Carbon and nitrogen isotopic composition of sedimenting particulate material at Station Papa in the subarctic northeast Pacific

Deep-Sea Research II 46 (1999) 2793}2832

Carbon and nitrogen isotopic composition of sedimenting particulate material at Station Papa in the subarctic northeast Paci"c Jinping Wu , S.E. Calvert *, C.S. Wong
, F.A. Whitney
School of Earth and Ocean Sciences, University of British Columbia, Vancouver, BC, Canada V6T 1Z4
Institute of Ocean Sciences, Sidney, BC, Canada V8L 4B2 Received 5 April 1998; received in revised form 17 December 1998; accepted 17 December 1998

Abstract The dC and dN of sedimenting particulate organic matter (POM) collected biweekly by sediment trap at 3800 m at Ocean Station Papa (OSP: 503N, 1353W) in the NE subarctic Paci"c from 1982 to 1990 changed signi"cantly on seasonal and annual time-scales. dC ranged .-+ from !25.3 to !22.0, and dN ranged from 0.24 to 7.75, over the entire period, .-+ isotopically depleted values occurring mainly in summer and heavier values occurring in winter. Extreme depletion in dC values also occurred in the winters of 1982}83 and 1988}89 and .-+ in the late summer of 1985; these were not matched by signi"cant changes in dN . The .-+ changes in isotope ratios are related to the annual changes in settling particulate #uxes only in a general way; #ux maxima in particulate organic carbon (POC) and particulate organic nitrogen (PON) occurred in mid- and late summer in most years, but there is not a one-to-one correlation between these changes and the isotope variations. In some years, the isotope ratios begin to changed before the summer increase in settling #uxes. A one-year record of sedimenting dC and dN (1989}90) at three depths (200, 1000 and 3800 m) at the same location .-+ .-+ showed a marked carbon isotope enrichment with depth, consistent with decomposition or/and food-chain enrichment during particle settling, but very small changes in the nitrogen isotope composition of the same particles, suggesting that C and N are released from sedimenting particles via di!erent pathways. Suspended dC and dN values increased signi"cantly .-+ .-+ with depth and were higher than those of sedimenting POM below the euphotic zone, suggesting that the two types of POM do not interact in deep water. Seasonal variations in surface temperature, irradiance, phytoplankton growth rate, species composition and carbon "xation pathways do not appear to be important controls of the observed changes in dC ; .-+ the increases in temperature, irradiance and phytoplankton growth rate in the summer months

* Corresponding author. Fax: #1-604-822-6091. E-mail address: [email protected] (S.E. Calvert) 0967-0645/99/$ - see front matter  1999 Elsevier Science Ltd. All rights reserved. PII: S 0 9 6 7 - 0 6 4 5 ( 9 9 ) 0 0 0 8 4 - 3

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should lead to enriched dC values rather than the observed isotopically light values in this .-+ season. Likewise, the summer increase in the growth of diatoms should produce isotopically heavy particles in view of the reported C-enrichment of this group, and this should be augmented by the decrease in [CO ] due to the summer increase in surface temperature.    Opposing these possible controls, the planktonic food chain becomes shorter in the spring/early summer months, probably due to the migration to the surface of copepodites and their direct grazing on phytoplankton, and this results in C enrichment relative to the winter months when the food chain is more complex. The relationship between sedimenting dN and the .-+ macro-nutrients at OSP is complicated by the fact that ammonium and urea are important phytoplankton substrates, and generally more so than nitrate. The change from isotopically heavy winter values to lighter summer values begins before the major drawdown of the surface nitrate, and the observed change is opposite to that observed in other ocean regimes, probably because nitrate never reaches limiting levels in this High Nutrient Low Chlorophyll regime. The change of phytoplankton composition from winter to summer also should lead to N-enrichment, the opposite of the trends observed. Finally, the changes in sedimenting dN at OSP do not appear to be related to phytoplankton growth rate. We conclude that .-+ the nitrogen isotopic signal in settling POM at OSP re#ects seasonal changes in food-web structure, the simpler (shorter) spring/summer plankton community causing a smaller isotopic fractionation from the nutrient substrate to sedimenting POM.  1999 Elsevier Science Ltd. All rights reserved.

1. Introduction The stable isotopic composition of settling particulate material in the ocean constitutes a tracer of surface ocean biogeochemical processes, which, when properly calibrated, may provide further insight into the physical, chemical and biological factors that govern the magnitude of the #ux and the composition of the particulate material settling into deep water. Moreover, the link between surface biogeochemical processes, particulate #uxes and isotopic signals potentially provides the basis for hindcasting past oceanographic changes from sediment records. In order to establish this link, we require a series of long-term seasonal and interannual studies of particle #uxes in di!erent oceanic regimes, with concomitant determinations of the physical and chemical processes that control production, particle formation and export. The "rst study of interannual variations of dC and/or dN of sedimenting particulate organic matter (POM), and of seasonal variations of dC and/or dN of suspended POM and plankton was conducted at Station S in the Sargasso Sea, where a six-year (1978}1984) seasonal record of dN of sedimenting POM at 3200 m was obtained by Altabet and Deuser (1985). The study showed a strong inverse correlation between the downward #ux of particulate organic carbon (POC) and variations of sedimenting dN , suggesting a direct connection between the nitrogen isotopic .-+ signature of sedimenting particles and primary production. The second study, a three-year record of dN in settling particles at three stations in the northern North Atlantic from 1986 to 1989 (Voss et al., 1996), also showed a strong correlation between dN and mass #ux, while dC showed no clear relationship with the .-+ .-+

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particle #ux. Both of these studies revealed the fact that the isotopic compositions of sedimenting particles record surface biogeochemical processes and that surface signals are transported to deeper waters. In the third study, Altabet et al. (1991) and Rau et al. (1992), investigating the sources and transformations of sedimenting and suspended POM at a JGOFS station (NABE 473N, 203W) in the north Atlantic Ocean using dN and dC, respectively, demonstrated a tight coupling between surface and deep waters. They showed that seasonal variations in dC and dN of both suspended and sedimenting .-+ .-+ particles in the upper water column were associated with seasonal changes in nearsurface carbon and nitrate concentrations and particle #uxes. The signals from the near-surface changes propagated rapidly into deep water, but were modi"ed depending on the phase of the seasonal production cycle. Altabet et al., (1991) also found that the dN values decreased with depth, whereas the dN values of suspended .-+ POM increased with depth, suggesting that sedimenting and suspended particles did not interact extensively in the ocean and that there might exist a source of sedimenting POM other than recent surface production. The trophic transfer of carbon and nitrogen is another important process that a!ects the isotopic signals (Minagawa and Wada, 1984; Wada et al., 1987; Fry, 1988; Rau et al., 1990). From these studies, average increases of approximately 1 for carbon and 3.4 for nitrogen per trophic level have been determined. A relatively short trophic transfer, for example, might be from diatoms to mesozooplankton, whereas a longer trophic transfer leads from nanophytoplankton to microzooplankton and then to mesozooplankton (Parsons et al., 1967; Ryther, 1969). The trophic structure of marine ecosystems is generally determined by size-fractionation measurements (Parsons and LeBrasseur, 1970) and gut content analysis (Mackas and Boher, 1976; Morales et al., 1990). These methods cannot provide an integrated measurement of trophic position, which is required for studies of material #ows and budgets, but such a measurement can be provided by stable isotopic data. Dru!el et al. (1986) reported that the dC values of sediment trap POM at 3800 m collected in the spring and summer of 1983, together with C data, pointed to another source of organic material settling to the sea #oor at OSP, probably via land input from the coastal margin or via atmospheric transport. No previous studies of the nitrogen isotopic composition of deep-water sedimenting POM at OSP have been published, although Saino (personal communication) determined dC and dN of POM in the euphotic zone and found that the isotopic values were !24, for dC and 1 for dN in May 1986, lower than those in other regions in the Paci"c. In the northwest Paci"c, Nakatsuka et al. (1995) and Nakatsuka and Handa (1997) measured nitrogen #uxes and the nitrogen isotopic ratios of sedimenting POM at four di!erent sites, using year-long time-series sediment traps. They found that the factors controlling variations of the nitrogen isotopic ratio are phytoplankton blooms, resuspended sedimentary particles and horizontal advection. In this paper, we investigate the carbon and nitrogen isotope systematics in the NE subarctic Paci"c by examining long-term records of isotopic variations of sedimenting POM and vertical pro"les of isotopic variations of suspended POM at OSP (Wong et al., 1999). Sampling at bi-weekly intervals has permitted high-resolution

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determination of seasonal, as well as annual, changes in #uxes and particle compositions. We also determined dC and dN at 200, 1000 and 3800 m depth over .-+ .-+ an annual cycle (1989}1990) in order to estimate the changes in isotopic signals within the water column, and we compare the vertical variations in dC and dN of sedimenting and suspended POM in the upper 1000 m. Isotopic data on bulk suspended POM, medium-sized particles (50}253 lm, dominated by diatoms), "ne particles ((5 lm, dominated by nanophytoplankton) and several major groups of zooplankton provide some insight into isotopic fractionation in photosynthetic processes and the trophic transfer of the isotopes in the near-surface planktonic food web. Finally, we pro"led nitrate dN to determine the isotopic composition of the deep-water nitrogen source and the relationship between the dNO\ and [NO\]   and between the dNO\ and sedimenting and suspended dN .  .-+ 2. Materials and methods A time-series sediment trap was deployed at OSP at 3800 m depth at OSP from 1982 to 1990 and at 200, 1000 and 3800 m depths for 1 year in 1989}90. Details of the deployment and sample collection periods as well as the sample treatment protocols are given by Wong et al. (1999). The traps contained sodium azide to retard degradation of the collected material and NaCl to minimize di!usive loss of the preservative. Pro"les of suspended POM were obtained by collecting 10}30 l of water from the surface to 500 m depth with Go-#o bottles. The "ltrate from the suspended POM collection was used for nitrate dN determination following the methods described by Wu (1997). Size-fractionated suspended POM (50}253 and (5 lm) was collected with two net "ltration devices (Wu, 1997). Zooplankton were collected with a zooplankton net. Large zooplankters, such as chaetognaths, amphipods, euphausiids and occasional salps, were removed and analyzed separately. The remaining material was dominated by copepods, and was "ltered onto a Nuclepore "lter (0.45 lm). For carbon isotopic determinations, about 50 mg dry POM samples were weighed into glass vials, and 1 ml 1N HCl was slowly added to remove carbonate. The samples were then dried without washing at 503C for 48 h. About 5 mg of the dry acidi"ed samples were then placed in tin cups, the cups were crimped and weighed and then placed in the carousel of a CHN Elemental Analyzer (1006 Carlo Erba) connected to the mass spectrometer (Prism Series II, VG IsoTech) for measurement. Suspended POM samples on GF/F "ber glass "lters were "rst de-carbonated with about 1 ml 1 N HCl and dried in an oven. They were prepared for Dumas combustion by "rst grinding in an agate mortar with 1 g CuO; they were then placed in a 23 cm;6 mm o/d Vycor tube with 0.5 g copper granules, the tube was evacuated to less than 3.0;10\ mbar and then #ame-sealed. The sealed tube was heated to 9003C in a furnace for 2 h and then cooled overnight to convert any CO to CO . The CO was released in a tube-cracker   and cryogenically puri"ed before introduction into the mass spectrometer. The Dumas method also was used to prepare samples for dN determination. The N gas was puri"ed cryogenically and trapped on a molecular sieve (5 As , Alltech ASS 

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Inc.) at liquid N temperature (!1963C). The ampoule with the trapped N was then   heated to 1503C and the N was introduced directly into ion source of the mass  spectrometer. All isotopic results are expressed in the conventional d notation: R !R ;1000 d"    R  where d() is dC() or dN(); R and R are the ratios of C/C and     N/N for samples and reference, respectively. PDB is the reference standard for dC, and air nitrogen is the standard for dN. The external precision for both isotope measurements was better than 0.2, including the internal instrument precision (0.02).

3. Results Material collected in the OSP traps consisted of aggregated, "ne-grained, structureless particles with small numbers of recognizable whole and fragmented diatoms, radiolaria, silico#agellates, foraminifera and pteropods. Material coarser than 63 lm seldom constituted '20}50 of the mass, and faecal pellets were collected very infrequently. The bulk of the "ner material is probably amorphous organic matter and comminuted diatom frustules. The sum of biogenic components (organic matter, carbonate and biogenous silica) comprised on average 95$8 of the total mass collected over the period (Wong et al., 1999). 3.1. Carbon isotopes 3.1.1. Vertical variations in yuxes and sedimenting dC MPE?LGA Total and POC #ux maxima at 200 m during 1989}90 occurred at the end of May, followed by a smaller peak in July, after which there were very low #uxes in winter and early spring (Fig. 1A). Total and POC #uxes at 1000 and 3800 m similarly increased from the low winter values to maxima in June and August. The sedimentation rate estimated from the delay in #ux maxima with depth was 177$40 m\ (Wong et al., 1999), consistent with the rate estimated from radiolaria #ux data for 1982}84 by Takahashi (1987a). Annual average values of sedimenting dC increase with increasing depth    from !24.57 at 200 m to !23.40 at 1000 m and then to !22.84 at 3800 m (Fig. 1B). At 200 m depth, the dC begins to decrease in January, and continues    to decrease to March, these changes coming well before the large increase in carbon #ux in May. Changes in carbon #ux and dC at 1000 and 3800 m depth are    similarly lagged. Thus, the changes to lighter carbon isotope values at OSP occur signi"cantly before the changes in downward carbon #ux, showing that the isotope signals are uncoupled from the processes controlling the transfer of particulate organic matter to deep waters.

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Fig. 1. Variations of (A) POC #ux and (B) sedimenting dC at 200, 1000 and 3800 m at OSP from .-+ November 1989 to November 1990.

3.1.2. Eight-year variations of yuxes and dC One hundred and seventy-two samples of sedimenting POM were obtained from 16 separate sediment trap deployments from 1982 to 1990. Variations in the total, C , N and biogenic silica (biosilica) #uxes during the 1982}90 period are     described by Wong et al. (1999) and are summarized in Fig. 2. The principal features are the more-or-less regular seasonal changes in the #uxes of all components, with maxima in the summer/fall and minima in winter. The exceptional #ux maximum in 1983 re#ects the unusual oceanographic conditions in this part of the North Paci"c in response to the intense 1982 El Nin o event (Wong and Honjo, 1984), which evidently enhanced summer production (Wong et al., 1998). The maxima in total #uxes are matched by maxima in organic C, N and biosilica, showing that the #uxes are driven by the annual cycle of organic production. The seasonal variability in diatom and silico#agellate #uxes during 1983}86 have been discussed by Takahashi (1986, 1987a,b)). Variations in dC are shown in Fig. 3. Most of the trap recoveries and    redeployments were made in the spring and autumn of each year; no signi"cant

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Fig. 2. Time-series of total, organic carbon, total nitrogen and biogenous silica #uxes at 3800 m depth at OSP, 1982}1990.

change was found in the data between contiguous deployments. In a 2-year degradation experiment, a change of 0.00066 d\ in dC due to storage of the wet    samples at 53C was found (Wu, 1997). This is signi"cantly smaller than the value of 0.002d\ for zooplankton stored in formalin reported by Mullin et al. (1984). The values obtained here have not been corrected for this e!ect because the appropriate functionality (linear vs. exponential) of the degradation process is unknown. However, since we are interested in seasonal variations in the isotope signals rather than long-term trends this will not a!ect the main results. Extreme values in the data, such as the most negative values observed in the winters of 1982 and 1988/89 and in the fall of 1985, were re-analyzed in duplicate or triplicate. The time-series of dC values of sedimenting POM show a regular annual    variation over the eight-year period (Fig. 3). The range of the values is from !25.3 to !22.0, with an average of !23.2. Over the annual cycle, minima (sometimes double minima) occur in summer and fall and maxima occur in winter. There are also extreme minima in the fall/winter periods of 1982, 1985 and 1988, and several sporadic events, with either light or heavy values, in all seasons. Most of the extreme values in the record are de"ned by several data points. The isotope signals that are propagated into deep water are given by the #uxweighted average values for a given time period. A comparison between such values

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Fig. 3. Eight-year variations of POC #uxes and dC at 3800 m at OSP from 1982 to 1990. .-+

Table 1 Annual mean values of dC ($1p) of sedimenting POM at 3800 m at OSP Year

Arithmetic mean

1983 1984 1985 1986 1987 1988 1989 1990

!23.14$0.49 !23.23$0.42 !23.39$0.63 !22.87$0.36 !22.80$0.39 !23.13$0.37 !23.71$0.63 !22.82$0.42

Grand mean

!23.20$0.62 (n"167)

(n"20) (n"22) (n"23) (n"18) (n"24) (n"14) (n"26) (n"20)

Mass #ux weighted mean !23.06 !23.24 !23.53 !23.10 !22.96 !23.29 !23.63 !22.93

(n"20) (n"22) (n"23) (n"14) (n"22) (n"14) (n"26) (n"20)

!23.22 (n"161)

Note: Unit". n"number of samples.

and the arithmetic averages of the values for each year, which represent original surface isotopic signals, are shown in Table 1. Note that there are small samples (n"13) for two years (1986 and 1988), so the averages of these years have larger uncertainties than the other years. The average POC-#ux-weighted dC value is !23.56, !0.36 lower than the non-weighted data. The relationship between the #ux variations and dC in each of the eight years is shown in Fig. 4. dC changes to lighter values coincident with the POC #ux increases in May}June 1983, April and August 1984, September 1985 and April}July 1987. The exceptional late summer #ux maximum in 1983 has a modest increase in dC    following the small minimum earlier in the summer. There are several #ux maxima in the records that are matched by very minor changes in dC , especially in   

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Fig. 4. POC #uxes and POM dC at 3800 m in each of the years between 1983 and 1990.

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August}September 1983, August 1986, September 1988, May 1989 and June 1990. In addition, the 1988 record is marked by a continuously decreasing trend of dC    from the winter values to July}August, followed by a small rise to September. In 1989, the dC values increase slowly from February to December, following the very    low values recorded in the winter (1988}89) period; a small decrease is seen just before the June}July #ux maximum. In 1990 there is no signi"cant isotope change associated with the major June #ux maximum, but there is a small decrease during a secondary #ux peak in August. Finally, there is only a very small change in dC during the    extreme #ux maximum in August}September 1983 the large negative excursion in dC in 1985 occurs during a minor #ux peak in September, and the large    negative dC change in the winter of 1988}89 occurred during the very low    winter #ux period. These observations show that the changes in settling POM dC recorded at 3800 m depth at OSP are not directly related to the seasonal    change in #uxes, which are themselves tied reasonably well to the seasonal changes in production (Wong et al., 1999). Thus, other factors must be involved in producing the isotopic signals. A comparison between sedimenting POM dC and the biosilica #uxes    provides information on the degree to which the changes in the #uxes and the isotopic composition of a particular component of the phytoplankton, namely diatoms, silico#agellates and radiolaria, might be coupled (Fig. 5). This shows that the dC changes are somewhat more closely correlated with the #ux changes,    especially during 1984, 1985, 1986, 1987 and 1990, and that the dC changes do    not lead the increases in #uxes in biosilica. The very light dC values in late 1982    and in the autumn of 1985 both occur during biosilica #ux maxima; however, the dC minimum in winter 1988}89 occurs during a very low #ux period. More   over, there are very small changes in dC in 1988 and 1989 during major    changes in biosilica #uxes. 3.1.3. Suspended POM and Plankton dC Surface water size-fractionated POM and plankton dC data (Table 2) show that the (5 lm fraction, comprising mainly nanophytoplankton, is much lighter isotopically than the bulk SPOM and plankton. In addition, some samples of the (50 lm fraction also have values as light as !27. In contrast, the bulk suspended POM has a dC value of !23.2. The results for OSP show that di!erent phytoplankton    appear to have di!erent dC values, with the smaller and dominant nanophytop   lankton having lower dC values and diatoms having higher values.    The dC values of the mesozooplankton are in the range !24}!25 in    spring and !21}!22 in autumn. Large components of the zooplankton samples, such as euphausiids and amphipods, have dC values ranging from    !21}!24, and are generally heavier than, or close to, the copepod values. Amphipods have the highest isotopic values, re#ecting their position at the highest trophic level in the zooplankton community. Euphausiids, with intermediate values, appear to lie between copepods and amphipods. The dC values of mesozooplankton are generally similar to those of bulk    suspended POM, but are higher than those of "ne suspended POM ((5 lm). The

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Fig. 5. Biogenous silica #uxes and POM dC at 3800 m in each of the years between 1982 and 1990.

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Table 2 Suspended POM (SPOM) and plankton dC values at OSP Sample SPOM SPOM SPOM SPOM Bulk Bulk Bulk Bulk Bulk Bulk Bulk

Date (50}253 mm) ((50 mm) ((50 mm) ((5 mm)

SPOM SPOM SPOM SPOM SPOM SPOM SPOM

Zooplankton Mesozooplankton

Euphausiids Amphipods

May 04/91 Mar 31/92 Apr. 06/92 May 20/93

Depth (m) 5 1}2 1}2 5

dC () !24.6 !24.5 !27.1 !27.3

Apr. 06/92 Apr. 06/92 Apr. 06/92 Apr. 06/92 Apr. 06/92 Apr. 06/92 May 20/93

0 50 100 200 300 500 5

!24.2 !25.2 !24.2 !23.3 !23.8 !23.7 !23.2

Feb. 28/91 Feb. 29/91 May 03/91 May 03/91 Oct. 24/91 Feb. 10/92 Apr. 01/92 Apr. 06/92 Apr. 06/92 Apr. 06/92

100}0 100}0 200}0 200}0 200}0 200}0 200}0 200}0 200}0 200}0

!24.0 (N) !24.5 (D) !24.8 !24.3 !20.6 !22.3 !24.0 !24.0 !22.6 !23.7

Note: Samples were collected during several cruises from February 1991 to May 1993. N"night; D"dawn.

dC values of mesozooplankton collected in autumn and winter are higher than    those collected in spring and summer, suggesting that seasonal changes of plankton dC values are coincident with those of sedimenting POM.    3.2. Nitrogen isotopes 3.2.1. Variations of total N yuxes and sedimenting dN The pattern of particulate N (PN) #uxes at three depths (Fig. 6A) is similar to that of the C #uxes in 1989}90 (Fig. 1A). The maximum N #ux at 200 m, up to    8 mg N m\d \, occurred in May and June, followed by a smaller peak in July and August. Smaller N #uxes, 0.5 to 1 mg N m\d \, occurred in the winter and early spring. The lowest N #ux and the highest dN occur in winter (February}April), and the highest N #ux corresponds to a decrease in dN in summer (Fig. 6B). However, the decrease in sedimenting dN began at the end of March, while the increase in

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Fig. 6. Variations of (A) PON #uxes and (B) sedimenting POM dN at 200, 1000 and 3800 m at OSP from October 1989 to October 1990.

N #ux started 2 weeks later, in mid-April. The sedimenting dN remained low for about three to four months, while there was an increase of N for a single month. It therefore appears that the N #ux and dN are correlated only for a short time period in the spring when the PN #ux increases dramatically. The highest value of sedimenting dN in winter is 5.19 and the lowest value in summer is 1.70, with a non-weighted average of 3.19$1.12 (1p, n"19) and a N-#ux weighted value of 2.76 (n"19). The di!erence between the two seasons (3.49) is roughly the same as the isotopic fractionation between one level trophic transfer in the zooplankton community (Wu et al., 1997). The changes in dN with depth are much smaller than the changes in dC    (Fig. 1B). Thus, sedimenting particle dN values decrease slightly with depth in winter (with an exception in early March 1990), and remain constant or increase slightly with depth in summer. Thus, the largest changes in sedimenting dN are con"ned to the winter months when the #ux is lowest. Similar observations were made by Saino and Hattori (1987) in the northwest Paci"c Ocean, by Wada et al. (1987) in the Antarctic Ocean and by Altabet et al. (1991) and Voss et al. (1996) in the north Atlantic Ocean.

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3.2.2. Eight-year variations of yuxes and sedimenting dN The eight-year time-series shows consistent annual changes of sedimenting dN, which range between 0.24 and 7.55 (Fig. 7). The eight-year average of dN at OSP is roughly 1 higher than in the Sargasso Sea (Altabet and Deuser, 1985) and similar to that in the northern North Atlantic Ocean (Voss et al., 1996). The pattern of variability of the sedimenting dN appears to be somewhat simpler than that of sedimenting dC (Fig. 3), in that there is an annual cycle, with the lightest values    in summer and the heaviest values in winter, and episodic events, consisting of high values that occur randomly in all seasons. The comparison between the #ux-weighted annual average isotope values and the arithmetic means (Table 3) shows that the isotopically lighter values occur during the summer #ux maxima.

Fig. 7. Eight-year variations of sedimenting PON #uxes and POM dN of at 3800 m at OSP from 1982 to 1990. Table 3 Annual mean values of dN ($1p) of sedimentingPOM at 3800 m at OSP Year

Arithmetic mean

Mass #ux weighted mean

1983 1984 1985 1986 1987 1988 1989 1990

3.16$0.72 3.65$0.82 3.34$1.33 3.36$0.88 3.89$1.30 3.03$0.78 2.36$1.23 2.59$1.09

3.00 3.26 3.34 3.11 3.26 2.78 1.56 2.32

Grand mean

3.16$1.16 (n"161)

Note: Unit"; n"number of samples.

(n"19) (n"19) (n"20) (n"13) (n"22) (n"15) (n"27) (n"20)

(n"19) (n"19) (n"20) (n"13) (n"20) (n"14) (n"26) (n"20)

2.84 (n"157)

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When considered on a year-to-year basis (Fig. 8), the #ux and isotope records for 1984, 1986, 1989 and 1990 show a reasonably good correspondence between increasing PN #ux and decreasing dN, while 1985, 1987 and 1988 reveal a much lower degree of correlation between these variables. In 1983, an anomalous year, the very large #ux maximum in August}September is marked by a very small change in dN, and the same is true for the smaller #ux maxima in August}September 1987 and 1988. The correspondence between dN and biosilica #uxes (Fig. 9) is somewhat better, the larger changes in dN occurring when there were large changes in #uxes. But again, many of the large decreases in dN in the late winter/spring occur before increases in #uxes. 3.2.3. Suspended POM dN A limited number of determinations of the isotopic composition of suspended POM at OSP are available for examining the changes in isotope ratios with respect to the hydrographic and ecosystem changes on a seasonal basis (Table 4). The dN values of (5 lm POM range from 2.34 to 2.80 (average"2.70$0.21, 1p, n"3), while those of total POM range from 2.63 to 2.95 (average"2.78$0.16, 1p, n"3). A di!erence of ca. 1 was found between the dN of medium POM (50}253 lm) collected in May 1991 and (5 lm POM collected in May 1993, possibly re#ecting a larger isotopic fractionation during the utilization of nitrate by diatoms and isotopically lighter ammonium utilization by the nanophytoplankton. There appears to be a small seasonal di!erence in the isotopic composition of the bulk suspended POM, the mean dN value for early spring samples (April 3, 1992) being slightly lower than those for late spring samples (May 22}24, 1993). This may be due to di!erences in the relative abundance of nanophytoplankton (isotopically light) and diatoms (isotopically heavy) during the di!erent seasons. The dN of surface suspended POM appears to be less variable than dC, which is very di!erent for di!erent phytoplankton groups. It therefore will be somewhat easier to interpret changes in dN induced during trophic transfer. dN values of zooplankton (Table 5) show that, in general, euphausiids and bulk mesozooplankton (dominated by copepods) have lower dN values than amphipods. Two other zooplankton groups (chaetognaths and pteropods) were occasionally sampled and analyzed. Chaetognaths had the highest value (8.34$0.55, 1p, n"4) at OSP in May 1993, while the dN values of amphipods, bulk mesozooplankton (dominated by copepods) and euphausiids from the same haul were 6.33$0.81 (1p, n"3), 6.23$0.21 (1p, n"2), and 5.61, respectively. Pteropods had a lower dN value (4.23) than bulk mesozooplankton (dominated by copepods) (5.88) in Spring 1992. Among the three groups, namely bulk mesozooplankton (dominated by copepods), euphausiids and amphipods, where a comparison can be made for their trophic positions due to a higher sampling frequency, the highest values are found in amphipods (Table 5). 3.2.4. Nitrate dN The concentration and dN of nitrate were determined in the upper 500 m at OSP in May 21, 1993 (Fig. 10B). The nitrate concentration was approximately 8 lM in the

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Fig. 8. PON #uxes and sedimenting POM dN collected at 3800 m each year between 1983 and 1988.

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Fig. 9. Biogenous silica #uxes and sedimenting POM dN at 3800 m in each of the years between 1982 and 1990.

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Table 4 The dN values of the bulk, medium (50}253 lm) and "ne ((5 lm) surface suspended POM (SPOM) at OSP Sampling time (Starting)

50}253 lm SPOM dN ()

1600 h 0000 h 0630 h 1130 h 1800 h 1000 h 1230 h 1500 h 2230 h 1000 h 2400 h

3.69 3.81

May 02 1991 May 04 1991 Oct. 24 1991 Oct. 24 1991 Mar. 31 1992 Apr. 03 1992 May 22 1993 May 22 1993 May 22 1993 May 24 1993 May 24 1993

Bulk SPOM dN ()

(5 lm SPOM dN ()

3.09 2.65 1.63 1.69 2.80 2.74 2.75 2.63 2.95

2.34

euphotic zone and increased to 40 lM at 400 m, while dNO\ was 7.6 at the  shallowest depths and then decreased rapidly from 50 to 100 m and more gradually to about 3.5 at 400 m. This latter value is close to the annual average sedimenting POM (Table 3) at this site. The deep water value is identical to that reported by Altabet (1988) in the Sargasso Sea and by Voss et al. (1996) in the northern North Atlantic, but signi"cantly lighter than the values found in the Central Paci"c Ocean and northern North Atlantic Ocean by Liu and Kaplan (1989) and in the subAntarctic and Antarctic waters of the Indian Ocean by Sigman et al. (1997).

4. Discussion Previous work suggests that a wide range of environmental and physiological factors can in#uence the isotopic composition of POM in the ocean. For the carbon isotopes, these include ambient temperature (Fontugne and Duplessy, 1981), pH (Hinga et al., 1994), light (Durako and Hall, 1992; Thompson and Calvert, 1994), plankton photosynthesis (Degens et al., 1968a,b), species composition (Wong and Sackett, 1978; Falkowski, 1991), food web structure (Peterson and Fry, 1987; Fry, 1988; Checkley and Miller, 1989; Altabet and Small, 1990) and surface water CO /[CO (aq)] (Rau et al., 1989; Franc7 ois et al., 1993a). For the nitrogen isotopes,   dominant factors appear to be the relative extent of NO\ utilization (Wada and  Hattori, 1976; Altabet, 1988; Franc7 ois et al., 1993b), species composition (Montoya and McCarthy, 1995) and trophic transfer (Minagawa and Wada, 1984). It is useful in this discussion to consider separately environmental factors that could a!ect the isotopic changes observed and the intrinsic biological, i.e. biochemical and physiological, factors that also are probably involved.

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Table 5 Bulk suspended particulate organic matter (SPOM) and mesozooplankton dN at OSP between May, 1991 and May, 1993 Depth (m)

dN ()

23/93 23/93 23/93 23/93 23/93 23/93 23/93 23/93

0 10 30 50 100 300 400 500

4.8 4.4 5.2 5.2 7.2 8.8 9.3 9.7

Bulk Zooplankton

Feb. 28/91 Mar. 03/91 May 03/91 Oct. 24/91 Feb. 10/92 Apr. 06/92 Apr. 06/92 Oct. 20/92 May 23/93

100 100 200 200 200 200 200 200 150

5.7 5.7 7.4 4.7 5.7 5.9 5.3 5.6 6.2 (n"2)

Pteropodes

Apr. 06/92

200

4.2

Euphausiids

Apr. 06/92 May 20/92 May 23/93

200 200 150

5.5 5.5 5.6

Amphipods

Apr. 06/92 Feb. 10/92 May 23/93

200 200 150

6.1 7.0 6.3 (n"2)

Chaetognaths

May 23/93

150

8.3 (n"4)

Sample

Date

Bulk Bulk Bulk Bulk Bulk Bulk Bulk Bulk

May May May May May May May May

SPOM SPOM SPOM SPOM SPOM SPOM SPOM SPOM

4.1. Annual variations of climatic, hydrographic and ecological factors at OSP Sea surface temperature at OSP shows a marked annual variation from a maximum (12}133C) in late summer or early autumn to a minimum (5}63C) in late winter or early spring, the seasonal range being ca. 73C (Tabata, 1965,1989). In the upper 30 m, salinity reaches a minimum in late summer or early autumn, and a maximum in late winter or early spring. At depths of 75 and 100 m, the annual cycle appears to be opposite in phase to that in the surface layers, that is, the maximum occurs in autumn and the minimum in spring (Tabata, 1965). Solar radiation reaches a maximum at the end of June and a minimum at the end of December in the temperate regions of the northern hemisphere (Welschmeyer et al.,

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Fig. 10. Pro"les of the concentration and dN of nitrate at OSP in May 21, 1993.

1993). The mixed layer at OSP is deepest in winter and shallowest in summer (Parsons and LeBrasseur, 1968), but winter stocks of autotrophs and microheterotrophs are similar to those observed in summer (Boyd et al., 1995). The relatively shallow winter mixed layer permits relatively high standing stocks of phytoplankton and consequently of microheterotrophs, which are grazed throughout the year by microzooplankton (Miller et al., 1991; Miller, 1993). From May through October, light intensity increases and the critical depth is much greater than the maximum depth of mixing, resulting in an increase in primary production (Parsons and LeBrasseur, 1968). Macro-nutrients (nitrate, phosphate and silicic acid) are abundant all year around, but the maximum concentration for all three nutrients is in winter and the minimum is in summer (McAllister et al., 1960; Wong et al., 1998). Although the maximum in primary production occurs in late spring and late summer see (see Boyd and Harrison (1999) for the most recent summary of the data), average concentrations of Chl-a show little change with season (McAllister et al., 1960) due to intensive microzooplankton grazing which commences simultaneously with the spring increase in primary productivity (Miller and the SUPER Group, 1988; Miller, 1993; Boyd et al., 1995). Ammonium (Wheeler and Kokkinakis, 1990; Varela, 1997) and iron (Martin and Fitzwater, 1988; Boyd et al., 1996) are both considered to limit nitrate utilization by phytoplankton in this region, this probably being responsible for a low f-ratio (Eppley and Peterson, 1979) and the dominance of pico- and nanophytoplankton (Miller et al., 1991). The dominant phytoplankters at OSP are smaller than 5 lm in size and include mainly autotrophic #agellates and the cyanobacterium Synechococcus, with lesser

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numbers of pennate diatoms (Booth et al, 1993; Boyd and Harrison, 1999). The (3 lm (Welschmeyer et al., 1993) or (5 lm (Boyd and Harrison, 1999) fractions account for most of the primary production. Occasional `bloomsa of larger phytoplankton ('20 lm) are composed mostly of diatoms and dino#agellates (Booth, 1988; Booth et al., 1993). There are only small changes in this size distribution through the annual cycle (Boyd et al., 1995). The 3800 m-deep traps at OSP record large changes in biosilica #uxes over the annual cycle (Fig. 2; Wong et al. 1999). Apart from 1984, an anomalous year possibly due to the intense 1982}83 El Nin o Wong et al., 1998), biosilica #uxes increased signi"cantly from May to August in every year between 1983 and 1990, and in some years the increase began in April and lasted until September. Takahashi (1987b) and Takahashi et al. (1990) showed that diatoms are largely responsible for the biosilica #ux maxima, and that centric diatoms (dominated by Rhizosolenia spp. and Thalassiosira spp.) constituted the most important group in 1983 and 1985. Mesozooplankton biomass is minimal in winter at OSP, and reaches a distinct maximum in spring and summer (Brodeur et al., 1996; Goldblatt et al., 1999). The spring increase is coincident with the appearance of early life stages of the dominant copepods. Thus, early copepodites migrate to and develop in the surface waters from February through May, and "fth copepodites (CV) descend from the surface layer in late May to early June and mature immediately; this population appears to be a diapause phase (Miller et al., 1984; Miller and Clemons, 1988). Spawning occurs at the end of January and larvae migrate once more to the surface. Parsons and Lalli (1988) pointed out that the one-year life cycle of the copepods of the subarctic Paci"c Ocean constitutes one of the important di!erences between the pelagic ecosystems of the North Atlantic and Paci"c Oceans. 4.2. Relationship between the isotope signals and the POC yux Voss (1991) showed that sedimenting POM dC values in deep waters in the Norwegian Sea do not appear to be related in a simple manner to any easily determined, or understood, environmental factor. This inability to relate sedimenting particle dC values uniquely to oceanographic variables could be due to the complexity of the oceanographic regimes so far studied and/or to sample collection problems. Sporadic changes in surface conditions, such as [CO (aq)], plankton  composition and growth rates could lead to short-term variations in isotopic abundance that are not correlated with the sedimenting #ux of POM. The period of collection may be too short to reveal the real relationships between the isotopic signals and environmental variables, and the collection intervals (often 2 months) may be too long to permit the identi"cation of short-term or episodic forcing variables. The eight-year, high-resolution record of the isotopic composition of sedimenting POM at OSP displays large changes that contain information on surface physical and biogeochemical processes, although these signals are modi"ed by water column processes. In order to remove the e!ects of such processes on the isotopic compositions of the POM, we "rst examine the relationship between the isotopic signals and the #ux variations. The 1-year record (October 1989 to October 1990) of POC #uxes

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at 200 m depth (Fig. 1A and B) appears to be generally in phase with the changes in surface production, with a maximum in summer and a minimum in winter (Wong and Honjo, 1984; Takahashi et al., 1989; Honjo, 1990; Wong et al., 1999). In detail, the POC #ux maximum of 60 mg m\ d\ at 200 m occurred at the end of May and the beginning of June, and this was followed by a smaller peak in July. There were very low #uxes (1}3 mg m\d \) in winter and early spring. Over this period, the changes in sedimenting POM dC (Fig. 1B) are not well correlated with the changes in the POC #uxes. That is to say, the large decrease in dC begins in February and continues to late March/early April, whereas the large increase in #ux begins in mid-April. The dC minimum in mid-July however, does correspond with the secondary #ux maximum. Similar lack of strict phasing between #ux and dC is .-+ evident in the records from 1000 and 3800 m depth (Fig. 1A and B); dC begins to decrease well before the summer increases in #uxes at these two depths. On the other hand, as in the case of the #ux variations, the isotopic changes do show similar features at the three depths. Notably apparent is the lag in the minimum in dC in the summer, which is later at 1000 m by 2 weeks relative to the 200 m level, and later by roughly 4 weeks at 3800 m relative to 1000 m level. The annual mean di!erence between 200 and 3800 m (ca. 1.73) is probably due to the trophic transfer e!ect, whereby the heavier isotope is enriched in the particulate products during food chain transfer, and partly due to the decomposition of sedimenting POM, which would cause the heavy isotope to be enriched in the residual material. A comparison between the #uxes and the isotope data for the 8-year record at 3800 m shows (Fig. 3) that although dC is generally high (less negative) in winter and low in summer, the degree of correspondence between the two time-series is weak if the records for each individual year are considered (Figs. 4 and 5). This shows that there are often very small changes in dC during large POC #ux increases, and both increases and decreases in dC before changes in #uxes. In addition, although the relationship between the isotopic signals and biosilica #uxes appears to be somewhat closer, there is not a one-to-one correspondence between these records. Moreover, if diatom production were important in controlling the isotope values in the settling POM, one would expect the isotope values to increase rather than decrease during periods of increased silica #ux in view of the isotopically heavy isotope values reported for these phytoplankters (Fry and Wainwright, 1991). Once again, therefore, we conclude that the isotope changes observed must be in#uenced by other environmental or physiological factors, in addition to the increase in summer production which then leads to increased settling #uxes. 4.3. Environmental factors The e!ect of temperature on phytoplankton dC, 0.3/3C (Wong and Sackett, 1978; Fontugne and Duplessy, 1981), should produce an increase in dC of about 2 from winter to late summer at OSP due to the 73C temperature increase in the euphotic zone (Wu, 1997). However, the sedimenting POM dC decreases from spring to summer, showing that temperature cannot be responsible for the winter} spring changes in sedimenting POM dC. Temperature could be critical in the late

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summer}autumn, when the change amounts to 43C and dC increases by roughly 1.2 between the summer low values and the succeeding autumn values. The anomalous warming of surface water at OSP was teleconnected with ENSO during 1957}58 and 1982}83 (Tully and Barber, 1960; Tabata, 1961; Tabata and Peart, 1985). The composition of the plankton in the subarctic Paci"c Ocean also responds to ENSO events (Wooster and Fluharty, 1985; Takahashi, 1987b; Takahashi et al., 1989). Wong et al. (1998) showed that periods of greater than average surface nitrate drawdown at OSP between 1965 and 1990 were in phase with negative North Paci"c Index values (Emery and Hamilton, 1985). The 1983 extreme #ux maxima in all components at OSP are coincident with the strong 1982}83 ENSO, and there are also higher than average #uxes in the summer of 1987 (Wong et al., 1999). However, although the change in dC during 1983 shows a slight decrease to lighter values during the "rst #ux maximum, there is little change during the second peak (Fig. 3), suggesting that the isotope ratio is not directly related to the #ux of siliceous plankton. The lowest values of sedimenting POM dC 1982 and 1985, on the other hand, are coincident with the highest siliceous plankton #uxes. Although Rau and co-workers (Rau et al., 1991,1992) suggested that the carbon isotopic composition of marine phytoplankton is closely correlated with surface water [CO ] via the direct temperature control of CO solubility, Goericke and Fry    (1994a,b) found that this control by itself is inadequate to account for the full range of dC changes observed in marine phytoplankton. Bidigare et al. (1997) showed that the isotopic composition of haptophytes varies systematically with growth rate and with the concentration of dissolved phosphate. Most of the variations observed in isotopic fractionation appear to result from variations in cell growth rate, with little dependency on external cell [CO ]. Pancost et al. (1997) found that this relation  ship also applies to diatoms from the Peru upwelling region, but the small fractionation factors for this algal group suggest that the diatoms actively transport carbon into the cells, weakening the direct link between dC and [CO ]. This has been   supported experimentally by Tortell et al. (1997), who showed that intracellular DIC concentration in cultured diatoms can be 10 times higher than that outside the cell, which can support high rates of photosynthesis at low ambient DIC. This is consistent with their observations of steady-state growth rates that were signi"cantly larger than the maximum possible rates that could be supported by CO di!usion to the cell  surface, con"rming the results of Korb et al. (1997). The concentration of CO in the surface waters at OSP changes seasonally due to  the temperature e!ect on gas solubility (Wong and Chan, 1991). Thus, the increase in summer temperature would lead to a decrease in [CO ] , which should lead to   isotopic enrichment in the algal biomass if di!usional transport of the gas to the algal cells is the critical control on carbon acquisition (Riebesell et al., 1993; Rau et al., 1996,1997). This change is the reverse of the trend observed, suggesting that CO  concentration or availability is not a primary factor a!ecting the isotopic signals, or alternatively that a carbon concentrating mechanism is being used by the algae (Fielding et al., 1998). In addition, the temperature e!ect on the isotopic fractionation by phytoplankton (#0.3 3C\) would produce an additional increase, making the discrepancy larger.

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Using laboratory cultures, Hinga et al. (1994) reported an increase in carbon isotopic fractionation by S. costatum of about 9 over a pH increase from 7.5 to 8.3 (at a constant [CO ]). This suggests that the ionic balance of the cell a!ects carbon   uptake or "xation. A possible mechanism for this e!ect involves the transport of CO  and HCO\ across the cell membrane while the cell endeavours to maintain a constant  internal pH under variable external conditions. As Hinga et al. (1994) pointed out, the pH e!ect will be in the opposite direction to the [CO (aq)] e!ect, especially at high  pH and low [CO ], where the latter would be greater than the former. The relative   importance of CO vs. HCO\ uptake by marine phytoplankton is a matter of debate   (Riebesell et al., 1993; Goericke and Fry, 1994a; Thompson and Calvert, 1994; Laws et al., 1995; Korb et al., 1997; Tortell et al., 1997), and a resolution of the e!ects of di!erent carbon substrates on the resultant carbon isotopic composition of marine phytoplankton awaits further research. Seasonal changes in irradiance are large at the latitude of OSP, and this also could lead to changes in the isotopic composition of phytoplankton over the annual cycle. Thompson and Calvert (1994,1995) showed from laboratory culture experiments that a coastal diatom, Thalassiosira pseudonana, and an oceanic coccolithophorid, Emiliania huxleyi, that was isolated from OSP fractionate the carbon isotopes to a greater extent at higher irradiance, presumably because of the larger energy availability when light is more abundant. A trend of increasing isotope depletion during the summer therefore should be expected if this e!ect is manifest in natural phytoplankton populations, consistent with the trends observed at OSP. 4.4. Biological factors Physiological and biochemical factors that could in#uence carbon isotopic fractionation during phytoplanktonic photosynthesis have been extensively investigated, as summarized by Thompson and Calvert (1994) and Bidigare et al. (1997). These factors include the biochemical make-up (speci"cally the lipid content) of the cells, the cell growth rate, and carbon "xation pathways, as well as the type of the organism (the so-called species e!ect). The "rst of these factors is probably not important at OSP because, even though marine lipids characteristically have signi"cantly lighter dC values (!26}!30, see Degens et al., 1968b; Sackett, 1991) than whole cells, suspended POM from the upper 1000 m at this site have low concentrations (5}10) of this biochemical class (McAllister et al., 1960). It has been proposed that a higher growth rate will result in lower isotopic fractionation in marine phytoplankton (Fry and Wainwright, 1991; Nakatsuka et al., 1992). This e!ect would cause an increase in the isotopic composition of POM during the summer increase in production at OSP (see Boyd and Harrison, 1999), the opposite of the trend observed. Di!erent species or groups of marine plankton are known to have di!erent carbon isotopic compositions (Wong and Sackett, 1978; Falkowski, 1991), and this factor could in#uence the annual cycle of dC if there were a change in the type or .-+ succession of plankton through the year. At OSP, direct examination of the plankton suggests that there are only small changes in phytoplankton species composition

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between winter and summer (Boyd and Harrison, 1999). However, the large increase in biosilica #uxes during the summer months (May}September in most years, see Wong et al. 1999) could be an indication of increased diatom production. On the other hand, Deibel et al. (in prep.) found that large copepods at OSP cannot regulate the abundance of large diatoms in the spring or summer, suggesting that the lack of grazing control could be responsible for the peaks in diatom #uxes during these seasons. The isotopic composition of di!erent size classes of POM from OSP (Table 2) shows that the "ne-fraction ((5 lm) of the suspended POM is signi"cantly lighter isotopically than the coarser fractions or the bulk suspended POM. The "nest fractions consist predominantly of nanophytoplankton, whereas diatoms and other larger-celled organisms are more abundant in the large size-fractions (Booth et al., 1993). It is unlikely that the change to lighter isotope ratios in the summer months is caused by the higher production of diatoms because these members of the phytoplankton have heavier (C-enriched) values than smaller-celled phytoplankton (Table 2; Fry and Wainwright, 1991). Hence, the change to lighter values by other members of the plankton community during the summer #ux maxima are probably even larger than observed because of the contribution of isotopically heavier diatomaceous organic matter to the traps. The lighter POM dC is therefore partly caused by the growth of nanophytoplankton with a lighter carbon isotopic composition and their gazing by micozooplankton. The relationship between isotope signals and biosilica #uxes is further complicated by the fact that silica can be contributed to the trap #uxes by both phyto- (diatoms and silico#agellates) and zooplankton (radiolaria). Hence, phytoplanktonic silica may settle directly or after being grazed by zooplankton, and radiolaria also may graze siliceous and non-siliceous phytoplankton and then settle into deep water. Takahashi et al. (1990) estimated that diatoms in fact contributed signi"cantly more carbon to traps at 3800 m (by factors of between 2 and 5) compared with radiolaria, and that silico#agellates were an insigni"cant carbon vector. Size fractionation of the sediment trap samples provides a means of investigating the importance of phytoplankton versus zooplankton processes on the isotopic signals in sedimenting POM at OSP. During spring and summer 1988 the large size ('1 mm) component was almost unchanged, lying in the range 5}15 of the total (Fig. 11A). The small-size ((63 lm) component, however, decreased through the summer from 70 to 20%, and the medium-size (63}1000 lm) component increased concomitantly from 20 to 70% of the total, re#ecting the repackaging of small particles into larger ones. In May}June, most (70%) of the sedimenting material was composed of (63 lm particles (small size), whereas in August}September, the material was composed predominantly of 63}1000 lm particles (medium size), re#ecting the growth or succession of zooplankton during this period (Goldblatt et al., 1999). The dC of particles changed in concert with their sizes from spring to autumn (Fig. 11B). The dC values of the large particles are 0.5}1.0 higher than those of medium and small particles, suggesting that these large particles were derived from higher-level animals or from the remains of zooplankton. The dC values of the total settling POM at Station P are generally similar to those of the medium-sized particles, suggesting that most of material fell in this size range. The dC of the three size

2818

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Fig. 11. (A) Relative abundances of large ((1 mm), medium (63}1000 lm) and small ((63 lm) sedimenting particles collected at 3800 m at OSP in spring and summer, 1988. (B) dC of total and size.-+ fractionated samples shown in (A).

fractions and the total POM increased simultaneously in the spring and summer of 1988, re#ecting the seasonal succession of the phytoplankton and the superimposed fractionation of the isotopes by zooplankton processes. Therefore, there are two processes that a!ect the dC of sedimenting POM at OSP from spring to autumn, one being controlled by a change in temperature, irradiance, [CO (aq)] and/or  phytoplankton species succession, and one being linked to zooplankton processing of the material. An increase in temperature and growth rate from spring to autumn would lead to an increase in dC (Degens et al., 1968a,b; Wong and Sackett, 1978), as would the recycling of the organic matter by zooplankton feeding, whereas the spring increase in irradiance would cause a decrease in dC. Thus, the variations in the annual cycle of dC from year to year are caused by changes in the relative importance of these factors. Simultaneous measurements of these variables, at the same resolution of the trap time-series, will be required to test this conclusion. Modi"cation of oceanic POM by zooplankton has been discussed by many authors (Lee et al., 1988; Longhurst and Harrison, 1989; Wefer, 1989; Banse, 1990). Of interest

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here is the possibility that a change in trophic transfer among the plankton community at OSP over the annual cycle contributes to the variation of sedimenting POM dC. This could be important in view of the roughly 1 change per trophic level observed by Fry and Sherr (1988). Miller et al. (1984) and Goldblatt et al. (1999) found that calanoid copepods are dominant species of the mesozooplankton at OSP and they are known to have a distinct annual life cycle, as described earlier in this paper. Of relevance here is the fact that CV copepodites possibly play an important role in the transformation of POM by shortening the food chain in the upper layer in the spring period, although they are of course grazed by other mesozooplankton at this time. Pigment analysis of short-term #oating trap samples at OSP showed that zooplankton faeces accounted for roughly 50% of the total chloropigments (Thibault et al., 1999), suggesting that zooplankton are responsible for a signi"cant fraction of the vertical #ux of pigmented organic matter. The seasonal changes in the zooplankton assemblage and the change in food sources for the di!erent planktonic groups suggest that the food web at OSP changes over the annual cycle. The ecosystem possibly oscillates between a microbial web in winter, a stable state wherein autotrophic pico- and nanoplankton grow mainly on ammonium recycled by microzooplankton (ciliates, protozoa and #agellates), and a multivorous web (Legendre and Rassoulzadegan, 1995) in spring}summer, another stable state characterized by herbivorous as well as microbial grazing. In a multivorous web, the food chain is shortened by the direct grazing of early copepodites on nanophytoplankton and of adult copepods on aggregates containing nanophytoplankton (Dagg, 1993), and there will consequently be a greater loss of particulate matter to sinking. 4.5. Nitrogen isotope variations The annual variation in the #ux of material to deep water at OSP is correlated with that of surface nitrate drawdown, with a maximum in summer and a minimum in winter (Wong et al., 1999). Comparisons between long-term variations (1982}1990) of sedimenting POM dN and PON #uxes at 3800 m show (Fig. 7), however, that, as in the case of the carbon isotopes, the isotopic composition of nitrogen in sedimenting particles at OSP is related only in a general way to the variations in particle and constituent #uxes over the annual cycle. dN is generally higher in the winter and lower in the summer, some years showing (Figs. 8 and 9) a reasonably good correspondence between increasing PON and biosilica #ux and decreasing dN. In other years, there is a much lower degree of correlation between these variables. Noteworthy is the decrease in dN before increases in #uxes in some years, and the fact that the large #ux maxima in August}September 1983 and 1988 are marked by a very small change in dN. Thus, although there appears to be a general relationship between PON and biosilica #uxes and dN, this relationship is only signi"cant in some of the years. Previous work on particulate #uxes in the ocean has suggested that an increase in relative nitrate utilization causes an increase in sedimenting POM dN values because phytoplankton dN increases with a decrease in surface [NO\] (Altabet 

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et al., 1991). At "rst sight, results from OSP are not consistent with this pattern, since the decrease in surface [NO\], and hence the increase in nitrate drawdown, in spring  and summer produces lighter dN . This is probably related to the fact that surface .-+ macro-nutrient levels decrease to near-zero values in the Atlantic, where the pattern described by Altabet et al. (1991) was observed, whereas they decrease in the summer by only 50% from very high winter values in the NE Paci"c. The critical questions concerning the control of the annual change in dN are then: what sets the winter .-+ isotope ratios, and what causes the isotopic depletion in the summer? The isotopic fractionation from nitrate to phytoplankton can be simply estimated from the di!erence between the isotopic values of simultaneously collected phytoplankton or suspended POM and nitrate. This value is approximately 4 for diatoms and 4.2. for suspended POM (SPOM) (Wu et al., 1997). These values, derived from "eld data, are very similar to those determined for Thalassiosira pseudonana in laboratory culture by Waser et al. (1998a). There appears to be a signi"cantly lower fractionation for nano#agellates compared with diatoms in culture (Montoya and McCarthy, 1995). The dN values in the planktonic ecosystem at OSP are generally consistent with their trophic positions: zooplankton (ca. 6.2), diatoms (ca. 3.7), nanoplankton (ca. 2.2) and nitrate (ca. 7.7). The systematically lower dN values of these members of the ecosystem at OSP compared with those in the coastal region of the NE Paci"c (Wu, 1997) are interpreted to re#ect the fact that the nitrate utilization rate is lower and the recycling rate is higher in the oceanic regime (Varela and Harrison, 1999). Wu et al. (1997) found that the maximum di!erence in dN among zooplankton groups along Line P in spring and autumn is 3.7, which they took as the maximum value for isotope trophic fractionation from a prey mesozooplankton to its predator (assuming one trophic level transfer in mesozooplankton, a reasonable assumption based on relative body sizes and animal densities). This value would be consistent with the suggestion that the isotopic fractionation from mesozooplankton prey to predator is larger than that from phytoplankton to herbivorous zooplankton, which was observed in coastal waters where diatoms are dominant and the heavy isotopic enrichment from phytoplankton to herbivorous zooplankton was 2.17$0.36 (1p, n"6) (Wu et al., 1997). This value is close to the trophic isotopic enrichment value (2.4) for shrimp in an aquaculture pool reported by Parker et al. (1988) and lies in the range of 1.3}5.3 recommended by Minagawa and Wada (1984). Information on this problem is limited, since we can only determine trophic positions at single locations rather than over large areas. Our results (Table 5) suggest that most of the mesozooplankton are probably omnivorous, especially in the open ocean where nanophytoplankton are abundant and ammonium utilization is dominant, because the trophic enrichment of N is signi"cantly lower than 3.4, an average value widely accepted as indicating a single trophic transfer of the N isotopes. At OSP, 70% of the biomass is composed of very small phytoplankton ((5 lm), which are mainly grazed during the spring and summer by microzooplankton (Miller, 1993). The microzooplankton are then grazed by mesozooplankton. On the other hand, Dagg (1993a) analyzed copepod gut contents from OSP using a #uorescence technique and argued that copepods could

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directly graze nanophytoplankton, probably via aggregates. Wu et al. (1997) estimated that ca. 80% of the nanophytoplankton were probably grazed by microzooplankton and ca. 20% were grazed directly by copepods at OSP in May 1993. 4.6. Relationship between changes in dC and dN The isotopic fractionation due to biochemical processes during formation of sedimenting POM is di!erent for carbon and nitrogen (Table 6). Therefore, comparison of the changes in the two isotopic systems can potentially provide useful information on such biogeochemical processes. Annual variations of dC and dN of sedimenting POM collected at 200 m at Station P from 1989 to 1990 (Figs. 1 and 6) show that the heaviest isotopic values occur in winter and the lightest values occur in summer. However, the changes are not exactly in phase; dC of sedimenting POM increased from November 1989 to a peak in January 1990, decreased from January to June, 1990 and then increased from June to December, 1990; dN decreased from November to January, increased to a maximum in February and then decreased to August. The eight-year time-series of dC and dN of sedimenting POM collected from 1982 to 1990 (Figs. 3 and 7) shows that this pattern is consistent from year to year. Evidently, some key processes and factors that regulate the incorporation and fractionation of the carbon and nitrogen isotopes in sedimenting POM are di!erent during the annual cycle and, possibly, internally. It might therefore be better to look at their relationship on a seasonal basis rather than over the 8-year period of observation, since the annual cycles of carbon and nitrogen utilization are not totally similar. Based on the annual cycles of temperature, macro-nutrients, primary production and zooplankton life cycles, we can divide the annual cycle at OSP into three periods, namely winter to spring, spring to autumn and autumn to winter. Two of these periods (winter to spring and autumn to winter) are especially important because

Table 6 Responses of dC and dN to some processes and factors from photosynthesis in the euphotic zone to settlement on sea #oor Process or factor

dC

dN

Temperature increase Surface substrates Isotopic fractionation in photosynthesis Di!erent phytoplankton groups Trophic transfer

Increase dC (!7)(dC \(1) &!!ca. !20 (lighter)

Increase dN\ (7.7); dN > (?) ,,& ca. !5 (lighter)

Maximum di!erence ca 3 ca. 1 per trophic level with large uncertainty

Sedimenting and suspended POM Decomposition of sinking POM

dC (dC     Increase with depth

Maximum di!erence ca. 1 2.2 from phytoplankton to zooplankton and 3.7 in zooplankton dN (dN     Flux-dependence

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Fig. 12. Relationships between *dC and *dN of sedimenting POM at 3800 m at OSP in (A) the spring (March}May), (B) the summer (June}September) and (C) the autumn/winter (October}January) from 1982 to 1990.

environmental conditions and biological processes are changing markedly. For these comparisons, di!erences of dC and dN between two adjacent samples (*dC and *dN, respectively, that is the di!erences between a given value and the value two weeks earlier) are compared. The results show (Fig. 12A) that there is a positive correlation between *dC and *dN of sedimenting POM from March to May, and a negative correlation from November to January over the period 1982}1990. In the early spring [CO (aq)] and [NO\] reach their highest values because primary and   secondary production are lowest in winter, the temperature is still low, and mixing homogenizes the hydrographic properties of the surface mixed layer. Hence, the phytoplankton growing during the early part of the spring will be isotopically light. In the meantime, the growth of CV during this season shortens the food chain, for they may graze the nanophytoplankton during this period, thereby producing sedimenting POM with lighter C and N isotopic compositions. This conclusion may be complicated by the fact that both isotope enrichment and depletion of faecal material relative to food have been described in di!erent zooplankton groups (summarized in Montoya, 1994). Other processes tend to dampen these changes. For example, dC and dN increase as temperature increases (Goering et al., 1990), and .-+ .-+ hence there will be a positive change in dC and dN in spring. There are no major changes in phytoplankton composition from winter to spring (Boyd et al., 1995), so

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there would be no e!ect of this factor on the variations in isotopic compositions at this time of year. Hence, the decreases of dC and dN of sedimenting POM in spring are mainly regulated by the high concentrations of inorganic macro-nutrients, rapid nanophytoplankton and copepodite growth, and the shortening of the food chain, this resulting in a signi"cant positive correlation between the two isotope systems in sedimenting POM. During summer and early autumn (July and August), a larger number of factors and processes are involved that could a!ect the carbon and nitrogen isotopic compositions of POM. For example, [CO ] reaches its lowest level in August and Septem  ber (Wong and Chan, 1991), whereas [NO\] is still at a relatively high level. These  two conditions would lead to an increase of phytoplankton dC (Rau et al., 1989) and would maintain dN values similar to those in spring (Wu et al., 1997). On the other hand, [NO\] decreases steadily through the summer season due to increasing  strati"cation during which there is a relative higher degree of nitrate utilization (Varela and Harrison, 1999), causing an enrichment in dN. Also, based on the changes in the #ux of biosilica in the traps, which generally peaks between May and September (Wong et al., 1999), diatom production is high at this time (Takahashi et al., 1989) and this would lead to a heavier dC in the euphotic zone. Concur.-+ rently, the development of diatom-grazing mesozooplankton may follow the growth of diatoms, and this would accentuate the enrichment of the heavier isotope in POM. These variations may be responsible for the lack of signi"cant correlation between *dC and *dN during this period (Fig. 12B). The cause of the negative correlation between *dC and *dN of the settling POM from autumn to early winter (Fig. 12C) is not clearly understood. Temperature and trophic transfer are not important e!ects because these two factors produce a positive correlation between changes in dC and dN. One possibility is a control by the supply of new nitrate, since [NO\] increases in this period due to increased  vertical mixing (Parsons and LeBrasseur, 1968; Anderson et al., 1969), and this would cause the isotopic composition of the source nitrate to fall because deep nitrate is isotopically much lighter than that in the surface layers (Fig. 10B). On the other hand, if the growth of diatoms increases due increased radiation and/or an increase in dissolved Fe concentrations (Martin, 1992), this will produce a heavier carbon isotopic signature (the isotopic di!erence between nanophytoplankton and diatoms is about 3) and, because the diatoms grow rapidly and settle without being signi"cantly grazed (Takahashi, 1986), a lighter nitrogen isotopic composition would result. The three exceptionally light dC peaks in the autumn/winters in 1982, 1985 .-+ and 1988 (Fig. 3) are not accompanied by similar large excursions in dN values (Fig. 7). The lowest values of sedimenting POM dC are probably coincident with the highest radiolarian #uxes in the autumn of 1982 and 1985 (Takahashi, 1987a,1989), but there was no exceptional biosilica #ux in the late of autumn of 1988 or early 1989. Low dC values can be produced by radiolarians because these microzooplankton graze nanophytoplankton, which have lower dC values (ca. !27), and they may sink rapidly without being grazed to a large extent. However, they would not change sedimenting POM dN values signi"cantly because the dN of suspended POM and nanophytoplankton at the surface are similar and the dN of faecal pellets of

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mesozooplankton are lower than those of animals and higher than those of their food, including nanoplankton and microzooplankton. This would result in faecal pellets having a similar nitrogen isotopic composition to the large fast-sedimenting siliceous microzooplankton. Therefore, production of radiolaria would not signi"cantly change the sedimenting POM dN. 4.7. Relationship between suspended and sedimenting POM It is well known that suspended and sedimenting POC/N decrease in absolute and relative amounts with depth in a water column. The mechanism for this phenomenon is not well understood. The behaviour of, and the interactions between, suspended and sedimenting POM are probably two of the most important factors involved. Honjo (1990) suspected that all suspended particles eventually settled out after aggregation into large particles and faecal pellets, most likely being transformed into di!erent sizes many times. His hypothesis is supported by the fact that nearly 100% of uraniumseries nuclides generated in the water column above a trap are found in the sediment trap (Bacon et al., 1985). However, recent measurements of the nitrogen isotopic composition of sedimenting and suspended POM (Altabet et al., 1991) show that these two particle types do not extensively interact in the open ocean as previously proposed. Observations at OSP add support to this conclusion. Most of the fast-sedimenting POM formed in the euphotic zone is consumed by biological activities below the euphotic zone, repackaging sedimenting POM, producing smaller organic-rich suspended POM, and releasing dissolved organic matter (DOM). The "ne-grained organic-rich suspended POM is more easily decomposed by free heterotrophic bacteria, producing dissolved organic as well as inorganic carbon and nitrogen and smaller slowly sedimenting or suspended particles. These suspended particles will have heavier and heavier carbon and nitrogen isotopic compositions due to the preferential release of the lighter isotopes of carbon and nitrogen in inorganic forms. Therefore, it can be hypothesized that the sedimenting POM from the euphotic zone is possibly the source of suspended POM in the water column, and fresh suspended POM is the source of dissolved nitrate and inorganic carbon in deeper water. Unaltered or less-altered rapidly sedimenting POM constitutes an independent microecosystem, that is recycled in deeper waters or settles intact on the sea-#oor. Thus, the sedimenting POM formed in the surface waters that escapes zooplankton destruction and bacterial attack preserves information on the surface environment, whereas the suspended particulate matter represents a long-term, highly processed average of the material delivered to deeper waters from the sea surface. This hypothesis is supported by two lines of evidence. First, at OSP dC and dN of suspended POM below the euphotic zone are both higher than those of sedimenting POM: the average suspended POM dC below 200 m at OSP is !23.62$ 0.26 (n"3) (Wu, 1997), while the annual instantaneous average of the sedimenting POM dC collected with sediment traps at 200 m is !24.61$0.61 (n"20) (Fig. 1B). Similarly, the average of the dN values of suspended POM below 100 m is 9.28$0.44 (n"3), while the instantaneous average of the dN values of sedimenting POM at 200 m and 1000 m are 3.99$1.12 (n"20) and 3.61$0.99

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(n"21), respectively (Fig. 6B). These results show that the dC and dN values of suspended POM are 1 and 5 higher than those of sedimenting POM below 200 m, respectively. Suspended and sedimenting POM most likely follow di!erent transformation pathways below this depth, thereby producing particles of di!erent isotopic compositions. This is because the lighter isotope is more easily released from newly produced suspended POM, which is composed of non-living detritus, than from sedimenting POM, which constitutes a microecosystem. Unfortunately, we have no information on the dN of suspended POM below 600 m to follow the di!erences between the two particle populations into deeper waters. Second, sedimenting POM dC increases with depth (Fig. 1B) while dN only increases (slightly) with depth in low-#ux periods and decreases with depth in high-#ux periods (Fig. 6B). Sinking POC and PON not only decrease in absolute masses with depth, but also decrease relative to the total #ux, suggesting that some components of the POC and PON are released during settling, or slow-sedimenting inorganic matter dilutes the organic contents of the sediment traps. Sinking POC decreases faster than sedimenting PON between 200 and 1000 m depth (Wong et al., 1999). Bacterial activities in sedimenting POM produce polysaccharides, which can act as a glue-like material that scavenges other sedimenting particles to produce larger sedimenting POM (Alldredge and Silver, 1988; Silver and Gowing, 1991). This process would recycle nitrogenous nutrients and deplete organic carbon in the particle microecosystem. The constant dN values of sedimenting POM with depth might then re#ect the lower dN of bacteria that compensates for the higher dN of the remaining residual POM at successive depths. Altabet et al. (1991) also suggested that the decrease in settling POM dN observed in the North Atlantic could be due to the release of proteins, in which nitrogen is isotopically heavy.

5. Conclusions The dC and dN of sedimenting particulate organic matter (POM) collected at 3800 m at OSP (503N, 1353W) had seasonal ranges of 3.3 and 7.5, respectively, over the period 1982}1990, with isotopically depleted values occurring mainly in summer and heavier values occurring in winter. The changes in isotope ratios do not appear to be closely related to the annual changes in particulate #uxes, and in some years the isotope ratios began to change before the summer increase in particle #uxes. Seasonal variations in surface temperature, irradiance, phytoplankton growth rate, species composition, [CO ] or carbon "xation pathways do not appear to be important    controls of the observed changes in dC ; the increases in temperature, irradiance .-+ and phytoplankton growth rate in the summer months should lead to enriched dC values rather than the observed isotopically light values in this season. .-+ Likewise, the summer increase in the growth of diatoms should produce isotopically heavy particles in view of the reported C-enrichment of this group, and this should be augmented by the decrease in [CO ] due to the summer increase in surface    temperature. Opposing these possible controls, the planktonic food chain becomes

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shorter in the spring/summer months, probably due to the migration of copepodites and their direct grazing on the newly produced phytoplankton, and this results in C enrichment relative to the winter months when the food chain is more complex. The relationship between sedimenting dN and the nutrients at OSP is com.-+ plicated by the fact that ammonium and urea are important phytoplankton substrates, and generally more so than nitrate. The change from isotopically heavy winter values to lighter summer values begins before the major drawdown of the surface nitrate, and the observed change is opposite to that observed in other ocean regimes, probably because nitrate never reaches limiting levels in this High Nutrient Low Chlorophyll regime. The change of phytoplankton composition from winter to summer also should lead to N-enrichment, the opposite of the trends observed. Finally, the changes in sedimenting dN at OSP do not appear to be related to .-+ phytoplankton growth rate. We conclude that the nitrogen isotopic signal in settling POM at OSP re#ects seasonal changes in food-web structure, the simpler (shorter) spring/summer plankton community causing a smaller isotopic fractionation from the nutrient substrate to sedimenting POM. Changes in sedimenting dC and dN (1989}90) between 200, 1000 and .-+ .-+ 3800 m depth at the same location shows a marked carbon isotope enrichment with depth, but very small changes in the nitrogen isotope composition of the same particles. Thus, C and N are processed via di!erent pathways during sedimentation. The large di!erences between sedimenting and suspended POM dC and dN values and below the euphotic zone suggest that the two types of POM do not interact in deep water, consistent with other observations.

Acknowledgements This study could not have been completed without the extensive assistance provided by the ship-board and laboratory personnel during OSP and Line P cruises of the Institute of Ocean Sciences and the Canadian JGOFS project. The authors are grateful to Bente Nielsen of the Department of Earth and Ocean Sciences, University of British Columbia for the stable isotope determinations. We thank Philip Boyd for very helpful comments and suggestions and three anonymous reviewers for their reviews. This research was supported by The Centre for Ocean Climate Chemistry of the Institute of Ocean Sciences of the Canadian Department of Fisheries and Oceans and the Natural Sciences and Engineering Research Council of Canada. This is a contribution to the Canadian JGOFS research program.

References Alldredge, A.L., Silver, M.W., 1988. Characteristics, dynamics and signi"cance of marine snow. Progress in Oceanography 20, 41}82.

J. Wu et al. / Deep-Sea Research II 46 (1999) 2793}2832

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Altabet, M.A., 1988. Variations in nitrogen isotopic composition between sinking and suspended particles: implications for nitrogen cycling and particle transformation in the open ocean. Deep-Sea Research 35, 535}554. Altabet, M.A., Deuser, W.G., 1985. Seasonal variations in natural abundance of N in particles sinking to the deep Sargasso Sea. Nature 315, 218}219. Altabet, M.A., Deuser, W.G., Honjo, S., Steinen, C., 1991. Seasonal and depth-related changes in the source of sinking particles in the North Atlantic. Nature 354, 136}139. Altabet, M.A., Small, L.F., 1990. Nitrogen isotopic ratios in fecal pellets produced by marine zooplankton. Geochimica et Cosmochimica Acta 54, 155}163. Anderson, G.C., Parsons, T.R., Stephens, K., 1969. Nitrate distribution in the subarctic Northeast paci"c Ocean. Deep-Sea Research 16, 329}334. Bacon, M.P., Huh, C.-A., Fleer, A.P., Deuser, W.G., 1985. Seasonality in the #ux of natural radionuclides and plutonium in the deep Sargasso Sea. Deep-Sea Research 32, 273}286. Banse, K., 1990. New views on the degradation and disposition of organic particles as collected by sediment traps. Deep-Sea Research 37, 1177}1195. Bidigare, R.R., Fluegee, A., Freeman, K.H., Hanson, K.L., Hayes, J.M., Hollander, D., Jasper, J.P., King, L.L., Laws, E.A., Milder, J., Millero, F.J., Pancost, R., Popp, B.N., Steinberg, P.A., Wakeham, S.G., 1997. Consistent fractionation of C in nature and in the laboratory: Growth-rate e!ects in some haptophyte algae. Global Biogeochemical Cycles 11, 279}292. Booth, B.C., 1988. Size classes and major taxonomic groups of phytoplankton at two locations in the subarctic Paci"c Ocean in May and August, 1984. Marine Biology 97, 275}286. Booth, B.C., Lewin, J., Postel, J.R., 1993. Temporal variation in the structure of autotrophic and heterotrophic communities in the Subarctic Paci"c. Progress in Oceanography 32, 57}99. Boyd, P.W., Harrison, P.J., 1999. Phytoplankton dynamics in the NE subarctic Paci"c. Deep-Sea Research II 46, 2405}2432. Boyd, P.W., Muggli, D.L., Varela, D.E., Goldblatt, R.H., Chretien, R., Orians, K.J., Harrison, P.J., 1996. In vitro iron enrichment experiments in the NE subarctic Paci"c. Marine Ecology Progress Series 136, 179}193. Boyd, P.W., Strom, S., Whitney, F.A., Doherty, S., Wen, M.E., Harrison, P.J., Wong, C.S., Varela, D.E., 1995. The NE subarctic Paci"c in winter: I. Biological standing stocks. Marine Ecology Progress Series 128, 11}24. Brodeur, R.D., Frost, B.W., Hare, S.R., Francis, R.C., Ingraham, W.J., 1996. Interannual variations in zooplankton biomass in the Gulf of Alaska, and covariation with California Current zooplankton biomass. California Cooperative Oceanic Fisheries Investigation Report 37, 80}99. Checkley Jr., D.M., Miller, C.A., 1989. Nitrogen isotope fractionation by oceanic zooplankton. Deep-Sea Research 36, 1449}1456. Dagg, M., 1993. Grazing by the copepod community does not control phytoplankton production in the Subarctic Paci"c Ocean. Progress in Oceanography 32, 163}183. Degens, E.T., Behrendt, M., Gotthard, B., Reppmann, E., 1968a. Metabolic fractionation of carbon isotopes in marine plankton. II. Data on samples collected o! the coast of Peru and Ecuador. Deep-Sea Research 15, 11}20. Degens, E.T., Guillard, R.R.L., Sackett, W.M., Hellbust, J.A., 1968b. Metabolic fractionation of carbon isotopes in marine plankton. I. Temperature and respiration experiments. Deep-Sea Research 15, 1}9. Dru!el, E.R.M., Honjo, S., Gri$n, S., Wong, C.S., 1986. Radiocarbon in particulate matter from the eastern sub-Arctic Paci"c Ocean: evidence of a source of terrestrial carbon to the deep sea. Radiocarbon 28, 397}407. Durako, M.J., Hall, M.O., 1992. E!ects of light on the stable carbon isotope composition of the seagrass Thalassia testudinum. Marine Ecology Progress Series 86, 99}101. Emery, W.E., Hamilton, K., 1985. Atmospheric forcing of interannual variability in the northeast Paci"c Ocean: connections with El Nino. Journal of Geophysical Research 90, 857}868. Eppley, R.W., Peterson, B.J., 1979. Particulate organic matter #ux and planktonic new production in the deep ocean. Nature 282, 677}680.

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J. Wu et al. / Deep-Sea Research II 46 (1999) 2793}2832

Falkowski, P.G., 1991. Species variability in the fractionation of C and C by marine phytoplankton. Journal of Plankton Research 13, 21}28. Fielding, A. S., Crawford, D., Turpin, D.H., Harrison, P.J., Calvert, S.E., Guy, R.D., 1998. In#uence of the carbon concentrating mechanism on carbon stable isotope fractionation by a marine diatom. Canadian Journal of Botany, in press. Fontugne, M.R., Duplessy, J.-C., 1981. Organic carbon isotopic fractionation by marine plankton in the temperature range !1 to 313C. Oceanologica Acta 4, 85}90. Franc7 ois, R., Altabet, M.A., Goericke, R., McCorkle, D.C., Brunet, C., Poisson, A., 1993a. Changes in the dC of surface water particulate organic matter across the subtropical convergence in the S.W. Indian Ocean. Global Biogeochemical Cycles 7, 627}644. Franc7 ois, R., Bacon, M.P., Altabet, M.A., Labeyrie, L.D., 1993b. Glacial/interglacial changes in sediment rain rate in the SW Indian sector of subantarctic waters as recorded by 230Th, 231Pa, U, and *15N. Paleoceanography 8, 611}630. Fry, B., 1988. Food web structure on Georges Bank from stable C, N and S isotopic compositions. Limnology and Oceanography 33, 1182}1190. Fry, B., Sherr, E.B., 1988. dC measurements as indicators of carbon #ow in marine and freshwater ecosystems. In: Rundel, P.W., Ehleringer, J.R., Nagy, K.A. (Eds.), Stable Isotopes in Ecological Research. Springer, Berlin. Fry, B., Wainwright, S.C., 1991. Diatom sources of 13C-rich carbon in marine food webs. Marine Ecology Progress Series 76, 149}157. Goericke, R., Fry, B., 1994a. Physiology of isotope fractionation in algae and cyanobacteria, In: Lajtha, K., Michener, B. (Eds.), Stable Isotopes in Ecology. Blackwell Scienti"c, Boston, MA, pp. 199}233. Goericke, R., Fry, B., 1994b. Variations of marine plankton dC with latitude, temperature and dissolved CO in the world ocean. Global Biogeochemical Cycles 8, 85}90.  Goering, J., Alexander, V., Haubenstock, N., 1990. Seasonal variability of stable carbon and nitrogen isotope ratios of organisms in a north Paci"c Bay. Estuarine Coastal and Shelf Science 30, 239}260. Goldblatt, R.H., Mackas, D.L., Lewis, A.G., 1999, Mesozooplankton community characteristics in the NE subarctic Paci"c. Deep-Sea Research II 46, 2619}2644. Hinga, K.R., Arthur, M.A., Pilson, M.E.Q., Whitaker, D., 1994. Carbon isotope fractionation by marine phytoplankton in culture: the e!ects of CO2 concentration, pH, temperature and species. Global Biogeochemical Cycles 8, 91}102. Honjo, S., 1990. Ocean particles and #uxes of material to the interior of the deep ocean; The azoic theory 120 years later. In: Ittekkot, V., Kempe, S., Michaelis, W., Spitzy, A. (Eds.), Facets of Modern Biogeochemistry. Springer, Berlin, pp. 62}73. Korb, R.E., Saville, P.J., Johnston, A.M., Raven, J.A., 1997. Sources of inorganic carbon for photosynthesis by three species of marine diatom. Journal of Phycology 33, 433}440. Laws, E.A., Popp, B.N., Bidigare, R.R., Kennicutt, M.C., Macko, S.A., 1995. Dependence of phytoplankton carbon isotopic composition on growth rate and [CO2]aq: theoretical considerations and experimental results. Geochimica et Cosmochimica Acta 59, 1131}1138. Lee, C., Wakeham, S.G., Hedges, J.I., 1988. The measurement of oceanic particle #ux } are `swimmersa a problem? Oceanography 1, 34}36. Legendre, L., Rassoulzadegan, F., 1995. Plankton and nutrient dynamics in marine waters. Ophelia 41, 153}172. Liu, K.-K., Kaplan, I.R., 1989. The eastern tropical Paci"c as a source of N-enriched nitrate in seawater o! southern California. Limnology and Oceanography 34, 820}830. Longhurst, A.R., Harrison, W.G., 1989. The biological pump: pro"les of plankton production and consumption in the upper ocean. Progress in Oceanography 22, 47}123. Mackas, D.L., Boher, R., 1976. Fluorescence analysis of zooplankton gut contents and an investigation of diel feeding patterns. Journal of Experimental Marine Biology and Ecology 25, 77}85. Martin, J.H., 1992. Iron as a limiting factor in oceanic productivity. In: Falkowski, P.G., Woodhead, A.D. (Eds.), Primary Productivity and Biogeochemical Cycles in the Sea. Plenum Press, New York, pp. 123}137.

J. Wu et al. / Deep-Sea Research II 46 (1999) 2793}2832

2829

Martin, J.H., Fitzwater, S.E., 1988. Iron de"ciency limits phytoplankton growth in the north-east Paci"c subarctic. Nature 331, 341}343. McAllister, C.D., Parsons, T.R., Strickland, J.D.H., 1960. Primary production at Ocean Station P in the northeast Paci"c Ocean. Journal Conseil International pour l''Exploration de la Mer 25, 240}259. Miller, C.B., 1993. Pelagic production processes in the Subarctic Paci"c. Progress in Oceanography 32, 1}15. Miller, C.B., Clemons, M., 1988. Revised life history analysis for large grazing copepods in the subarctic Paci"c Ocean. Progress in Oceanography 20, 293}313. Miller, C.B., Frost, B.W., Batchelder, H.P., Clemons, M.J., Conway, R.E., 1984. Life history of large, grazing copepods in a Subarctic Ocean Gyre: Neocalanus plumchrus, Neocalanus cristatus, and Eucalanus bungii in the Northeast Paci"c. Progress in Oceanography 13, 201}243. Miller, C.B., Frost, B.W., Wheeler, P.A., Landry, M.R., Welschmeyer, N., Powell, T.M., 1991. Ecological dynamics in the subarctic Paci"c, a possibly iron-limited system. Limnology and Oceanography 36, 1600}1615. Miller, C.B., the SUPER Group, 1988. Lower trophic level dynamics in the oceanic subarctic Paci"c Ocean. Bulletin of the Ocean Research Institute, University of Tokyo 26, 1}26. Minagawa, M., Wada, E., 1984. Stepwise enrichment of N along food chains: further evidence and the relation between dN and animal age. Geochimica et Cosmochimica Acta 48, 1135}1140. Montoya, J.P., 1994. Nitrogen isotope fractionation in the modern ocean: implications for the sedimentary record. In: Zahn, R., Kaminski, M., Labeyrie, L.D., Pedersen, T.F. (Eds.), Carbon Cycling in the Glacial Ocean: Constraints on the Ocean's Role in Global Change. Springer, Heidelberg, pp. 259}279. Montoya, J.P., McCarthy, J.J., 1995. Isotopic fractionation during nitrate uptake by phytoplankton grown in continuous culture. Journal of Plankton Research 17, 439}464. Morales, C.E., Bautista, B., Harris, R.P., 1990. Estimates of ingestion in copepod assemblages: gut #uorescence in relation to body size. In: Barnes, M., Gibson, R.N. (Eds.), Trophic Relationships in the Marine Environment. Aberdeen University Press, Aberdeen, pp. 565}577. Mullin, M.M., Rau, G.H., Eppley, R.W., 1984. Stable nitrogen isotopes in zooplankton: some geographic and temporal variations in the North Paci"c. Limnology and Oceanography 29, 1267}1273. Nakatsuka, T., Handa, N., 1997. Reconstruction of seasonal variation in nutrient budget of a surface mixed layer using dN of sinking particle collected by a time-series sediment trap system. Journal of Oceanography 53, 105}116. Nakatsuka, T., Handa, N., Imaizumi, S., 1995. Spatial and temporal variation of dN in sinking particles in deep waters: its implication for the origin and transport of particulate organic matter. In: Sakai, H., Nozaki, Y. (Eds.), Biogeochemical Processes and Ocean Flux in the Western Paci"c. Terra Scienti"c Publishing Company (TERRAPUB), Tokyo, pp. 355}374. Nakatsuka, T., Handa, N., Wada, E., Wong, C.-S., 1992. The dynamic changes of stable isotope ratios of carbon and nitrogen in suspended and particulate organic matter during a phytoplankton bloom. Journal of Marine Research 50, 267}296. Pancost, R.D., Freeman, K.H., Wakeham, S.G., Robertson, C.Y., 1997. Controls on carbon isotope fractionation by diatoms in the Peru upwelling region. Geochimica et Cosmochimica Acta 61, 4983}4991. Parker, P.L., Anderson, R.K., Lawrence, A., 1988. A dC and dN tracers study of nutrition in aquaculture: Penaeus vannamei in a pond growout system. In: Rundel, P.W., Ehleringer, J.R., Nagy, K.A. (Eds.), Stable Isotope inEcological Research. Springer, Berlin. Parsons, T.R., Lalli, C.M., 1988. Comparative oceanic ecology of the plankton communities of the Subarctic Atlantic and Paci"c Ocean. Oceanography and Marine Biology Annual Review 26, 317}359. Parsons, T.R., LeBrasseur, R.J., 1968. A discussion of some critical indices of primary and secondary production for large-scale ocean surveys. California Marine Resources Commission, CalCOFI 12, 54}63. Parsons, T.R., LeBrasseur, R.J., 1970. The availability of food to di!erent trophic levels in the marine food chain. In: Steele, J.H. (Ed.), The Marine Food Chain. University of California Press, Berkeley, pp. 325}343.

2830

J. Wu et al. / Deep-Sea Research II 46 (1999) 2793}2832

Parsons, T.R., LeBrasseur, R.J., Fulton, J.D., 1967. Some observations on the dependence of zooplankton grazing on the cell size and concentration of phytoplankton blooms. Journal of the Oceanographic Society of Japan 23, 10}17. Peterson, B.J., Fry, B., 1987. Stable isotopes in ecosystem studies. Annual Review of Ecology and Systematics 18, 293}320. Rau, G.H., Froelich, P.N., Takahashi, T., Des Marais, D.J., 1991. Does sedimentary organic dC record variations in quaternary ocean [CO (aq)]? Paleoceanography 6, 335}347.  Rau, G.H., Riebesell, U., Wolf-Gladrow, 1997. CO -dependent photosynthetic C fractionation in the  ocean: a model versus measurements. Global Biogeochemical Cycles 11, 267}278. Rau, G.H., Riebesell, U., Wolf-Gladrow, D., 1996. A model of photosynthetic C fractionation by marine phytoplankton based on di!usive molecular CO uptake. Marine Ecology Progress Series 133, 275}285.  Rau, G.H., Takahashi, T., Des Marais, D.J., Repeta, D.J., Martin, J.H., 1992. The relationship between dC of organic matter and [CO (aq)] in ocean surface water: data from a JGOFS site in the northeast  Atlantic Ocean and a models. Geochimica et Cosmochimica Acta 56, 1413}1419. Rau, G.H., Takahashi, T., Marais, D.J.d., 1989. Latitudinal variations in plankton dC : implications for CO and productivity in past oceans. Nature 341, 516}518.  Rau, G.H., Teyssie, J.-L., Rassoulzadegan, F., Fowler, S.W., 1990. C/C and N/N variations among size-fractionated marine particles: implications for their origin and trophic relationships. Marine Ecology Progress Series 59, 33}38. Riebesell, U., Wolf-Gladrow, D.A., Smetacek, V., 1993. Carbon dioxide limitation of marine phytoplankton growth rates. Nature 361, 249}251. Ryther, J.H., 1969. Photosynthesis and "sh production in the sea. Science 166, 72}76. Sackett, W.M., 1991. A history of the dC composition of oceanic plankton. Marine Chemistry 34, 153}156. Saino, T., Hattori, A., 1987. Geographical variation of the water column distribution of suspended particulate organic nitrogen and its N natural abundance in the Paci"c and its marginal seas. Deep-Sea Research 34, 807}827. Sigman, D., Altabet, M., Michener, R., McCorckle, D., Fry, B., Holmes, R.M., 1997. Natural abundancelevel measurement of the nitrogen isotopic composition of oceanic nitrate: an adaptation of the ammonia di!usion method. Marine Chemistry 57, 227}242. Silver, M.W., Gowing, A.A., 1991. The particle #ux: origins and biological components. Progress in Oceanography 26, 75}113. Tabata, S., 1961. Temporal changes of salinity, temperature, and dissolved oxygen of the water at Station P in the northeast Paci"c Ocean, and some of their determining factors. Journal of the Fisheries Research Board of Canada 18, 1073}1124. Tabata, S., 1965. Variability of oceanographic conditions at Ocean Station `Pa in the Northeast Paci"c Ocean. Transactions of the Royal Society of Canada 3, 367}418. Tabata, S., 1989. Trends and long-term variability of ocean properties at Ocean Station P in the northeast Paci"c Ocean, In: Peterson, D.H. (Ed.), Aspects of Climate Variability in the Paci"c and the Western Americas, American Geophysical Union Geophysical Monograph 55, Washington, DC, pp. 113}132. Tabata, S., Peart, J.L., 1985. Statistics of oceanographic data based on hydrographic/STD casts made at Ocean Station P during August 1956 through June 1981. Canadian Data Report of Hydrography and Ocean Sciences, Canadian Data Report of Hydrography and Ocean Sciences, Vol. 31. Takahashi, K., 1986. Seasonal #uxes of pelagic diatoms in the subarctic Paci"c, 1982}1983. Deep-Sea Research 33, 1225}1251. Takahashi, K., 1987a. Radiolarian #ux and seasonality: climatic and El Nino response in the subarctic Paci"c. Global Biogeochemical, Cycles 1, 213}231. Takahashi, K., 1987b. Response of Subarctic Paci"c diatom #uxes to the 1982}1983 El Nino disturbance. Journal of Geophysical Research 92, 14387}14392. Takahashi, K., 1989. Silico#agellates as productivity indicators: evidence from long temporal and spatial #ux variability responding to hydrography in the northeastern Paci"c. Global Biogeochemical Cycles 3, 43}61.

J. Wu et al. / Deep-Sea Research II 46 (1999) 2793}2832

2831

Takahashi, K., Billings, J.D., Morgan, J.K., 1990. Oceanic province: assessment from the time-series diatom #uxes in the northeastern Paci"c. Limnology and Oceanography 35, 154}165. Takahashi, K., Honjo, S., Tabata, S., 1989. Siliceous phytoplankton #ux: interannual variability and response to hydrographic changes in the northeastern Paci"c, In: Peterson, D.H. (Ed.), Aspects of Climate Variability in the Paci"c and the Western Americas, American Geophysical Union Geophysical Monograph 55, Washington, D.C., pp. 151}160. Thibault, D., Roy, S., Wong, C.S., Bishop, J.K., 1999. The downward #ux of biogenic material in the NE subarctic Paci"c: importance of algal sinking and mesozooplankton herbivory. Deep-Sea Research II 46, 2669}2697. Thompson, P.A., Calvert, S.E., 1994. Carbon isotope fractionation by a marine diatom: the in#uence of irradiance, daylength, pH, and nitrogen source. Limnology and Oceanography 39, 1835}1844. Thompson, P.A., Calvert, S.E., 1995. Carbon isotope fractionation by Emiliania huxleyi. Limnology and Oceanography 40, 673}679. Tortell, P.D., Reinfelder, J.R., Morel, F.M.M., 1997. Active uptake of bicarbonate by diatoms. Nature 390, 243}244. Tully, J.P., Barber, F.G., 1960. An estuarine analogy of the sub-arctic Paci"c Ocean. Journal of the Fisheries Research Board of Canada 17, 91}112. Varela, D.E., 1997. Nitrogenous nutrition of phytoplankton from the northeastern subarctic Paci"c Ocean: Unpub. Doctoral Thesis, University of British Columbia, 198 pp. Varela, D.E., Harrison, P.J., 1999. Seasonal variability in nitrogenous nutrition of phytoplankton assemblages in the northeastern subarctic Paci"c Ocean. Deep-Sea Research, in press. Voss, M., 1991. Raumliche und zeitliche Verteilung stabiler Isotope (dN, dC) in suspendierten und sedimentierten Partikeln im Nordlichen Nordatlantik: Unpub. Doctoral Thesis, Christian-AlbrechtsUniversitat zu Kiel, 102 pp. Voss, M., Altabet, M.A., Bodungen, V., 1996. dN in sedimenting particles as indicator of euphotic-zone processes. Deep-Sea Research 43, 33}47. Wada, E., Hattori, A., 1976. Natural abundance of N in particulate organic matter in the North Paci"c Ocean. Geochimica et Cosmochimica Acta 40, 249}251. Wada, E., Terazaki, M., Kabaya, Y., Nemoto, T., 1987. N and C abundances in the Antarctic Ocean with emphasis on the biogeochemical structure of the food web. Deep-Sea Research 34, 829}841. Waser, N.A.D., Turpin, D.H., Harrison, P.J., Nielsen, B., Calvert, S.E., 1998a. Nitrogen isotope fractionation during the uptake and assimilation of nitrate, nitrite, ammonium and urea by a marine diatom. Limnology and Oceanography 43, 215}224. Wefer, G., 1989. Particle #ux in the ocean: E!ects of episodic production. In: Berger, W.H., Smetacek, V.S., Wefer, G. (Eds.), Productivity of the Ocean: Present and Past. Wiley, New York, pp. 139}153. Welschmeyer, N.A., Strom, S., Goericke, R., Ditullio, G., Belvin, M., Petersen, M., 1993. Primary production in the Subarctic Paci"c Ocean } Project SUPER. Progress in Oceanography 32, 101}135. Wheeler, P.A., Kokkinakis, S.A., 1990. Ammonium recycling limits nitrate use in the oceanic subarctic Paci"c. Limnology and Oceanography 35, 1267}1278. Wong, C.S., Chan, Y.-H., 1991. Temporal variations in the partial pressure and #ux of CO at Ocean  Station P in the subarctic northeast Paci"c Ocean. Tellus 43B, 206}223. Wong, C.S., Honjo, S., 1984. Material #ux at weather station Papa; high frequency time series observations through production cycles. Transactions of the American Geophysical Union 65, 225. Wong, C.S., Matear, R.J., Whitney, F.A., Iseki, K., 1998. Enhancement of new production in the northeast subarctic Paci"c Ocean during negative North Paci"c Index events. Limnology and Oceanography 43, 1418}1426. Wong, C.S., Whitney, F.A., Crawford, D.W., Iseki, K., Matear, R.J., Johnson, W.K., Page, J.S., Timothy, D., 1999. Seasonal and interannual variability in particle #uxes of carbon, nitrogen and silicon from time series of sediment traps at Ocean Station P, 1982}1993: relationship to changes in subarctic primary productivity. Deep-Sea Research II 46, 2735}2760. Wong, W.W., Sackett, W.M., 1978. Fractionation of stable carbon isotopes by marine phytoplankton. Geochimica et Cosmochimica Acta 42, 1809}1815.

2832

J. Wu et al. / Deep-Sea Research II 46 (1999) 2793}2832

Wooster, W.S., Fluharty, D.L., 1985. El Nino North: Nino e!ects in the Eastern Subarctic Paci"c Ocean, University of Washington Sea Grant Program, Seattle, Pages. Wu, J., Calvert, S.E., Wong, C.S., 1997. Nitrogen isotope variations in the subarctic northeast Paci"c: relationships to nitrate utilization and trophic structure. Deep-Sea Research 44, 287}314. Wu, J.-P., 1997. The carbon and nitrogen isotope compositions of particulate organic matter in the subarctic northeast Paci"c Ocean: Unpub. Doctoral Thesis, University of British Columbia, 252 pp.