Primary production off northwest Africa: the relationship to wind and nutrient conditions

Deep-Sea Research, 1977, Vol. 24, pp. 25 to 33. Pergamon Press. Printed in Great Bdtain

Primary production off northwest Africa: the relationship to wind and nutrient conditions SUSAN A. HUNTSMAN* a n d RICHARD T. BARBER*

(Received 29 March 1976; in revisedform 10 May 1976; accepted 15 May 1976) Abstract The flux of carbon in a eutrophic coastal upwelling region was studied in the Cap Blanc area off northwest Africa from March through May 1974. Primary production was consistently between 1 and 3 g C m 2 day - 1 except inshore, where turbidity limited light penetration. Productivity reached a maximum in the mid-shelf zone and then decreased as the water moved offshore and nutrient levels declined. Chlorophyll a averaged 63 mg m- 2 and was distributed similarly to carbon fixation. Assimilation numbers were inversely related to the intensity of the northeast trade wind. Photosynthesis was depressed during periods of deep mixing because the phytoplankton were maintained at an average depth corresponding to about the 10~ light level. The data indicate that mixing can limit primary productivity on a time scale of days and can make the difference between a moderately productive and highly productive upwelling system.

INTRODUCTION

A PREDICTIVEunderstanding of marine ecosystems that is useful to man will be based on a hierarchy of generalizations. The fundamental generalizations relating phytoplankton growth to the nutrient content of seawater have been established by REDFIELD (1934), RILEY (1947), SVERDRUP (1953), and others. These authors have established that broad scale variations in primary production both temporally and spatially are related to variations in the supply of inorganic nutrients and light. The advection of nutrient-rich deep water to the surface and the subsequent stabilization of the nutrient-laden water in the euphotic zone by solar heating is the fundamental mechanism supporting the high biological productivity of coastal upwelling ecosystems. In the decade since 1966 we have gained considerable ability to generalize about the upwelling phenomenon (SMITH, 1968; RYTHER, 1 9 6 9 ; DUGDALE, 1 9 7 2 ; WALSH, 1972). It has become clear that the next step in this process is to understand the functional characteristics that are responsible for the distinct differences among the world's major upwelling regions. Differences in meteorology, topography, and circulation may 25

have large consequences for the resulting ecosystem, determining what species can exploit the upwelling process and how abundant they will be. This paper is intended to be a step in expanding our knowledge from the direct relationship between primary production and nutrient levels to the more subtle relationship between primary production and changes in physical forcing functions. JOINT-I was an intensive study of the upwelling system in the Cap Blanc region of northwest Africa. Hydrography and productivity over the continental shelf were measured almost daily from late March to mid-May 1974. The relatively calm period of November through January had been replaced by steady winds averaging 10 m s- t and upwelling was well established. Aerial surveys made before the cruise revealed surface isotherms oriented parallel to the coast with no indication of plume development. Thus maximum resolution of spatial and temporal patterns in the system and optimal use of resources were achieved by concentrating on a single cross-shelf line. A transect at * Duke University Marine Laboratory, Beaufort, North Carolina 28516, U.S.A.

26

SUSAN A. HUNTSMANand RICHARDT. BARBER

18 °

,,

,j,

~50'

~

22 °

) / /"

G

•

•

/\

.(..,.

[]

17°~

cobo

[eO,.Q~_lU[]e

[A

z2 °

/ D~I::

IC~•CIeIi!: ;a

I'~1

,...,o:.

3Q'

•..::,. '. ". ...... •-:::;:...., ..

N

,

,

-..., .

~o

•

•

?

•

•

•

~.~;..

~°

.'..~:

I

18 o

Fig. 1. Location of productivity stations occupied during JOINT-I. G, O, U. R, and D designate reference locations routinely sampled on hydrographic tnmsects.

21°40'N that extended from 2 to 55 km off the coast was chosen. Figure 1 shows the location of productivity stations occupied during the cruise. The letters G, O, U, R, and D identify reference locations that received emphasis in the sampling scheme. Seven arrays moored along the same transect gave continuous wind and current records through much of the study period. This simultaneous coverage of meteorology, water circulation, hydrography, and primary productivity provides the data base necessary to characterize the response of the nutrient and phytoplankton fields to changes in the direction and intensity of the local wind stress. The dynamics of the hydrographic regime during the first half of the study have been described in detail by BARTON, HUYER and SMITH (1977). MITTELSTAEDT, PILLSBURY a n d SMITH (1975) reported circulation patterns during the same per-

iod. In summary, their data showed that the coastal upwelling regime was bounded offshore by a northward-flowing countercurrent that shifted its position between the outer shelf and 100 km offshore in response to the wind stress. Intensive subsurface onshore flow occurred over the mid to outer shelf at depths between 50 and 90m. Maximum vertical velocities (of the order of 10-" to 10 -2 cm s- l ) occurred at the shelf break, where water rose up the slope from 100 to 150 m and then became trapped in the subsurface onshore flow. The upwelled water reached the surface as a band whose width varied with the wind velocity. The maximum offshore surface flow, close to the coast, averaged 10 cm s- 1 (Fig. 2). Fluctuations in the wind occurred at I0- to 20-day intervals when an eastward shift occurred and the velocity diminished for periods of about 3 days. When the wind abated the surface offshore flow diminished almost immediately, and the countercurrent moved in close to the shelf break. MATERIALS AND MEYHODS

The water samples for determination of simulated in situ carbon productivity were collected between 0800 and 0900 in 30-liter Niskin bottles with a rosette sampler (General Oceanics) from the depths to which 100, 50, 30, 15, 5, and 1~o of the incident light penetrated as determined with a submarine quantum meter (Model EI-185, Lambda Instruments Corp.) Three samples were drawn from each bottle into screw-cap glass 150ml bottles encased in nickel screens (Perforated Products, Inc.) that reduced the light intensity to the same level as that occurring at the depth from which the sample was collected. To each sample bottle 10~tCi of NaH~4CO3 were added. One bottle of each set was incubated under natural illumination for 6 h (from 0900 to 1500) and one for 24 h. The third sample was immediately filtered to give an initial chlorophyll value and to determine the abiotic particulate carbon-14 incorporation, which was subtracted from the total activity fixed during the incubation. The relationship between carbon fixation (C) in the 6and 24-h incubation periods was consistent throughout the study (C24 = 1.72 × C6 +0.27).

Primary production off northwest Africa: the relationship to wind and nutrient conditions

G

0

U

'

'

R

~ "-----

e~'----'----JL- 0

D

'~,

I0

27

" ~

I00 E 200

f £3 5@0

I 80

I 60

]~/I1

I

40 Disfonce offshore,

l

I

i

20

0

km

Fig. 2. The mean onshore (positive) and offshore (negative) current velocities (cm s ~) in the study area from February through April. Closed circles represent current meter locations. Redrawn from M ITTELS'rAmT, PIt, LSRURYand Smm~ (1975).

All hourly values reported herein are based on 6-h incubations. Daily values are based on 24-h incubations. For determination of particulate carbon fixation, the water was filtered onto AA Millipore,~ filters (0.8pm) and rinsed with 0.01NHC1 in seawater. The filters were subsequently dissolved in 10ml of Aquasol (New England Nuclear Corp.), allowed to stand overnight to reduce chemiluminescence, and counted on a Beckman Model LS133 liquid scintillation counter. A counting efficiency of 70% was determined by the addition of internal standards of 14C-toluene. The activity of the 14C-bicarbonate label was monitored regularly because it declined somewhat with time due to exchange with atmospheric CO 2. Chlorophyll a was determined using the fluorometric method of LORENZEN (1966) on 25ml aliquots taken at the beginning and end of the 6- and 24-h incubations. The average of the initial and final values was used in computing assimilation numbers [mgC (mg Chla)- 1 h- 1]. Samples from each depth were filtered onto 0.8pm silver filters (Selas Flotronics) for determination of particulate organic carbon. The filters were dried for 24 h at 60°C and stored in tightly capped precombusted vials. Analyses were made upon return to the laboratory based on a modification of the technique of MENZEL and VACCARO (19641 using a Coleman model 33

carbon-hydrogen analyzer linked to a Beckman model 215B infrared analyzer. Blank values were derived from a second filter placed under the filter receiving the surface sample at each station and were subtracted from each of the six samples. During April and May potential productivity and chlorophyll a were determined on samples taken from 5-liter Niskin bottles on the hydrographic transects and from over the ship's side with a small PVC bucket every 15 rain while the ship steamed over the study area. The treatment of these samples differed from the simulated in situ samples in that incubations lasted only 2 h, during which all bottles received the same light intensity (3.9 × 10 2 peinsteinsm -2 s- ~) in a Sherer model CEL 34-7 incubator. This light intensity, equivalent to about 40% of full sunlight, was found to be saturating but not inhibiting for photosynthesis. The values for nitrate and silicate concentrations were taken from the report by FRIEBERTSHAUSER, CODISPOTI,

BISHOP,

FRIEDERICH

and WESTHAGEN(1975).

RESULTS

The cross-shelf distribution of productivity and nutrients The mean cross-shelf distribution of chlorophyll a, particulate organic carbon (POCk primary production, nitrate, and silicate in the euphotic

28

SUSAN A. HUNTSMAN and RICHARD T. BARBER

ions was only 70% of that on the mid to outer shelf, confirming the relatively poor physiological condition of the population. Low assimilation num6O bers in other upwelling systems have been ascribed 40 .._...O-...... "O.~ to the absence of natural chelating agents in the 20 oPOC g m-2x I0 water (BARBERand RYTHER, 1969 ; BARBER,DUGt I I I I I o DALE, MACISAAC and SMITH, 1971). Chelation Carbon fixed 4 g ri 2 day-I assays, which tested for growth stimulation upon 5 addition of the artificial chelator ethylenediaminetetraacetic acid (EDTA), were run at six of the nine inshore stations. In five of these stations no 0 I I I I I I enhancement of growth rate occurred in the Assimilation 5 number presence of 10-6M EDTA, indicating that an 4 ~ ~ mgC mqChto-lh-I absence of biogenic chelating agents generally was not the factor responsible for the low assimilation 2 numbers in the near-shore region. Probably reI duction of the euphotic zone by the high levels of 0 I I I I I I suspended sand and vigorous mixing, which main12 tained the cells below this zone for long periods, • Nitrate combined to produce a completely shade-adapted lO~'kx'N o Silicate 8]_ ~xk /zg o,oms I-' phytoplankton population with reduced photoI x. 6[- . . . . . ". k x , ~ . ~ synthetic capacity. As the water moved offshore primary production increased rapidly and then leveled off at 2 O[ D I R I l U I 0 i G I to 3 g C m - 2 d a y - I over the entire shelf. The I0 20 50 40 50 60 carbon: chlorophyll a relationship now reflected Distance offshore, km lower detrital carbon levels (Fig. 4). The regression Fig. 3. Changes in primary productivity and nutrient levels of carbon against chlorophyll, C = 91 +23 Chl a, with distance offshore along the line at 21°40'N. Values are had a correlation coefficient r = 0.69 indicating averages over the euphotic zone for the entire cruise period {March through May). almost one-half of the carbon variability could be accounted for by chlorophyll a. Assimilation numzone is described in Fig. 3. Next to the coast was a bers increased briefly then fell again as the water band of nutrient-rich water. However, high levels moved further offshore and nutrients decreased. of resuspended sediments and aeolian sand (MILLIMAN, 1977) in this region reduced the The relationship to the physical field A temporal picture of the cross-shelf primary euphotic zone to as little as 5 m, and productivity was low despite the high nutrients. A plot of production can be obtained by serially aligning carbon against chlorophyll a shows the large and surface potential productivity values observed variable fraction of non-chlorophyll associated between March 31 and May 10 from both hycarbon responsible for the turbidity of these waters drographic transects and surface maps. The result(Fig. 4). The low productivity at the inshore ing composite (Fig. 5) reveals pulses of high stations cannot be explained simply as the result of productivity during early April and early May. a reduction of the euphotic depth because assimi- Both occurred during periods of high and steady lation numbers [mg C (mg Chla)- 1 h- 1] were wind stress, and in both cases, chlorophyll a and also low, reflecting a reduced photosynthetic cap- carbon fixation increased simultaneously, so no acity of the phytoplankton (Fig. 3). The chlor- enhancement of assimilation efficiency was obserophyll a:phaeophytin ratio for the inshore stat- ved. These pulses, therefore, can probably be I ©0 8O

• Chlorophyll o

~

2

Primary production off northwest Africa: the relationship to wind and nutrient conditions

(a)

29

b) 400

400

3OO

300

°: •

•I *e •eeew

o c~

•

20C

•

%• • , . • ,,,

•

o•,

|

":~, 3; •

•t 8

.•

•

!

~0¢

I00

• •

0

I

I

I

I

I

2

5

4

0 Chlorophyll

o,

•

:-..

....~.~ •

Fig. 4.

o ee

#

2OC

•

--"

..

e•

I

I

I

I

I

I

I

I

I

i

2

3

4

5

6

7

8

9

mg m -5

Particulate organic carbon and chlorophyll relationships of (a) inshore stations and [b) mid to outer shelf stations. The low chlorophyll and highly variable detrital carbon values of the inshore zone are clearly indicated.

attributed to physical advection of a denser population or to changes in grazing pressure, but not to physiological enhancement produced by the introduction of favorable environmental conditions, which would increase the carbon fixation per unit of chlorophyll a. By equating potential productivity and 50~ light depth in situ values, sufficient data were available to define the temporal pattern of assimilation numbers. Figure 6 compares the changes in assimilation number in the mid-shelf region (28 to 4 2 k m from the coast) with wind velocity and nitrate levels. The correlation between nitrate and assimilation numbers (AN) was low; for all midshelf productivity stations during the cruise the relationship was A N = 27.2+2.3(NO3) with a correlation coefficient r = 0.47. On the other hand, the peaks in assimilation efficiency coincided closely with periods of reduced wind speed. Between April 7 and 8, assimilation numbers increased from 3.5 to 6.5. The wind at this time declined from 8 to 2 m s- 1 and reversed from northeast to southwest, a direction unfavorable for upwelling. Nutrient levels declined rapidly as uptake increased and replenishment through deep mixing declined. The northeast trade winds returned on April 10. By

17o30'

Longitude 17~dO'

17o25'

17°15 '

17010 '

I ...7~05'

I

~"-~"

".,4" °

•

U w ~•

• i i

• ,

• •e

.M ,

•

• 25-%

•~ •

,•

• .b"

' •, •

,. 60

~ . ': • '." .'.

t

" "' . . . .

• .'-<_

"'. •

-

d

~')

J . # . " . , 50

• •

• •

° •

\,/.

• i~

..

".." ."4 .'" .'. '. ~ _---~

,0LL ' f

•

. •

./ . . . . "

"~.

• /•-

•e •

'sLL

.'----_z •

15

40

Disf(~nce offshore,

•

"29 _t_~: •

20

50

•

".1' •

13

I0

km

Fig. 5. The temporal distribution of surface productivity (mg C m 3 h ~) over the shelf at 21°40'N during JOINT-I. These data are taken from potential productivity samples rather than simulated in situ samples (see Methods section). The vertical dashed line indicates the shelf break at 100 m.

30

SUSANA. HUNTSMANand RICHARDT, BARBER

(a)

Wind velocity

2I\

ms

"''i

/'"

6

",/

5

L4 I l v i /\ Assimilation number e/ \ m g C mg ChL °-' h-'

/\

I

I

I

/ \

/

\g

..~

• • Potentiol o In

• 50% o 01%

~-o

i

= o

Nitrate /~g atoms t-

i

i

i

lightdepth light depth

I

1

I

I

I

I

1

I

|

i

i

i

1

I

I

l

(b)

o

production

i

~3 6 ~2 E

production

situ

i

i

•

i

5

~4

/ ~ 2

,.,.

'%._

x., .

\.<,"

,

"~.~', 0

April

May

1

I

I0

20

30 40 50 60 70 80 Per cent incident i r r o d o t i o n

I

I

9o

I00

Fig. 6. The relationship of assimilation number to wind velocity and nitrate levels in the mid-shelfregion (28 to 42 km offshore). Assimilation numbers were taken from both surface potential productivitysamplesand from the 50% light depth of simulated in sit, productivity stations.

Fig. 7. Thelight-dependent responseof assimilation numbers of phytoplankton sampled during two differcnt wind regimes. (a) samples taken from 3 m (50% light) and 33 m (0.1% light) on April 9 during a low-wind (2 m s - 1) period when the mixed layer depth was less than 10m. (b) sample taken from 2m on April 3 during a high wind (14 m s- ~) period when the mixed depth was between20 and 30 m.

April 12 assimilation numbers had returned to their normal levels of 2 to 4 mg C (mg Chla) -1 h-1. A second 3-day low-wind period occurred from April 26 to 28. Assimilation numbers were again high on April 26, but had declined sharply by the time of the measurement of April 29, when the wind had begun to increase. Nitrate levels responded to the low wind and reached a minimum by April 29. High nitrate levels were not observed again in this series despite continued high winds.

for a sufficiently long period to become fully adapted to high light intensities, a process reported to require up to 2 days (STEEMANN NIELSEN and JORGENSEN, 1968). Consequently, productivity during high winds was lower than under stratified conditions, although not so low as in the turbid inshore region. Figure 7 compares the assimilation numbers from a stratified and from a mixed station as a function of light intensity. Samples in Fig. 7a were taken from a stratified station. The differentiation of the shallow (sun-adaptedl and deep (shade-adaptedl populations is seen in the higher assimilation values at higher light conditions in the near-surface sample. In contrast, a near-surface sample from a well-mixed station (Fig. 7b) showed a marked depression in assimilation efficiency at high light levels similar to that of the shadeadapted deep population (Fig. 7a). It was possible to initiate sun adaptation in this sample by maintaining it under full incident illumination for

DISCUSSION

The high winds produced a mixed layer that extended 5 0 m or more below the surface. Although this vigorous mixing maintained a continuous supply of nutrients to the euphotic zone over the inner shelf region, the data indicate that photosynthetic efficiency was reduced during these periods. Apparently, the strong mixing prevented the cells from residing in the upper euphotic layers

Primary productionoffnorthwest Africa: the relationshipto wind and nutrient conditions

Y ~7

L)

4° E

o

31

• Peru

<

180 o NW

~

i

/ .Q:

Africa

160

O0 o

120

E o

QO

,o ' ~o ' ~o ' ~

~

Per c e n t i n c i d e n t

~o '

¢o

~

~

,oo '

radiation

Fig. 8. Adaptation of assimilation efficiencyto high light intensities by phytoplankton from the same station shown in Fig. 7b. The near-surfacesample was permittedto adapt to full incident light for 24 h. & Before adaptation. • After adaptation. 24h (Fig. 8). Assimilation numbers increased sharply at the 30, 50, and 100~ light intensities, while there was little or no change at lower light levels giving a net increase of 1.3-fold over all light intensities. The low assimilation values at high light intensities (Fig. 7b) were characteristic of the simulated in situ samples collected during the study. Two-thirds of these stations demonstrated maximum assimilation efficiencies at the 15 or 30yo light levels, the remainder being at the 509/0 light level. The concept of depth of the mixed layer limiting productivity was first expressed by SVERDRUt' (1953). Although this process is normally related to seasonal patterns in the wind and temperature regimes, the studies of the northwest African system during JOINT-I revealed its importance on a time scale of days. Thus the continued high winds that produce strong upwelling may cause reduced productivity through light limitation. The brief calm periods during this study were too infrequent to increase significantly the overall productivity of the region. In contrast, the strikingly high productivity offthe Peruvian coast (RYTHER,MENZEL, HULBURT,LORENZENand CORWIN, 1971) may be attributed in part to the moderate (5 m s- t) and steady winds typical of the region. However, nutrients, which off Peru varied with distance from the coast rather than wind velocity, also play an

c o t~ E

o o o o

60

00 •

6

o 40

2O

o

%

• •

•

Q 000

• •

•

)~o°° °°

iL2 Nifr~¢e,

i~

z~

~a

/za_ a t o m s I-~

Fig. 9. A comparisonof the assimilationnumbersand nitrate levels off Peru and northwest Africa. The correlation of the enhanced photosyntheticefficiencyof the former region to its higher nutrient levelsis evident. important role in determining the assimilation efficiencies of the two regions. Figure 9 compares the nitrate values and the corresponding assimilation numbers (AN) measured during JOINT-I with those from a cruise off Peru in the spring of 1969 (ANONYMOUS, 1970). Assimilation numbers and nitrate concentrations are expressed as the mean values for the euphotic zone. Assimilation numbers are based on 24-h incubations because no 6-h incubations were made during the Peruvian cruise. The regression through all points is AN = 23.7+3.75(NO3) with r = 0.68. The relationship is surprising because MACISAAC and DUGDALE (1969) have shown that nitrate uptake by phytoplankton generally increases with nitrate concentration only to nitrate levels of about 4 p.g atoms l-1, then levels off. The coupling of carbon fixation to the uptake of inorganic nutrients needs further examination to explain this apparent discrepancy. JOINT-I was unusual not only in terms of the variety of variables that were measured but also in terms of the spatial and temporal intensity of

32

SUSAN A. HUNTSMANand RICHARDT. BARBER

sampling over the continental shelf. In comparing mixed layer (NEHRING, SCHEMAINDA and the results reported above with data from cruises SCHULZ, 1973 ; SCHULZ, SCHEMAINDA a n d NEHR o off northwest Africa, differences in sampling loc- 1NG, 1973). Although uncertainties are introduced ations and dates must be considered. GRALL, through the variations in methodology in these LABORDE, LE CORRE, NEVEUX, TREGUER and studies, it appears that the values for primary THIRIOT (1974) sampled several nearshore stations production obtained during JOINT-I are characduring CINECA-CHARCOT cruises I and III in teristic of the spring-summer upwelling season off the winter of 1971 and the summer of 1972. These northwest Africa, and are probably at or near the cruises between Cap Dra (29°N) and Cap Cantin maximum found during the entire year. (32°N) were in a zone whose upwelling source CONCLUSIONS water, North Atlantic Central Water, contained lower concentrations of nutrients than the South 1. The average value for primary production off northwest Africa during the spring of 1974 was Atlantic Central Water supplying the upwelling 2 m g C m - 2 d a y -1 region near Cap Blanc. Lower production would thus be expected in the northern zone, and in fact, 2. The average chlorophyll a value was 68 gm -2. productivity rates of only 0.2 to 1.7 g C m- 2 day - 1 were measured during the winter cruise. However, 3. Assimilation numbers were lower than in the during the period of strong upwelling and more Peruvian upwelling system. This depression intense radiation during July and August mean was partly attributed to lower nutrient levels rates of 2 to 3 g C m- 2 day- 1 were observed. and partly to light limitation resulting from a A 5-day drogue study was made by HERBLAND, deep and relatively constant mixed layer. LE BORGNEand VOITURIEZ(1973) in the region of 4. In the near-shore zone further reduction in Cap Timiris, 18 to 19°N, during early April 1972. photosynthetic efficiency resulted from even Here productivity reached 4.8 g C m -2 day- 1. more intensive light limitation caused by high However, upwelling in this region is not typical of levels of suspended material. the northwest African system, because of the 5. Both strong and weak winds can reduce primintensifying effect of a submarine canyon off Cap ary productivity in an upwelling ecosystem. Timiris. Surface nitrate levels exceeded 201.tg Strong winds produce a deep mixed layer and a atoms 1-1 compared to a maximum of 11 ~tg light-limited phytoplankton population. Weak atoms 1-1 encountered during JOINT-I, and it is winds, if prolonged, disrupt the upwelling process and the renewal of nutrients in the surface likely that areas of even higher productivity were layer, inducing nutrient limitation. present than were encountered on the drogue track. LLOYD (1971) reported productivity measurements on two transects in the Cap Blanc Acknowledgements We wish to thank Dr. RICHARD DUGDALE and Ms. JANE J. MACISAACfor their helpful discussions. region during the intense upwelling period of late Mr. BURTON JONES provided invaluable help in collecting and May and early June. On the nine stations oc- processing the productivity data. This work was supported by cupied, productivity ranged from 1.1 to the Coastal Upwelling Ecosystems Analysis program (CUEA), a program of the International Decade of Ocean Exploration 3.4 g C m-2 day-l, highest values being just (NSF Grant ID072-06422). beyond the shelf break rather than near shore. ESTRADA (1974) computed daily fixation rates REFERENCES during March 1973 to be generally below ANONYMOUS (1970) R/V T. G. Thompson cruise 36 (PISCO). Part I: Hydrography and productivity. Special Report. I g C m-2 d a y - 1 but no stations were occupied Department of Oceanography, University of Washington, Data over the mid or inner shelf. No seasonal studies of Report, 42, 97 pp. primary production have been published for this BARBER R. T. and J. H. RYTHER (1969) Organic chelators: factors affecting primary production in the Cromwell Curregion, but cruises of the Alexander yon Humboldt rent upwelling. Journal of Experimental Marine Biology and in the spring and fall of 1971 showed productivity Ecology, 3, 191 199. to be higher in the spring despite the deep wind- BARBERR. T., R. C. DUGDALE,J. J. MACISAACand R. L. SMITH

Primary production off northwest Africa: the relationship to wind and nutrient conditions

(1971 ) Variations in phytoplankton growth associated with the source and conditioning of upwelling water, lnvestigacibn pesquera, 35, 171 193. BARTON E. D., A. HUYER and R. L. SMITH (1976) Temporal variation observed in the hydrographic regime near Cabo Corveiro in the northwest African upwelling region, February April 1974. Deep-Sea Research, 24, 7 23. DUGDALE R. C. (1972) Chemical oceanography and primary productivity in upwelling regions. Geoforum, l 1, 47 61. ESTRADA M. (1974) Photosynthetic pigments and productivity in the upwelling region of NW Africa. T&hys, 6, 247 260. FRIEBERTSHAUSERM. A., L. A. CODISPOTI,D. D. BISHOP,G. E. FRIEDERICH and A. A. WESTHAGEN (1975) JOINT-I Hydrographic station data, R/V Atlantis II cruise 82. Coastal Upwelling Ecosystems Analysis Data Report 18, 243 pp. GRALL J. R., P. LABORDE,P. LE CORRE,J. NEVEUX,P. TREGUER and A. THIRIOT (1974) Caract~ristiques trophiques et production planctonique dans la r6gion sud de l'atlantique Marocain. ROsultats des campagnes CINECA-CHARCOT Iet IIl. Tbthys, 6, 11 28. HERBLAND A., R. LE BORGNE and B. VO1TURIEZ (1973) Production primaire, secondaire et r6g6n6ration des sels nutrifs dans I'upwelling de Mauritaine. Documents Scientifiques, Centre de Reeherehes Oc~anographiques, Ahidjan, 4,1 25. LLOYD I. J. (1971) Primary production off the coast of northwest Africa. Journal du Conseil. Conseil permanent international pour rexploration de lamer, 33, 312 323. LORENZEN C. J. (1966) A method for the continuous measurement of in vivo chlorophyll concentration. Deep-Sea Research, 13, 223-227. MACISAAC J. J. and R. C. DUGDALE (1969) The kinetics of nitrate and ammonium uptake by natural populations of marine phytoplankton. Deep-Sea Research, 16, 415-422. MENZEL D. W. and R. F. VACCARO(1964) The measurement of dissolved organic and particulate carbon in seawater. Limnolo¢ly and Oeeanoctraphy, 9, 138 142. MILLIMAN J. D. (1977) Effects of arid climate and upwelling upon the sedimentary regime off southern Spanish Sahara.

33

Deep-Sea Research, 24, 99-103. MITTELSTAEDT E., D. PILLSBURYand R. L. SMITH (1975) Flow patterns in the northwest African upwelling area. Deutsches hydrographische Zeitschrift, 28, 145-167. NEHRINGD., R. SCHEMAINDAand S. SCHULZ (1973) Beitr~tge der DDR zur Erforschung der kiastennahen Wasserauftriebsprozesse im Ostteil des n6rdlichen Zentralatlantiks. Tell II: Das ozeanographische Beobachtungsmaterial der Messfahrt vom 23.3 25.6. 1971. Geoddtische und Geophysikalische Veroffentlichungen, Reihe IV, heft 9, 62 pp. REDEIELD A. C. (1934) On the proportions of organic derivatives in sea water and their relation to the composition of plankton. James Johnstone Memorial Volume, pp. 176 192. University of Liverpool Press. RILEY G. A. (1947) Factors controlling phytoplankton populations on Georges Bank. Journal of Marine Research, 6, 54 73. RYTHER J. H. (1969) Photosynthesis and fish production in the sea. Science, 166, 72 76. RYTHERJ. H., D. W. MENZELE. M. HULBURr, C. J. LORENZEN and N. CORWIN (1971) The production and utilization of organic matter in the Peru coastal current, lnvestioaeidn pesquera, 35, 43 59. SCHULZ S, R. SCHEMAINDAand D. NEHRING (1973) Beitr~ge der DDR zur Erforschung der kiistennahen Wasserauftriebsprozesse im Ostteil des n6rdlichen Zentralatlantiks. Tell IIl: Das ozeanographische Beobachtungsmaterial der Messfahrt yore 16.9-17.12. 1971. Geoddtische and Geophysikalische Ver6ffentlichungen, Reihe IV, heft 10, 66 pp. SMITH R. L. (1968) Upwelling. Oeeanoyraphy and Marine Biology Annual Review, 6, 11-46. STEEMANN NIELSEN E. and E. G. JORGENSEN (1968) The adaptation of plankton algae. I. General part. Physiologia phmtarum, 21,401 ~113. SVERDRUP H. U. (1953) On conditions for the vernal blooming of phytoplankton. Journal du Conseil. Conseil permanent international pour rexploration de hi mer, 18, 287 295. WALSH J. J. (1972) Implications of a systems approach to oceanography. Science, 176, 969475.