On the production, composition, and distribution of organic matter in the Western Arabian Sea

Deep-Sea Research, 1965, Vol. 12, pp. 199 to 209. Pergamon Press Ltd. Printed in Great Britain.

On the production, composition, and distribution of organic matter in the Western Arabian Sea* J. H. RYTHEr';" and D. W. MENZEL';" ( Received 22 October 1964)

INTRODUCTION

DURING the period September-November, 1963, the R.V. Anton Bruun worked in the Western Arabian Sea, between Karachi and the Gulf of Aden, as a part of the U.S. Program in Biology, International Indian Ocean Expedition (IlOE). Similar cruises by other ships have been or will be made in the same area during the IIOE. Not until the results of these several surveys are compiled and compared can there be hope of understanding the complex circulation of the Arabian Sea on a seasonal basis and in relation to the reversing monsoon wind system. The following account will describe conditions in a limited area and at just one time of year, the calm interval in autumn between the Southwest and Northeast Monsoons. Its purpose is to illustrate the unusual physical and chemical environment in the Arabian Sea and the extraordinary levels of primary productivity which result. A second objective is to present new data relating to the authors' interests in the relationship between living and dead organic matter in the ocean, a study which was facilitated by the extreme range of biological productivity which was observed in the Arabian Sea and the waters immediately to its south. Cruise 4A of the Anton Brmm departed Mauritius on September 25, 1963, and occupied l0 stations (161-170) between Mauritius and Cape Guardafui, Somalia, befole reaching the Arabian Sea. Data from these l0 stations are included in the results to be discussed herein. In the Arabian Sea itself, 30 stations were occupied which together comprised a NE section along the central axis of the sea parallel to the Arabian coast, three sections from the central basin into and normal to the Arabian coast, and short sections across the Gulf of Oman and the Gulf of Aden (Fig. 1). At all of the 40 stations referred to above Nansen bottle casts were made, usually to the bottom but in some cases to only 2000 m, and the following variables were measured: temperature, salinity, dissolved oxygen, phosphate, nitrite, nitrate, silicate, dissolved and particulate iron, and dissolved organic carbon. Also at each station samples were taken with a large-volume plastic sampler from 5-8 depths within the euphotic zone for subsequent determination of part!culate carbon, nitrogen, and phosphorus, phytoplankton pigments, and carbon assimilation by the C 14 technique. Samples for the latter were taken from the depths to which *Contribution No. 1519 of the Woods Hole Oceanographic institution. This work represents a part o f the U.S. Program in Biology o f the International Indian Ocean Expedition. It was also partially supported by NSF Grant 1525 and AEC Contr_act AT(30-1)-1918 and Nonr 2196. ~Woods Hole Oceanographic Institution, Woods Hole, Massachusetts, U.S.A.

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100, 50, 25, 10 and 1 per cent of the incident light penetrated. The uptake of C :4 was measured for 24 hr on deck in incubators fitted with neutral density screens, thereby exposing the samples to the same fraction of incident sunlight to which they had been subjected in situ: In a second series of samples C~4-uptake was measured for 4 hr under artificial illumination of approximately 1000 foot candles. 65"

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All data from the cruise will be available from the National Oceanographic Data Center, Washington, D.C. The present discussion will be limited to consideration of certain aspects of the temperature, phosphate, oxygen, chlorophyll-a, primary productivity, and particulate organic carbon~. The concentration and distribution of dissolved organic carbon has been described elsewhere (MENZEL, 1964). NLLTRIENTS

AND

PRODUCTIVITY

The physical structure and chemical characteristics of the surface layers of the Arab;an Sea may be illustrated by means of a profile showing the distribution of ~:Refercnces to methods used : Phosphate (MuRPmr and RILEY 1962); chlorophyll-a (RICHARDS with THOMPSON, 1952 and CREITZ and RaCH^RDS, 1955, substituting Whatman GF/C glass filters for Millipore® filters); primary productivity (STEEMANNNIELSEN, 1952) with minor modifications; particulate carbon (MENZEL and VACCAgO, 1964); oxygen (Winkler titration with biniodate standardization).

On the production, composition, and distribution of organic matter in the Western Krabian Sea

201

properties along a line consisting of five stations in the central basin roughly 100 miles apart and extending in a S W - N E line towards Karachi. For contrast, a similar profile is shown for the North Atlantic (Sargasso Sea) as constructed from five stations occupied by R.V. Chain in February, 1962, along the 65°E meridian between 34 ° and 26°N (Fig. 2). By this it is not meant to be implied that the Sargasso Sea represents some kind of " standard " or " normal" ocean, but the differences between the two regions will serve to emphasize the features of the Arabian Sea which are especially pertinent to the following discussion. I,~RGAS$O 469

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The Sargasso Sea is ch~iracterized by relatively weak thermal stratification in the region of the permanent thermocline, which extends approximately from 600 to 900 m. At the latitudes illustrated there are seasonal changes in the surface waters with the development of a summer thermocline in the upper 100 m. The

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Arabian Sea, on the other hand, is permanently and strongly stratified near the surface with a gradient of 10-15°C in the upper 200 m. There is nothing comparable to the deep permanent thermocline of the North Atlantic. Nutrient levels in the Arabian Sea increase sharply with depth beginning very near the surface, and fertile waters lie close to if not within the limits of the euphotic layer (50-100 m in the Central Arabian Sea). A comparable nutrient gradient in the Sargasso Sea is seen only within the deep, permanent thermocline, so that the euphotic zone in that region is underlaid by several hundreds of meters of impoverished water. In addition to this difference, the general level of nutrients in the Arabian Sea are appreciably higher than in the North Atlantic. Phosphate concentrations within the upper 200 m of the Arabian Sea exceed those found at any depth in the Sargasso Sea. Phosphate is used here merely as an index of nutrients in general. Nitrate and silicate, which were measured, and undoubtedly other non-conservative nutrient elements are distributed much the same as is inorganic phosphorus. For example the nitrate maximum at Stn. 182 (Arabian Sea) was 56-2/~gA/l as compared to 29.0 jzgA/l at Chain Stn. 473 (Sargasso Sea). Roughly speaking, it could be said that nutrient concentrations in the Arabian Sea are about twice those in the North Atlantic. Clearly these two factors, the high levels of nutrients and their proximity to the surface, set the stage for high biological productivity in the Arabian Sea. Any vertical pertubation, whether it be wind-induced upwelling, divergence at current boundaries, Langmuir-type circulation, internal waves, or simple wind mixing, that can break down, disrupt or shift upwards even slightly the barrier of thermal stratification will turn the potential productivity to reality. Just as clearly, it is the monsoons which provide the energy required for these dynamic processes. It is not within the scope of this paper to describe or illustrate the various ways in which these forces may operate in the Arabian Sea. Many if not all of those named above are probably important at different times and places. In all likelihood they are highly localized and irregular in both time and space. One of the most obvious characteristics of the plankton production in the Arabian Sea during the cruise of the Anton Bruun was its patchy distribution. Commonly, the ship would drift, while on station, through areas of extremely dense plankton blooms which might vary in size from a hundred yards or less to several miles in diameter, but which were often sharply delineated by extremely clear and unproductive water. To describe in general terms the productivity of such a region is clearly a problem. The vertical distribution of dissolved oxygen further reflects the productivity of the Arabian Sea (Fig. 2). In contrast to the Sargasso Sea, where high levels of oxygen prevail to depths of 1000 m or more, the oxygen concentration in the Arabian Sea drops sharply immediately below the euphotic zone, in mirror image of the nutrient distribution. Concentrations below 1 mi/l were found as shallow as 100-200 m and only trace amounts were occasionally measured within the 5001000-meter depth interval. No anoxic water was found either during Cruise 4A or earlier the same yea, (January 1963) when the Anton Bruun first arrived in the Indian Ocean and made the Arabian Sea crossing between Aden and Bombay. Scientists on the Soviet Vessel Vityaz did, however, report anoxic sulfide-containing water at mid-depths in the Arabian Sea during the fall of 1960 (IVANENKOV and ROZANOV, 1961).

On the production, composition,and distribution oforganic matter in the Western Arabian Sea 203 The inverse relationship between high surface nutrient and productivity levels and low concentrations of dissolved oxygen in the underlying waters is a common aspect of fertile marine areas. Presumably, it results from the sinking of organic matter produced at the surface and its subsequent decomposition and oxidation below the euphotic zone. Most frequently this combination occurs in the upwelling regions along the west coasts of continents as in West Africa (HART and CURRIE, 1960), Peru (GUNTHER, 1936), and California (SvERORUr' and FLEMING, 1941). It is perhaps less common as far offshore as the central Arabian Sea and suggests that vertical turbulence with concomitant high productivity occurs throughout the entire region. Probably the most wide-spread and predictable example of high productivity in the Arabian Sea is that associated with upwelling along the Somali and Arabian coasts. Even here, however, the factors causing the upwelling are complex and undoubtedly vary seasonally as well as locally. During the Southwest Monsoon 194

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the strong and persistent winds which blow offshore or parallel to the coast may directly transport surface waters offshore with a resulting vertical replacement of deep, nutrient-laden water. These conditions were encountered by Discovery during the summer of 1963. In the preliminary report of that cruise (IIOE RRS. Discovery Cruise 1, the Royal Society, London; December 1963) profiles from offshore into the coast o f Arabia showed a marked shoreward uptilting of isotherms and phosphate isopleths, the 18° isotherm in one case rising frem 200 m at the offshore end of the section to the surface at the shoreward end. STATION =75

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In the same report the surface currents were described as a " predominantly north-eastward flow close to the coast." I* cannot be certain whether these water movements were local phenomena produced in situ by the monsoon winds or whether they were part of a much broader surface circulation, perhaps involving the entire Arabian Sea. If the latter, the associated upwelling could be considered as geostrophic in nature rather than directly wind driven.

On the production,composition,and distributionof organic matter in the WesternArabian Sea 205 During October-November, on the other hand, the above question did not arise. This was the period between the Southwest and Northeast monsoons : the wind was calm and the sea, flat. What little breeze did develop usually blew from the north or east. There could be no possibility of the surface water being wind driven offshore from the Arabia., coast under these circumstances. Yet strong surface currents could be detected by the ship's drift, northeasterly in direction at a distance of 100-200 mi offshore and southwesterly close along the Arabian coast from the Gulf of Oman to the Gulf of Aden. The "doming " of the isopleths at a distance of about 200 mi offshore could be intepreted as a divergence produced at the front between two opposing currents, though other explanations are possible. Upweiling (using the term in its general sense) was unquestionably associated with these currents, as illustrated by the distribution of both temperature and phosphate along the two sections described by Stns. 194-200 and 175-180 respectively (Figs. 3 and 4). Off the Gulf of Oman (Stns. 194 and 195) rates of production were 5.7 and 6.4 g carbon/rn~/day, values which are, to the authors' knowledge, higher than ever before reported for the ocean. While these rates were extraordinary and represent " bloom " conditions, the mean production rate for all 40 stations was 1.5 and for the 30 Arabian Sea stations 1.8 g carbon/m~/day, a level which is an order of magnitude greater than that of the oceans as a whole.

PRODUCTIVITY

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Figure 5 shows the relationship between carbon assimilation (measured at 1000 foot candles) and particulate carbon at each of the five depths sampled within the euphotic zone and for all 40 stations occupied on Cruise 4A. The filled circles show the regression of carbon assimilation on total particulate organic carbon. The open circles represent the regression on particulate carbon associated with phytoplankton, or "living carbon," as it will be referred to henceforth. The latter has been calculated by multiplying values for chlorophyll-a by 35, the relationship between carbon and chlorophyll in healthy growing cultures of phytoplankton found at this laboratory (MENZEL, unpublished data). Actually, this is a minimal value, since ratios of 35-70 : 1 were measured in the algal cultures, this range being essentially in agreement with those reported by HARRISand RILEY(1956), MCALLISTER et al. (1964) and others. Higher ratios (ca. 50 : 1) were also found from the regression of chlorophyll on particulate carbon in the North Atlantic (MENZEL and RYTHER, 1964). The use of the minimal ratio is based on the authors' hypothesis, advanced in the above mentioned publication, that higher ratios measured both in cultures and natural populations reflect the presence of dead cells or detritus as the case may be. The filled and open triangles are plots of carbon assimilation against total and living particulate carbon respectively for the very high values which, to enable them to be shown on the graph, have had both variables divided by ten. The relationship between carbon assimilation and total particulate carbon is obviously non-linear and highly scattered suggesting the presence of large and variable quantities of dead o1' detrital carbon in the particulate matter. The open circles show rather less scatter and better linearity indicating that chlorophyll is probably a better index of living, photosynthetically-active carbon. The very high values (triangles) are particularly interesting in that the chlorophyll-based (living)

206

L H. RVTHEg and D. W. MENZEL

and the total particulate carbon values for the most part agree well with each other indicating that, when very large concentrations of particulate carbon were present, as in a dense plankton bloom, it wasmostly in the form of healthy, living organisms. Much of the scatter seen in Fig. 5 in the relationship between photosynthesis and living carbon can be reduced if values arc used for carbon assimilation under natural illumination and if carbon assimilation, living carbon, and total particulate carbon each arc integrated over the entire euphoric zone. This is shown in Fig. 6 for all 40 stations. In this figure the values for chlorophyll (used to calculate living

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carbon) have been adjusted b y correcting for the amount of phaeophytin in the samples, using the method of YENTSCH and MENZ~L (1963). This correction Was applied only for values of chlorophyll above 0-1 g/m s, since the change at lower concentrations was not great enough to be significant. Again the total carbon values show no sign of a linear relationship to productivity, but now the regression of carbon assimilation on living carbon is clearly linear and the fit, with a few exceptions, is surprisingly good enough, in fact, to inspire some confidence that the estimation of living carbon by this means may be quite reasonable. l: follows that the difference between living and total carbon is equivalent to detrital carbon and these values have been plotted serially for ~ach station in Fig. 7. The irregularity of the curves in this figure merely reflect the fact that the ship passed in and out of areas containing variable amounts of organic matter and may recall what was said earlier concerning the patchy distribution of life in the Arabian Sea. What is evident from this figure is that the living phytoplankton represents no more

On the production, composition, and distribution of organic matter in the Western Arabian Sea I

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than 10--20 per cent of the total organic matter, though the two appear to increase and decrease in phase. The exceptions to this were the few stations where phytoplankton blooms were encountered (e.g. Stns. 194, 195). There the integrated living carbon for the whole euphotic zone accounted for 60 per cent of the total carbon, while at individual depths near or at the surface virtually all the carbon was represented by living organisms (Fig. 5). It should perhaps be reiterated here that the living carbon fraction may have been underestimated by taking the minimal carbon:chlorophyll ratio ( 3 5 : 1 ) t2

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208

J . H . RYTHEKand D. W. MENZEL

which we found in laboratory cultures. As we pointed out earlier, however, there is some justification for thinking that higher ratios in cultures may be due to the presence there of dead cells, which would be no different from the detritus we are attempting to measure in nature (MENZEL and RVrIaER, 1964). A small increase (e.g. 50 : I) would not significantly affect the relative proportion of living and dead material. The implications of this relationship with respect to such matters as the food available to zooplankton are worth some consideration. The broken line in Fig. 7 shows the daily rate of primary productivity plotted in the same units. In view of the uncertainties in the calculation of the living carbon fraction, minor differences are probably not significant. It is obvious, however, that the standing crop of living organisms represents on the average approximately one day o f primary production while the turnover rate of total carbon ranges from about a week to I0 days. This is perhaps not surprising in the tropics. It does illustrate not only the rapid turnover of organic matter but also the potential biological instability of such an area. If conditions are otherwise favourable for the existence of animal populations and the primary production is in the form of a food which the animals can utilize, enhanced productivity of these higher forms of life will be favored. If, on the other hand, animal populations are not present in adequate numbers or are otherwise unable to consume the primary production, and if an appreciable fraction of it sinks below the euphotic zone, its subsequent oxidation could easily lead to the anaerobiosis discussed above and its attendant threat to the animal life. Mass mortalities will, of course, accentuate the problem and tend to make it self-perpetuating, not only indirectly by contributing still more oxygen demand to the system but also in removing the trophic levels capable of utilizing the primary organic production. REFERENCES CREITZ, G. I. and RXCHARDSF. A. 0955) The estimation and characterization of plankton populations by pigment analysis. Ill. A note on the use of " Millipore" membrane filters in the estimation of plankton pigments. J. Mar. Res., 14 (3), 211-216. GUNTHER E. R. (1936) A report on oceanographical investigations in the Peru Coastal Current. Discovery Repts., 13, 109-296. HARRIS E. and Rn.~Y G. A. 0956) Oceanography of Long Island Sound, 1952--1954. VIII. Chemical composition of the plankton. Bull. Bingham. Oceanogr. Coll., 15, 312-323. HART J. T. and CuRRm R. I. (1960) The Benguela Current. Discovery Repts. 31, 123-298. IVANeNKOV V. N. and ROZANOV A. G. (1961) The hydrogen sulfide contamination of the intermediate water layers of the Arabian Sea and the Bay of Bengal. (In Russian). Okeanologiya, Akad. Nauk, SSSR, l, (3), 443-449. MCALLISTER C. D., SHAH N. and STRICKLAND J. D. H. (1964) Marine phytoplankton photosynthesis as a function of light intensity : A comparison of methods. J. Fish. Res. Bd., Can., 21, (l), 159-181. MENZEL DAVID W. 0964) The distribution of dissolved organic carbon in the Western Indian Ocean. Deep-Sea Res., ll, (5), 757-766. MENZEL D. W. and R~rHER J. H. 0964) The composition of particulate organic matter in the Western North Atlantic. Limnol. and Oceanogr., 9, (2), 179-186. MENZEL DAVID W. and VACCARORALPH F. 0964) The measurement o dissolved organic and particulate carbon in sea water. Limnol. and Oceanogr., 9, (1), 138-142. MURPHY J. and RILEYJ. P. (1962) A modified single solution method for the determination of phosphate and total phosphate in seawater. Anal. Chira. Acta, 27, 31-36. RICHARDS F. A. (with THOMPSONT. G.) 0952) The estimation and characterization of plankton populations by pigment analysis. 11. A spectrophotometric method for the estimation of plankton pigments. J. Mar. Res., II, 156-172.

On the production, composition, and distribution of organic matter in the Western Arabian Sea 209 RYTHER J. H. and YENTSCH C. S. (1957) The estimation of phytoplankton production in the ocean from chlorophyll and light data. Limnol. and Oceanogr., 2, 281-286. STEEMANN NIELSEN E. (1952) The use of radioactive carbon (C14) for measuring organic production in the sea. J. du Conseil, 18, 117-140. SVERDRUPH. U. and FLEMINGR. H. (1941) The waters off the coast of Southern California, March to July, 1937. Bull. Scripps Inst. Oceanogr., 4, 261-378.