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Interdisciplinary Studies on Environmental Chemistry—Marine Environmental Modeling & Analysis,Eds., K. Omori, X. Guo, N. Yoshie, N. Fujii, I. C. Handoh, A. Isobe and S. Tanabe, pp. 169–178.© by TERRAPUB, 2011.

The Roles of Marine Phytoplankton and Ocean Circulation inDetermining the Global Fate of Polychlorinated Biphenyls

Toru KAWAI1, Itsuki C. HANDOH2,3 and Noriyuki SUZUKI1

1Research Center for Environmental Risk, National Institute for EnvironmentalStudies (NIES), Onogawa 16-2, Tsukuba 305-8506, Japan

2Center for Marine Environmental Studies (CMES), Ehime University,Bunkyo-cho 2-5, Matsuyama 790-8577, Japan

3The Futurability Initiatives, Research Institute for Humanity and Nature,457-4 Motoyama, Kamigamo, Kita-ku, Kyoto 603-8047, Japan

(Received 15 October 2010; accepted 19 November 2010)

Abstract—A high-resolution (0.5° × 0.5° × 54 layers) ocean compartment ofthe Finely-Advanced Transboundary Environmental model (FATE) wasdeveloped to assess the global fate of persistent organic pollutants in theoceans. The new ocean compartment hosts three dimensional advectivetransports, bioconcentration in marine phytoplankton, and degradation. In thisstudy, we ran the improved FATE for a polychlorinated biphenyls congener(PCB153), and discussed the roles of ocean circulation and marine phytoplanktonin determining distributions of loads and sinks of PCB153 in the global oceans.Our model results suggested that the horizontal distributions of PCB153 couldvary significantly with water depths: In the middle and lower layers of theepipelagic zone, PCB153 were accumulated in the sub-tropics. By contrast, inthe bathypelagic and abyssopelagic depths, relatively high concentrations werefound at high latitudes in the North Atlantic and the Antarctic, where deepwaters such as North Atlantic Deep Water and Antarctic Bottom Water areformed. The biological PCB153 exports (i.e., phytoplankton detritus settling)appeared to be much smaller than the net physical downward transports to thedeep ocean.

Keywords: Finely-Advanced Transboundary Environmental model (FATE),Polychlorinated Biphenyls (PCBs), deep sea exports, global dynamics

INTRODUCTION

Polychlorinated Biphenyls (PCBs) supplied to the ocean from the atmosphere aretransported to below the ocean surface layer by ocean circulation, or are taken upby marine organisms such as phytoplankton followed by exports to the deepocean through their detritus settlings. Numerical modelling is a useful approachin predicting and quantifying such oceanic fates of PCBs. Recent modellingworks have suggested that PCBs exports to the deep ocean by both of the physical(i.e., deep water formation) and the biological (i.e., organic carbon settling)

170 T. KAWAI et al.

processes could be important sinks of PCBs in the environment (Dachs et al.,2002; Wania and Daly, 2002; Axelman and Gustafsson, 2002; Lohmann et al.,2006). However, these processes have been poorly understood.

The authors have recently developed a high resolution ocean compartmentof our global multi-compartment model for persistent organic pollutants namedFinely-Advanced Transboundary Environmental model (FATE; Kawai andHandoh, 2009; Kawai et al., 2009). The new ocean compartment enables us topredict three dimensional distributions of PCBs as a result of advective transports,and to quantify the amounts of PCBs exports to the deep ocean by phytoplanktondetritus settling. The objectives of this paper are to describe the internal processesof the new ocean compartment, and to discuss the roles of ocean circulation andphytoplankton in determining distributions of loads and sinks of PCBs.

MATERIALS AND METHODS

The FATE is a global high resolution multi-compartment model that computesnon-steady POPs biogeochemical cycles in and across the five environmentalcompartments (atmosphere, ocean, vegetation, soil, and cryosphere). Both abiotic(transport, phase partition, degradation, dry and wet depositions, and inter-compartment exchange processes) and biotic (bioconcentration in vegetation andin marine phytoplankton) processes associated with POPs dynamics areparameterized (see Fig. 1). The spatial resolutions of the atmosphere and theocean are 2.5° × 2.5° × 27 σ-layers and 0.5° × 0.5° × 54 layers , respectively. In

Fig. 1. Schematic diagram of FATE internal processes.

Global Fate of Polychlorinated Biphenyls 171

the next section, we describe the internal processes in the ocean compartment.The other processes have been summarized in Kawai and Handoh (2009).

The ocean compartment of the FATE

The ocean compartment of the FATE hosts 3D oceanic transports of dissolvedphase POPs, bioconcentration in marine phytoplankton, and the degradation. For3D transports, we used the same scheme as in the atmospheric transports, exceptfor the diffusion and source/sink terms parameterizations. Two governing equationssolved are the conservation equations for POPs (Eq. (1)) and the fluid (Eq. (2))masses, which are expressed, respectively, as

∂∂

= − ∂∂

− ∂∂

− ∂∂

+ + ( )ρφ

ρλ φ

φ ρφ

ρC

t a

u C

a

v C w C

zK SU V W

1 11

cos cos

cos,, ,

and

∂∂

= − ∂∂

− ∂∂

− ∂∂

( )ρφ

ρλ φ

φ ρφ

ρt a

u

a

v w

z

1 12

cos cos

cos,

where C is the tracer mixing ratio (i.e., concentration divided by density), ρ is thedensity, a is the radius of the earth; λ, φ, z and are the longitude, latitude, anddepth, respectively; u, v, and w are zonal, meridional, and vertical velocities,respectively; KU,V,W is horizontal and vertical diffusion terms, and S is source/sink term. In solving equations (1) and (2), the improved Botts’ advection schemewith fourth order accuracy was employed (Bott, 1989a, b; Li and Chang, 1996).This scheme is positive definite and mass-conservative, and therefore, appropriatefor use in the scalar transport sub-models. KU,V are computed by the simplestsecond order diffusion equation with horizontal diffusivities parameterized bySmagorinskys’ first order closure. No internal sources are assumed in the oceans,so that S is equivalent to the sum of degradative sink and net planktonic uptakeof POPs described below.

The two compartment model of Dachs et al. (1999) is used to describe POPswater-phytoplankton exchange processes. In this model the time changes ofconcentrations of phytoplankton matrix and cell are, respectively, calculatedfrom Eqs. (3) and (4).

dC

tk C k C k CP M

u W d P M G P M,

, ,∂= − − ( )3

dC

tk C k C k CP S

ad W des P S G P S,

, ,∂= − − ( )4

172 T. KAWAI et al.

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thly

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nd U

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ns.

Global Fate of Polychlorinated Biphenyls 173

where, CP,M, CP,S, and CW are the POPs concentrations of phytoplankton matrixand cell, and the dissolved phase in seawater, respectively; ku, kd, kad, and kdes arethe POPs-specific constants for uptake, depuration, adsorption, and desorptionrates, respectively; and kG is the growth rate. FATE does not solve the settlingprocesses explicitly, but simply assumes that the amount of detritus exports to thedeep ocean is equivalent to the phytoplankton growth within the euphotic zone(i.e., our model assumes that phytoplankton biomass does not change within atime integration interval). Given ku, kd, kad, kdes, and kG, Eqs. (3) and (4) aresolved. Also, the phytoplankton biomass (Bp) and euphotic layer depth (zeu) arerequired as inputs, because CP,M and CP,S are mass concentrations. For kG, Bp, andzeu, we estimated these values from satellite-based chlorophyll concentrations asdescribed in the next section.

The amounts of POPs degradative sinks at each grid are computed by solvingthe simplest first order equation as,

dC

dtk CW

O W= ( ), 5

where kO is the POPs specific degradation rate constant. In the current version ofthe FATE, spatial variation of kO is not taken into account.

Simulation settings and input/forcing data used

The model was run for PCB153 for the periods from 1931 to 2009, which isapproximately the past 80 years. To force the model, five categories of global datawere used as listed in Table 1. The “high scenario” of the Breiviks’ inventory(Breivik et al., 2007) and the climate data from the National Centers forEnvironmental Prediction and the National Center for Atmospheric Research(NCEP/NCAR) Reanalysis 1 (Kalnay et al., 1996) are, respectively, used foremission and as meteorology. The oceanic forcing data (i.e., velocities andtemperatures) are prepared using the outputs from the Ocean general circulationmodel For Earth Simulator (OFES; Masumoto et al., 2004). The last 10-yearsmonthly data of the original 50-years simulation are averaged and repeatedlyused. The biological input data (i.e., phytoplankton biomass and growth rate) areestimated from the Sea-viewing Wide Field-of-view Sensor (SeaWiFS) data andthe Carbon-based Production Model (CbPM; Behrenfeld et al., 2005). By usingCbPM, we could estimate the spatial and seasonal variability of the phytoplanktonbiomass and the growth rate and therefore the biological export fluxes to the deepocean. The global average of the monthly growth rates, which is equivalent to theinverse of the phytoplankton turnover time, varies from 0.3 to 0.9 (day–1). It isnoted that such turnover time tend to be shorter than the typical equilibrium timeof bioconcentration in phytoplankton (Seto and Handoh, 2009).

RESULTS AND DISCUSSIONS

We, at first, discuss FATE-predicted spatial distributions of PCB153 loads

174 T. KAWAI et al.

Fig

. 2.

Hor

izon

tal d

istr

ibut

ions

of P

CB

153

(a) e

mis

sion

from

the

yea r

s 19

31 to

199

0, a

nd th

e F

AT

E-

pre d

icte

d a n

nua l

me a

n c o

nce n

tra t

ions

for

the

yea r

199

0. T

he r

e sul

ts a

t (b)

sur

fac e

oc e

a n (

8 m

),(c

) lo

we r

mos

t la y

e r o

f th

e e u

phot

ic z

one

(84

m),

and

(d)

ba t

hype

lagi

c z o

ne (

1907

m)

a re

show

n.

Global Fate of Polychlorinated Biphenyls 175

and sinks for the year 1990, when oceanic PCB153 contents exhibited thetemporal peak. Four panels shown in Fig. 2 are (a) PCB153 emission from 1931to 1990, and (b), (c), and (d) the horizontal distributions of FATE-predictedannual mean concentrations in the oceans. We discuss, here, the results at thefollowing three different water depths: The surface layer (8 m) which interactsdirectly with the atmosphere (Fig. 2(b)), the lowermost layer of the euphotic zone(84 m), which indirectly interacts with the atmosphere and is biologicallyproductive (Fig. 2(c)), and the bathypelagic zone (1970 m; Fig. 2(d)).

PCB153 predominantly emitted from the industrial countries in the NorthernHemisphere such as the United States, European countries, and Japan (Fig. 2(a))were transported eastwards by temperate westerlies and mid-latitude surfacecurrents through the air-sea interactions. As a result, a zonal patch of pollutionwas formed in the mid-latitude surface oceans (Fig. 2(b)). The horizontaldistributions at 84 m differed considerably from the surface ocean (Fig. 2(c)). Atthis depth, PCB153 were intensively accumulated into the subtropics. In particular,elevated concentrations were found in the North Atlantic (we will call these “theoceanic hotspots of PCB153”). Although the physical mechanism causing thistendency may differ between the hydrographical sections, the hotspots in theNorth Atlantic could be explained by the clockwise subtropical gyre with weaksubsidence flow of high-salinity water originating from the Mediterranean.PCB153 transports to deeper oceans occurred at hydrographically-limited sections(Fig. 2(d)). At the bathypelagic zone, relatively high concentrations of PCB153were found in high latitudes in the North Atlantic and the Antarctic Ocean suchas the Weddell Sea. This could be explained by formations of deep waters suchas the North Atlantic Deep Water (NADW) and the Antarctic Bottom Water(AABW). Levels of concentrations at this depth, which are approximately threeorders of magnitude lower than the surface oceans, are very sensitive to thedegradation rate constant, kO, in Eq. (5). It should be noted that kO, which wasfixed to a uniform value throughout the globe, has a significant uncertainty; forkO in the deep ocean could be much smaller than that in the surface ocean, currentbathypelagic PCB153 concentrations are very likely to have been underestimated.

Figure 3 shows FATE-predicted monthly horizontal distributions of PCB153export fluxes by phytoplankton detritus settlings (Fbio.). Figure 3 also shows thelatitudinal distributions of Fbio., zonal and euphotic zone average of dissolvedphase concentration (CW

eu) and the growth rate (kGeu) for discussions. Not

surprisingly, the horizontal distributions of Fbio. were influenced by the horizontaldistribution of CW

eu. Therefore, Fbio. was elevated in the temperate and subtropicaloceans in the Northern Hemisphere. Quantitatively, Fbio. showed a distinctseasonal cycle; Fbio. was larger in the boreal summer than in the winter. Suchseasonality could be explained by the seasonal variation of kG

eu (i.e., in theNorthern Hemisphere, kG

eu is much larger in the boreal summer than in thewinter), because seasonal variations of CW

eu is not significant.In the preceding paragraphs, we discussed the spatial distributions of

PCB153 loads and sinks. Here, we quantified the amounts of physically- andbiologically-driven PCB153 exports to the deep ocean. The former and the latter

176 T. KAWAI et al.

Fig

. 3.

Hor

izon

tal d

istr

ibut

ions

of m

onth

ly P

CB

153

e xpo

rt fl

uxe s

by

phyt

opla

nkto

n de

trit

us s

e ttl

ing

(Fbi

o.).

Zon

a l a

nd e

upho

tic

z one

ave

rage

of la

titu

dina

l dis

trib

utio

ns o

f Fbi

o., d

isso

lve d

pha

se c

onc e

ntra

tion

(C

W),

and

phy

topl

a nkt

on g

row

th ra

te (k

G) a

re s

how

n in

the

righ

t. U

ppe r

a nd

low

e r p

a ne l

s a r

e th

e re

sult

s in

Ja n

uary

and

Jul

y fo

r th

e ye

a r 1

990,

re s

pec t

ive l

y.

Global Fate of Polychlorinated Biphenyls 177

are, respectively, defined as the net downward fluxes by ocean circulation tobelow the ocean mixed layer (∑Fphys.), and the export fluxes by phytoplanktondetritus settling (∑Fbio.). ∑Fphys. and ∑Fbio. were estimated to be 7.4 and 1.0(tons), respectively. From this result, we could conclude that physical PCB153exports to the deep ocean dominated biological counterparts in the past 80 years.Uncertainty and sensitivity analysis of our FATE predictions to prescribed inputparameters of FATE such as degradation rate constants is expected to complementthis study and to better understand POPs dynamics in the oceans.

Acknowledgments—This work was funded by the Ehime University Global COE“Interdisciplinary Studies on Environmental Chemistry” Programme under the Ministryof Education, Culture, Sports, Science and Technology, the Government of Japan. TK andICH were supported, respectively, by the Japan Society for the Promotion of ScienceGrants-in-Aid for Young Scientists (B) No. 21710033 and 22710044.

REFERENCES

Axelman, J. and Ö. Gustafsson (2002): Global sinks of PCBs: A critical assessment of the vapor-phase hydroxy radical sink emphasizing field diagnostics and model assumptions. GlobalBiogeochem. Cycles, 16, 1111.

Behrenfeld, M. J., E. Boss, D. A. Siegel and D. M. Shea (2005): Carbon-based ocean productivityand phytoplankton physiology from space. Global Biogeochem. Cycles, 19, GB1006.

Bott, A. (1989a): A positive definite advection scheme obtained by nonlinear renormalization of theadvective fluxes. Mon. Wea. Rev., 117, 1006–1015.

Bott, A. (1989b): Reply. Mon. Wea. Rev., 117, 2633–2636.Breivik, K., A. Sweetman, J. M. Pacyna and K. C. Jones (2007): Towards a global historical emission

inventory for selected PCB congeners—A mass balance approach-3. An update. Sci. TotalEnviron., 377, 296–307.

Dachs J., S. J. Eisenreich, J. E. Baker, F. C. Ko and J. D. Jeremiason (1999): Coupling ofphytoplankton uptake and air-water exchange of persistent organic pollutants. Environ. Sci.Technol., 33, 3653–3660.

Dachs, J., R. Lohmann, W. A. Ockenden, L. Mejanelle, S. J. Eisenreich and K. C. Jones (2002):Oceanic biogeochemical controls on global dynamics of persistent organic pollutants. Environ.Sci. Technol., 36, 4229–4237.

Kalnay, E., M. Kanamitsu, R. Kistler, W. Collins, D. Deaven, L. Gandin, M. Iredell, S. Saha, G.White, J. Woollen, Y. Zhu, M. Chelliah, W. Ebisuzaki, W. Higgins, J. Janowiak, K. C. Mo, C.Ropelewski, J. Wang, A. Leetmaa, R. Reynolds, R. Jenne and D. Joseph (1996): The NCEP/NCAR 40-year reanalysis project. Bull. Amer. Met. Soc., 77, 437–471.

Kawai, T. and I. C. Handoh (2009): Towards state-of-the-art dynamical modelling and riskassessment of Persistent Organic Pollutants (POPs) in the global environment. Int. StudiesEnviron. Chem., 2, 1–9.

Kawai. T., I. C. Handoh and S. Takahashi (2009): The rise of the Finely-Advanced TransboundaryEnvironmental model (FATE): A state-of-the-art model prediction of the global sink ofpersistent organic pollutants. Organohalogen Compd., 71, 1610–1615.

Li, Y. and J. S. Chang (1996): A mass-conservative, positive-definite, and efficient eulerianadvection scheme in spherical geometry and on a nonuniform grid system. J. Appl. Meteol., 35,1897–1913.

Lohmann, R., E. Jurado, M. E. Pilson and J. Dachs (2006): Oceanic deep water formation as a sinkof persistent organic pollutants. Geophys. Res. Lett., 33, L12607.

Masumoto, Y., H. Sasaki, T. Kagimoto, N. Komori, A. Ishida, Y. Sasai, T. Miyama, T. Motoi, H.Mitsudera, K. Takahashi, H. Sakuma and T. Yamagata (2004): A fifty-year eddy-resolvingsimulation of the World Ocean—Preliminary outcomes of OFES (OGCM for the earth simulator).

178 T. KAWAI et al.

J. Earth Simulator, 1, 35–56.Seto, M. and I. C. Handoh (2009): Mathematical explanation for the non-linear hydrophobicity-

dependent bioconcentration processes of persistent organic pollutants in phytoplankton.Chemosphere, 77, 679–686.

Spivakovsky, C. M., J. A. Logan, S. A. Montzka, Y. J. Balkanski, M. Foreman-Fowler, D. B. A.Jones, L. W. Horowitz, A. C. Fusco, C. A. M. Brenninkmeijer, M. J. Prather, S. C. Wofsy andM. B. McElroy (2000): Three-dimensional climatological distribution of tropospheric OH:Update and evaluation. J. Geophys. Res., 105, 8931–8980.

Wania, F. and G. L. Daly (2002): Estimating the contribution of degradation in air and depositionto the deep sea to the global loss of PCBs. Atmos. Environ., 36–37, 5581–5593.

T. Kawai (e-mail: kawai.toru@nies.go.jp)