Deep-SeaResearch,Vol. 28A,No. 9, pp. 901 to 919, 1981. Printed in Great Britain.

0198-0149/81/090901-19 $02.00/0 1981PergamonPress Ltd.

The Pacific shallow oxygen maximum, deep chlorophyll maximum, and primary productivity, reconsidered
ERIC SHULENBERGER* and JOSEPH L. REID? (Received 18 September 1980; in revisedform 10 January 1981; accepted 1 February 1981)

Abstract--In the open mid-latitude Pacific in summer, a subsurface oxygen maximum with saturation ratios reaching 120%or more is found below the maximum of primary productivityand above the deep chlorophyll maximum. This feature appears to arise from the photosynthetic production of oxygen,which is prevented from escapingto the atmosphere by a density cap created by surface warming during the summer. In high and low latitudes, or in areas where most photosynthesistakes place nearer the surface,or where the density cap is weaker, this accumulation may not be so effective and the degree of saturation may be less, even though the primary productivity may be greater. The excess oxygen (above saturation) found in the subsurface maximum can be used to estimate minimal rates of primary productivity at those depths. Productivity estimated from oxygen accumulation is much greater than the primary productivity measured by the 14C method. This suggests that the 14C method substantially underestimates true productivity not only in these regions but generally. INTRODUCTION THE SUMMER subsurface shallow oxygen maximum (the SOM) and its excess saturation (i.e., above 100~) have been encountered by many investigators, but most of the studies have dealt with nearshore areas, e.g., RICHARDS(1957) (fjords, English Channel, Gulf of Maine, and shallow waters near Iceland and Greenland) and SEIWELL (1934) (North Atlantic western basin). The cause of the SOM has been debated. DITTMAR (1884) found 0 2 supersaturation in some upper-layer Challenger expedition samples and concluded that, while supersaturation was possible at the sea surface as a result of warming, the measurements indicating supersaturation in the depth range 20 to 30 m must be in error, as he assumed photosynthetic production could not balance respiratory consumption at those depths. KNUDSEN (1899) found near-surface supersaturation around Iceland in May to July and ascribed it to production by phytoplankton. JACOBSEN(1912) noted a supersaturated SOM in the Mediterranean and also proposed that it was the result of production by phytoplankton. RAKESTRAW(1933) noted supersaturation of up to 114~o at l0 to 30 m in the Gulf of Maine and on Georges Bank in August; GRAN (1933) concluded that at those stations photosynthesis had been more intense at SOM depths than at the surface and pointed out that the depth of maximum saturation corresponded to the depth of maximum phytoplankton abundance. In nearshore waters east of Greenland, JAKHELLN(1936) found

* Natural History Museum, P.O. Box 1390, San Diego, CA 92112, U.S.A.
t Scripps Institution of Oceanography,A-030, University of California, La Jolla, CA 92093, U.S.A. 901

902

~.R. SIII~LIzNBFR(',I(Rand JOSEPtl [... RI~11)

up to 110",, saturation at 10 to 25 m in July and August, and related the values t,~ production beneath the strong summer density gradient of the upper few meters. That the excess saturation may result from photosynthesis was also mentioned by THOMPSOn,. THOMAS and BARNES (1934), STEFANSSON and RICHARDS (1964). ANDERSOr~ (1969). and HERBLAND and VOITURIEZ (1979). We propose that the high 0 2 saturation ratios found near the SOM in summer in midocean (a region not addressed by most of the earlier studies) are a result of in situ photosynthetic injection of O 2 into the water column. The 0 2 accumulates over the summer, because the overlying density cap retards its equilibration with the atmosphere.

"IHE DATA BASE

The sets of data best suited to this study were described by McGOWAN and WILLIAMS (1973), but on most expeditions it has not been possible to collect them. A minimal data set for this study should include T, S, 02, chlorophyll-a concentrations, and primary productivity measurements, all taken from the same set of bottles on the same cast, with close vertical spacing extending deep enough to define the maxima. These requirements appear seldom (if ever) to have been met in available data. Consequently, the data we will use must be drawn from many sources in order to describe the various features.

SHALLOW OXYGEN MAXIMUM

Over much of the North Pacific the depth of the 10017o 0 2 saturation ratio* (Fig. 1) corresponds roughly to maps of the depth of the winter mixed layer prepared by BATHEN (1972) and ROaINSON (1976). Exceptions are in the far northwest, where the 100% isopleth lies quite shallow in summer, and in the eastern equatorial zone, where the upwelling rate is such that the saturation ratio in the entire column is less than 100%. In winter the O/ saturation ratio in the mixed layer is about 100/o. In summer, however, there is a subsurface maximum nearly everywhere north of 10"N. Rein (1962) attempted to account for this maximum by physical processes alone. He proposed that the summer warming of the upper few meters and subsequent equilibration between the warmer surface waters and the atmosphere would reduce the near-surface 0 2 concentrations; the deeper, less thermally-disturbed remnant of the winter O2-rich water would remain and exhibit a subsurface maximum. Under these processes, the greatest 0 2 increment ( 0 2 concentration at the SOM less 0 2 concentration at the surface) might occur in regions where the seasonal range of sea-surface temperature is greatest. The latter occurs near 35 to 40 c' of latitude and it is in that zone that the O2 increment is greatest, reaching as high as 2 ml 1The above explanation may be appropriate in higher latitudes, but over a broad latitude band in the central ocean (about 25 to 4 5 in the North Pacific) the process does not account for the magnitude of the concentrations near the SOM. This is illustrated by the profiles of summer and winter 0 2 concentrations and saturation ratios (Fig. 2). The surface
* It is usual to calculate the 02 saturation value of a subsurface sample from its potential temperature, in situ salinity, and at a pressure of l atm regardless of in situ pressure. This is because exchanges with the atmosphere can take place only at the sea surface. The ratio of the actual 02 concentration to the equilibrium concentration, or saturation value, will be called the saturation ratio. It will be expressed in per cent to avoid confusion with other units. We use WEJss' (1970) formula for solubility of 02 in seawater.

The Pacific oxygen maximum, chlorophyll maximum, and primary productivity

903

Fig. 1. Depth (m) at which the O2 saturation ratio is 100%in summer. Data from the NORPAC, EQUAPAC, and EASTROPIC expeditions.

values are lower in summer than in winter, as might be expected because of warmer surface water, but in the depth range of the SOM 0 2 concentrations are higher in summer than in winter. In the central North Pacific the depth of the SOM corresponds fairly closely to the depth of the maximum saturation ratio. Maps of the maximum 0 2 saturation ratio at stations occupied during northern summer and the depth of the maximum are shown in

OXYGEN (mill) __~L.O i

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SATURATION

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f
(c)

lit~/t31/
~o
,

ZOO

,~o

o" (d)

% SATURATION

% SATURATION

,~o

Fig. 2. Profiles of dissolved 02 and 02 saturation in the North Pacific Ocean in winter (solid lines) and summer (dashed lines). (a)Hugh M. Smith Sta. 59; 26 Feb. 1954; 3531'N, 14700'W. NORPAC Horizon Sta. 60; 23 Aug. 1955; 3508'N, 14800'W. (b) Hugh M. Smith Sta. 68; 3 March 1954; 3102'N, 14300'W. NORPAC Stranger Sta: 80; 27 Aug. 1955; 3108'N, 14339'W. (c) Hugh M, Smith Sta. 84; 13 March 1954; 2800'N, 14658'W. Proteus Sta. 1320; 16 Sept. 1971 ; 2750'N, 14627'W. (d)Hugh M. Smith Sta. 82; 12 March 1954; 2503'N, 14658'W. Townsend Cromwell Sta. 0370; 17 Sept. 1964; 2500'N, i4759'W.

904
r

ERIt SHUt,ENBERGER JOSEPHL. R~]D and

Fig. 3. Saturation ratio (%) at the depth of the maximum 02 saturation ratio. Data from the NORPAC, EQUAPAC, and EASTROPICexpeditions.

Figs 3 and 4. The maximum ratios are found along 35 to 45N, where REID (1962) found the strongest 0 2 increments. Two other physical processes for providing the excess 0 2 might be considered. The first is in situ warming by radiation. If the temperature were increased and the 0 2 concentration held constant, an apparent excess 0 2 would result. However, the great excess of 0 2 found in the mid-latitude zone occurs at 25 to 50 m, much deeper than radiant heating is directly effective, and warming would not produce the summer increase in absolute concentration of 0 2 evident in Fig. 2. Secondly, the solubility of 0 2 is not a linear function of temperature and salinity, hence mixtures of O2-saturated waters of different temperatures and salinities can be supersaturated. This process cannot account for the high saturation ratios observed. Choosing realistic ranges for the central North Pacific, mixing of O2-saturated waters with temperatures from 10 to 20C and salinities from 34.5 to 35.0 x 10 -3 could yield at best only about 101'~o 0 2 saturation. Clearly the ratios observed in the summertime SOM (~> 120%)cannot have been created by such mixing. Deeper 0 2 maxima can also be produced by lateral spreading from high-latitude cold surface waters in winter, but this process does not result in saturation ratios above 100~o.

Fig. 4. Depth (m) of the maximum 0 2 saturation ratio in summer. Data from the NORPAC, EQUAPAC, and EASTROPIC expeditions.

The Pacific oxygen maximum, chlorophyll maximum, and primary productivity

905

STEFANSSONand RICHARDS(1964) studied the relation of dissolved 02 to water density off the coasts of Washington and Oregon. They found substantial supersaturation both inshore and offshore from April to October. Offshore, the subsurface 02 maximum occurs well below the primary productivity maximum; they felt it could not be attributed to local photosynthesis. They proposed that the offshore 02 maximum results from an offshore spreading along isopycnals of water bearing excess 02, photosynthetically produced in the surface layer inshore. While this explanation might apply for the coastal upweiling areas of the California Current, in the central ocean the greatest supersaturation is found beneath the sea surface (Fig. 4), at potential densities whose intersections with the sea surface do not show such high saturations.
DEEP CHLOROPHYLL MAXIMUM (DCM)

A summertime DCM occurs near 50 to 140 m over the central Pacific Ocean (Fig. 5). It does not appear to occur so deep in high latitudes (>~ 40o), in regions of high upwelling activity (e.g., the eastern tropical Pacific: PATZERT,1978; LOVE, 1970, 1971), in the coastal waters of the California Current, or in the zonal current system near the equator (VENRICK, McGOwAN and MANTYLA,1973). It has also been observed elsewhere: The Sargasso Sea (RILEY, STOMMELand BUMPUS, 1949; HoasoN and LORENZEN, 1972), the eastern tropical Atlantic (DANDONNEAU, 1975; GIESKES, KRAAY and TIJSSEN, 1978; HERBLAND and VOITURIEZ,1979), the Indian Ocean (LoRENZEN,1965), and the Gulf of Mexico (STEELEand YENTSC8, 1960; STEELE, 1964). The mid-latitude Pacific DCM appears to be a spatially continuous, transoceanic phenomenon and is principally a summertime feature (VENRICKet al., 1973; REVELANTE and GILMARTIN, 1973) (see Fig. 6). A shallower chlorophyll maximum may persist throughout the year near the equator. The Pacific DCM is widespread (Figs 5, 8) and usually very pronounced (Figs 6, 7, 8); it may vary somewhat in depth and intensity from station to station, perhaps as a function of internal wave activity (e.g., VENRICKet al., 1973 ; SHULENBERGER, 1978; DANDONNEAU,1979).

PRIMARY PRODUCTIVITY

Primary productivity is more difficult to measure than is chlorophyll and there are fewer productivity profiles available. Many productivity profiles are calculated (not measured) from other data such as surface irradiance, using chlorophyll measurements and measured (or assumed) extinction coefficients for light. We have used only data from ~4C measurements of primary productivity (usually simulated in situ productivity using the methods of STRICgLANDand PARSONS,1972).* Measured profiles usually show a subsurface maximum in primary productivity, considerably shallower than the DCM (VENRICKet al., 1973; SCRIPPS INSTITUTIONOF OCEANOGRAPHY(S.I.O.), 1974; KIEFER, OLSON and HOLMHANSEN, 1976). Figure 8 illustrates this relation, using data from several dates and locations in the North Pacific.
* We use 1(C measurements as reported. We are aware of the numerous problems in interpretation of t4Cuptake measurements of primary production (see, inter alia, YEtqTSCH, 1974; EPPLEYand SHARP, 1975 ; HOaSON, MORRISand PIRQUET,1976; EPPLEY, 1981, and contained references). It is beyond the scope of thispaper either to resolve those problems or to attempt to modify in detail the original investigators' data.

906

ERIC SHULENBERGI!R Josl PH L. RHI) and

Fig. 5. Locations where the deep chlorophyll maximum has been observed. For this figure, 'deep' means that chlorophyll profiles show a pronounced maximum at ~ 40 m, usually deeper than 60 m. Lines mark transects that included such observations; X's mark individual observations. Stippled area centered on ON, 180W is approximate (DANDONNEAU,1979). References: (1) SHULENBERGER (1978). (2) ANDERSON al. (1972). (3) ANDERSON(1969). (4) REVELANTE GILMARTIN(1973). et and (5) SAIJO,IlZUKAand ASAOKA(1969). (6) STEELE(1964). (7) LONGHURST(1976). (8) VENRICKet al. (1973). (9) DANDONNEAU (1979). (10) KIEFERet al. (1976). (11 ) LORENZEN(1965) (station positions not given). (12) LOVE(1970). (13)VENRICK(1979); S.I.O. (1978). (14) LOVE(1971). (15) KAWARADA and SANO(1969). (16) MARUMO(1970). (17) C.S,I.R.O. (1967).

The chlorophyll at the D C M shows a low, but positive, net rate of carbon fixation (ANDERSON, 1969; VENRICK e t al., 1973; KIEFER e t al., 1976), despite often being well below the 1~o light level, the traditional b o t t o m of the 'euphotic zone'. The net c a r b o n fixation occurring within the D C M can be up to 15 to 30~o of the total integrated water column primary productivity (ANDERSON, 1969; REVELANTE and GILMARTIN, 1973; KmFER e t al., 1976). There are occasional indications of a small

T h e Pacific o x y g e n m a x i m u m ,

chlorophyll maximum,

and primary productivity

907

SUMMER
0 0 ,04 .08 I J I I
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TEMPERATURE

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TEMPERATURE (C)

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F i g . 6. P r o f i l e s o f c h l o r o p h y l l a a n d t e m p e r a t u r e in the N o r t h P a c i f i c c e n t r a l gyre. T o p r o w : t h r e e stations from mid-summertime cruise TSDY-3 along 1978). Bottom row: four s t a t i o n s f r o m w i n t e r t i m e c r u i s e Zetes, a l o n g 1970). Dots represent actual sample depths.

28N UE BX E , ( S 155WH LN E GX (S.I.O.,

secondary maximum of primary productivity within the DCM [see Fig. lc in KIEFERet al. (1976); Table 2 in REVELANTE and GILMARTIN (1973); Fig. 1 in ANDERSON (1969), reproduced here as Fig. 8B]. We are not able to determine whether the percentage (above) or the presence of a secondary maximum are general features of oceanic productivity.
MEASUREMENTS MADE ON THE SAME CAST

On both TSDY-3 and INDOPAC-16 expeditions, CTD (conductivity-temperaturedepth) measurements were made simultaneously (on the same cast) with O2-chlorophyll bottle casts; the casts permit examination of the vertical spatial relationships of the SaM, DCM, and density gradients. On all 23 stations of cruise TSDY-3 (July and August 1973, along 28N from 16230'W to 14315'E; contoured sections in SHULENBERGER, 1978), both the DCM and the SaM showed clearly, with the SaM shallower than the DCM (Fig. 9). INDOPAC-16 data (July 1977, along 35N from 163 to 139W; data in S.I.O., 1978; contoured sections in VENRICK, 1979) also show a pronounced SaM distinctly shallower than the DCM (Fig. 10). Figures 9 (TSDY-3) and 10 (INDOPAC-16) show the density cap clearly; it is less than 30 m thick in the area of Figs 9, 10, and 11 in July (ROBINSON, 1976), and its pronounced density gradient inhibits vertical mixing of the near-surface waters with those below. The DCM occurs well below the strong density gradient. The

90~

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o- ~ (c) "~ t'k,.Sl'o.4(162*W) Sto. 8(~,58"W)

~\Sto 53 22-26's oT*4ew) I -,'l-~, " '

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7 O CHLOROPHYLL- .25 (mg/m 3 ) ,,50 2'5

Fig. 7. Data from several Pacific Ocean locations showing the large maximum in chlorophyll a concentration at depth and also showing station-to-station consistency of the deep chlorophyll maximum. (a) June to July, along 28N (SHULENBERGER, 1978). (b) September, at 28N, 155W (S.I.O., 1974). (c) July, along 35N (S.I.O., 1978). (d) South Pacific central gyre: note the much greater depth of the DCM here than in the North Pacific data (a to c, above). (South Pacific data from Piquero expedition, March to April 1969, courtesy Drs E. BRINTONand E. L. VENRUCK.
S.I.O.)

maximum 0 2 value usually occurs in the sample immediately below the m a x i m u m density gradient (Figs 9, 10, 11) and well above the DCM. Primary production goes on in both density cap and deeper waters. The greatest productivity occurs nearer the surface, usually within the density cap. It may be much higher than that at the depth of the m a x i m u m excess 0 2, but photosynthetically evolved 0 2 can outgas to the atmosphere only from water in the upper part of the density cap. Water below the density cap accumulates O2 faster than diffusive processes can export it and respiration can use it (see below), hence just below the cap a pronounced maximum in 0 2 concentration is developed. Autumn storms destroy the m a x i m u m by deep vertical mixing, which allows outgassing. The sequence of seasonal development and collapse of the SOM were illustrated by REID (1962) for North Pacific weather stations Papa (50N, 145W), Tango (29N, 135E), and Extra (39N, 153E), and for a CaICOFI (California Cooperative Oceanic Fisheries Investigations) station off Baja California (2632'N, 11748'W). Oxygen data from the N o r t h Atlantic central gyre [BRooKs and BERMUDA BIOLOGICALSTATION (B.B.S.), 1968] indicate a similar course of development.

The Pacificoxygen maximum,chlorophyllmaximum,and primaryproductivity

PHOTOSYNTHESIS (m~ C m'3 doy"t) CHLOROPHYLL-o (m9 m"3) 4 ~ 8 I0 12 14

909

0 E 0

,2 .4 .6 .8 tO ~ i i 1i ~ , , .' , .'
E

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OXYGEN (ml t"l)

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t

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t )

.40

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9O

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CHLOROPHYLL-o (m~m "31

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Fig. 8. Primary productivity and concentration of chlorophyll a vs depth for several North Pacific locations. (A) 28N, 155W, September 1973 (KIEFER et al., 1976). (B) 45N, 127W, July 1968 (ANDERSON, 1969; Fig. 1). ( C ) F o u r days' data from 28N, 155W, September 1968 (cruise C L I M A X - I ; S.I.O., 1974). (D) Data from June 1978 cruise INDOPAC-15, all near 28N, 155W (S.I.O., 1978). Chlorophyll and primary productivity were measured on separate bottle casts; each plot includes the most nearly simultaneous pair of casts; the usual separation was a few hours. (D~ = chl. Sta. 8; 1 prod. Sta. 1. D 2 = chl. Sta. 17; 1 prod. Sta. 2. D 3 = chl. Sta. 22; 1 prod. Sta. 3. D4 = chl. Sta. 26; 1 prod. Sta. 4. D~ = chl. Sta. 29; 1 prod. Sta. 5.) No oxygen data taken. * Productivity data (S.I.O., 1978) given as "Total production, m g C m - 3 " ; time unit not specified but assumed to be per day.

PRIMARY P R O D U C T I O N

CALCULATED FROM THE OXYGEN EXCESS

If the high 02 saturation ratios observed below the density cap are a consequence of primary productivity, then the excess of 02 over the equilibrium value may be a minimal measure (less respiratory and diffusive losses) of the primary production over the period of accumulation. We assume this excess 02 is produced by photosynthesis. The observed period of development of the excess 0 2 may be as short as 30 days (data from BROOKSand B.B.S., 1968), or as long as 6 months. Most of the available series suggest no longer than 4 months. We (conservatively)assume 120 days for production.
37

910

ERIC SHULENBERGERand JOSEPH L, REID

O-

CHLOROPHYLL-a (mg/m 3 ) ,02 .04 ,06 ,08 .~0

Station 2

C H L O R O P H Y L L - a (mg/m 3 )

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4.5 ~ 5,5 O X Y G E N (ml/l)
I I I I1 I I 1 II~l

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I' I "~1 I I I 50 5.5 O X Y G E N (ml/I)

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OXYGEN (ml/I) 22.5 23 24

cr t

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Cr t

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o-l

Fig. 9.

Data from crmse TSDY-3, July 1973, along 28N from ~162W

to ~ 1 4 3 E

(SHULENBERGER, 1978). Oxygen and chlorophyll determinations were on samples drawn from the
same Nansen bottle, or, calculated using CTD data taken during the same cast as O2 and chlorophyll sampling. No primary productivity data were taken. Bottle spacing was varied from station to station in an attempt to place the highest sampling density at the expected depth of the DCM. ? = suspect 0 2 value.

The Pacific oxygen maximum, chlorophyll maximum, and primary productivity

CHLOROPHYLL- a (mg/m 3 ) .,o .~ .~ .40 .so ' ' Station '4

911

i J I I P'~'".-....~

CHLOROPHYLL-o ( m g / m 3 ) .,0 2o I I I I I" Stotion

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CHLOROPHYLL-a ( m g / m
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I I I I I I l L

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CHLOROPHYLL-a ( m g / m 3 ) .10 .20 30

i = i l [ i i i i [ i

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,

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i I

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o-1

Fig. 10. Oxygen, chlorophyll, and , from four stations in the North Pacific in July, INDOPAC16 expedition. Sta. 2, 3046'N, 1633ffW. Sta. 4, 35N, 162W. Sta. 6, 35N, 160W. Sta. 8, 35N, 158W. (Data from S.I.O., 1978; contoured sections in VENRICK, 1979.) ? = uncertain value.

We emphasize that in much of the ocean's photosynthetic volume the Oz released by photosynthesis does not accumulate, but escapes to the atmosphere. The extreme case is the central anticyclonic gyr in winter: primary productivity still occurs at substantial rates (S.I.O., 1970), but stirring occurs often enough to allow effective exchange with the atmosphere, and the saturation ratio is very nearly 10W/o in the upper layer. The accumulation of O, released by photosynthesis in summer is strongly dependent upon the presence and intensity of the summer density cap. The greatest excess Oz concentrations in the open ocean are in the latitudinal zone of greatest seasonal temperature range at the sea

912

Es~<: SHULENBERGERa n d

JOSEPH

L. REID

rn~j C m - 3 hour'l Z.~k8 24.0 24.5

rn(j C

m-3

oI

L_
~ 25,4 I .I

0i5 J t J

hqur-I

"r
I I

~5
I I I I A 1 I .....

Pri. p r o d

""' .,........,...,.

"-../

.-/- K)0%o~

"

(a)

._.21 ....

~I,O0~ 02

4/-/
'%)
4.~ ~o ~
OXYGI:'N (ml I "I)

)
~:o
(rag m-3)

200

go

~
O X Y G E N (ml I" t)

6:o
(rng m - 3 )

~b

O'LOR(OHYLL-o

,b

.,~

8
o
, ~ i 23.5

~'~
oi5

CHLO~LL-o

.,b

.~

o
C ' " i i i J

oi~

rng C m "3 hour "1

mg (3 m "3 hour -I

,,~
i

,.?
l i i

,.o crt
24.5

ti~
2~0

t:.~.~/

24~0

..

.-........

02

-o2
'P" , /o

/(c)
ZOO

1
V , /o

OXYOZN I'~) (rot Jb

15

Jk

~h
~

/o

#,~ m-a)

Fig. 11. Data from 28N, 155W, cruis CLIMAX-2 (August to S=ptoraher, 1969; S.I.O., 1975). Three separate bottle casts are used in each composite graph; one for chlorophyll, one for Oz and at, and one for primary productivity. Each graph includes the three bottle casts nearst together in time, but the pictures are to an unknown degree spatially and temporally imprccis due to lack of simultaneity. Major points are: (i) productivity peak near surfaoc, (ii) ~ chlorophyfl maximum, (iii) shallow 02 maximum below the break in ot (usually betwn the peaks of productivity and chlorophyll). Data used (station numbers and bottle cast numbers by S.I.O., 1975): (a) Chl. [A1(12)], 02 and a, [A-1(16)], pri. prod. [A-I]. (b) Chl. [A-2-O6(a)], 02 and 6, [A-24)4], pri. prod. [A-2]. (c) Chl. [A 3-061, 02 and ar [A-3-04], pri. prod. [A-3]. (d) Chl. [A 7~6], O z and a t [A 7~4], pri. prod. [A-7].

The Pacific oxygen maximum, chlorophyll maximum, and primary productivity

913

surface ( a b o u t 40 latitude), which p r o v i d e s the strongest s u m m e r stratification in the u p p e r few meters a n d i m p e d e s the escape o f 0 2 to the a t m o s p h e r e . This zone is n o t necessarily the zone o f highest p r i m a r y p r o d u c t i v i t y . A t best, the excess 0 2 c a n n o t reflect all the p r o d u c t i v i t y , even in regions o p t i m a l for its a c c u m u l a t i o n , b e c a u s e even there the p r o d u c t i v i t y m a x i m u m lies n e a r e n o u g h to the sea surface for s u b s t a n t i a l escape to occur. W h e r e stratification is weaker, m o r e o f the 0 2 p r o d u c e d can escape a n d the a c c u m u l a t e d excess m a y indicate o n l y t h a t p r o d u c t i v i t y has t a k e n place a n d m a y b e a r no useful r e l a t i o n to its intensity. I t is u n f o r t u n a t e t h a t there are n o r e p o r t e d m e a s u r e m e n t s o f p r i m a r y p r o d u c t i v i t y in the zone o f greatest seasonal t e m p e r a t u r e range in m i d - o c e a n , where the greatest excess 0 2 is a c c u m u l a t e d (Fig. 3). O u r c o m p a r i s o n s o f excess 0 2 a n d p r i m a r y p r o d u c t i v i t y (below) are m a d e from 28N in the central Pacific, where the seasonal range o f t e m p e r a t u r e is only a b o u t 5 , at the station n e a r B e r m u d a in the N o r t h A t l a n t i c central gyre (range a b o u t 8), a n d at a b o u t 45N, quite n e a r the Pacific's east coast, hence n o t necessarily a p p l i c a b l e to mid-ocean.

Table 1. Comparison of rates of 02 production implied by 14C uptake and excess 02 measurements

Implied 02 production Max. excess oxygen (A) Central North Pacific (28N, 155W) Sta. A-l* Sta. A-2* Sta, A-3* Sta. A-4* KIEFERet al. (1976) t4C primary productivity
From 14C rate

Excess 02 + 120 days

0.77 ml 1-1
(at 66 m)

0.26mgC m-3 h -t
(at 6 4 m)

2.92 m l m -3 d - l ? 1.23 m l m -3 d-l"[ " 0.67 m l m -3 d - l ? 1.23 m l m -3 d - t ? 0.93 m l m - 3 d - i

6.42 m l m - 3 d - 1 4.42 m l m - 3 d - I 4.92 m l m -3 d -I 4.67 m l m - 3 d - i 6.0mlm-S d -~

0.53 mll -x
(o~ 60 m)

0.11 mgCm-3 h -t
(at 61 m)

0.59 ml I- t
(al 66 m)

0.06 mg C m - 3 h - 1
(at 64 m)

0.56 mi 1-t
(at 65 m)

0.11mgC m-3 h -t
(at 68 m)

0.72 ml 1- t (,, 6s ,) 0.84mll -t catso ,,~

0.5 I~gC 1- 1 d - t (day length not specified)

Cat 65 m)

(B) Sargasso Sea (B.B.S., 1960)

1.12mgCm-3d -1 (day length not specified)

Cat 47 m)~

2.09 m l m - S

d -I

7.0ml m-3

d-I

(C) NE North Pacific (ANDERSON, 1969)

1.23 mll -I (,~sg,~

1-2 mgCm-3 d -t (day length not specified)

(at 60 m)

1.9-3.8 ml m-3 d -t

10.3 mlm-3 d -1

Note that excess 0 2 may accumulate in fewer than 120 days, but is unlikely to take > 120 days, hence rates of 0 , production calculated from excess 02 may be much too low, but are unlikely to be too high. All possible losses of 02 are ignored. * Simulated in situ productivity data near 28N, 155W in August. Primary productivity station numbers from S.I.O. (1975). Oxygen data are taken from the hydrocast closest in time to the productivity casts (A-I and hydrocast AI-16; A-2 and hydrocast A2--O4;A-3 and hydrocast A2-16; A-4 and hydrocast A3-04) (op. cir.). t Daily productivity assumed equal to 6 times the hourly rate (see footnote on p. 914). ~: Average over May to September.

914

ERIC SHULENBERGER JOSEPHL. REID and

An ideal data set for such an estimate must include detailed 0 2, primary productivity, T, and S profiles taken on the same hydrocast. We have been unable to locate any such set. We have, however, been able to piece together sufficient data to allow reasonable calculations for three areas. The photosynthetic quotient (PQ) is the molar ratio of O 2 produced to CO 2 consumed, and we have assumed PQ = 1.0. More commonly, PQ is found to be between 1.1 (PARSONS, TAKAHASH1and HARGRAVE, 1977) and 1.35 (RYTHER, 1956; mean ---1.25), and occasionally as high as 1.5 to 2.0 (WILLIAMS,RAINE and BRYAN. 1979). The differences between a PQ of 1.0 and the observed P Q are a function of the form of nitrogen being utilized for protein synthesis by the plants, e.g., use of ammonia yields no 'extra' evolved 0 2, but use of nitrate does yield 'extra' 02. We choose to use a uniform PQ of 1.0, but point out that use of the extreme P Q values (1.5 to 2.0) would not resolve the discrepancy (see below) between primary productivity estimates based on excess 0 2 and 14C uptake. We neglect all uptake or release of 0 2 by zooplankton or bacteria, all inorganic sources and sinks, and all losses of 0 2 from the SOM by vertical transport processes; we believe these are conservative assumptions. (1) The most nearly ideal data set comes from the North Pacific central gyre (S.I.O., 1975). Four composite stations were developed (Fig. 11, Nos 1 to 4); each includes chlorophyll, tr,, O2, and primary productivity data from the set of hydrocasts closest together in time and space (see caption of Fig. 11). Because of the well-developed density cap (Fig. 11), these four stations appear well suited for preserving the SOM as it develops and provide sufficient data to calculate how tong it would take to accumulate the observed excess 0 2, given photosynthesis at the observed (t4C) depth-specific rate. The degree of saturation was calculated for all four stations (Fig. 4). At Sta. A - l , the maximum excess 02, 0.77 ml 1-1, was at 66 m. This was well below the pycnocline (Fig. I la). At 64 m, primary productivity was 0.26 mg C m - 3h t. As 1 mAC fixed yields 1.87 ml Oz, an excess 0 2 of 770 ml m -3 corresponds to 412 mg C m -3 fixed. Allowing 120 days (May to August) for accumulation, this 412 mg C m -3 yields a rate of 3.43 mg C m 3 d-~. This is twice the 14C rate of 0.26 mg C m -3 h l measured at 64 m at Sta. A - I , which would accumulate the excess 0 2 at that depth in 1584 daylight hours, or 264 6-h days.* At the other three stations in Fig. 11, calculated and 14C productivity values are in even worse disagreement (Table 1). The 0 2 production rates calculated from excess O z are probably low, because the sampling (done with bottles) is almost certain to have missed the peak 0 2 concentrations. Bottle sampling is equally likely to have missed peak productivity values ; however, available 0 2 profiles often show one or more extremely high values in the depthrange where primary productivity profiles show low values. All calculated 0 2 production rates are radically higher than (up to 5.4 times) the rates implied by 14C uptake measurements at the depth of the SOM. KIEFER et al. (1976) revisited 28N, 155'~W from 29 August to 2 September 1973 and measured a productivity rate of 1 mg C m -3 d - t at 5 a n d 30 m, and 0.5 mg C m -3 d -t at 50 m. The maximum excess O 2, at 50 m, was 0.72 ml 1-1, corresponding to a productivity of 3.2 mg C m - 3 d-- ~ if accumulated over 120 days (6 times that measured by

14C).
* EPPLEY and SHARP (1975) suggested that the total productivity over a 24-h period is about equal to the productivity measured (t4C technique) in a 6-h incubation experiment. The hourly productivity data for Stas A-- 1 and A ~ , (Table 1 ) are derived from such 6-h measurements (S.l.O., 1975 ); a more aceurate daily rate is probably 6 times the hourly rate and has been used in Table 1.

The Pacificoxygenmaximum,chlorophyllmaximum,and primary productivity

915

(2) Comparable features exist in other oceans. Oxygen measurements reported from the Sargasso Sea show the SOM in summer, with saturation ratios as high as 115~. We have compared the values of productivity estimated from the excess 02 at Sta. 236 in August (BROOKS and B.B.S., 1968) with the profile of primary productivity (B.B.S., 1960). The maximum excess of O2, 0.84 ml ! - 1 at 50 m, would require a primary productivity rate over 120 days of ~3.7 m g C m -a d -1. The value of primary productivity at 47 m, averaged May to September, was 1.12 mg C m -3 d -1 and would require 402 days to produce the excess 02 observed. MENZEL and RYTHER(1960), in their treatment of these data, presented the productivity rates in summer only per unit area of sea surface rather than volume; these cannot be compared directly with the calculation based on oxygen. (3) ANDERSON(1969) published one profile of 02, primary productivity, and chlorophyll at 4510'N, 12656'W on 26 July 1968. His values (using 02, T, and S as reported from the National Oceanographic Data Center) are: (1) 0 2 excess, 1.23 ml 1-~ at 59 m and (2) primary productivity at SOM, ~ 1 to 2 mg C m -3 d -1 at 60 m (read from his Fig. 1). The excess 02 would require 325 to 650 days' primary production at the rate he reported at SOM depth. The excess 0 2, however, requires a productivity of 5.5 mg C m -3 d -1 to accumulate in 120 days, or 3 to 5 times the rate observed at that depth and half the rate observed at 10 m, the productivity maximum. The foregoing calculations are summarized in Table 1. The 14C productivity observed near the SOM at 28N would have required 264 to 670 days to produce the 0 2 excess observed (ignoring losses). Even larger excesses of 0 2 occur near 40N (Fig. 3) in the area of the strongest summer density cap, but we have no 14C measurements to compare with them. While there are no complete seasonal sequences of all the appropriate quantities, there are enough 02 data within the area of maximum O2-saturation ratio near 40N (Fig. 3) to show that the O2 maximum is a seasonal feature, absent in winter and present in summer (Fig. 2). Choosing an extreme station in that area (Hugh M. Smith Sta. 97, at 3857'N, 15730'W, 8 August 1955 ; NoRPAc COMMI'FFEE,1960), the maximum saturation ratio is 130~o at 32 m, with an 02 excess of 1.69 ml 1-1, corresponding to 0.90 mg C 1-1. Allowing 120 days (April to July) for the excess 02 to develop implies a rate of -,~7.5 mg C m -3 d -1 (0.62 mg C m -3 h -1 over a 12-h day) at the depth of the maximum saturation ratio. For the entire water column above the depth of 100~ saturation (i.e., < 66 m) the mean excess 0 2 is 0.90 ml l- 1, corresponding to 0.48 mg C l - 1. This yields a rate for the column of 265 mg C m -2 per day, or an average for the column of 4 mg C m - 3 per day, even though the productivity of the upper few meters is not measured properly by excess oxygen. On the map of phytoplankton production prepared by F.A.O. (1972) the values for that area are about 100 mg C m -2 d - l , rising northward to about 150 mg C m -2 d -1 at 42N. Both values are less than the production estimated herein from total excess 0 2 in the water column, but our estimates must be a lower limit, because losses by outgassing, diffusion, and respiration have not been taken into account.
RESPIRATORY OXYGEN REQUIREMENTS

Although 02 production may be greatest at the primary productivity maximum, in the central ocean the excess 0 2 maximum lies deeper than the productivity maximum (Figs 8, 11). There are two obvious possible explanations: (1) that the productivity

916

[,;k~( SHULENBERGER JOS~PHL. RHD and

maximum occurs within the density cap (allowing outgassing) and (2) that there exists pronounced peak in 02 consumption at the depth of the productivity maximum In the open Pacific, zooplankton biomass appears to be relatively uniformly distributed (vertically) within the upper ~ 100 m. Available data do not support the existence within the upper 100m of a significant maximum of net-captured zooplankton or of microzooplankton (and by inference an 0 2 consumption maximum) near the depth of the productivity maximum. 'Net" zooplankton data from the North Pacific central gyre fail to show aggregation of zooplankton at the general depth of the productivity maximum (see Fig. 8 in McGOWAN and WALKER, 1979). Total microplankton carbon, total seston dry weight, and ATP (BEERS, REID and STEWART, 1975) also fail to show pronounced peaks within the upper IOO m. There is no clear evidence of a peak of 0 2 utilization by zooplankton anywhere within the upper ~ 100 m. There appears to be no general estimate of total metabolic activity of zooplankton vs depth (see ANDERSON, FROST and PETERSON, 1972; MENZEL, 1974; PARSONSet al., 1977), especially on fine scales in the upper 100 to 200 m. Therefore, we will estimate community O z consumption strictly from data on zooplankton caught in nets, ignoring phytoplankton, bacteria, nekton, much of the 'net-sized' macroplankton (e.g., successful net-avoiders), and microplankton. Mean 'net zooplankton' biomass over 0 to 100 m at 28N, 155W is ~35cc (10OOm)3 (McGowAN and WALKER, 1979; S.I.O., 19741. IKEDA'S formula (1974, p. 14, equation 4) implies a respiratory requirement of ,,~5.6710-61m-3h i 02 [mean mixed-layer temperature was ~24.5C during zooplankton sampling, S.I.O. (1974), Stas 1 and 2]. This converts to 73 ~tg C fixed m 3 d(24-day) needed to supply respiratory 0 2 for net zooplankton; this appears to be 11 to 2~ orders of magnitude smaller than the 02 production implied by 14C productivity measurements (Table 1: KIEFER et al., 1976; VENRICK et aI., 1973). The contribution of microzooplankton and bacteria to total respiratory requirements may be large (perhaps up to 90~; : see AZAMand HODSON, 1977). Including this requirement would increase the discrepancy between ~4C and excess 02 productivity estimates. It seems likely that the disappearance of the SOM, the change in 0 2 content, and the return to equilibrium result not from respiration but from fall convection and storms that mix the column and permit outgassing.
CONCLUSIONS

Much of the Pacific Ocean shows a pronounced excess in oxygen for a large fraction of the year, below the maximum in primary production and above the deep chlorophyll maximum (Fig. 11). In summer, the maximum 02 concentration and saturation ratio occur just below the strong shallow density gradient. For the large mid-latitude areas of high saturation ratio the SOM cannot be a remnant of deep winter overturn and cannot result from mixing processes. In those areas the SOM is probably caused by photosynthesis releasing 0 2 beneath the thermal cap; there it accumulates as excess 0 2 until the autumn overturn, when it escapes to the atmosphere. Our conclusion that primary productivity accounts for the SOM and the associated excess 02 can apply only to the large mid-latitude regions of the ocean where there is a strong density cap in summer. There is a summer density cap also in the subarctic Pacific, but in that zone the excess 02 occurs so near the surface that physical processes may make a substantial or even dominant contribution to the 0 2 profile. Near the equator,

The Pacific oxygen maximum, chlorophyll maximum, and primary productivity

917

photosynthesis takes place in a shallow upper layer of much weaker stratification and little or no excess O2 is observed. Rates of 02 evolution implied by several sets of ~4C uptake measurements at the depths of the SOM (i.e., below the density cap) are substantially lower than the minimal rates obtained from 02 concentration. We therefore conclude that the rates of primary productivity believed to hold in these specific locations (Table 1) and at the depths of the SOM are much too low [see also GIESKES et al. (1978), p. 199; TIJSSEN (1979) and contained references; EPPLEY(1981 ) and contained references]. The overall productivity of the open ocean may have been seriously underestimated.
Acknowledgements--We have benefitted from discussions with others, many of them at Scripps, and hope we have
not misinterpreted what they have told us. We particularly thank J. A. McGOWAN, R. W. EPPLEY, J. R. BEERS and M. M. MULLIN.S. ANDERSONand F. WILKESof S.I.O. were invaluable in ferreting out data from hidden or forgotten sources. E. L. VENRICK, E. BRnCrON and K. E. KENYON provided access to unpublished or newlypublished data. S. McBRIDE typed the manuscripts. Funding came from the U.S. Navy Olfice of Naval Research, Code 480 (Contract No. N00014-79-C-0200 to the San Diego Society of Natural History; No. N00014-79~2~0159 to Scripps Institution of Oceanography), the National Science Foundation, and the Marine Life Research Program of S.I.O.

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918

ERt( SHULENBERGERand JOSEPH L. REID

GIESKESW. W. C., G. W. KRAAYand S. B. TIJSSEN(1978) Chlorophylls and their degradation products in the deep pigment maximum layer of the tropical North Atlantic. Netherlands Journal ~['Sea Research, 12, 195- 204. GRAN H. H. (1933) Studies on the biology and chemistry of the Gulf of Maine, II. Distribution of phytoplanktot~ in August, 1932. Biological Bulletin. 64, 159 182. HERBLAND A. and B. VOITURn~Z(1979) Hydrological structure analysis for estimating the primary production in the tropical Atlantic Ocean. Journal of Marine Research, 37, 87 101. HOBSON L. A. and C. J. LORENZEN (1972) Relationship of chlorophyll maximum to density structure in the Atlantic Ocean and Gulf of Mexico. Deep-Sea Research, }9, 297 306. HOB.SONL. A., W. J. MORRISand K. T. PIRQUET(1976) Theoretical and experimental analysis of the '4C technique and its use in studies of primary production. Journal 0/ the Fisheries Research Board o! Canada. 33, 1715 1721. 1KEDA T. (1974) Nutritional ecology of marine zooplankton. Memoirs o/ the Faculo, of Fisheries. HokkaMo Universio,. 22, 1 97. JACOBSEN J. P. (1912) The amount of oxygen in the water of the Mediterranean. In: Report on the Danish oceanographical expeditions 1908-1910, Vol. l, pp. 207-236. JAKHELLNA. (1936) Oceanographic investigations in east Greenland waters in the summers of 1930-t932. Skritter om Svalbard og lshavet, 67, 79 pp. KAWARADAY. and A. SAYO(1969) Distribution of chlorophyll and phaeophytin in the western North Pacific. The Oceanographical Magazine, 21, 137 146. KIEFER D. A., R. J. OLSONand O. HOLM-HANSEN(1976) Another look at the nitrite and chlorophyll maxima in the central North Pacific. Deep-Sea Research, 23, 1199-1208. KNUDSEN M. (1899) Hydrography. The Danish lngolfexpedition, Copenhagen, Vol. l, Part 2, pp. 23 161. LONGHURST A. R. (1976) Interactions between zooplankton and phytoplankton profiles in the eastern tropical Pacific Ocean. Deep-Sea Research, 23, 729 754. LORENZEN C. J. (1965) A note on the chlorophyll and phaeophytin content of the chlorophyll maximum. Limnology and Oceanography, 10, 482 -483. LOVE C. M. (1970) Eastropac atlas, Vol. 4. NOAA Fisheries Circular No. 330. LOVE C. M. (1971) Eastropac atlas. Vol. 2. NOAA Fisheries Circular No. 330. MARUMO R. (editor) (1970) Preliminary report of the Hakuho Maru cruise KH-69-4, August 12-November 13, 1969. The North and Equatorial Pacific Ocean. Ocean Research Institute, University of Tokyo, 68 pp. McGowAN J. A. and P. W. WALKER(1979) Structure in the copepod community of the North Pacific central gyre. Ecological Monographs, 49, 195 225. McGowAN J. A. and P. M. WILLIAMS (1973) Oceanic habitat differences in the North Pacific. Journal o! Experimental Marine Biology and Ecology, 12, 187-217. MENZEL D. W. (1974) Primary productivity, dissolved and particulate organic matter, and the sites of oxidation of organic matter. In: The sea, Vol. 5, M. N. HILL, editor, Wiley-Interscience, New York, pp. 659-678. MENZEL D. W. and J. H. RYTHER (1960) The annual cycle of primary production in the Sargasso Sea off Bermuda. Deep-Sea Research, 6, 351 367. NORPAC COMMITTEE(1960) Oceanic observations of the Pacific: 1955, the NORPAC Data. Berkeley and Tokyo, University of California Press and University of Tokyo Press, 532 pp. Pxgsorqs T. R., M. TAKArlASHI and B. HARGRAVE (1977) Biological oceanographic processes, 2nd edition, Pergamon Press, New York, 332 pp. PA'rZERTW. C. (1978) El Ni~o watch atlas of physical, chemical, and biological oceanographic and meteorological data. Scripps Institution of Oceanography Reference Series 78-7, 24 pp., 318 figures. RAKESTRAWN. W. (1933) Studies on the biology and chemistry of the Gulf of Maine. I. Chemistry of the waters of the Gulf of Maine in August, 1932. Biological Bulletin, 64, 149-158. REID J. L. (1962) Distribution of dissolved oxygen in the summer thermocline. Journal t~f Marine Research, 20, 138 148. REVELANTE N. and M. GILMARTIN (1973) Some observations on the chlorophyll maximum and primary production in the Eastern North Pacific. Internationale Revue der Gesamten Hydrobiologie, 58, 819-834. RICHARDS F. A. (1957) Oxygen in the ocean. In: Ecology, Vol. I, Treatise on Marine Ecology and Paleoecology, J. W. HEDGPETH, editor, Memoirs of the Geological Society of America, 67, 185-238. RILEY G. A., H. STOMMELand D. F. BUMPUS(1949) Quantitative ecology of the plankton of the western North Atlantic. Bulletin of the Bingham Oceanographic Collection, 12, 1-169. ROBINSON M. K. (assisted by R. A. BAUER)(1976) Atlas of North Pacific Ocean monthly mean temperatures and mean salinities of the surface layer, Naval Oceanographic Office Reference Publication 2 (NOO RP-2), i-xix, 173 figures. RYTHER J. H. (1956) The measurement of primary production. Limnology and Oceanography, l, 72-84. SAIJOY., S. }IZUKAand O. ASAOKA(1969) Chlorophyll maxima in Kuroshio and adjacent area. Marine Biology, 4, 190 196. SCRIPPS INSTITUTION OF OCEANOGR^PHY (1970) Data report, physical, chemical, and biological data, Zetes Expedition, leg 1 (11-24 January 1966). Scripps Institution of Oceanography Reference 70--5, 67 pp.

The Pacific oxygen maximum, chlorophyll maximum, and primary productivity

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