Prog. Oceanog. Vol. 32, pp.l-15, 1993. Printed in Great Britain. All rights reserved.
0079 - 6611/93 $24.00 © 1993 Pergamon Press Ltd
Pelagic production processes in the Subarctic Pacific CHARLESB. MILLER
College of Oceanography, OregonState University, Corvallis, Oregon 97331-5503, USA
CONTENTS 1. 2. 3. 4. 5. 6. 7. 8. 9.
The background of the SUPER Program The phenomenon Hypothesesand their fate under test The new SUPERsynthesis Additionalcomments on the iron limitation hypothesis SUPERpapers outside this volume Furtherstudies in the Subarctic Pacific Acknowledgement References
1 2 2 4 7 8 10 11 I1
1. THE BACKGROUNDOF THE SUPERPROGRAM This volume of Progress in Oceanography contains papers with detailed results from a research program called SUbarctic Pacific Ecosystem Research, or SUPER. Our acronym was considerably more grandiose than the program, which only amounted to three spring and three late summer cruises to the central Gulf of Alaska. Each cruise was about four weeks with three weeks of station work. Several of the expeditions involved two ships, thanks toj oint work by ourmulti-institutional US group and a Canadian group based at the Institute of Ocean Science, Patricia Bay, British Columbia. While this is a small number of visits to the region under study, a modem oceanographic expedition with electronic hydrography, electrically controlled multiple nets, and large numbers of people inoculating, incubating, and scintillation counting can make a huge amount of data and a mountainous backlog of samples in three weeks. Many of the samples and all of the data take prolonged labor ashore to convert them to ideas about the ocean. In both the cruises and laboratory analysis SUPER has been supported throughoutby the United States National Science Foundation, whose program managers have sustained an interest in us and our scientific problem through some very complex justification and review processes. S UPER has taken valuable advice throughout from Karl Banse, who was a cosigner of our early letters to NSF proposing a program of subarctic Pacific studies. All of the following were SUPER principal investigators for all or part of the program: Beatrice Booth, Michael Dagg, Kenneth Denman, Steven Emerson, Bruce Frost, Ann Gargett, Dian Gifford, David Kirchman, Michael Landry, Joyce Lewin, the late Carl Lorenzen, David Mackas, Laurence Madin, Charles Miller, Mary Jane Perry, Thomas Powell, Jennifer Purcell, Nicholas Weischmeyer and Patricia Wheeler. Many other scientists participated as students, laboratory and field workers, and marine technicians. Bruno
Forster, AI Chamberlin, Paul Frost, Ray Womack and Cianton Clampitt were masters of the ships carrying our expeditions. My warmest thanks go to all of you, to the ships' crews, and to every wife, child, accountant, port captain, dean and anonymous reviewer who helped with this prolonged effort. SUPER developed a general understanding of pelagic ecosystem processes in the oceanic portion of the subarctic Pacific. We eventually termed this understanding the "New SUPER Synthesis". We have already presented this synthesis in two papers. One (MILLER, FROST, WHEELER,LANDRY,WELSCHMEYERand POWELL,1991a) is slightly more technical and complete. The other was written for a general audience (MILLER, FROST,BOOTH,WHEELER,LANDRYand WELSCHMEYER,199 lb). I will only outline the synthesis here, without repeating the contents of those papers. The reader who wants an overview decorated with figures and tables should see MILLER et al (1991a). 2. THE PHENOMENON SUPER sought an explanation for the continuous absence ofphytoplankton blooms in the part of the subarctic Pacific farther offshore than about 300km. On the basis of classical understanding of pelagic producti on processes, the continuous avail ability in the region' s euphoric zone of nitrate, phosphate and silicic acid, coupled with strong seasonal stratification, should allow phytoplankton stocks to rise in a springbloom. The plants should deplete the mixedlayernutrients, becomenutrient limited, then crash andremain low until autumn winds again increase vertical mixing. This does not happen in the subarctic Pacific. Long term observations from Canadian Coast Guard weatherships patrolling at Station P (50°N, 145°W) show that there are no phytoplankton blooms of substantial magnitude. Phytoplankton chlorophyll remains close to 0.3mg m -3 year round. Moreover, major nutrients never drop to limiting levels; mixed layer nitrate concentration has a typical annual low of 6ktM. In some fashion the production dynamics of the subarctic Pacific are "balanced" (CUSHING, 1959), there is a sustained match between phytoplankton growth and phytoplankton stock losses. The absence of blooms in conditions apparently conducive to them requires an explanation. 3. HYPOTHESESAND THEIRFATEUNDERTEST When we began work on this problem, there was a reasonable hypothesis available for testing. It was originally suggested by HEINRICH(1957, 1962), and we termed it the "Major Grazer Hypothesis". The principal grazing zooplankton in the subarctic Pacific during spring (the period in which blooms would be most likely) are large, filter-feeding copepods of the genera Neocalanus (3 species), Eucalanus and Metridia. The Neocalanus species, which are the biomass dominants, reproduce after a summer-fall resting phase at depth without needing to feed in order to spawn. Their eggs are elaborated out of stored nutrients, particularly lipids which they carry into diapause in very large amounts. Winter spawning of large, oil-rich eggs ensures thatthe young will be present and ready to feed in copepodite stages before any incipient bloom could escape from grazing control. This life history pattern was in contrast to that of the dominant grazing zooplankter in the subarctic Atlantic, Calanusfinmarchicus. It requires abundant food, essentially bloom levels, in order to elaborate eggs and spawn. Since a bloom is required to initiate the next generation of grazers, blooms were inevitable. With this requirement lifted for the Pacific grazers, phytoplankton growth could be controlled by grazing, keeping plant stocks constant. We thought it possible that the acceleration of productivity up to about the summer solstice could be matched by increase of grazing resulting from individual growth of the copepods. Our initial efforts were tests of the
Pelagic production processesin the subarctic Pacific
predictions of this major grazer hypothesis. First Bruce Frost (unpublished) modelled the grazer-phytoplankton interaction, showing that phytoplankton stock control was quite critically dependent on the timing of Neocalanusreproduction. Another model, with similar conclusion about the importance of Neocalanus life history timing, became available at about the same time (PARSLOW, 1981). Therefore, we (MILLER, FROST, BATCHELDER,CLEMONSand CONWAY,1984; MILLERand CLEMONS,1988) obtained a year-long series of weekly, vertically divided plankton samples during the last year ofweathership patrols to Station P. These showed that the reproduction schedules were quite different from that modelled by Frost and different from that for Neocalanus in coastal regions (FULTON, 1973), but still quite suitable for providing control ofphytoplankton stocks. Second, on our 1984 cruises we compared the product of copepod abundance and individual grazing rates to that necessary to keep pace with phytoplankton growth rates measured simultaneously. Clearly, if the Maj or Grazer Hypothesis were correct, the copepods must graze as fast as the plants grow. We found that the installed copepod grazing capacity in spring was insufficient by about an order of magnitude for controlling phytoplankton stocks (MILLERand SUPER GROUP, 1988). Moreover, the copepods were not feeding to a significant extent on phytoplankton (DAGG and WALSER, 1987), although they could be shown to be growing at substantial rates (MILLERand NIELSEN, 1988). DAGG(1993) has now used our more recent data to finish putting the Major Grazer Hypothesis to rest. A few of us still feel as if we had lost an old and honored friend. However, we promptly replaced the major grazers with micrograzers. Our measurements (BOOTH, LEWINand LORENZEN, 1988; WELSCHMEYER,STROM,GOERICKE,DITULLIO,BELV1N and PETERSON, 1993) showed that the phytoplankton were growing at high rates, on the order of a doubling per day. Blooms would certainly be observed if the stock were notbeing continually and rapidly cropped. The obvious grazers for the task showed up in Beatrice BOOTH's (1987) microscopical studies of the flora. She found large stocks of heterotrophic microflagellates (of order 5-10~tm) and modest numbers of larger (>35p.m) ciliates. Protozoans have the obvious advantage as controlling grazers that they can achieve faster growth rates than their phytoplankton food (e.g. BANSE,1982; GOLDMANand CARON,1985; FENCHEL,1982). Phytoplankton are limited to about 2 doublings d l , while protozoans given sufficient food can increase at up to 5 doublings d"l. Thus, their rapid population response to increasing phytoplankton abundance can keep that abundance within narrow limits. Provided that the growth of protozoan grazers becomes food limited at relatively high phytoplankton levels, they will leave sufficient phytoplankton to sustain usual chlorophyll levels around 0.3mg m "3. We postulated (with help from EVANSand PARSLOW,1985), and still believe although it remains to be tested, that micrograzer control is favored in the subarctic Pacific because the producer-grazer linkage remains established and functional throughout the year. The relationship between phytoplankton and their micrograzers is not broken down by deep mixing in the winter months, thanks to the permanent halocline at about 110m. There is no such permanent barrier to mixing in the subarctic Atlantic, so that the entire water column is swept clear ofphytoplankton in winter (chlorophyll drops below 0.05mg m'3). Loss of the phytoplankton must nearly eliminate their grazers. Thus, the spring recovery of grazing relations is different in the Atlantic. Because of this role of mixing, we called this new explanation for balance in the subarctic Pacific the "Mixing and Micrograzer Hypothesis". FROST(1987) modelled this micrograzer control mechanism, and our 1987 and 1988 cruises were intended to test some of the requirements and predictions of the hypothesis as embodied in the model. To date the Mixing and Micrograzer Hypothesis has passed all of our tests. First, the hypothesi s
presume s that microzooplankton, not copepods or other large zooplankton, do mo st of the grazing ofphytoplankton. This was demonstrated by Nicholas Welschmeyer's application of the pigment budget comparison suggested by WELSCHMEYERand LORENZEN(1985). Results are reported in MILLER et al (1991 a). Second, similarly to the test of the Major Grazer Hypothesis, the numbers and feeding rates of the protozoan community must be sufficient to match the growth rate of the phytoplankton. This was tested most effectively by dilution experiments (LANDRY,MONGERand SELPH,1993; STROMand WELSCHMEYER,1991). Rates were not exactly equal in any short term measurement, but switching between times when la>g (phytoplankton growth greater than grazing) and times when g>tx was such that typical, small amplitude variations in phytoplankton stock are well explained. 4. THE NEW SUPERSYNTHESIS Our work at sea, combined with that of others, has led to amoderately complete understanding of the basic trophic-dynamic function of the pelagic ecosystem in the subarctic Pacific. Most of the parts of this understanding are embodied in a new model developed by FROST(1993). First, some aspect of the habitat selects aphytoplankton flora with very small cell sizes, predominantly less than 5 ~tm. During the course of our work, MARTINand FITZWATER(1988) publi shed the suggestion that the supply o firon might well limit the growth of larger cells with low surface area to volume ratio s, thus forcing the flora to very small sizes. This scheme is still under test in the regions that have come to be called high nutrient, low chlorophyll (HNLC) areas, including the subarctic Pacific, eastern tropical Pacific, and Southern Ocean. It is an attractive candidate cause for the diminutive flora of the subarctic Pacific (BOOTH,LEWINand NORRIS, 1982; BOOTHand MARCHANT, 1987; BOOTH, 1988; BOOTH, LEWlN and POSTEL, 1993). Second, because the phytoplankton are small, they are accessible to small, protozoan grazers. Grazingby microheterotrophs can overtake and crop back any substantial increase in phytoplankton stocks, thus enforcing an approximate balance. Third, protozoan grazers have very small excreta, and only moderate trophic efficiency. Thus, they are efficient recyclers of major nutrients with all excretion remaining in the euphotic zone. Fourth, most nitrogenous recycling will be in the form of ammonium, which is preferred by phytoplankton over nitrate so that ammonium uptake will supplant nitrate uptake essentially to the extent that it is available (WHEELERand KOKKINAKIS, 1990). Recycling is fast enough that the day-night difference between metabolic ammonium production and ammonium uptake by phytoplankton produces a diel oscillation in ammonium concentration in the field (WHEELER, KIRCHMAN,LANDRYand KOKKINAKIS, 1989). Efficient recycling of reduced nitrogen is responsible for incomplete utilization of nitrate over the course of the productive spring and summer seasons. Our calculations (MILLERet al, 1991a; WHEELER, 1993; ARCHER, EMERSON, POWELL and WONG, 1993) show that total nitrate utilization is considerably greater than the near-surface depletion from March through August because of continual supplybyupwelling and vertical eddy diffusion. The observations suggest that short-term variations in phytoplankton stock are primarily driven by (1) oscillations in illumination causedby variable cloudiness, and (2) shifts in mixedlayer depth. This mechanism is very nicely incorporated in Frost's model, replicating the scale and frequency of both the short-term variation in chlorophyll and the inversely correlated variation in ammonium which we observe in time series of field data. Afterhis 1987 paper, Frost's numerical model of the producer-grazer interaction in the subarctic Pacific has had two distinct iterations. In the first (FROST, unpublished), there was difficulty parameterizing mixing such that euphoric zone nitrate returned to the same level at the end of a simulated year. In the present version (FROST, 1991, 1993) this has been solved by addition of a
Pelagic production processesin the subarctic Pacific
detritus variable, which is coupled to microherbivore grazing as a representation of fecal "minipellet" production. This detritus reservoir builds to substantial levels over the productive season, continuously degrading with production of ammonium. Vertical mixing and dropping production rates remove this large detrital pool in the autumn. Addition of this reservoir serves as a"buffervariable" in the equation set, simplifying the balancing of the cycles of all of the system variables over the year. A detritus variable and associated equations were suggested to Frost by WHEELER'S (1993) observation of a large difference in suspended particulate organic nitrogen (PON) between spring cruises and late summer cruises. Thus, while the detrital organic matter pool is the sort of addition to the model that might have arisen in developing the theory, then sought in the field, in this case the improvement in the theory was suggested by the observation. In the model the detfital nitrogen leaps to high values over a short interval in spring. Subsequent examination of every aspect of the nitrogen cycle agrees with this feature. PON increased sharply through May in 1988 and most of the annual reduction in mixed layer nitrate occurs in the same period. In this and many other instances, interplay among modelling, observation, and interpretation hasbeen a powerful tool for generating understanding of subarctic Pacific production dynamics. As WHEELER(1993) explains, a large nearsurface PON pool which builds up in spring andbreaks down much later, means that no balance between new production and downward export flux from the euphotic zone will be observed in the short term. New production and organic nitrogen export can only be expected to balance on an annual basis. The year round observations necessary to demonstrate that equivalence are out of reach with presently available logistics. Criticism of a key tenet of the synthesis has already appeared. PRICE, ANDERSENand MOREL (1991), working in the eastern tropical Pacific, have investigated the effect of iron addition on nitrate uptake by the general phytoplankton community. They studiednitrate removal in incubations with and without added iron, showing that it was greater with iron than with out. Ammonium uptake was not lessened in the iron-added treatment to compensate for the nitrate uptake. On the basis of this observation, they question the conclusion of WHEELERand KOKKINAKIS(1990) that nitrate uptake is inversely correlated with available ammonium in the subarctic Pacific. PRICEet al ( 1991) are confusing time scales. The difference they observed between treatments sets in after three to four days of incubation. The time axis of their nitrate removal observation is 125 hours, allowing ample time for modification of the flora. That occurred, as they observed and reported. WHEELER and KOKKINAKIS(1990) were observing differences in uptake ofi sotope labelled nitrate on the day o f collection. Patricia Wheeler and I remain convinced that in short term incubations, and in the field, nitrate uptake is inversely correlated with ambient ammonium. There is nothing wrong with the observation of PRICE et al (1991). Given enough time, iron additions will stimulate floral change, enable nitrate reductase formation by cells previously crippled, and is likely to promote substantial nitrate utilization in the presence of significant ammonium. The result must not be extrapolated to the short term situation in the field, which remains iron limited. In correspondence, Price has clarified that PRICE et al never doubted the data of WHEELERand KOKKINAKIS(1990), only questioned whether the relationship could explain persistent high nitrate in the subarctic Pacific. We do not claim that suppressed nitrate in the prescence of ammonia operates alone; it is just a key part of the overall system dynamics. Their view, represented in the correspondence, is converging with ours on the basis of their recent results. It can be argued ad nauseam whether a negative correlation of nitrate uptake with ammonium concentration actuallyimplies suppression of uptake (DORTCH,1990). The mechanism creating the correlation is important to understand, but knowing it with certainty won't change its significance. If nitrate utilization is lower when ammonium is available, then rapid recycling of nitrogen as
ammonium through predominance of microheterotroph grazing can allow nitrate to remain unused in the euphotic zone. An apparent problem for the synthesis arises from our own data. We suppose a strong effect on total water column photosynthesis from day-to-day (that is, within season) variation in illumination acting at the level of the individual plant• In Frost's model this is represented by the functional relation of pigment-specific productivity to total daily irradiance via the Jassby-Platt equation. However, WELSCHMEYERet al (1993, their Fig.7) found no correlation of carbon uptake per unit chlorophyll with daily irradiance. That result appeared late in our arguments and came as a surprise. It is not exactly the test that is required, since the figure compares the maximum photosynthetic rate of surface phytoplankton to the irradiance available over the day. What is required is evaluation of the effect of varying daily isolation on the ratio of the vertical integral of carbon uptake to the vertical integral of chlorophyll (taking care that the lower integration limit is shallow enough that only active chlorophyll is included). WELSCHMEYERet al also made that evaluation (their Fig. 11), again finding no correlation. Nevertheless, all o ftheir in situ, l aC-uptake profiles show the expected decline in production with depth. Thus, the "P vs. I" relation is normal and can be adequately modelled by a Jassby-Platt equation. Returning to the output of the model (without changing any functional relations or input parameters), Frost (personal communication) showed (Fig. 1) that the "expected" correlation of [integrated production]/[integrated chlorophyll] to daily irradiance is positive but very weak within the spring and summer seasons. The reason is that multiple nonlinearities affect the relation between daily surface irradiance and photosynthesis. Chlorophyll-specific carbon uptake is nonlinearly related to in situ irradiance; in situ irradiance is exponentially related to depth via an absorption coefficient that depends upon chlorophyll; and chlorophyll is variably distributed with depth independent ofirradiance. Figure 1 shows the compound interaction of all those relationships• Variation in daily irradiance is important, but its effect is difficult to exhibit through data manipulations like those of Fig. 11 in WELSCHMEYERet al (1993). In fact, it is likely that no simple field demonstration of the impact of within-season irradiance variation can be formulated. This illustrates again the importance of modelling for generating understanding of pelagic production dynamics. ,o - • .-*..
Jz (O c7)
"7 "0 -t
E (O 25
E i n s t e i n s m "2 d I
Fig.l. Result from the model of Frost (1993). Primary production integrated from 0 to 50m normalizedby chlorophyll-aintegratedfrom 0 to 50m (chlorophyllvalues at the end of each day) plotted against total daily irradianee for model days 125 through 280. This is equivalent to the seasonal coverageof the SUPERexpeditions.The linear regressionis positiveand significant,but accounts for only a small part of the variance.
Pelagic production processesin the subarctic Pacific
5. ADDITIONALCOMMENTSON THE IRONLIMITATIONHYPOTHESIS A reading of all the papers included here will show that the SUPER participants take varying views of the role of iron limitation proposed by Martin (MARTINand FITZWATER,1988; MARTIN, GORDON,FITZWATERand BROENKOW,1989; MARTIN,GORDONand FITZWATER,1991; MARTIN, 1991). My personal and present opinion is that it is a very strong candidate mechanism for establishing a flora overwhelmingly dominated by tiny cells. Iron limitation, or something acting similarly, is responsible for the small stocks of large cells with low surface to volume ratios (MOREL, HUDSONand PRICE, 1991). The small cells that remain are not severely iron limited. Their growth is light limited for the water column as a whole, and their stocks must be limited by grazing. Others have had more difficulty accepting the possibility that iron limitation is significant. I have not exercised editorial discretion or authority on any opinion concerning iron limitation. Readers primarily interested in the iron issue are left to find variant opinion s in the papers and may evaluate those without my help. If iron limitation in fact causes the persistence of major nutrients in the euphoric zone of the subarctic Pacific or other HNLC regions, then the supply of available iron sets the possible total of new production in the DUGDALE and GOERING (1967) sense. Since iron is reasonably hypothesized to arrive from the atmosphere (DONAGHAY, LISS, DUCE, KESTER, HANSON, VILLAREAL,TINDALEand GIFFORD,1991), not through verrical mixing from a concentrated supply at depth, it is to be expected that there will be large interannuai variations in new production. Those variations will be driven by year-to-year differences in Asian dust storm activity and in aeolian transport from Asia to the Pacific. The importance of year-to-year variations in subarctic pacific production was made evidentby the long-term zooplankton sampling program from the weatherships (FULTON, 1983; FROST, 1983; MILLER,FULTONand FROST, 1992). An attempt to use net oxygen production at Station P as a direct measure of interannual variation of new production has been made by Steven Emerson. His initial application of this method (EMERSON, 1987) involved serial data from the weathership, which suggest that annual new production varies from 100-300mg C m'2d -l. He and his colleagues participated in four SUPER expeditions and made an extended effort (EMERSON,QUAY, STUMP,WILBURand KNOX, 1991) to check the method' s several assumptions about exchange rates. They concluded that the calculation is reliable. A short-term comparison (EMERSON, QUAY and WHEELER, 1993) of net oxygen production to 15N-traced nitrate uptake showed agreement within a factor of two, which suggests reliability of the method better than the calculated three-foldinterannual variation. However, netoxygen production (producrion-respiration) is not strictly ameasure of new production, since respiration can vary independently of production and there is reason to suppose that it does (MILLERet al, 1992). Readers interested in net oxygen production should also see THOMAS, GARCONand MINSTER(1990), and the parallel work on carbon dioxide exchanges (ARCHER,EMERSON,POWELLand WONG, 1993; GARCON,THOMAS, WONG and MINSTER, 1992). Given the apparent importance of iron limitation to global oceanic productivity, a thorough reexamination of net oxygen production and other measures of new production is in order for the subarctic Pacific. One aspect of this should be direct determination of variation in iron delivery, which should be pursued despite its technical difficulties. There are some large phytoplankton in the subarctic Pacific (e.g. CLEMONSand MILLER, 1984, HORNERand BOOTH, 1990). As we now understand the system, their growth (which may ormay not be iron-limited) must be matched by mesozooplankton grazing. Our attempts to demonstrate this aspect of the SUPER synthesis remain uncompleted. Studies of growth rates of large phytoplankton (removed from the matrix of highly productive, smaller cells) are possible. A start was made on the SUPER cruises by WELSCHMEYER,GOERICKE, STROMand PETERSON(1991)
using 14C accumulation in specific pigments (see GOERICKE and WELSCHMEYER, 1993) as markers of the growth of taxonomically restricted groups. They took reasonable precautions to avoid iron contamination of their incubations and concluded that fucoxanthin containing cells (presumably mostly diatoms) were the fastest growing component of the flora. Possibly these were small diatoms. Nitzschia cylindroformis, which is less than 4~tm, is a recurring and occasionally dominant component of the flora in the region. If larger diatoms were involved, and iron limitation does not occur in the subarctic Pacific, then some other factor must be found to explain the consistent domination of the flora by very small cells. Mesozooplankton grazing cannot match the increase of phytoplankton if they are doubling daily. Gut content studies ofmesozooplankton aimed at evaluating ingestion of large phytoplankton show that there is such ingestion. The report was never finished because the observer left us for a software development position. He has proved the alternate, previously unconsidered hypothesis that there is human life outside oceanography. His attempt at quantification of the large cell ingestion rates using copepod incubations with natural assemblages was also not completed. Eventually somebody must compare these growth and removal rates for large cells. 6. SUPERPAPERSOUTSIDETHIS VOLUME This is not the place for a full literature review on the region. A good recent review by PARSONS and LALLI(1988) serves that purpose, and readers are referred to it. No sign appears in that review of an explanation for ecosystem balance in the subarctic Pacific resembling the SUPER synthesis. That is probably because we have been slow getting to press. It makes the review more useful as a contrast to our present understanding. Descriptive physical oceanography was brilliantly summarized in two monographs: DODIMEAD, FAVORITE and HIRANO (1963) and FAVORITE, DODIMEADand NASU(1976). They are essential reading for students of the region. There has been substantial physical work since 1976, but little of it provides insight essential for ecological understanding. At least we haven't used it extensively. Exceptions are the work on upper water column mixing of the MILE program (e.g. DILLONand CALDWELL,1980), recent contributions by TABATA(1989, 1991; TABATAand PEART, 1985), and studies by Kenneth Denman and Ann Gargett oflOS in cooperation with the SUPER program (DENMANand GARGETI', 1988; GARGETI', 1991). There has been significant ecological work in the subarctic Pacific during the 1980s, apart from SUPER and from the VERTEX expeditions supporting Martin' s experimentation with iron. Much of this has been stimulated by the ongoing interest in the region at IOS, particularly through the studies of C.S. Wong. However, full review of work not directly connected to SUPER will not be provided here. A considerable number of papers have been published earlierbased on the SUPER expeditions. I will discuss here only thosenot already mentioned. Our 1987 and 1988 cruises included extensive microbiological studies by David Kirchman and his coworkers. He was far more direct and prompt in publishing his work than the rest of us. We included his work in SUPER because of the likely importance of the microbial loop in systems where grazing is dominated by protozoans. It was postulated that the return of dissolved organic matter to particulate form by bacteria could well act as a "fly wheel" for the grazer-phytoplankton interaction. Bacteria would be an alternate food source, sustaining the protozoan community through low times in phytoplankton availability or productivity. Thatrelation was not directly established, but a great deal was learned about subarctic microbiology by Kirchman and the several colleagues he recruited to help (KEIL and K~RCHMAN, 1991a, 1991b; KIRCHMAN, 1990, 1992; KIRCHMAN,KEIL, SIMON and WELSCHMEYER,1993;
Pelagic production processesin the subarctic Pacific
KIRCHMAN,KEIL and WHEELER, 1989, 1990; MONTGOMERY,WELSCHMEYERand KIRCI-IMAN, 1990; SIMON, 1991; SIMON, WELSCHMEYERand KIRCHMAN,1992). An additional feature of the "microbiological revolution" which swept through SUPER as it swept through all of biological oceanography is the newly recognized importance of bacterial photosynthesis. This has been accounted for in all the floristic analyses of Beatrice Booth, which included counts of Synechococcus from 1984 on. Susanne NEUER(1992) contributed a study of growth rates in these prokaryotic plants by the frequency-of-dividing-cells method. She showed large seasonal variation with highest growth rates in spring of 1 doubling d "1. To understand microheterotrophy, we must know the life and times of oceanic Protozoa in detail. Considerable work in this direction was included in SUPER. Beatrice BOOTH (1990) examined the choanoflagellate fauna, adding descriptions oftwo new species. Suzanne Stromused culture techniques to begin the analysis of feeding biology in heterotrophic dinoflagellates (STROM, 1991 ) and oligotrichous ciliates (STROM, 1990). She has al so examined the impact ofphytopl ankton pigment digestion by herbivorous protozoa on the pigment budget method (STROM1993a) and she has contributed a field study of ciliate abundance and vertical distribution to this volume. Bruce MONGERand Michael LANDRY(1990) have been working on a theory of the particle interception mechanics affecting the feeding of protozoans. An experimental test of their ideas (MONGERand LANDRY, 1991) was accomplished in the field during the SUPER expeditions. Landry's group has also contributed work on the details of feeding biology in heterotrophic microflagellates (LANDRY, LEHNER-FOURNIER,SUNDSTROM,FAGERNESSand SELPH, 1991). On our September cruise of 1984 there were considerable numbers of both solitary and aggregate phases of Cyclosalpa bakeri. This salp is weak bodied, resembling mucous in the consistency of the whole animal. However, they reach several decimeters in length and produce very large fecal masses. It seemed possible that they were significant grazers. Their soft bodies, however, made them difficult to study and required a direct and gentle approach. We recruited Jennifer Purcell and Laurence Madin to study this animal using SCUBA, and they participated in the late summer cruises of 1987 and 1988. The result was not what we anticipated. Cyclosalpa bakerimakes a classical diel vertical migration from day depths around 70m to close to the surface at night. However, the feeding schedule is inverse to the usual one for migrators. There was no elaboration of feeding webs and thus no feeding atnight, but only during daylight at depth. The rise to the surface atnight is apparently to facilitate exchange of sperm by concentration in a thin stratum at the surface. PURCELLand MADIN(1991) speculate that feeding webs are eliminated so as not to interfere with passage of sperm to the genital apertures. They have also (MADINand PURCELL, 1992) evaluated feeding, respiration, and excretion rates by C. bakeri. Since the large copepods endemic in this region don't feed to a significant extent on phytoplankton, yet are growing and developing almost continuously (MILLER, 1993), they must be preying upon the herbivorous protozoans. Dian Gifford and Michael Dagg made a substantial effort to evaluate the losses from microciliate stocks to copepod predation and the contribution of ciliates to copepod nutrition. Their work included a warm-up study of the nutrition ofdcartia tonsa in the Gulf of Mexico (GIFFORDand DAGG, 1988) and a comparison of the results to those for Neocalanusplumchrus in the Gulf of Alaska (GIFFORDand DAGG, 1990). Both DAGG(1991) and GIFFORD(1993) have reevaluated the experiments in later publications. We made an extended attempt to evaluate the impact of large copepods, particularly N. plumchrus, on the system dynamics. Part ofthi s work sought to show exactly which strata the large, interzonal migrator species occupy while grazing. They divide the euphotic zone among them in sharply defined fashion (MILLER and SUPER GROUP, 1988; MACKAS, SEFTON, MILLER and RAICH, 1993). Neocalanus plumchrus and N. flemingeri occupy the surface layer above the
incipient seasonal thermocline, Eucalanus bungii and Neocalanus cristatus occupy the zone from that point down to about the halocline. DAGG(1993) has suggested that at least N. cristatus feeds primarily on detritus. Possibly it is dependent upon the upper layer species pair to produce sinking particles. However, DAGGand WALSER(1986) showed that at oceanic food levels the pellets of N. plumchrus would be small for this large species, reduced in density, and would sink relatively slowly. Clearly the details of this complex of species interactions remain to be worked out. Other studies involved deck incubations in "mesocosms", including stories of grazing on phytoplankton in general and specifically on larger cells, feeding on ciliates, and the role ofcopepods in nutrient regeneration. A report on the results is provided here (LANDRY,GIFFORD,KIRCHMAN,WHEELER and MONGER, 1993), which amplifies earlier reports on various aspects of the mesocosm work (LANDRY and LEHNER-FOURNIER,1988, 1992; MILLER et al, 1991a; LANDRY and LEHNERFOURNIER, 1992). Because the exact phenology of large copepods was important in the Maj or Grazer Hypothesis, SUPER included studies of life history details. In fact the program began with this work (MILLER, FROST, BATCHELDER, CLEMONS and CONWAY, 1984). Eventually we recognized that the copepods we identified as N. plumchrus were in fact a compound of two, distinct species. Description of the new form as Neocalanus flemingeri MILLER (1988) allowed a life history analysis showing that it matures just prior to entering diapause and rests as the fertilized female (MILLERand CLEMONS, 1988). Timing of growth has been studied in each spring SUPER cruise (MILLERand NIELSEN, 1988; MILLER, 1993). One of the many ancillary projects undertaken by SUPER participants showed that N.plumchrus has a much more variable phenology in the western subarctic than in the Gulf of Alaska (MILLERand TERAZAKI, 1989); another showed the year-toyear variability in body size ofN. plumchrus and N.flemingeri during their deep resting phase in the Gulf of Alaska (MILLER, etal, 1992). In addition to work on Neocalanus, an extensive effort by Harold Batchelder was devoted to the biology of Metridia paciica (BATCHELDER, 1985, 1986a,b; BATCHELDERand MILLER, 1989), and several studies of chaetognaths utilized our weathership samples (TERAZAKIand MILLER, 1982, 1986). Additional papers will appear from time to time. however, all of the participants are now distracted by other projects, and these publications may have to wait for the final excavation of our files after we individually retire from active work. Therefore, I will not attempt to anticipate those papers that I hope will be written. 7. FURTHERSTUDIES1NTHE SUBARCTICPACIFIC Ecological understanding of the subarctic Pacific is far from complete. Just atthe lowest trophic levels that have been the focus of SUPER there are many outstanding problems. As stated above, the significance and mechanisms of iron limitation are ripe for further work. Microherbivores in our model are certainlymatchedbyreal protozoans in the Gulf of Alaska, butnearly everything remains to be learned about them. Is there a stock cycle equivalent to that in FROST'S (1993) model? The taxonomy and biology of oceanic protozoans is an open issue everywhere, not just in the subarctic Pacific. The character of the system in winter requires much further study, and we now have the large ships capable of winter expeditions. Further developments for working from those ships in stormy conditions will enable analysis of winter ecology. SUPER attempted to obtain a fairly complete nitrogen budget. This work was not satisfactorily finished, although some important components were well measured, particularly nitrate uptake rates for spring and summer (WHEELERand KOKKINAKIS, 1990; WHEELER, 1993). It remains desirable to obtain a full nitrogen budget, nitrogen being an ideal proxy for biologically mediated
Pelagic production processes in the subarctic Pacific
elemental cycles in general because of the correspondence of nitrogen oxidation states to specific biological transformations. As stated above, balancing of the nitrogen budget cannot be done on the basis of brief or seasonal visits to this strongly seasonal, oceanic ecosystem. The vertical transfer and biological transformation terms of the nitrogen budget can only balance on an annual basis. Much remains to be learned about the mesozooplankton of the subarctic Pacific in late summer. Our work, particularly mine, has concentrated on the interzonal migrator species abundant in spring, neglecting the more complex and variable results of the summer expeditions. This needs to be remedied. We know (JOHN FULTON, unpublished) that the zooplankton of the later productive season varies between years with Calanuspacificus dominant one year, Metridiapacifica another, and so on. We don'tknow much about this season, and SUPER did not make as large a contribution as it should have done. We did not tackle any aspect of higher trophic level ecology of the subarctic pacific. A rich and varied nektonic fauna, including squid, oceanic salmon, saury, pomfret, and numerous species of marine mammals and sea birds, draws sustenance from the balanced food web of the region. Coupling of these stocks to the production base is an almost untouched research area. 8. ACKNOWLEDGEMENT Preparation of this ingoduction was supported by NSF (OCE-9012295). 9. REFERENCES ARCHER, D., S. EMERSON,T. POWELLand C.S. WoN~ (1993) Numerical hindcasting of sea surface pCO 2 at
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