Spectral Weighting Functions for the Effects of Solar Ultraviolet Radiation on Phytoplankton

Photosynthesis

Patrick J. NealeSmithsonian Environmental Research Center, Edgewater, MD

Supported by US-NSF(OPP & OCE), EPA and Smithsonian Institution

Inhibition of Phytoplankton Inhibition of Phytoplankton PhotosynthesisPhotosynthesis

•• Photosynthesis is limited by low Photosynthesis is limited by low irradiance (~ 1% incident)irradiance (~ 1% incident)

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Light Limited

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Light Limited Light Saturated

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Light LimitedLight Saturated

Inhibited

•• Photosynthesis attains a Photosynthesis attains a maximum, saturated rate at maximum, saturated rate at moderate irradiance (~10% moderate irradiance (~10% incident)incident)

•• Photosynthesis decreases from a Photosynthesis decreases from a maximum as irradiance nears maximum as irradiance nears midday levels (50midday levels (50--100%)100%)

NearNear--Surface Photosynthesis is Surface Photosynthesis is inhibited in inhibited in LagoLago TiticacaTiticaca

Neale 1987 Topics in Photosynthesis. 9Villafañe, et al. 1999 Freshwater Biol. 42: 215

Investigations of UV effects on Investigations of UV effects on phytoplankton photosynthesisphytoplankton photosynthesis

1964 Comparison of 14C photosynthesis in quartz vs. glass bottles shows that solar UV inhibits (Steeman-Nielsen, J. Cons. Perm. Int. Explo. Mar)

1980 Initial work with spectral treatments, showed that both UVA and UVB were important (e.g. Smith et al, Photochemistry and Photobiology)

1990s Several groups define weighting functions for UV inhibition of phytoplankton in culture and natural assemblages in Antarctica

From the beginning, the approach is based on combined exposures to PAR and varying amounts of UV

Biological Weighting Functions Biological Weighting Functions quantify quantify wavelengthwavelength--dependent effectsdependent effects

A tool to assess the effect of wavelength dependent changes in UV (climate change, O3 depletion)

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ChloroplastAntarctic Phytoplankton Lab DiatomDNA

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e R

espo

nse

Wavelength (nm)

UV Affects Multiple TrophicLevels:

•Bacterial Assimilation

•Phytoplankton Production

•Zooplankton and Fish Larvae Survival

280 300 320 340 360 380 400

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nerg

y

Wavelength (nm)0 500 1000 1500 2000

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hoto

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Total Irradiance280 300 320 340 360 380 400

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nerg

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Wavelength (nm)0 500 1000 1500 2000

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Total Irradiance0 500 1000 1500 2000

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Total Irradiance0 500 1000 1500 2000

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Total Irradiance280 300 320 340 360 380 400

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nerg

y

Wavelength (nm)0 500 1000 1500 2000

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hoto

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Total Irradiance280 300 320 340 360 380 400

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ativ

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nerg

y

Wavelength (nm)

Photosynthetic Photosynthetic Response to Response to

UV + PAR UV + PAR

280 300 320 340 360 380 400

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ativ

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nerg

y

Wavelength (nm)0 500 1000 1500 2000

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hoto

synt

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Total Irradiance

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Total Irradiance0 500 1000 1500 2000

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Total Irradiance280 300 320 340 360 380 400

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nerg

y

Wavelength (nm)

BWF/PBWF/P--I I modelmodel

PB = PsB (1− e

−EPUR

Ek )1

1+ Einh∗

Einh* = ε (λ ) ⋅ E(λ ) ⋅ Δλ

λ =280 nm

700 nm

∑

Cullen et al. 1992 Science 258: 646

Production Model for the Production Model for the Rhode RiverRhode River

•Measured BWFs May-Jul (n=8)•Irradiance Spectra

•28 d, June-July 1999•Measured with SR18 290-324 nm•Extended with full RT 325-400 nm•Spectra for range of Ozone using RT

•Measured Attenuation Spectra (n=16)

00.20.40.60.8

11.21.41.6

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Dep

th (m

)

P(UV+)/PM

P(UV-)/PM

Describing the effects of solar UV Describing the effects of solar UV on phytoplankton photosynthesis on phytoplankton photosynthesis

•• Responses are a composite of effects at Responses are a composite of effects at multiple wavelengths (UVmultiple wavelengths (UV--B, UVB, UV--A, PAR)A, PAR)

•• NearNear--surface residence times can vary surface residence times can vary from minutes to hoursfrom minutes to hours

Quartz CuvetteFilter Orientation

280 305 350370

335 295 320 395

The Photoinhibitron

2.5kW Xe

A Polychromatic Incubator for Experimental UV Exposures

Long Pass Filter

The Rhode River: Shallow Subestuary of Chesapeake Bay

PhotoinhibitronPhotoinhibitron TravelogueTravelogue1. A Temperate Estuary1. A Temperate Estuary

BWFs on monthly samples during 1995-1996 (n=23)

See: Banaszak and Neale, Limnol. Oceanogr. 2001

RHODE R.

D. C.

CHES

APE

AKE

BA

Y

BALT.

50 km

Continuous monitoring of optical propertiesSpectral irradiance profile stations

PhotoinhibitronPhotoinhibitron TravelogueTravelogue2. Antarctica2. Antarctica

Weddell-Scotia Confluence

Palmer Station

Field Seasons: October-December 1991, 1993, 1997-1999

About 40 BWFs in all

Our Research Platform: The RV Laurence M. Gould

There are clear variations in the There are clear variations in the sensitivity of photosynthesis to UVsensitivity of photosynthesis to UV

C-280 D-295 E-305 F-320 B-335 G-350 A-370 H-395

Palmer Station,

Antarctica

Ice Algae in Surface Ice Slurry

Phytoplankton, Moderate Pack Ice

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Irradiance (μmol m-2 s-1)

(gC

gC

hl-1

h-1

)

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tosy

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gC

hl-1

h-1

)

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ctiv

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Constant repairexceeds damage

Damage exceeds constant repair

Repair proportional to damage

No repair

Linear Transitional Steady State

Photosynthetic response to UV Photosynthetic response to UV is nonis non--linearlinear

Irradiance (BWFE)

Cumulative Exposure (BWFH)

The BWFThe BWFEE/P/P--I model I model

•• Inhibition is a function of doseInhibition is a function of dose--rate when damage and rate when damage and recovery balancerecovery balance

•• Kinetics of Kinetics of FF’’vv/F/F’’

mm (PAM): P steady after 15 min(PAM): P steady after 15 min•• Good model of PGood model of PBB over 1 h exposure to UVover 1 h exposure to UV--B,UVB,UV--

A+PAR (RA+PAR (R22 > 0.9)> 0.9)

PB = PsB (1− e

−EPUR

Ek )1

1+ Einh∗

Einh* = ε (λ ) ⋅ E(λ ) ⋅ Δλ

λ =280 nm

700 nm

∑

Ppot f

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0.25

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0.35

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Bonaparte Pt. X-21

Qua

ntum

Yie

ld

Time (min.s)

ψf/ψ0 = 0.58

τ = 6 min

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hoto

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Total Irradiance280 300 320 340 360 380 400

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ativ

e E

nerg

y

Wavelength (nm)

BWF/PBWF/P--I modelI modelPB = Ps

B (1− e−

EPUREk )

11+ Einh

∗

Einh* = ε (λ ) ⋅ E(λ ) ⋅ Δλ

λ =280 nm

700 nm

∑

Estimating a BWF Estimating a BWF --Difference MethodDifference Method

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AB

Wavelength (nm)

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Diff

Wavelength (nm)

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DiffEffect

Sum EnergyWeight =

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Sum Energy

Another Approach:Another Approach:Fit BWF to a general equationFit BWF to a general equation

ε(λ ) = e(m0 +m1λ +m2λ2 ) + c

ε(λ ) = e(m0 +m1λ )

Simple

Complex

As described by Rundel (1983)

N. P. Boucher, B. B. Prézelin, Mar. Ecol. Prog. Ser. 144, 223-236 (1996)

10 -6

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ε E (λ

) (mW

m-2

)-1

Boucher & Prézelin

300 400Wavelength (nm)

- 10 -5

- 10 -6

Estimating a BWF Estimating a BWF -- PCA PCA MethodMethod

00.020.040.060.08

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Component 1

-0.15-0.1

-0.050

0.050.1

0.150.2

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Component 2

-0.15-0.1

-0.050

0.050.1

0.150.2

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Component 3

10 -6

10 -5

0.0001

0.001

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0.1

280 300 320 340 360 380 400Wavelength (nm)

Weighting Function (εH(λ))

Weight

H1C1

H2C2

H3C3

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Eight Spectral Treatments

Irrad

iance

Sca

led to

390 n

m

Wavelength (nm)

BWF/PBWF/P--I model provides accurate I model provides accurate predictions of UV responsepredictions of UV response

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E*

inh (dimensionless)

Palmer - Lo

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11.21.4

Palmer - Hi

Photosynthesis is inversely related to UV weighted by estimated BWFs

PB =Ps

B

1 + Einh*

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ε E (m

W m

-2)-1

Wavelength

εE Palmer-Hi

εE Palmer-Lo

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Sensitivity of Chesapeake Bay Sensitivity of Chesapeake Bay Phytoplankton varies by an order Phytoplankton varies by an order

of magnitudeof magnitude

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X-13-94XI-3-94XI-21-94I-11-95III-7-95IV-6-95IV-18-95V-3-95V-16-95V-31-95VI-1-95VII-12-95VII-18-95VII-27-95VIII-2-95VIII-8-95VIII-22-95IX-13-95X-25-95XI-20-95

ε(m

W -1

m2 )

Wavelength (nm)

UV-B UV-A

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Average fallAverage winterAverage springspring -95% C.I.spring +95% C.I.Average summer

Wavelength (nm)

UV-B UV-A

But seasonal average sensitivity is less variable!

BWFsBWFs vary 10 fold in All vary 10 fold in All EnvironmentsEnvironments

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ε E o

r εH

-1 (m

W m

-2)-1

Wavelength

εE Palmer-Hi

εE Palmer-Lo

εH-1

WSC

εE MCM

10-6

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10-2

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ε Rhode Riverε Antarctica

Swiss Lakes

Weight of 1 h Exposure for Cumulative Exposure (H) BWFs

Average Sensitivity is Similar in Average Sensitivity is Similar in Temperate and Polar EnvironmentsTemperate and Polar Environments

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ε E or ε

H-1

(mW

m-2

)-1

Wavelength

ε Rhode River

ε Antarctic

Average Sensitivity is Similar in Average Sensitivity is Similar in Temperate and Polar EnvironmentsTemperate and Polar Environments

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10-2

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ε E or ε

H-1

(mW

m-2

)-1

Wavelength

ε Rhode River

ε Antarctic

Cf. Behrenfeld, et al. 1993

Behrenfeld et al.

UVUV--A is more important than A is more important than UVUV--BB

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a)

water column Egrowth E

irrad

ianc

e (m

W m

-2 n

m-1

)

Wavelength (nm)

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b)

weighted water column Eweighted growth E

wei

ghte

d irr

adia

nce

(nm

-1)

Wavelength (nm)

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c)

weighted water column E (DNA)weighted growth E (DNA)

wei

ghte

d irr

adia

nce

(mW

m-2

nm

-1)

Wavelength (nm)

UV Effects on WSC (S. UV Effects on WSC (S. Ocean) ProductivityOcean) Productivity

Average range of integral daily water column production (±46% overall)

Factor

Ozone Depletion (50%) -1 to -8%

Mixed Layer Depth ± 24%

Sensitivity (BWF) ± 28%

See: Neale,Cullen, Davis, Nature 1998

(± is the half range of (max-min)/avg)

What are the sources of What are the sources of variation in variation in BWFsBWFs??

•• Inherent differences between Inherent differences between taxataxa•• Nutrient availabilityNutrient availability•• Resource tradeoffs (survival vs. Resource tradeoffs (survival vs.

defense)defense)

Here’s where culture studies are useful!

Natural Assemblages are Natural Assemblages are More Sensitive than Cultures More Sensitive than Cultures

10-6

10-5

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10-2

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ε E or ε

H-1

(mW

m-2

)-1

Wavelength

ε Natural Assemblages

ε Cultures

Strong Exposure Does Result in Strong Exposure Does Result in Resistant AssemblagesResistant Assemblages

10-6

10-5

10-4

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10-2

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ε E or ε

H-1

(mW

m-2

)-1

Wavelength

ε Natural Assemblages

ε Cultures

MCM Culture

What is contribution of Differential Survival vs. Acclimitization?

Can Aquatic Organisms Modify their Sensitivity to UV ?•• Accumulation of sunscreens Accumulation of sunscreens

((MAAsMAAs))•• AntiAnti--oxidantsoxidants•• Repair capacityRepair capacity

–– DNADNA–– Proteins, lipids, etcProteins, lipids, etc

Corals on Great Barrier Reef photo from Walt Dunlap, AIMS

Variation in Variation in PhotoprotectionPhotoprotectionMAAs accumulation decreases sensitivity in wave band of absorbance

Neale et al. (1998) J. Phycol.34:928

Estuarine dinoflagellate, Akashiwosanguineumgrown in high vslow PAR

00.10.20.30.40.50.60.70.8

00.010.020.030.040.050.060.070.08

300 400 500 600 700

Abs

orba

nce

(m2 m

g C

hl-1

)

Wavelength (nm)10-6

10-5

10-4

10-3

10-2

280 300 320 340 360 380 400

ε (m

W m

-2)-1

Wavelength (nm)

LL

HL

Sensitivity to UV increases Sensitivity to UV increases under Nunder N--limitationlimitation

10-5

10-4

10-3

10-2

280 300 320 340 360 380 400

Gymnodinium

wavelength, nm

5μMN

N-replete

25μMNεE(λ)

Litchman, Neale & Banaszak Limnol. Oceanogr. (2002) 47:86-94

Polychromatic Polychromatic vsvsMonochromatic Experimental Monochromatic Experimental

ApproachesApproaches

•• Polychromatic more appropriate to Polychromatic more appropriate to predicting responses to solar radiationpredicting responses to solar radiation

•• Monochromatic studies more appropriate to Monochromatic studies more appropriate to mechanistic studies of damage and repair mechanistic studies of damage and repair mechanismsmechanisms

–– Mechanisms of inhibition by UVA exposureMechanisms of inhibition by UVA exposure–– Regulation of Regulation of photorepairphotorepair–– Efficacy of Efficacy of photoprotectionphotoprotection at cellular length scalesat cellular length scales

•• Poly Poly vsvs Mono comparison: Generality of Mono comparison: Generality of spectral shape (Flint & Caldwell)spectral shape (Flint & Caldwell)

•• Advantage of FEL Advantage of FEL –– high output in the UVA, high output in the UVA, narrow bandwidth, flexibility in time of narrow bandwidth, flexibility in time of exposureexposure

Thanks!Thanks!

Production Model for the Production Model for the WSCWSC

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4 8 12 16 20

P T (t) (

mgC

m-2

h-1

)

Time (hour of day)

•Measured BWFs•Broad Band Irradiance Measurements•Modeled Irradiance Spectra

•Single Day Climatology•Range of Ozone

•Average Attenuation Spectra•Range of Mixing Depths and Speeds

Next StepsNext Steps

•• Establish a simple assay system Establish a simple assay system to measure effect of to measure effect of monochromatic exposure (e.g. monochromatic exposure (e.g. PSII fluorescence)PSII fluorescence)

•• Test for nonTest for non--linear (2) photon linear (2) photon processesprocesses

BWF variation modifies inhibition BWF variation modifies inhibition and the effect of Oand the effect of O33 depletiondepletion

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No Mixing Shallow Mixing Deep Mixing

26 Oct27 Oct28 Oct30 Oct3 Nov4 Nov

Wat

er C

olum

n In

hibi

tion

(PT -

P Tcon

t)/P

Tcon

t

BWF

Production Model for the Production Model for the Rhode RiverRhode River

•Measured BWFs May-Jul (n=8)•Irradiance Spectra

•28 d, June-July 1999•Measured with SR18 290-324 nm•Extended with full RT 325-400 nm•Spectra for range of Ozone using RT

•Measured Attenuation Spectra (n=16)

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11.21.41.6

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Dep

th (m

)

P(UV+)/PM

P(UV-)/PM

UV Effects on Rhode UV Effects on Rhode River ProductivityRiver Productivity

Average range integral midday water column production (±18% overall)

Factor

Irradiance ± 5%

Transparency ± 7%

Sensitivity (BWF) ± 8%

See: Neale 2001 J. Photochem. Photobiol. B 62:1-8

“±” is the half range of (max-min)/average

The Next StepsThe Next Steps•• UV Responses Under Realistic Mixing UV Responses Under Realistic Mixing

RegimesRegimes–– Kinetics of Damage and RepairKinetics of Damage and Repair–– Measurements of Mixing RatesMeasurements of Mixing Rates

•• Systematic Understanding of BWF Systematic Understanding of BWF VariationVariation

–– Consistent differences between Consistent differences between taxataxa–– Nutrient limitation (cultures and natural populations)Nutrient limitation (cultures and natural populations)–– Resource tradeoffs (survival vs. defense)Resource tradeoffs (survival vs. defense)

Long Term ObjectivesLong Term Objectives

•• BWFsBWFs for multiple for multiple trophictrophic levelslevels• Photochemical transformations• Bacteria• Zooplankton

•• Predictions of Ecological ResponsesPredictions of Ecological Responses•• Shifts in Community StructureShifts in Community Structure•• Shifts in Shifts in TrophicTrophic StructureStructure

It couldnIt couldn’’t have been done t have been done without a lot of help!without a lot of help!

•• Rhode RiverRhode River–– AniaAnia BanaszakBanaszak, UNAM marine lab, Puerto , UNAM marine lab, Puerto

MorelosMorelos, MX, MX

•• Culture Studies, Swiss LakesCulture Studies, Swiss Lakes–– Elena Elena LitchmanLitchman, Rutgers University, NJ, Rutgers University, NJ

•• AntarcticaAntarctica–– Jennifer Fritz, RSMAS, Miami, FLJennifer Fritz, RSMAS, Miami, FL

Thank you!