll improved measure conditionsof (van F The der al.2014). Tol potential et mayevenrelations depending adapted showoppositehigh is ifa tolowor light plant mainly andconstants thephotosynthetic apparatus dependent in ofrate non-linear andthusis demonstrating this property using airborne data and covering several species. F demonstrating property species. covering this and airborne using data several indicated in groundstudies (e.g. (Damm TheF sensitivityof andConclusions future studies al. Guanterfluorescence inFig (E emission which agreement isin tothe 3), findings of as well as seasonal anddroughts other environmental constraints (Bergh ecosystems, which are subjected to frost-induced activation and deactivation of photosynthesis greatly inevergreenmayfunctional efficiency photosynthesis uncertainties reduce of by(Simmer etthe largest press). al. in direct of On scaling non-linear measurements scale, on thescale influence and scale) of (km mesoscale meters, and surface atmosphere dynamics

Accepted Article(2014). 760 y (van Tol der (Fig 6 ). The relationship between relationship The F 760 et al. for theactual andefficiency photosynthetic often was hypothesized 4 species corn and , 2009), provide understand inputto dynamics vegetation thatoccur 760 and F et al. 687 Miscanthus sp. Miscanthus showed a a within dramatic few increase 3-fold 760 , 2010)), but this is the first study thefirst is , 2010)), butthis

and photosynthetic transport is electron 760 toreflect the actual statusof

showed high of values et al. et al. , 1998). The two 760 , 2015). is not in et the This article isprotected rights by All copyright. reserved. Daumard response (Agati, an 1998, thatis interplay functional structural between and regulation peaksvegetationimprove ourability will thedynamic stress andunderstand predict to nature affect the first peak of the fluorescence emission to a greater extend. Therefore measuring both U. study Rascherconceived and designed the Author contributions Association.investment grant oftheHelmholtz Schüttemeyer. T. Hyvärinen, J. Jussila, and K.KatajaJussila, J. developSchüttemeyer. T. Hyvärinen, Moreno, M.Drusch,organized and withthe andJ. assistance of data D. analysis acquisition Schickling operated andF. A. A. Burkart, Pinto, supported theinstrument development activities. andcalibration KraftS. characterizationperformed and calibration of laboratory theinstrument. the et al. limitations ofthe photosynthetic capacity are (Long indicator anyield for excellent reductions oftenyield, does directlybioeconomy.agricultural not but finaldetermine Photosynthesis precisionof inafuture agriculturelarge-scale agricultural management and production local, regional, and global carbon modeling. Additionally, it may serve as a novel indicator for Thus, sun-induced fluorescence may serve as an early indicator of limitation photosynthetic in 2010). FLEX satellite mission thatFLEX mission being satellite currentlyevaluat is In theproposed stress etscale, thefuture, indicator (Guanter al.,2014). a maynovel provide AcceptedSFB/TR32 HyFlex and campaign.ESA funded campaign Data4000107143/12/NL/FF/If). acquiredjoint (ESA were during contract the of theHyFLEX the framework within financialAgency additional provided support (ESA) projectThe by theDeutsche D2,funded EuropeanForschungsgemeinschaft Space (DFG). Soil-Vegetation- gratefullyWe the support financial acknowledge the SFB/TR “Pattern in by 32 Acknowledgements paper. complement airborne this measurements as presented in Article aims for a global fluorescence mapping may target these objectives on the large scale and could , 2006, Zhu et al. , 2010, Flexas , 2010, et al. Atmosphere Systems: Monitoring, Modelling, and Data Assimilation” Atmosphere Assimilation” Monitoring, Systems: Data Modelling, and HyPlant , 2010), and sun-induced fluorescence, which can be mapped on the large during the campaigns. F. Pinto and A. Damm developed and the during A. Damm F. Pinto thecampaigns. et al. , 2002,Fournier HyPlant Hy Plant et al. ed . He wascampaigns and ofthe PI

was developed by a was large-scale by developed , 2012,Pfündel, 1998,Thoren by

the European Spaceand the Agency ed and built and built HyPlant and et al. ,

Installation of (b)(B).Additionally, attached theGPS/IMU positioning thatis (C). unit isshown tothe rack thehigh fluorescenceconsistingand resolution dual (A) ofthe module band module broad This article isprotected rights by All copyright. reserved. C provided thesignificantly data. atmospheric C. Kokkalis to the data P. contributed analysis. and performed and Rossini, M. ground M. Pikl referenceJulitta, the measurements Verrelst Cogliati,S. T. J. calculatedand product. the retrievedchlorophyll maps. fluorescence L. and all flight Prey lines processing Pinto processed fluorescence F. pipeline for retrieval. Airborne spectrometer imaging Fig. and discussions contributions from allco-authors. U. Rascherthe paper3. O.Muller helped with wrote tointerpretresults. the physiological of theresults inFig tointerpretation and Klein-AltendorfCampus experiments contributed on ground, and grey dots represent F represent dots grey and ground, overpasses. Corresponding fields were manually selected and the field average of of average field the and ground selected above manually m fluorescence nmwas compared at between the twoflight values 760 heights. (1,780 were high fields and ground) Corresponding above overpasses. m (600 low from measured values resolvesabsorption O thetwooxygen lines high-resolution fluorescencefluorescence module The respectively. spectrally module, the dualtargetfrom andthe target (blue), and (black), dark (green), vegetation (red) bare soil a isvisible brightacquisition radiance unit (D). from d) (c, Representative measurements Error bars indicate the spatial variability of F of variability spatial the indicate bars Error ibrebsd loecne aus rm w slce co tps n si. lc dots Black soil. (F and fluorescence sun-induced types to crop correspond selected two from values fluorescence airborne-based airborne of Validation 2 Fig. at 750nm. featuresnarrowFraunhofer lines inthe solar toabsorption thatare atmosphere due are visible Additionally vapor 705and water absorption Even 735nmare bandsbetween very visible.

Accepted Articleilia producedKraskaT. theland and Pudecoordinate the classification. cover R. scientific 1

HyPlant within a Cessnacampai aircraft during within 2012 HyPlant 760 HyPlant F values retrieved form data flown 1,780 m above ground above m 1,780 flown data form retrieved values 760 measurements. . 2 (a) Schematic drawing the Schematic (a) of -A O and 760 760 ) retrievals from data flown 600 600 flown data from retrievals ) within the selected areas. (b) Fluorescence (b) areas. selected the within 2 -B nm, respectively. at and 760nm 687

a Cmaio o gon- and ground- of Comparison (a) gn . In back, . thedata the HyPlant

se m nsor above ) . radiance normalized The difference at nm.(c) vegetation NDVIwas 758 calculated index as used green,I bluechannelfor and thered, image. (b) ofthe files. (a)For image bands reflectance the pseudo-RGB geo-referencedwas radiances calculated using thelaboratoryat-sensor were calibration and agriculturalof Germany (50° thecity Jülich, fieldssouth of The+noon. area by 2h), after solarareawhich approximately is 1hour was dominated 2h) (50° 37 (UTCImage23 August + time different 2012,15:33local corn (E). varieties recorded was The23 Augu flight on recorded was line the from WesternGermany agricultural area in an derived fromthe fluorescencemodule of Fluorescence mapmeasured using the fields ofthe (D)from plots perennial and the experimental C the treesugar beet Significantly, plantations. was the highest from recorded fluorescence a pixel resolution of1m a pixel Airborne maps fluorescenceAirborne different of (F sun-induced vegetation and products 4 Fig. according3FLD O methodin the oxygenmodified tothe University Bonn, Germany. Germany. University Bonn, and (B parkingC ofthe lots experimental and station; (A) roofs, bare center anddifferent foil-coveredand streets the fluorescence in soil emission: fluorescence.of theresearch showgreatly station types and vegetation Different plots in physical was tocalculate correction andatmospheric units applied top-of-canopy This article isprotected rights by All copyright. reserved. Fluor 3 Fig. process regression method (Verrelstprocess regression method Accepted through approach.classification supervised a effective therelevant transmittance in wavebands. fluorescence(F Article HyPlant escence m escence ’N isrmn. instrument. 6° 59 760 aps of the agricultural research station Campus Klein-Altendorf, the agricultural station Campus research of Klein-Altendorf, aps . (d) Leaf. (d) chlorophyll (LCC) content usingGaussian was calculated the ) was calculated methodwithanempirical correction using the3FLD of ’E). . . 2 . Sun-induced fluorescenceat(F 760nm (a) : pseudo-RGB composite from the research station. (b) frompseudo-RGB theresearch composite station. et al. HyPlant st , 2012,Verrelst 2012 from 600 m height, at 13:50 local600 mheight, (UTC time 2012from at 13:50 sensor from resultingground above 600m sensor in (f) ) Landcover wasclassification obtained at commercialexperimental apple and 696 nm, 708 nm, andnm, 677 nm are 696nm,708 2 et al.

-A line. Fluorescence isexpressed 758 52 4 species

’N re , 2013).Sun-induced (e) fers top-of-canopy tothe 6° 27 760 ) was calculated Miscanthus sp. Miscanthus ’E) . The flight line and 760 : ) 2h) The 2013from flight 600mheight, local on18June (UTC recorded time line + was at13:32 HyPlant the of from site Fig. study asin the fluorescencemodule the 4derived sanme from Barton CVM, North PRJ (2001) canopyBarton Remote PRJ sensing useefficiency of light CVM,North the using the fieldsDuringwere avoided. of time overpass High fieldsregions. andin homogeneous spatial regions of edges variabilityfields within or Fromofabout interest75 regionswe theflight of line 4 and Fig (ROI) manually 5, selected vegetationproperties. This article isprotected rights by All copyright. reserved. fluorescenceCorrelation of sun-induced (F analysis 6 Fig. 1997) (Huetealeq.9 according eton thesame to inFig.calculated algorithms EVI as 4.The was maps fluorescenceAirborne different of sun-induced vegetation and (F products 5Fig. Berk AndersonA, Cooley TW, GP factorsBerghLinder S(1998) Mcmurtrie controlling RE, theproductivity Climatic of J, Asner GP, (2006) Martin PM RE,Carlson KM,Rascher U, Vegetation-climate Vitousek Agati G(1998) ofthe chlorophyll invivo Response environmental fluorescence to spectrum References 4f. and The plotted. the symbols color ofFigure crop represents type the shownin average siz withan grasslands.beet, ROIs pixels and rangingcorn, to71,508 insize differed 1,059 from Accepted GuanterL,L, L, Moreno Amoros-Lopez J, Alonso J J, J, Gomez-Chova Calpe Vila-Frances Article (50° 52’N 6° 27’E). Sensing of Clouds andtheSensing ofClouds Atmosphere Ix, scattering band modelwithauxiliary andspecies multiple options. practical 1106-1117. Environment, photochemical Model andsensitivity index: reflectance analysis. 127 Norway analysis. spruce: A model-based interactionsHawaiian and among native invasivespecies in rainforest. factors wavelength.excitation and laser quantification. fluorescenceImproved(2008)method for Fraunhofer vegetation line discrimination isrmn. instrument. e – 139. of 13,597 pixels. From theROIs, of were 13,597pixels. andcalculated deviations mean standard

78 IEEE Geoscience and Remote Sensing Letters,IEEE Geoscience Sensing andRemote

, 264 Vegetationwere indices fluorescence and sun-induced derived based – 273. 273. et al. (2004) MODTRAN5: atmospheric Areformulated (2004) Pure and Applied Optics, Pure and es Forest Ecology andManagement,Forest

5571 green bydominated was vegetation sugar 760 , 78 )

– with other remote sensing 85.

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7 , 797 – 624. Ecosystems, – 807.

Remote 110 760 , )

9 , This article isprotected rights by All copyright. reserved. Carlson TN, Ripley Onthe between (1997) relation DA NDVI, fractional cover, vegetation Damm A, Guanter L,DammLaurent A,Guanter SchaepmanME, Schickling VCE, A,Rascher U (2014) Damm Meroni A,ErlerA, Hillen W, Schaepman M, ME,Verhoef U Rascher W, (2011 DaumardIF, FournierS, OunisA,Hanocq ChampagneA (2010) Moya A, Y, JF, Goulas Dolman AJ, Gerbig C, Noilhan J, Sarrat GerbigDolman AJ, Miglietta J, C, Noilhan F C, (2009) Detecting variability regional ErlerA Damm A,Elbers J, Flexas J, Escalona JM, Evain Moya Escalona JM, Flexas GuliasJ, J, S, I, (2002)Osmond CB, Medrano H FrankenbergFisher Worden J JB, C, FournierA, Daumard F,Champagne OunisA,GoulasI S, Y, Effect Moya canopy (2012) of Guanter L, Alonso L, Gomez-Chova L, Amoros-Lopez J, Vila MorenoL, J, J, GuanterL,L, J (2007) Estimation Alonso Gomez-Chova Amoros-Lopez Inoue Gamon J, GarbulskyJ, IFilella MF, Y, Peñuelas (2011) photochemical reflectance The AcceptedLyapustinHilkerHall T.A. N.C.,Drolet T., Coops F.G., (2009) G.,Black A., Wang An Y.J., LyapustinHall F.G., T., N.C., Hilker Coops E.,Margolis K.F., A.,Huemmrich H., Middleton GuanterL,Zhang YG, Jung M Guanter DudhiaL,C, A Frankenberg Article and leafarea index. 1882-1892. ofchlorophyll sun-induced fluorescence. Modeling spectral theimpact configurations onthe of FLD sensor accuracy retrieval resolution airborne spectroscopy data. FLD Change Biology, improvegross modeling courses ofdiurnal primary (GPP). of production Transactions onGeoscienceTransactions andRemote Sensing, fieldcontinuous measurementfor platform canopy of fluorescence. in sources and sinks of carbon dioxide: a synthesis. in sources a synthesis. and ofcarbon sinks dioxide: productivity. Patternscarbongross of plantfluorescence GOSAT: primarycycle from with plants. C(3) ofwater-stress net CO(2) in andstomatal assimilation during conductance Steady-statefluorescence chlorophyll(Fs) as followvariations atoolto measurements and Remote Sensing, chlorophyllstructure onsun-induced fluorescence. Research Letters, of solar-induced fluorescence vegetation from space measurements. 281 efficiencies: meta-analysis. Areview and (PRI)index and theremote sensing leaf, andcanopy ecosystem of use radiation of Sciences America,States of theUnited of photosynthesis chlorophyll with fluorescence. Sensing ofEnvironment, terrestrialchlorophyllfluorescencespace GOSAT measurements. from Environment 112, 3201-3211.Environment 112, Environment, 113, 2463-2475.Environment, atmospheric impactsPRI on and directional reflectance. Remote of Sensing assessment space: of photosynthetic light Modeling the useefficiency from by observing sensing remoteDroletMulti-angleforest(2008) G.,Black useefficiency of T.A. light – -based retrieval-based chlorophyll spectral medium fluorescence ofsun-induced from 297. Physiologia Plantarum, Geophysical Research Geophysical Letters, PRI

16

variation withcanopy variation shadow fraction. Remoteof Sensing 34 et al. , 171-186. Remote SensingRemote ofEnvironment, . .

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114 – (2011) Newglobal ofthe observations terrestrial 251. 251. , 231 (2012) Retrievalglobalassessment (2012) of and Remote Sensing of Environment, of Remote Sensing – Remote Sensing ofEnvironment, Remote 240. Remote Sensing ofEnvironment, Remote

111 38 Proceedings of the National Academy oftheProceedings National , L17706. , , E1327-E1333. , E1327-E1333.

48 ISPRS Journal ofPhotogrammetry Biogeosciences,

, 3358 62 , 241 – 3368. 3368. – 252. 252.

IEEE 6 Geophysical , 1015

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115 115 , 256-266. – 1026. , , ) Joiner Yoshida LA,Y, VasilkovJoiner AP,Yoshida Y,Corp J, First Middleton EM(2011) GuanterL.,LindstrotJoiner J, Voigt R., E.M.,HuemmrichVasilkov M., A.P.,Middleton This article isprotected rights by All copyright. reserved. Long ZhuXG, SL, SP, Can Naidu Ort improvement (2006) increase inphotosynthesis DR Huete,Liu,Batchily, A.R.,Leeuwen H. K. van and of (1997) Vegetation W. A Comparison MalenovskyZemekZ, MishraF,L KB, Nedbal and U, Scientific Rascher technical (2009) Sun-induced GüntherMaier KP, M(2003) toolfor fluorescence: SW, Stellmes Anew Meroni M, Busetto L, Colombo R, Guanter R, L,MeroniL, Busetto Verhoef M, Performance Colombo J, (2010) Moreno W of CogliatiMeroni Barducci S M, A, Meroni M, Rossini M, Guanter L, Alonso L, Rascher U, Colombo R, Moreno J (2009) J Moreno M,GuanterL,L, R, Meroni Rossini M, Alonso U, Rascher Colombo Pfündel E(1998)I Estimating thecontribution leafchlorophyll tototal ofPhotosystem Rascher U, Liebig M, Luttge U (2000) Evaluation of instant light-response curvesRascherLiebigLuttge U, of of instant light-response M, Evaluation U(2000) RascherFioraniF Blossfeld U, S, Rascher U, Nedbal L (2006) Dynamics of photosynthesis in fluctuatingRascher Dynamics in LNedbal(2006) U, ofphotosynthesis light Panigada C, Rossini M, Panigada Rossini C, Meroni M Plascyk GabrielFC Fraunhofer line (1975) discriminator JA, airborne MKII: instrument An AcceptedL RascherAgati U, G,Alonso Article Environment Biogeosciences, observationsglobal seasonal of space. terrestrial and chlorophyll fluorescence from 3883 Discuss Meas 6, Atmos Methodology, and Tech application simulations, toGOME-2. fluorescence measurements:from resolution near-infrared spectral moderate satellite K.F.,Frankenbergmonitoring Yoshida (2013)chlorophyll C. Y., ofterrestrial Global crop yields? crop ImagesIndices a ofTM Set Over E Global for Crop Science Crop Inc.;American, Science SocietyInc. of Soil Society ofAmerican, Inc.; Society ofAgronomy, Schepers TartlyPage. L) J, WI, pp Madison, American Experimental Botany, challengesfluorescence. sensing ofplantand reflectance inremote canopy Precision Physiology. Agriculture andCrop precisionIn: farming. Scientific Instruments, andinstrument for unattended long-term spectroscopy field measurements. Environment, spectral vegetation quantification. for fitting fluorescence methods applications. Remote sensing chlorophyll fluorescence: and Review ofsolar-induced ofmethods enhanced inbean. performance traits Current Opinion in Plant Opinionin Current Biology, Observation andGeoinformation, for stress water incereal detection crops. fluorescence. 1181-1198. on site inthefield.on site chlorophyll a portable with parameters chlorophyll fluorescence obtained fluorometer sun-induced bands. inthe oxygen fluorescence absorption quantify theregionefficiencyfrom to measuring by the leaf photosynthetic on Instrumentation and Measurement, for ecological precise and standardized luminescence measurement. – 3930. Plant Plant andCell Environment,

Remote Sensing of Environment, of Remote Sensing 59

Photosynthesis Research,Photosynthesis 114 , 440-451. , 440-451.

8 , 637 , 363 Plant Cell andEnvironment, Cell Plant

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6 Journal of Review of , Sabater N, Alonso L, Vicent J, Cogliati Verrelst Moreno S, Sabater (2014)L, J, J, Afluorescence N,Alonso J Vicent Nedbal L., A., Guanter L., L., Bur Ač Alonso M., Rossini This article isprotected rights by All copyright. reserved. Meroni Migliavacca M, M, Rossini M SchurrFunctional dynamicsgrowth U,Walter A,(2006) and plant U Rascher of Thoren Schmidhalter D,Thoren P, UInfluence (2010) ambient temperature light of on and Va Verhoef ofhyperspectral Bach W, Simulation H (2003) images directional radiance and A.Berry, andvan U.Rascher der of (2014), Tol, J. Models C., K.E. P. Campbell, Verhoef Bach W, atmosphere transfer soil-leaf-canopyradiative Coupled H (2007) and Verrelst J, AlonsoL, (2012) MorenoVerrelst ofvegetation Retrieval G,Delegido J, J J, Camps-Valls Verrelst J, Rivera Moreno G(2013)Verrelst JP, Camps-Valls J, Gaussianuncertainty processes J, Zarco-Tejada PJ, CatalinaZarco-Tejada Martin (2013) PJ, MR, A,Gonzalez P between Relationships net AcceptedI., MasbouM.,Insa C., S., Simmer Thiele-Eich Bogena Amelung W., H.,Crewell LongZhuImproving Ort (2010) DR SP, XG, yield. photosynthetic efficiencygreater for Article n Der Tol C, Verhoef W, Timmermans J, Verhoef Timmermans J, W, Tol Verhoefn Der Z C, A, (2009) Su Anintegrated model of measure photosynthesis. ofplant a Rascherchlorophyll as (2015) fluorescence far Red U. and red Sun-induced Novotny Panigada F., Pinto Schickling C., J., A.,SchüttemeyerF.,Zemek D., Damm R., A.,Drusch T.,Janoutova Moreno J., KokkalisJulitta P., M.,Hanus J., doi:10.1002/2014GL062943 and Forest Meteorology, grossmeasurements inarice estimating ecosystem production for field. (WHISPERS). Hyperspectral Remote Imaging Processing: in andSignal Evolution Sensing In: retrievalFLEX mission. tandem the Sentinel-3 method for photosynthesis Plant Cell andEnvironment, Cell Plant Agronomy, laser-induced fluorescence chlorophyll measurements. balance. soil-canopyand spectral energy radiances, fluorescence, photosynthesis, temperature, of Environment, andatmosphericusing coupled transfer radiative biophysical models. doi:10.1002/2014JG002713. Geophys.chlorophyll J. fluorescence, Biogeosci., 119, Res. fluorescenceand for photosynthesis interpreting ofsolar-induced measurements radiance data. modeling hyperspectral tosimulate and multi-angular reflectance surface TOA GeoscienceSensing, andRemote biophysical using Gaussian parameters process techniques. ISPRS Journal ofPhotogrammetry andRemote Sensing, LAI estimateschlorophyll Sentinel-2 inexperimental and leaf retrieval. content hyperspectral imagery. photosynthesis andsteady-state chlorophyll fluorescenceretrievedairborne from modeling The Transregional theterrestrial system from to catchments: pores Vereecken Waldhoff T. G.,Zerenner J., Kruk (2014) andMonitoring H., van J., der Schneider Shao M.,Vanderborght Y.,Shrestha Stiebler P., K.,Schween M.,Sulis J., LangensiepenN., KolletLöhnert K., M., A.S.M.M., RascherU., U., Rahman Kemna A.,HuismanFranssen J.A., Klitzsch H., HendricksDiekkrügerF., B., Ewert Annual Review Biology, Plant of Biogeosciences,

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, 166-182. kart A., Cogliati S., Colombo R., R., Colombo A., S., Cogliati kart European Journal of European Journal of

136 86 , 157 IEEE Transactions on on IEEE Transactions , 247 Workshop on – 42 – 167. 258. , Remote SensingRemote Agricultural Agricultural This article isprotected rights by All copyright. reserved. 1 Table Table 1: Characteristics of the of Characteristics 1: Table for vegetation monitoring and to retrieve sun-induced fluorescence. sun-induced retrieve to and monitoring vegetation for flight data using several flight lines and a forward modelling of atmospheric absorption absorption atmospheric of modelling forward Signal- characteristics. a and lines flight several using for data designed on flight performed is were that table this nm) in 780 given characteristics to Performance (670 retrievals. rangefluorescence spectral red the in resolution spectral high a having module fluorescence the (ii) and nm) 2500 to (380 region spectral infrared near and visible the in measure reflectance surface to module dual-channelbandbroad the (i) modules: measurements. Accepted [m] track) (across interval sampling Spatial [m] Swath [deg] view of field Instantaneous view [deg] of Field pixels Spatial performance Spatial [%] Stay light and pixel talkcross signal with full-scale SNR performance Radiometric [nm] Smiling [nm] shift Spectral [nm] broadening Band [nm] (FWHM) resolution Wavelength [nm] interval sampling Wavelength Bands [nm] range Wavelength performance Spectral Article

: System. CollaborativeCentre Soil-Vegetation-Atmosphere Research onPatterns inthe Performance characteristics of of characteristics Performance Sensor Sensor B Am Soc. Meteorol to -noise ratios (SNR) (data in brackets) are calculated from laboratory from calculated are brackets) in (data (SNR) ratios -noise HyPlant 380 doi: 10.1175/BAMS-D-13-00134.1 10.1175/BAMS-D-13-00134.1 doi: (510) (510) 384 350 to 970 970 to 0.4 1.2 0.2 4.0 1.7 HyPlant imaging spectrometer that was specifically designed designed specifically was that spectrometer imaging

Dual-Channel Module Module Dual-Channel

1140 at 1780 m agl agl m 1780 at1140 2.94 at 1780 m agl m at 2.941780 380 at 600 m agl m at 380600 0.98 at 600 m agl agl m at 0.98600

0.0832 0.0832 32.3

970 to 2500 2500 970 to 1

(1100) (1100) 13.3 384 272 1.2 2.4 0.2 5.5

HyPlant Fluorescence Module Module Fluorescence consists of two of consists 1140 at 1780 m agl agl m 1780 at1140 2.94 at 1780 m agl m at 2.941780 0.98 at 600 m agl agl m at 0.98600 380 at 600 m agl agl m at 380600 < 0.01 at O < 0.01 0.03 at 0.03O at 0.01O at 0.23O at 0.25O 0.0 670 to 780 780 670 to 0.0832 0.0832 < 0.04 < 0.04 1 at O 1 (240) (240) < 0.5 < 0.5 1024 32.3 0.11 384

2 2 2 2 2 -B -B -A -B -A -B -B 2 -A -A eodd n h suy ra ehue (ua be: 50.87142° N beet: (sugar Selhausen area study the in recorded were Data 2010. (September) autumn and (July) summer between maize and beet sugar in (ETR transport electron photosynthetic maximum of rates level leaf in Changes 2: Table linearsensitivity. in 2012. of years acquisition severalairborne our and 2010 in measurements PAM the between occurred trends similar that on assume to Based safe is it leaves. varieties, crop the single of stability of physiological the and number measurements large a of integrate they because ETR The (22). extracted were canopy r te ft ih sml non- simple a with fit then are points data All canopy. the in leaves selected randomly Data 150 of minimum 2000). a at recorded al. were et (Rascher characteristics response light derive to protocol measurement a and analyser yield fluorescence chlorophyll Mini-PAM the using 6.44736°) E 50.87304°; This article isprotected rights by All copyright. reserved. Sugar beet Maize 1 2 Dynamic range [bit] range [bit] Dynamic Type Sensor type agl: above ground level. Accepted ArticlesCMOS:

“s cientificCMOS

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chip

– Summer (27 July) (27 July) Summer new CCD chip technology that combines different enh differentcombines technology that chip CCD new 253.0 10.7± 253.1 7.2± li er oe, n mxmm lcrn rnpr rts f the of rates transport electron maximum and model, near CMOS CMOS max 12

values are representative of canopy photosynthesis photosynthesis canopy of representative are values

Autumn (3 Sept) (3Sept) Autumn 296.8 19.7± 160.9 4.0±

MCT MCT ancements to achieve high light sensitivity withsensitivitylight high achieveto ancements 14

; .49° mie N maize: 6.44792°; sCMOS sCMOS 16

max 2

) This article isprotected rights by All copyright. reserved. Accepted Article

This article isprotected rights by All copyright. reserved.

Accepted Article

This article isprotected rights by All copyright. reserved. Accepted Article

This article isprotected rights by All copyright. reserved. Accepted Article

This article isprotected rights by All copyright. reserved. Accepted Article