low light adaptation and export production in the deep chlorophyll maximum layer in the northern...

Deep-Sea Research II. Vol. 40. No. 3. pp. 737 752. 1993. 0967~1645/93 $6.00 + 0.00 Printed in Great Britain. Pergamon Press Ltd

Low light adaptation and export production in the deep chlorophyll maximum layer in the northern Indian Ocean

FALK POLLEHNE,* BERT KLEIN a n d BERNT ZEITZSCHEL

(First received 19 March 1991 ; in revised form 8 July 1992; accepted 24 November 1992)

Abst rac t - -Phytoplankton standing stock and primary production rates were measured in the central northern Indian Ocean at 65°E and 18°N in the inter-monsoon period in May 1987. As the algal populations were dominated by minute forms difficult to assess by routine microscopic methods, main algal groups were identified by pigment patterns derived from HPLC-analysis.

Profiles of chlorophyll a showed a distinct max imum between 50 and 80 m depth, with up to 10- fold higher values than in the surface mixed layer. The main portion of this deep max imum was situated below rather than above the sharp chemocline at 50 m, which analyses of particulate C, N and P showed to be a biomass max imum as well.

In the mixed surface layer cyanobacteria dominated phytoplankton biomass and primary production, whereas the deep chlorophyll maximum was composed of small successive layers of cyanobacteria, coccolithophorids, dinoflagellates and diatoms. Prochlorophytes could be detected by the presence of divinylchlorophyll a throughout the whole water column.

Highest absolute rates of primary production were encountered at the nitracline at 50 m depth. Over nearly all of the photic zone, primary production rates were closely related to POC values, leaving the P/B ratio at about the same value from the 100% irradiation level at the surface down to about 1% at 60 m depth.

This adaptational ability was achieved by an increased pigmentat ion with depth, indicated by constantly decreasing POC/Chl a ratios in the water column. It seemed to be enhanced by a strict vertical succession of different phytoplankton groups that, by means of different sets of accessory pigments, might have obtained an additional advantage in low light adaptation.

The main ecological significance of the deep chlorophyll max imum layer at that time was its role as a source of export production while importing "new" nutrients from below the nitracline. HPLC and elemental analyses of sediment trap material proved this layer to be the source of most of the sedimenting particles. Calculations of nitrogen fluxes suggested the import and export terms to be well balanced.

I N T R O D U C T I O N

EVEN after more than a decade of intense investigations it is difficult to distinguish between that part of primary production that is recycled in the photic zone, and that portion that leaves the surface layer and fuels the energy demand of deep-sea life. Rates of this export are coupled to the nitrate based "new" production rates (DUGDALE and GOERING, 1967) on different temporal scales. In pelagic systems that approach steady-state as a result of physical stability these two rates should approach each other.

*Author to whom correspondence should be addressed, at: Institut fiir Ostseeforschung, SeestraBe 15, 0-2530 Rostock-Warnemiinde, Germany.

737

738 F. POLLEHNE et El.

There is, however, still a wide gap between the estimates of reduced carbon export to the deep sea and the measured rates of oxygen uptake of the deep sea benthos alone, even if the meso- and bathypelagic communities are neglected (JAHNKE et El., 1990). Particu- larly in the oligotrophic tropical oceans, the divergence between the view of a fast cycling, material limited epipelagic system, with virtually "nothing to lose", and the existing energy demand of mesopelagic and benthic biota that requires a certain export from the photic zone is conspicuous. To find an answer to this enigma two main issues must be investigated. One is the question of the rates, pathways and form by which reduced carbon is transported from the photic zone into the deep-sea. Although this problem has been addressed recently (KNAUER etal . , 1984; KARL etal . , 1988; CHo and AZAM, 1988; JAHNKE et El., 1990), a coherent answer is still not at hand. The second task, especially in tropical oceans, is to detect temporal or spatial structures in the pelagic system where "new" or export production can occur to a larger extent than previously thought. KNAUER et El. (1984) interpreted VERTEX sediment trap data by postulating a two layer production system in the tropical ocean that would work on different sources of nutrients and, therefore, comprise both modes of production in a vertical succession. COALE and BRULAND (1987) inferred this vertical separation of the production systems in the VERTEX-area from different 234Th residence times in the photic zone. GOLDMAN (1988) expanded this concept by additionally assuming periodic nitrate injection into the deeper production layer. This concept of spatial and temporal discontinuities was shared by PLArr et El. (1989) in a recent review.

During a cruise in the Indian Ocean in 1987 we studied production/sedimentation equilibria in the open Arabian Sea. At the end of the inter-monsoon period in May the pelagic system in this area is oligotrophic, it has a distinct vertical structure, and may in this way provide a model system for other tropical oceans with similar features.

MATERIAL AND METHODS

Samples were taken along the track of a drifter carrying sediment traps at 18°N, 65°E [Fig. l(a),(b)] during leg 3b of the R.V. Meteor cruise no. 5 in the Indian Ocean. Data discussed in this manuscript derive from the central drift station, which extended over 4 days, from 4 to 7 May, 1987. The only exception is a profile of HPLC-carotenoid measurements taken two days later (9 May) at the trajectory of the same drifter (Sta. 480).

Temperature and salinity were measured using a profiling Kiel Multisonde (ME- electronic, Trappenkamp) attached to the water sampler, and light profiles were obtained with a Licor-sensor (mod. 193b, Licor Inc., Nebraska).

Particulate and dissolved substances were sampled with a 12 bottle multisampler (General Oceanics). Dissolved inorganic nutrients (PO4, NH4, NO3, NO2, SIO4) were measured according to GRASSHOFF (1983) on an autoanalyzer.

Pigments filtered on GFF (Whatman) were estimated using two methods: Chlorophyll a was measured photometrically on board with the trichromatic method employing calculations described by JEFFREY and HUMPHREY (1975). Another set of filters was deep frozen and analyzed by HPLC-technique in the Kiel laboratory. For analysis and peak interpre- tation, methods of GIESKES and KRAAY (1984) were followed, including second runs of the extract for lutein/zeaxanthin separation. Divinyl- or red shifted chlorophyll a was analysed according to GIESKES and KRAAY (1983).

Particulate carbon and nitrogen (POC and PON), were analysed in a Perkin-Elmer

The deep chlorophyll maximum layer 739

(a) AREA OF RESEARCH

°N40 4.5 50 55 60 65 70 75 °E

INDIAN O C E A N 4 - - - - --~--~--- ~ ~k~

4.5 50 55 60 65 70 75 o

(b) Drift Track of Sediment Traps

and Hydrostations

ON

18,7

Leg 3b 18,5

434

. . . . . . . . . . . . . . . . . . \ ' 6 5 .......... ! . . . . . . . . . . . . . . . . . . . . i . . . . . . . . . . . . . . . . . . i .........

1 8 , I ............................................................... :: ..................... ~ ...... ~:93 ' : : .........

65,0 65,2 65,4 65,6 65,8 66,0 °E (a) Area of research; (b) drift track of sediment traps and hydrostations. Fig. 1.

~N

25

20

15

model B-140 elemental analyzer after the removal of inorganic carbonates by hydrochloric acid fuming. Particulate silica (PSi) was estimated after PAASCHE (1980). Due to analytical problems, absolute values may have been slightly underestimated, but the linearity of the measurement was verified. Primary production rates were measured with the X4C in situ incubation technique with 2-4 h incubation periods. A detailed description of the method and the results of fractionation experiments is given by JOCHEM et al. (1993).

Drifting sediment traps of the funnel-shaped Kid-trap type were deployed at 100 m depth, about 15-20 m below the lower end of the photic zone. The opening area was 0.5 m 2 and sampling glasses were exchanged in daily intervals. A more detailed description of the drifter, the preservation and preparation of the samples is given by Pollehne et al. (1993).

Density (sigma t]

24.0 25.0 I I

23.0 0

-20

-40

-60

-80

- t 0 0

740 F. POLLEHNE et al.

26.0 !

Depth (m] Sta. 464

Fig. 2. Physical structure of the watercolumn.

The profiles that are presented in the results section were measured while following the drift track of the sediment trap [see Fig. l(b) for trajectories]. During water sampling the ship kept as close to the drifter as possible, and there was no indication in any physical, chemical or biological parameter that the drifter moved differently from the water around it. The straight drift track indicates as well that no eddies or fronts were encountered. Two 40 x 80 mile grids with 40 stations each were covered before and after the drift station with profiles of temperature, salinity and fluorescence down to 150 m depth which showed homogeneous distribution in the whole area.

RESULTS AND DISCUSSION

The physical structure of the water column down to 100 m, which is typical for the whole open ocean leg, is presented in Fig. 2. The surface mixed layer was about 30 m deep during the whole period of observation. Profiles of inorganic nutrients (Fig. 3) showed a nitrate anomaly from 100 m downwards, where, due to bacterial nitrate reduction, the pool of nitrogenous nutrients is diminished. The N/P ratio in inorganic nutrients in the upper 1400 m of the water column never reaches the phytoplankton uptake ratio of 15 (REDFIELD et al . , 1963) so that phosphorus can accumulate even in the photic zone (we measured surface water concentrations of o r t h o - p h o s p a t e of >0.5/~mol all over the Arabian Sea). Nutrient profiles of the first 100 m show that the chemocline at about 55 m was in no way related to the mixed layer depth, and suggest a different regulation mechanism from physical mixing processes for the nutrient gradient. It seems to be solely controlled by the vertical distribution of algal populations.

Figure 4 shows the chlorophyll profile at the same station and the presence of an extensive deep chlorophyll maximum centered around the chemocline is obvious. There are observations that these maxima do not necessarily need to be biomass maxima as well (KIEFER et al . , 1976; PILLEN, 1989), but in this area the pigment maximum was clearly accompanied by peaks of organic carbon (Fig. 5). It shows the vertical distribution of


Nutrient S a l t s

0 0

20

40

60

80

t00

Depth

Fig. 3.

(umol am -3 ) , S t a . 4 6 5

3 6 9 t2 tB I I

( m ) Sta . 4 6 5

Vertical distribution of nutrient salts.

Chlorophy l ] a (mg m -3 )

0.0 0 .3 0 .6 0 .9 0 I I I

P

2 0 ~

6O

I

J t00

1.2 I

Depth ( m ) Sta . 4 6 3

Fig. 4. Vertical distribution of chlorophyll a.

particulate organic carbon and nitrogen (POC, PON) with values twice the surface concentration at the depth of the chlorophyll maximum. The question whether these particles may not as well be an assemblage of detritus can be best decided by looking at the C/N ratio of the material in the water column (Fig. 6). Particles throughout the observed depth range have an atomic C/N ratio of below 6 with an exception of a peak of close to 8 in about 60 m depth. This extremely low ratio for bulk organic mat ter is due to the fact that the largest part of the living biomass is in a very small size range of <5/~m, as shown by


Fig. 5.

POC , PON ( mmolm - 3 )

0

20

40

60

BO

100

2 4 6 8 |0 I I I I I

9

PON t POC

Depth ( m ) S t a . 4 6 3

Vertical distribution of particulate organic carbon and nitrogen.

4 0

-20

-40

-60

-BO

-iO0- Depth (m)

Fig. 6.

Sta. 463 C/N-Ratio of Papticles

8 10 12 [ [ [

6 I

'i ( O ~ o

O ~

Sta . 4 6 3

Atomic ratio between POC and PON.

JOCHEM et al . (1993) using fractionation techniques in biomass and production estimates. The composition of the phytoplankton population will be discussed later.

The dominance of organisms in the bacterial size range with a low proportion of structural carbon compounds and high protein content is the main reason for this low ratio. Microscopical examinations showed that most of the material was fluorescent or could be identified as bacteria, colorless algae or protozoans and only minor amounts of detrital particles were present. This again is backed up by the activity measurements in the chlorophyll maximum layer. Primary production rates (Fig. 7) closely follow the profile of particulate organic carbon at least down to about 60 m depth. This relationship can be


Primary Product ion Rate ( mg C m -3 h - t )

20

0.0 0

40

60

BO

100

0 .5 t . 0 t . 5 2 .0 2 .5

#

Depth ( m ) S ta . 4 6 3

Fig. 7. Primary production rate.

P/B-Ratio (rag C m - 3 h - t /mg C m - 3 )

0.00 0

20 '

40'

60

B0

t00

0.01 0 .02 0 .03 0.04 I I I I A O •

O ,1~O O •

A •

• O~, A •

A g O • A AqlO

l i d 0

I&O

Depth ( m ) S f a . 4 6 3 - - 5

Fig. 8. Ratio between primary production and POC at three stations.

bet ter seen in the ratio of production to POC [P/B, expressed as mg C (production) m -3 h-1/mg m -3 C (bulk POC)] in Fig. 8. This ratio had values between 0.01 and 0.02 within the top 55 m for the 4 days of the central drift station. No trend was evident over this depth range. Assuming a factor of 10-12 for the conversion from hourly to daily production rates, the turnover t ime of bulk POC from the surface to over 50 m depth would be in the range of 5-10 days.

If we consider the light conditions in the water column (Fig. 9, unfortunately the length of the light sensor cable limited the measurement to 45 m depth) the P/B ratio of the algae was independent of the incident light levels far into the deep chlorophyll maximum (1%


Light- IPP. ( /J EJnst. m -2 ) 0 500 t000 1500 2000

O " I I _ _ I $

~ level

-20

-40

-60

Depth (m) Sta. 4 6 4

Fig. 9. Vertical profile of light intensity (at noon).

POC / C h l . a Ratio 0

20

40

60

80

I00

200 400 600 I I I

d~°~° ~°'''''-'~°

P

Depth ( m ) Sta. 4 6 3

Fig. 10. Ratio between particulate organic carbon (mg C m-3) and chlorophyll a (mg Chl a, m 3).

light level at approx. 55-60 m) which covers more than 95% of the irradiation intensity in the photic zone. Similar observations were made by FURUYA (1990) who found no significant difference in algal growth rates between 10 m and the deep chlorophyll maximum layer in the western Pacific. This physiological ability may be due to adaptational processes that operated in two ways. Over the range of the constant P/B relation there is an increasing amount of chlorophyll a present in the material with increasing depth. The decrease of the POC/Chl a ratio with depth beneath the mixed layer (Fig. 10) shows a strong relationship to the decrease of light. At about 55-60 m depth, where this ratio does


Chlorophyll 8, b. Zeaxanthin

0.0 0.2 0.4 0.6 0.8 l.O 0 I I I I I

4O ~ C h l . a

60 ~ ~"Chl.b ?

@o

1oo

[rag m-3]

(a)

Depth ( m ] Sta. 480

F u c o x a n t h i n .

.0 0

20

40

6 0

BO

J O 0

t9-Hexanoyloxyfucoxanthln (mg m -3]

0.1 0.2 0.3 I I I

~ o

(b)

Depth ( m ) Sta. 4 8 0

Chlorophyll a

Dlvlnylchl. a

total Chl .a (mg m - 3 )

o.o 0.2 0.4 0.6 o.a ~.o 0 I L I I I

- 2 0

ZX • 0

-40 Dvc~hlaX'~hl~ca t. Chla I

-60 . ...,,A ~ . j o I

-aO (c)

- JO0 ( m Sta. 4 6 3 - 5

Fig. 11. Profiles of HPLC-Pigment analyses: (a) Chlorophylls a, b and zeaxanthin; (b) Fucoxan- thin and 19-hexanoyloxyfucoxanthin; (c) Chlorophyll a, divinylchlorophyll a and total

chlorophyll a.

not drop any further (here the physiological limitations of chlorophyll increase seemed to be reached), the P/B ratio shows a sudden decline. On the population level, increasing chlorophyll content per cell can be attributed to the dense vertical layering of different phytoplankton species assemblages. Normal routine counts of the samples with the inverted light microscope could not be performed because of the small size of the majority of the algae and because larger organisms like diatoms and dinoflagellates were too scarce in the usual counting volumes. Therefore, HPLC-pigment analyses were employed to identify single groups by their pigment patterns.


P a r t i c u l a t e Si ( nmol dm - 3 )

0

20

40

60

80

t 0 0

0 100 200 300 I I I

Depth ( m ) S t a . 4 6 4

Fig. 12. Profile of particulate silica.

Figures ll(a-c) show profiles that illustrate the close vertical succession of algal groups particularly in the chlorophyll maximum layer. High concentrations of zeaxanthin in the whole water-column indicate the presence of picocyanophytes (MANTOURA and LLEWEL- LYN, 1983); in its sole combination with chlorophyll a it proved them to be the dominant class in the upper part of the photic zone (microscopy showed no presence of Trichodes- m i u m or any other colonial cyanobacteria).

As chlorophyll b, zeaxanthin and divinylchlorophyll a coincided in the lower part of the chlorophyll maximum [Fig. l l(a) and (c)] in the absence of lutein (which would indicate chlorophytes), here a larger portion of the minute forms of algae consisted of prochlorophytes (GIESKES and KRAAY, 1983; CHISHOLM et aI., 1988). As we could perform only few analyses of divinylchlorophyll a we are not sure about the population size of these organisms in the upper part of the water column. Superimposed on the small forms in the deep chlorophyll maximum layer are prymnesiophyceans with their characteristic inven- tory of 19-hexanoyloxyfucoxanthin (MANTOURA and LLEWELLVN, 1983). Microscopical examination of material enriched over a 2/~m filter showed them to be coccolithophorids.

Below this coccolithophorid population, diatoms could be identified by their fucoxanthin content and a concomitant increase in particulate silica values (Fig. 12) at the same depth. The higher abundance of diatoms may explain the deviation of the C/N ratio at this depth as well (Fig. 6). The presence of these two latter groups could only be detected in the chlorophyll maximum layer, and the close layering particularly of these groups within a few metres substantiates the idea of a stable system where specialists had time enough to find their optimal place in the light/nutrient gradient (VENRICK, 1973). By this strong vertical layering an additional way of low light adaptation on the population level involving the inventories of accessory pigments of different algal groups may have developed.

As our main interest was to trace the pathways of export production, we followed these pigment fingerprints of the successive populations into the sediment traps below the photic zone. The results can best be visualized by comparing ratios between chlorophyll a and


15

14

13

12

11

10

9

8

7

6

5

4

3

2

1

0

Fig. 13.

Pigment Ratios (HPI.C) In 0 -30 m, 50-75 m I~/em and 100 m trap

chl o/chl b chl a/zea chl o/fuco chl o / 1 9 - h e x

But'face layer ~ Chl . -m~: lmum mmlrmmt W~p

Ratios between Chl a an(] accessory pigments in surface water, chlorophyll maximum layer and sediment trap.

accessory pigments in surface water, chlorophyll-maximum layer and sediment trap (Fig. 13).

There was a higher amount of chlorophyll degradation products detectable in the sediment traps than in the water samples. Due to the poisoning of the cups and the short (24 h) deployment, however, only a minor fraction of the chlorophyll a was lost as a result of degradation in the cups and no correction was made for this.

The ratio of Chl a/chl b is in about the same range in the chlorophyll maximum layer and in the trap but higher in the surface layer, suggesting a closer relationship between the former two particle groups. Chl a/zeaxanthin-ratios were low in the surface layer due to the dominance of picocyanophytes and high in the chlorophyll maximum zone both as a result of the general increase of chlorophyll a per unit cell carbon and the presence of other algal groups in this layer. The ratio in the sediment trap is in between, with a tendency towards the higher value. This can be due either to a mixture of sources with a higher proportion of the deeper layer or by a preferential sedimentation of zeaxanthin carrying material only out of the deeper layer. As a fair proportion of the total Chl a, the chlorophyll maximum layer could be identified as divinylchlorophyll a [Fig. 11(c)] belonging to prochlorophytes (CHIsHOLm, 1988) the probability exists that even these small organisms were (possibly


after being compacted in some form) sinking out of the productive layer. Unfortunately, trap material was not available for analysis of divinylchlorophyll a and microscopical methods can not identify prochlorophyte tissue in trap material, so that positive proof is still lacking.

An example of enrichment of compounds in the trap material, however, can be seen in both the Chl a/fucoxanthin and Chl a/19-hexanoyloxyfucoxanthin relation. Both pigments have a defined source. 19-hexanoyloxyfucoxanthin derives from coccolithophorids in the upper region of the chlorophyll maximum [Fig. 11(b)] and is preferentially present below the mixed layer but, as a small proportion of the population extends to above 30 m, it still can affect the ratio in the top layer because of the general low stock of chl a there. Fucoxanthin is an indicator of diatoms, and as it was highly enriched in trap material and as the only region where diatoms in the whole water column were accumulating was the center of the deep chlorophyll maximum, this area can be identified as a center of export production. Small amounts of peridinin in material from the chlorophyll maximum and the sediment traps suggest that dinoflagellates also played a role in export production.

There are at least qualitative indications on the mode of vertical transport. These can be drawn from SEM-electromicrographs of the trap material (kindly prepared by J. Goebel, Kiel). Figure 14(a)-(c) show different magnifications of the prominent particle type that could be observed in the trap material. These are faecal pellets in the range 200-400 pm and are presumably produced by calanoid copepods that were found primarily in the photic zone. Higher magnification [Fig. 14(b)] and a close up view of the contents of a broken one [Fig. 14(c)] show them to be completely filled with coccoliths and diatom fragments only covered by a thin peritrophic membrane. The inspected filters were densely covered with these pellets which contained (by rough visual comparison of volume) the largest fraction of particulate material on the filters.

With a synopsis of the observations described above, we return to the original problem. In the central Arabian Sea we found:

(a) a strong vertical layering of different phytoplankton populations with picocyanophytes dominating the surface region whereas the lower portion of the photic zone was occupied by diatom and coccolithophorid populations. As the former are generally classed with a "regenerating" type of microbial-loop system and the latter are more typical for "new" production environments, this suggests as well a vertical partitioning of the photic zone in different production systems.

(b) a phytoplankton population in the deep chlorophyll maximum layer that due to different modes of low light adaptation was able to utilize the high nutrient concentrations in and below the chemocline, thereby attaining the same specific and higher absolute primary production rates than populations in the upper mixed layer.

(c) qualitative indications are that a large portion of the particle flux out of the photic zone derives from the deep chlorophyll maximum layer in the form of faecal pellets.

These results show that the deep chlorophyll maximum layer, at least in the study area, is very likely a zone of export production in an otherwise regenerating pelagic system. In order to determine whether the rates of nitrate-based "new" production and the nitrogen losses from the photic system were quantitatively related, we compared nitrate fluxes into, and particulate nitrogen fluxes out of the photic zone. From the review of vertical nitrate flux estimates by MCCARTHY and CARPENTER (1983) we adopted an eddy diffusion constant (Kz) of 0.05 cm -2 s -1 and applied it to the mean values of the nitrate gradient in the chemocline of the central drift station [(6.04 + 1.24) × 10-6pmol • cm-4]. We chose a K z


Fig. 14. (a)-(c). Different magnifications of fecal pellets found in the sediment trap beneath the photic zone. Material inside the pellets consists almost solely of diatom and coccolitophorid

remains.

750 F. POLI~EnNE et al.


in the lower r ange as, in our case, the chemoc l ine was s i tua ted in a r a the r s tab le dens i ty g r ad i en t far be low the mixed layer (Figs 3, 4). The ca lcu la ted u p w a r d n i t ra te diffusion ra te was then (3.02 _+ 0.62) x 10 - 7 / ~ m o l N cm -2 s -1 or 260 + 53 ktmol m -2 day -1. M e a n

d o w n w a r d flux of pa r t i cu la te n i t rogen m e a s u r e d in the s ed imen t t raps a m o u n t e d to 235 _+ 105 # m o l N m -2 day -1. P r o v i d e d tha t the a s sumpt ions abou t the diffusion coeff icient are cor rec t and that d o w n w a r d diffusion of d isso lved organic n i t rogen can be neg lec ted , loss and gain t e rms in this pho t i c zone sys tem seemed to be well ba lanced . This s t a t emen t has to be qual i f ied , however , as an exact mass ba lance would have to t ake the c o m p l e t e inven tor ies of all forms of n i t rogen in the phot ic zone into account . W e were , however , not ab le to measu re d isso lved organic n i t rogen employ ing s t a te -o f - the -a r t me thods . A l t h o u g h dai ly var ia t ions of the i n t eg ra t ed values for P O N and D I N in the 75 m surface layer r e m a i n e d within a range that was much lower than the prec is ion of the me thods ( < 1% for the cen t ra l Stas 363-4) , a compa r i son of the P O N inven to ry (70,000 ktmol N m-2 ) with the flux ra tes of abou t 250 ktmol m 2 d a y - 1 shows that , even within the pa r t i cu la te poo l , an exact budge t ing is not poss ib le with our cur ren t ana ly t ica l prec is ion. Tak ing add i t iona l ly into account tha t the o b s e r v e d sys tem is la te ra l ly not c losed, we can mere ly s ta te that the pe lagic sys tem in the pho t i c zone s e e m e d to be work ing close to s t eady s ta te but with high par t ic le expor t ra tes . So at leas t in this case an add i t iona l input of n i t rogen due to i n t e rmi t t en t n i t ra te in t rus ions (PLATT et al . , 1989) was not necessary to expla in the loss ra tes . This may r a the r be the excep t ion than the rule , but if, due to the hyd rog raph i ca l condi t ions in the A r a b i a n Sea, it is at least a f r equen t p h e n o m e n o n in the i n t e r - m o n s o o n pe r iods , then this pa r t of the Ind ian Ocean might qual i fy as a good m o d e l sys tem for the t rop ica l ocean per se.

Acknowledgements--We acknowledge the kind help of R.V. Meteor's captain and crew. We thank P. Fritzsche, R. Hansen, U. Junghans and R. Werner for their work on board and in the Kiel laboratory and B. v. Bodungen for helpful discussions.

This research was funded by Deutsche Forschungsgemeinschaft grants DFG-Ze 119/t0 and DFG-Ne 99/21.

REFERENCES

COALE K. H. and K. W. BRULAND (1987) Oceanic stratified euphotic zone as elucidated by >4Th : ~2SU disequilibria. Limnology and Oceanography, 32, 198-200.

CHISHOLM S. W., R. J. OLSON, E. R. ZETTLER, R. GOERICKE, J. B. WATERBURY and N. A. WELSCHMEYER (1988) A novel free-living prochlorophyte abundant in the oceanic euphoric zone. Nature, 334, 340-343.

Cno B. C. and F. AZAM (1988) Major role of bacteria in biogeochemical fluxes in the oceans' interior. Nature. 332,441-443.

DUGDALE R. C. and J. J. GOEmN~ (1967) Uptake of new and regenerated forms of nitrogen in primary productivity. Limnology and Oceanography, 12, 196-206.

FURUYA K. (1990) Subsurface chlorophyll maximum in the tropical and subtropical western Pacific Ocean: vertical profiles of phytoplankton biomass and its relationship with chlorophyll a and particulate organic carbon. Marine Biology, 107,529-539.

GIESKES W. W. C. and G. W. KRAAY (1983) Unknown chlorophyll a derivatives in the North Sea and the tropical Atlantic Ocean revealed by HPLC-analysis. Limnology and Oceanography, 28,757-766.

GIESKES W. W. C. and G. W. KRAAY (1984) Phytoplankton, its pigments and primary production at a central North Sea station in May, July and September 1981. Netherlands Journal of Sea Research, 18, 51-70.

GOLDMAN J. (1988) Spatial and temporal discontinuities of biological processes in pelagic surface waters. In: Toward a theory on biological-physical interactions in the world ocean, B. J. ROTHSCHILD, editor, Kluwer Academic, pp. 273-296.

GRASSHOEE K., M. EHRHARDT and K. KREMLING (1983) Methods of seawater analysis, Verlag Chemie, Weinheim, 419 pp.


JAHNKE R. A. , C. E. REIMERS and D. B. CRAVEN (1990) Intensification of recycling of organic matter at the sea floor near ocean margins. Nature, 348, 50-54.

JEFFREY S. W. and G. F. HUMPHREY (1975) New spectrophotometric equations for determining chlorophylls a, b, cl and c2 in higher plants, algae and natural phytoplankton. Biochemie und Physiologie der Pflanzen, 167.

JOCHEM F. J., F. POLLEHNE and B. ZEITZSCHEL (1993) Productivity regime and phytoplankton size structure in the Arabian Sea. Deep-Sea Research II, 40,711-735.

KARL D. M., G. A. KNAUER and J. H. MARTIN (1988) Downward flux of particulate organic matter in the oceans: a particle decomposition paradox. Nature, 332, 438-441.

KIEFER D. A., R. J. OLSON and O. HOLM-HANSEN (1976) Another look at the nitrite and chlorophyll maxima in the central North Pacific. Deep-Sea Research, 35, 1199-1208.

KNAUER G. A., J. H. MARTIN and D. M. KARL (1984) Global ocean flux study. Proceedings of a workshop. National Academy Press, Washington D.C., pp. 136-150.

MCCARTHY J. J. and E. J. CARPENTER (1983) Nitrogen cycling in near-surface waters of the ocean. In: Nitrogen in the marine environment, E. G. CARPENTER and D. G. CAPONE, editors, Academic Press, New York, 487- 572.

MANTOURA R. F. C. and C. LLEWELLYN (1983) The rapid determination of algal chlorophyll carotenoid pigments and their breakdown products in natural waters by reverse-phase high-performance liquid chromatogra- phy. Analytica Chimica Acta, 151,297-314.

PAASCHE E. (1980) Silicon content of five marine diatom species measured with a rapid filter method. Limnology and Oceanography, 25,474-480.

P1LLEN T. (1989) Zur Phytoplanktonverteilung im Roten Meer und Golf von Aden w~ihrend der "Meteor"- Expedition (MINDIK 5/2) im Frfihjahr 1987. M.S. Thesis, Kiel University, 149 pp.

PLATI" T., W. G. HARRISON, M. R. LEWIS, W. K. W. Lt, S. SATHYENDRANATH, R. E. SMITH and A. F. ~'~zINA (1989) Biological production of the oceans: the case for a consensus. Marine Ecology Progress Series, 52, 77-88.

POLLEHNE F., B. ZE1TZSCHEL and R. PEINERT (1993b) Short term sedimentation patterns in the northern IndiuJ: Ocean. Deep Sea Research H, 40, 821-831.

REDFIELD A. C., B. H. KETCHUM and F. A. RICHARDS (1963) The influence of organisms on the composition of sea water. In: The Sea, Vol. 2, M. N. HILL, editor, Wiley and Son, New York, pp. 26-77.

VENRlCK E. L. (1982) Phytoplankton in an oligotrophic ocean: observations and questions. Ecological Monographs, 52,129-154.

low light adaptation and export production in the deep chlorophyll maximum layer in the northern...

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