Nitrogen, Phosphorus, and Eutrophication in the ...

Nitrogen, Phosphorus, and Eutrophication in the Coastal Marine Environment Author(s): John H. Ryther and William M. Dunstan Source: Science, New Series, Vol. 171, No. 3975 (Mar. 12, 1971), pp. 1008-1013 Published by: American Association for the Advancement of Science Stable URL: http://www.jstor.org/stable/1731314 Accessed: 15-01-2017 19:18 UTC REFERENCES Linked references are available on JSTOR for this article: http://www.jstor.org/stable/1731314?seq=1&cid=pdf-reference#references_tab_contents You may need to log in to JSTOR to access the linked references. JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected].

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REPORTS

phosphorus ratios by atoms in cultures

of Chlorella pyrenoidosa of 5.6: 1 for normal cells, 30.9: 1 for phosphorus-

Nitrogen, Phosphorus, and Eutrophication

deficient cells, and 2.9 : 1 for nitrogendeficient cells. A number of subsequent studies of both algal cultures (6, 7) Abstract. The distribution of inorganic nitrogen and phosphorus and bioassay and oceanic particulate matter (8, 9) experiments both show that nitrogen is the critical limiting factor to algalhave growth reported highly variable ratios of and eutrophication in coastal marine waters. About twice the amount of phosphate nitrogen to phosphorus. These ratios as can be used by the algae is normally present. This surplus results fromare the low somewhat difficult to interpret in nitrogen to phosphorus ratio in terrigenous contributions, including human waste,particulate matter, since living oceanic and from the fact that phosphorus regenerates more quickly than ammonia from algae may comprise a very small fracdecomposing organic matter. Removal of phosphate from detergents is therefore tion of the total particulate organic not likely to slow the eutrophication of coastal marine waters, and its replacement matter collected by the usual sampling with nitrogen-containing nitrilotriacetic acid may worsen the situation. methods, and the origin and nature of

in the Coastal Marine Environment

the remaining material are largely un-

The photosynthetic production plankton. of This relationship may have known. On the other hand, the chemiorganic matter by unicellular algaeresulted from adaptation of the orga- cal composition of algae grown in the nisms to the environment in which (phytoplankton) in the surface layers usual culture mediums may differ signithey live, but Redfield suggestedficantly a of the sea is accompanied by, is indeed from that of naturally occurthe microbial fixation of made possible by, the assimilation mechanism, of ring organisms. Despite these uncerelementary nitrogen, which could regu- tainties, the following generalizations inorganic nutrients from the surroundlate the level of fixed nitrogen in the may be made: (i) ratios of nitrogen ing water. Most of these substances sea relative to phosphorus to the same to phosphorus from less than 3: 1 to are present at concentrations greatly ratio as these elements occur in the in excess of the plants' needs, but some, over 30: 1 (by atoms) may occur in plankton. In other words, any delike nitrogen and phosphorus, occur unicellular marine algae; (ii) the ratio at no more than micromolar levels and ficiency of nitrogen could be made up varies according to the kind of algae by nitrogen fixation. may be utilized almost to the point grown and the availability of both of exhaustion by the algae. It is, in Such a process could, in times past, nutrients; and (iii) although there is

have adjusted the oceanic ratio of nitrofact, the availability of these nutrients no indication of any "normal" or "optigen to phosphorus to its present value, that most frequently controls and limits mum" nitrogen to phosphorus ratio in and it may be important in regulating the rate of organic production in the algae, values between 5: 1 and 15: 1 the level or balance of nutrients in

sea.

are most commonly encountered and

Harvey (1) was among the firstthe ocean as a whole and over geologian average ratio of 10: 1 is therefore

cal time. It is certainly not effective to point out that phytoplankton growth a reasonable working value. caused the simultaneous depletion of locally or in the short run. As analytical In seawater, a 15 : 1 atomic ratio methods have improved and as the both nitrate and phosphate from the may be typical of the ocean as a whole. ambient seawater. Much has since been subject has been studied more intenBut since 98 percent of its volume lies sively, it has become increasingly below clear the depth of photosynthesis and written about the interesting coincithat the concept of a fixed nitrogen togrowth, such mean values have dence that these elements are present plant

phosphorus ratio of approximately in seawater in very nearly the same little relevance to the present discus-

15 : 1, either in the plankton or in the proportions as they occur in the planksion. If one considers only the remainwater in which it has grown, has ing little ton (2-4). For example, Redfield (3) 2 percent of the ocean's volume, if any validity. reported atomic ratios of available the so-called euphotic layer, high ratios As early as 1949 Ketchum and Rednitrogen to phosphorus of 15 : 1 in seaappoaching 15: 1 occur only at the water, depletion of nitrogen and phos- field (5) showed that deficiencies of few times and places where relatively phorus in the ratio of 15: 1 during either element in culture mediums may deep water is mixed or upwelled into phytoplankton growth, and ratios of drastically alter their ratios in the al- the euphotic layer (9). Over the 16: 1 for laboratory analyses of phyto- gae. They reported (5) nitrogen to greater part of the sea surface, the

7I

7

6-

c o

;

-6

5

6,6E0

E_

\

(

0 0. 0

4

~~~~~~~~4- /*' ' \~~~ !-4

a.

73?00'

2

72?30'

2

0

l o I- .I . --- . . . ..Phytoplankton . 1 I

Fig. 1. The distribution of phytoplankton and inorganic phosphorus in Great South Bay, Moriches Bay, and Shinnecock Bay, Long Island, in the summer of 1952. Station numbers on the 2 4 map (above) correspond to station numbers on the abscissa of the figure (right).

"-----Inorganic phosphorus 00

5

11

30

15

19

21

Station number C

, -- Great South Bay -- Moriche

1008

SCIENCE, VOL. 171


two elements appear to bear no constancy in their interrelationship (5,

Table 1. Regeneration of nitrogen and phostion from tidal exchange via Great phorus accompanying the decomposition of South Bay to the west and Shinnecock mixed plankton [after Vaccaro (18)]. Excess 9-12). Bay to the east (Fig. 1). Further study phosphorus (last column) was calculated on the assumption that all nitrogen was assimiDetailed examination of the nutrient suggested that growth of the phytolated as produced and that phosphorus was data from the sea surface reveals that, plankton was actually confined to the assimilated at a nitrogen to phosphorus ratio tributaries themselves and that the alas the two elements are utilized, nitro- of 10: 1.

gen compounds become depleted more rapidly and more completely than does

NHa -+-

NOH + P04 Excess NO, + PO4 p NO3 (/ g N:P

phosphate. This is particularly true when only nitrate-nitrogen is con-

Days (1Ig atoms (by atoms atoms P/ atoms)

sidered. Both Vaccaro (9) and Thomas

N/ liter) liter)

liter)

(13) have pointed out, however, that ammonia may often be quantitatively

0 0.00 0.80 0.0 0.80 7 0.86 0.79 1.1 0.70

a more important nitrogen source than is nitrate in surface ocean waters, particularly when nitrogen levels in gen-

17 2.81 0.84 3.3 0.56

30 3.08 1.05 2.8 0.74

48 3.86 0.98 3.9 0.59

eral become reduced through plant

87 4.14 1.04 4.1 0.63

growth. But even when all known forms

of available nitrogen are considered

gae in the bays represented a nongrowing population that was able to persist for long periods of time, during which they became distributed in much the same way that a conservative oceanographic property (for instance, freshwater) would behave. Roughly coincident with the distribution of the phytoplankton was that

of phosphate, which reached a maximum concentration of 7.0 ,tmole per liter in eastern Moriches Bay and fell to levels of about 0.25 ,umole per liter at the eastern and western ends of the

together, they are often found to be reduced to levels that are undetectable

region (Fig. 1). fishery Phosphate, in fact, have supported a productive of was used throughout the study as the in the euphotic layer. In this event, oysters aland hard clams. Introduction most convenient diagnostic index most invariably a significant amountand of growth of the Long Island and duckling of pollution from the duck farms. phosphate remains in solution. There industry, centered along the tributary

streams of Moriches Analyses Bay, were resulted in also made for nitrois, in short, an excess of phosphate, gen compounds, nitrate, small but persistent and apparently the organic pollution of the including two bays ammonia, and uric acidof (uric ubiquitous, in the surface water of the and the subsequentnitrite, development ocean, relative to the amount of nitroacid is the nitrogenous excretory proddense algal blooms in the bay waters, uct of ducks). Except in the tributaries gen available to phytoplankton nutri- to the detriment of the shellfisheries. tion. This is true in both the Atlantic

As a result of studies by the Woods that were in direct receipt of the effluHole Oceanographic Institution during ent from the duck farms, no trace of 14). Thus, the ratio of nitrogen to the period 1950-55, the ecology of the nitrogen in any of the above forms phosphorus in surface seawater may region and the etiology of its planktonwas found throughout the region studied. It was tentatively concluded range from 15 : 1, where subeuphotic blooms were described in some detail that growth of the phytoplankton was water has recently been mixed or up- (15). The situation has since changed, welled to the surface, to essentially but certain of the unpublished resultsnitrogen-limited and that the algae quickly assimilated nitrogen in whatzero when all detectable nitrogen has of the study are especially pertinent to this discussion and will be reviewed been assimilated. Since most of the ever form it left the duck farms, exhere. surface waters of the ocean are nutrihausting the element from the water well up in the tributaries before it ent deficient most of the time, nitrogen During the period of dense phytocould reach the bay. to phosphorus ratios appreciably lessplankton blooms, the peak in the than 15: 1 are the common rule. abundance of phytoplankton occurred To confirm this theory, water samples A puzzling question remains to in beMoriches Bay in the region nearest were collected from a series of stations answered. If the ultimate source of the tributaries, where most of the duck (Nos. 2, 4, 5, 11, 15, 30, 19, and 21) farms were located. The algal populain Great South Bay and Moriches Bay nutrients is deep ocean water containtions decreased on either side of this and in the Forge River, one of the ing nitrate and phosphate at an atomic peak in a manner that suggested dilutributaries of Moriches Bay on which ratio of 15 : 1 and if the average physeveral duck farms were located. These toplankton cell contains these elements station locations are indicated by numat a ratio of about 10: 1, why is it 30r ber in Fig. 1. The water samples were that nitrogen compounds are exhausted Millipore-filtered, and each was then first from the water and that a surplus 2 4 U Ammonium enriched separated into three 50-ml portions. The of phosphate is left behind? How can [1 Phosphate enriched first of these served as a control while nitrogen rather than phosphorus be 18 the E3 Unenriched control the other two received separately limiting factor? Before turning to this NH4C1 and Na2HPO4 12H20 at conE question, we will present two examples (9, 10, 12) and Pacific oceans (11, 13,

x

-

12-

of nitrogen as a limiting factor to phytoplankton growth.

centrations of 100 and 10 ,umole per liter, respectively. All flasks received

Long Island bays. Great South Bay and Moriches Bay are contiguous and O- It=3Z

an inoculum of Nannochloris atomus, the small green alga that was the dominant species in the blooms. The cul-

U

6-

connected embayments on the south shore of Long Island, New York,

Inoculum 2 4 5 11 15 30 19 21 Station number

tures were then incubated for 1 week

formed by the barrier beach that Fig. ex- 2. Growth of Nannochloris atomus at 20?C and approximately 11,000 in unenriched, ammonium-enriched, and tends along much of the East Coast of lu/m2 of illumination, after which the phosphate-enriched water collected from the United States. They are shallow, cells were counted (Fig. 2). Great South Bay and Moriches Bay at averaging 1 to 2 m in depth, have a the station locations indicated by number The algae in the unenriched conhard sandy bottom, and traditionally in Fig. 1. trols increased in number by roughly 12 MARCH 1971

1009


two- to fourfold, the best growth ocBay, which suggests that some otherproductivity and cycles of organic matcurring in the water collected from nutrient became limiting in the latterter in the contiguous coastal waters. To within (station 30) or near (stations 11 series. One might surmise, from theobtain input data, samples were col-

and 15) the Forge River. No growth distribution of phosphate in the two lected inside the New York bight, at occurred in any of the samples en- bays (Fig. 1), that phosphorus was the locations where sewage sludge and riched with phosphate, with the excep- the secondary limiting factor in Greatdredging spoils from New York City

tion of that taken from the Forge River South Bay, but this possibility was notare routinely dumped, as well as from (station 30), in which the cell count investigated. There can be little doubt,up the Raritan and Hudson rivers. increased about threefold. In fact, the however, that nitrogen, not phosphorus, Of the 52 stations occupied during addition of phosphate seemed to in- was the primary limiting factor to algal the cruise, 16 will be discussed here. hibit the growth of the algae relativegrowth throughout the region. These stations constitute three sections to that observed in the unenriched conNew York bight and the eastern sea-originating in New York Harbor, one trols. In contrast, all the water samples board. In September 1969, an ocean-extending eastward along the contito which ammonia-nitrogen were added ographic cruise (R.V. Atlantis II, nental shelf south of Long Island and

supported a heavy growth of Nanno-cruise 52) was undertaken along the the New England coast, one extending chloris, resulting in cell counts an ordercontinental shelf of the eastern Unitedsoutheasterly along the axis of Hudson of magnitude greater than were attained States between Cape Cod and Cape Canyon and terminating at the in the control cultures. About twice as Hatteras. The primary objective of the edge of Gulf Stream, and one runmany cells were produced in the sam- cruise was to study the effects of polluning southerly along the coast of ples from Moriches Bay as were tion of various kinds from the populaNew Jersey to the mouth of Delaware produced in samples from Great South tion centers of the East Coast upon the Bay (Fig. 3A). The nearshore nontidal currents of the region are predominantly to the south (Fig. 3B), so that pollution emanating from New York Harbor would be expected to spread in that direction roughly along the axis

of section 3. Section 1 and the inshore

stations of section 2 might be consid-

ered as typical of unpolluted or moderately polluted coastal waters, whereas the two distal stations of section 2

(1513 and 1547) should be oceanic in character.

At the inshore end of the three sec-

tions, station 1507 was located in heavily polluted Raritan Bay. The water at that location was a bright apple-green

in color and contained nearly a pure culture of a small green alga identified in an earlier study of the area by Mc-

Carthy (16) as Didymocystis sp. Kar-

shikov. Stations 1505 and 1504 are the

respective dumping sites for dredging

spoils and sewage sludge for the city

of New York.

The distribution of total particulate organic carbon at the surface are shown

for the three sections in Fig. 4. The measurements were made by the meth-

od of Menzel and Vaccaro (17). It is

clear from the two sets of measure-

nents that living algal cells made up only a small fraction of the particu-

ate organic content of the water. On he basis of either criteria, one can see hat the high content of particulate organic matter characteristic of the New

York bight extends seaward for less han 80 km to the east and southeast, vhereas evidence of pollution occurs t least 240 km to the south (section ), along the New Jersey coast to Delware Bay, presumably the direction of

ow of the water flushed out of the ight.

The distribution of inorganic nitro1010

SCIENCE, VOL. 171


gen, as combined nitrate, nitrite, and ammonia, in the surface water of the three sections is shown in Fig. 5. If

relative to nitrogen in the plants is

14 ,

greater than it is in seawater, there are probably two explanations. One ex-

E \ Section 1

1.0-

,

.8

-

Section

3

one considers that the two terminal .2^~~~ s OH + NO (3)

a packed column cooled to liquid

nitrogen temperatures to remove iron carbonyl, which is present in CO taken from conventional steel cylinders. In our

CO samples the Fe(CO)5 concentraThe net reaction from these three steps tion of CO with OH (see reaction 1 tion was 0.15 percent. The purification is b:low) has an activation energy of approximately 1 kcal/mole and that the rate constant at 25?C is 8 X 107M-1

CO + 02 + NO - CO2 + NO2 (4)

procedure employed is effective only

if carried out carefully, in which case

it removes more than 99 percent of the Experimental evidence is presented here sec-1 (2), thus making this reaction iron carbonyl present. One of the exfor the effect of CO on the oxidation of possible significance in the atmoperiments shown in Fig. 1 was perof NO in polluted atmospheres. sphere. Experiments were performed in aformed with CO generated in a glass Recently Heicklen et al. proposed a 7.68-m3, Teflon-lined, constant-temsystem by the reaction of H2SO4 with mechanism to explain the previously 1013

12 MARCH 1971
