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A biomarker perspective on prymnesiophyte productivity in the northeast pacific ocean
Deep-Sea Research l, Vol. 40, No. 10, pp. 2061-2076, 1993. Printed in Great Britain.
0967-0637/93 $6.00 + 0.00 © 1993 Pergamon Press Ltd
A biomarker perspective on prymnesiophyte productivity in the northeast Pacific Ocean F. G . PRAHL,* R . B . COLLIER,* J. DYMOND,* M . LYLE* a n d M . A . SPARROW*
(Received 13 July 1992; in revisedform 28 December 1992; accepted 6 January 1993) Abstract--Long-chain alkenones derived from prymnesiophyte algae were analysed in 1-year sediment trap time series (September 1987-1988) from three sites along a 630 km offshore transect at -42°N in the northeast Pacific Ocean. Biomarker flux monitored at 1000 m water depth was evident throughout the year at all sites and showed a consistent seasonal maximum in late spring which increased in amplitude with distance offshore. The integrated annual biomarker flux was constant along the transect, despite differences in seasonality between sites. Alkenone unsaturation patterns were remarkably uniform throughout the time series, reflecting an algal growth temperature of 10.6 _+ 1.1°C. This value corresponds to regional water temperature at the seasurface in winter. It recurs in seasonal upwelling near the coast and at the depth of the subsurface chlorophyll maximum offshore during seasons of stratification. These biomarker observations, interpreted in view of trap data for total organic (TOC) and inorganic carbon and ancillary hydrographic information, help to clarify seasonal productivity patterns for alkenone-producing prymnesiophytes in the northeast Pacific Ocean. Sediments accumulating with distance offshore along the sampling transect change from suboxic and Mn-reducing at the water-sediment interface to aerobic throughout the depths penetrated by box coring. Comparison of alkenone and TOC accumulation rates in surface (0-1 cm) sediments with corresponding annual fluxes integrated by the trap time series, shows that the fraction of both properties accounted at the seafloor is highest and similar under sub-oxic conditions (-25%), and declines steeply and disproportionately as aerobic conditions are encountered farther offshore. Only 0.25 and 3.1% of the annual inventory for alkenones and TOC in traps are accountable in surface sediments from the slowest accumulating, most oxidizing site farthest offshore. Despite major loss of biomarker to early diagenesis, surface sediments and trap particles display consistent alkenone unsaturation patterns. Results from this study provide a necessary background for palaeoceanographic reconstruction of the northeast Pacific Ocean from stratigraphic analysis of alkenone abundances, unsaturation patterns and isotopic compositions in sediment cores.
INTRODUCTION A SEPaES o f l o n g - c h a i n ( C 3 7 , C 3 8 , C 3 9 ) , p r i m a r i l y di- a n d t r i - u n s a t u r a t e d a l k e n o n e s , w a s d i s c o v e r e d in o r g a n i c - r i c h s e d i m e n t s f r o m t h e B l a c k S e a a n d W a l v i s B a y , a n d s u b s e q u e n t l y w a s d o c u m e n t e d w i d e l y in o c e a n s e d i m e n t s (BRASSELL et al., 1986). T h e c o c c o l i t h o p h o r i d Emiliania huxleyi h a s b e e n i d e n t i f i e d as a s o u r c e o f this s e r i e s (VOLKMAN et al., 1980). S y s t e m a t i c e x a m i n a t i o n o f p h y t o p l a n k t o n c u l t u r e s h a s r e v e a l e d t h a t E. huxleyi is n o t t h e e x c l u s i v e s o u r c e . H o w e v e r , t h e a l k e n o n e s r e m a i n r e s t r i c t e d
*College of Oceanic and Atmospheric Sciences, Oregon State University, Corvallis, OR 97331, U.S.A. 2061
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taxonomically to only a few genera within the class Prymnesiophyceae and are considered biomarkers of such phytoplankton (MARLOWEet al., 1990). Alkenone compositions in living cells of E. huxleyi have two unique attributes. Unsaturation patterns within the series provide a well-behaved index (uk7 = [C37:2]/([C37:2 ] -k- [C37:3]) of algal growth temperature, and total alkenone content of the cell is relatively constant independent of growth condition (PRAHL et al., 1988). Both characteristics suggest these compounds play some role in cell membrane architecture and processes, although their specific physiological function remains unknown. Because of these attributes, long-chain alkenones have now been explored in a palaeoceanographic context on a variety of geological time scales to assess changes in productivity (e.g. PRAHL et al., 1989), sea-surface temperature (SST) (e.g. BRASSELLet al., 1986; McCAFFREYet al., 1990; SIKESet al., 1991; LYLEet al., 1992) and pCO2 in the atmosphere (JASPERand HAYES, 1990). Various factors limit environmental interpretation in such applications. These biomarkers are susceptible to degradation in sedimentary processes (PRArILet al., 1989), and the dependence of degradation on depositional setting is poorly understood beyond a qualitative level. Consequently, it is not yet possible to separate effects of productivity and diagenesis on the sediment record for alkenone content. Despite major losses of total alkenone content, unsaturation patterns appear to be insensitive to diagenetic alteration (PRAHL et al., 1989; McCAFFREYet al., 1990). Therefore, the sedimentary u3k7 record provides a potentially accurate measure of algal growth temperature in the overlying water column. However, the relationship between average growth temperature recorded by uk7 and mean SST remains unclear because the productivity patterns for alkenone-producers in the oceans are poorly understood. Finally, the possibility of appreciable alkenone flux to sediments from production in upwelled waters or waters at subsurface depths within stratified euphotic zones (LONGHURSTand HARRISON, 1989) challenges the utility of uk7 and 613C measurements on alkenones as reliable proxies of SST or atmospheric pCO2, respectively. This paper presents results from alkenone analyses of trap-collected particles and underlying surface sediments from three sites along an offshore transect at 42°N, in the northeast Pacific Ocean (Fig. 1). The data are from a one-year sediment trap deployment at 1000 m water depth in which samples were collected at approximately bimonthly intervals. The time series identifies when alkenone-producers are productive at each site and how the seasonality of productivity varies spatially in t-his region. We use U~7 values and contemporary hydrographic data to constrain the depth of alkenone production at each site. Also, we are able to estimate alkenone preservation at each location by comparing the annual integrated flux through 1000 m water depth with accumulation rates in underlying surface sediments. These results illuminate the strengths and limitations of using alkenone analyses for palaeoceanographic reconstruction of the northeast Pacific Ocean. EXPERIMENTAL METHODS Sample collection
All samples analysed in this study were collected in the first year of Multitracers, a project designed to monitor changes in particle flux and sediment accumulation across a gradient in primary productivity associated with the California Current System (LYLEe t
Prymnesiophyte productivity in the northeast Pacific Ocean
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Fig. 1. Map showing the region in the northeast Pacific Ocean where the three sampling sites (Nearshore, Midway, Gyre) are situated (solid diamonds)• The location of two NOAA weather buoys (No. 46027: 41.8°N, 124.2°W;No. 46002: 42.5°N, 130.4°W)is also indicated (open boxes). Solid circles depict sites farther north along the continental margin off Washington state where the alkenone composition of surface sediment has been previously reported (PRAIJLet al., 1988).
al., 1992). Particle flux was defined at three sites in the northeast Pacific Ocean by samples from sediment traps moored at 1000 m water depth. The three sites (Nearshore, Midway and Gyre) are situated -120, 270 and 630 km, respectively, off the coast of northern California along 42°N (Fig. 1). Each trap was equipped with six sampling cups that opened and closed sequentially at approximately bimonthly intervals over the one-year deployment time of each mooring (22 September 1987-16 September 1988). Trap construction was a modification of a previous design (SoUTARet al., 1977) and featured all plastic and fiberglass materials, a 2:1 height to diameter cone with 0.5 m 2 collecting area, and a honeycomb baffle at the mouth of the cone to limit turbulence and minimize particle sampling bias. Box cores were collected at Nearsfiore (2712 m water depth), Midway (3111 m water depth) and Gyre (3680 m water depth) on the deployment cruise (W8709A) for the sediment trap moorings using a 25 x 25 cm standard box corer. Gravity and piston cores penetrating the Late Pleistocene also were recovered from these sites at the same time. Sedimentation rates established by 6180 stratigraphy and 14Cdates for the cores averaged -20, 10 and 1.3 cm ky -1, respectively (LYLEet al., 1992). Chemical analyses Subsamples of particles collected in each sediment trap cup and surface (0-1 cm) box core sediments from the three sites were analyzed for long-chain alkenone content and
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composition, total organic (TOC) and inorganic (CaCO3) carbon content (Table 1). Lipid fractions enriched in long-chain alkenones and structurally related alkenoates (MARLOWE et al., 1990) were isolated from samples of freeze-dried trap particles and wet surface sediments and analysed by published methods (PRAHLand WAKEHAM,1987; PRAHLet al., 1989). All conditions for alkenone analysis by capillary gas chromatography were the same as previously described except for the use of a fused silica column (0.25 ktm film thickness, 30 m length × 0.32 mm i.d.;J&W Scientific) containing a methylsilicone (DB-1) rather than phenylmethylsilicone (DB-5) bonded phase. Selection of the DB-1 bonded phase improved resolution of the diunsaturated C36 methyl ester (ME) from the C37:2 methyl ketone, but merged the diunsaturated C36 ethyl ester (EE) with the C3s:3 ethyl ketone (PRAHL et al., 1988). TOC and CaCO3 content of trap particles and sediments were determined sequentially on each sample using a LECO analyser and the wet chemical technique of WEENSYet al. (1983). RESULTS AND DISCUSSION Seasonal fluxes o f alkenones
The vertical flux of alkenones through 1000 m water depth showed a common seasonal pattern at Nearshore, Midway and Gyre (Table 1). Fluxes were lowest in the fall to late winter period (cups 1-3), increased in early spring (cup 4) at Gyre, followed by a pronounced maximum in late spring (cup 5, mid-April to mid-June) at all three sites, then declined in summer to the levels observed at corresponding sites at the start of the time series (Fig. 2C). Although the timing of the peak in alkenone flux was synchronous at the three sites, the amplitude increased significantly offshore along the transect. Alkenone flux measured in cup 5 was ~ 2 x (Nearshore), ~ 6 x (Midway) and ~20x (Gyre) greater than that for the average of the other cups. These results imply that alkenone-producers are productive over the entire year, and oceanographic conditions extant during the latespring are conducive to a large-scale, synchronized bloom for these primary producers throughout the northeast Pacific Ocean. TOC and CaCO3 flux also varied seasonally in the trap series (Table 1). The coccolithophorid Emiliania huxleyi (Homo and OKADA,1974), an important primary producer in the ocean over the past -270 ky (Thai'AN, 1980), is a key representative of the alkenoneproducing prymnesiophytes living in today's ocean. Therefore, significant correlation between TOC, CaCO3 and alkenone flux might be expected. If the complete data set for the time series is considered, however, the correlation between TOC and alkenone flux (r 2 = 0.17) or between CaCO 3 and alkenone flux (r 2 = 0.014) is poor. Omitting all data for cup 5, TOC and CaCO3 fluxes correlate reasonably well with alkenone flux (r 2 = 0.75 and 0.67, respectively). Either alkenone-producers in surface waters are only minor contributors to the vertical flux of TOC and CaCO3 at these sites (SANCErrA, 1992), or decomposition and dissolution in the upper 1000 m decouple TOC and CaCO3 from the alkenones. Interestingly, no such decoupling occurred between the TOC and CaCO3 flux. These two properties are strongly correlated in the overall data set (r 2 = 0.67). We believe that alkenone-producing phytoplankton are only minor contributors to TOC and CaCO3 flux. The study of laboratory cultures (PRArlLet al., 1988) has shown that the alkenone content of E. huxleyi is constant (1.2 + 0.28 pg cell-l), independent of growth conditions, and constitutes a large percentage of total cellular organic carbon
N/A N/A N/A N/A N/A
340 0.87 0.00 0.44 11.9
0.68 0.19 0.053 18
270 0.97 0.04 0.44 11.8
295 0.98 0.00 0.42 11.2
0.21 0.098 0.019 N/A
1.9 0.47 0.11 30
200 1.09 0.12 0.45 12.2
320 0.92 0.13 0.42 11.2
0.9 0.25 0.07 21
8.5 1.1 0.33 68
12.8 1.3 0.43 140
Cup 2 10/25-12/24
400 0.96 0.00 0.40 10.5
0.36 0.90 0.025 10
290 1.02 0.09 0.43 11.6
6.4 1.9 0.25 72
180 0.85 0.12 0.42 11.3
25.8 2.1 0.67 120
Cup 3 12/24-2/22
560 1.06 0.00 0.38 10.0
2.6 0.75 0.13 74
290 1.12 0.17 0.42 11.2
8.7 2.0 0.35 100
240 1.12 0.23 0.37 9.8
20.7 2.8 0.69 170
Cup 4 2/22--4/22
2020 1.02 0.02 0.33 8.4
2.5 0.36 0.34 680
830 1.07 0.03 0.33 8.5
4.1 0.90 0.40 330
550 0.94 0.02 0.33 8.6
5.5 1.0 0.51 280
Cup 5 4/22~5/21
260 0.99 0.00 0.36 9.3
0.93 0.44 0.090 23
410 0.99 0.03 0.42 11.3
1.6 0.37 0.15 63
515 1.07 0.01 0.39 10.4
6.4 1.0 0.27 140
Cup 6 6/21-9/16
*K37/K3s: ratio of total C37-C38alkenone abundance; ME/K37: ratio of C 36 methyl alkenoate to total C 37 alkenone abundance. tWater temperature estimate from the calibration equation uk7 = 0.034 × T + 0.039 (PRAHLet al., 1988). :~Integrated annual average for time series.
Fluxes Mass (mg cm -2 )~-1) CaCO 3 (mg cm -2 y 1) TOC (mg cm -2 y - l ) Alkenones (ng cm -2 y-l) Compositions Atkenones (,ug gC- 1) K37]K38 ME/K37 U3k7 T (°C)*
Gyre
Fluxes Mass (mg cm -2 ),-1) CaCO3 (mg cm -2 y-l) TOC (mg cm -2 y) Alkenones (ng cm -2 y-l) Compositions Alkenones (,ug gC- l) K37/K3s ME/K37 Uak7 T(°C)
Midway
Fluxes Mass (mg cm -2 y-l) CaCO3 (mg cm -2 y - l ) TOC (mg cm -2 y - l ) Alkenones (ng cm -2 y - 1) Compositions Alkeuones ~ g gC -1 ) K37/K38* ME/K37* U~7 T(°C)t
Nearshore
Cup 1 9/22-10/25
100 1.18 0.24 12.0
1190 1.02 0.02 8.7
0.0034 0.35
0.6
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9.9
1.3 0.44 0.11 140
210 1.16 0.24
470 1.05 0.06
0.050 11
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3.96 1.00 0.23 110
260 1.14 0.26
0.13 33
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320 1.00 0.09
12.8 1.54 0.47 150
Ave:~
TOC, CaCO 3 and alkenone data from analysis of sediment trap particles collected in time series (22 September 1987 - 16 September 1988) at 1000 m water depth and of underlying surface (0-1 cm) sediments from three sites in the northeast Pacific Ocean (Nearshore, Midway and Gyre; Fig. 1)
Sampling periods
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Julian Day (since 1987) Fig. 2. Water temperature estimates from the analysis of alkenone unsaturation patterns (ok7) in the sediment trap time series for the Nearshore (A), Midway (B) and Gyre (B) sites are compared with the annual records for sea-surface temperature (SST) monitored hourly at 1 m water depth at two NOAA weather buoys located at the shelf break (No. 46027) and a more remote offshore site (No. 46002) (Fig. 1). Panel (C) displays the record for total alkenone flux in each sediment trap time series. The specific time intervals between 22 September 1987 and 16 September 1988 for each sampling cup in the sediment trap time series are defined in Table 1.
(8.0 + 2.9%). Alkenone concentrations normalized to T O C in sediment trap particles from the time series range from ~200 to 2000/~g gC -1 (Table 1). Using the ratio of concentrations measured in sediment trap particles to that expected for the living biomarker source suggests that alkenone producers contribute only 0.25-2.5% to the observed T O C fluxes. This estimate of source contribution to T O C is accurate only if the
Prymnesiophyteproductivityin the northeast PacificOcean
2067
fixed proportion of alkenone to organic carbon observed in the living algal cell is not disrupted significantly in the production of sedimentary particles. Nonetheless, the low estimates obtained by this exercise are maximum contributions, unless alkenones are more labile than cellular organic carbon during early sedimentation processes. The latter possibility seems unlikely at present (VOLgMAN et al., 1980), although it cannot be discounted yet on full experimental grounds. Annual fluxes of alkenones
An annual alkenone flux through 1000 m water depth at each site was calculated by averaging the time weighted individual fluxes (Table 1). The range of annual flux along this transect was 100-150 ng alkenone cm-2 y-1, close to constant. In contrast, the average annual fluxes for TOC and CaCO3 (Table 1) both decreased steadily offshore, -4-fold along the transect. Alkenone concentration reconstructed for average trap particles varied from 320 #g gC-1 at Nearshore through 470 #g gC-1 at Midway to 1190 #g gC-1 at Gyre. Thus, annual export productivity for alkenone-producing prymnesiophytes appears relatively constant over a wide spatial range in the northeast Pacific Ocean and comprises an increasing fraction of primary productivity seaward. Such inferences about prymnesiophyte productivity assume that alkenones are degraded similarly in the upper water column at all three sites, and that alkenone, TOC and CaCO3 fluxes measured in sediment traps relate directly to primary productivity in surface waters (e.g. SUESS, 1980). These assumptions seem credible but are equivocal and require more rigorous examination. Seasonal variations in alkenone unsaturation patterns
Alkenone unsaturation patterns were defined by measurement of U3k7in all samples collected in the sediment trap time series. Values range from 0.33 to 0.45, averaging 0.40 _+ 0.04 in the complete data set (n = 17, Table 1) and show that the composition of the alkenone series has remarkable uniformity in this region of the ocean. Unsaturation patterns in the aikenone series are related to the growth temperature of the prymnesiophyte source (BgASSELLet al., 1986). Laboratory study of a single strain of E. huxleyi has shown the relationship between U3k7and growth temperature is linear (U3k7 = 0.034 X T + 0.039, r 2 = 0.994) over the range 8-25°C (PRAHLet al., 1988). PRAHLand WAKEnAM (1987) and SIKES et al. (1991) tested this calibration equation in the field and concluded it provides realistic estimates of the water temperature associated with prymnesiophyte growth over a large geographic range of ocean conditions. Consequently, uk7 measures in the sediment trap time series were converted to water temperature estimates (Table 1), assuming the calibration equation also applies to the alkenoneproducing biomass in the northeast Pacific Ocean. The observed range of uk7 (0.33-0.45) corresponds to water temperatures between 8.4 and 12.1°C, averaging 10.6 + 1.1°C (n = 17). Inspection of the data (Fig. 2A and B) reveals that the recorded water temperature is not constant but follows a common seasonal pattern at Nearshore, Midway and Gyre. The lowest estimates (-8.5°C) were from trap particles collected in late spring (cup 5), the period corresponding to maximum alkenone flux at each site (Fig. 2C). A purely diagenetic process cannot explain the similarities between each time series. Despite substantial degradation of total alkenones in sedimentary processes, the unsaturation
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pattern in this biomarker series, once set, appears insensitive to alteration (e.g. PRAHLet al., 1989). The consistently low temperature estimate for cup 5 at all three sites more likely requires a biological explanation, For example, the prymnesiophyte assemblage contributing to alkenone flux may change systematically throughout the year and unsaturation patterns in species predominant during the productivity event in late spring could respond somewhat differently to temperature than suggested by the calibration equation for a single strain of E. huxleyi. The observation also might be explained biologically without invoking violation of the uk7 versus temperature calibration, however. The oceanographic process triggering the large-scale productivity event for alkenone producers throughout the region (Fig. 2C) may have distinctive hydrographic characteristics as reflected accurately by lower apparent growth temperature. A case is made in the following discussion for biological rather than geochemical factors controlling the uk7-based temperature record in trapped particles. Evidence for biological control on seasonal variations in unsaturation patterns
The alkenones occur as a series of C37, C3s and C39 homologues and are often accompanied by structurally related C36 methyl and ethyl alkenoates (MARLOWEet al., 1990 and references therein). Evidence for a seasonal shift in the prymnesiophyte species contributing to the alkenone record in trap particles is potentially imbedded in the overall composition of the biomarker series. Various compositional properties of the biomarker series were examined for this reason. Values for the proportion of total C37--C3s aikenones, monitored in each time series (K37/K38 values, Table 1), range from 0.85 to 1.12 but show no coherent seasonal variation within or between time series. The weighted annual average for K37/K3s is virtually indistinguishable at each site (-1.02, Table 1). If the prymnesiophyte species controlling alkenone flux change seasonally or differ between sites, it is not discerned by K37/K38 measurements. Values for this property measured in sediment trap particles and underlying sediments from the northeast Pacific Ocean (Table 1) are lower than those reported for a single strain of E. huxleyi grown in laboratory culture (PRAHL et al., 1988), but the difference is small and considered insignificant. Methyl and ethyl alkenoates structurally related to the aikenones were typical of lipid compositions isolated from many of the trap samples and all surface sediments. Values for the proportion of C36:2 methyl alkenoate (ME) (PRAHLet al., 1988) to total C37 alkenones were monitored in each time series (ME/K37 , Table 1) and display different temporal trends among sites. An abrupt shift occurs at Nearshore from high ME/K37 values in cups 1-4 (0.12-0.23) to low values in the remaining series (0.011-0.023). At Gyre, ME/K37 values as low or lower than those in cup 5-6 of Nearshore occur throughout the year. The situation at Midway is intermediate between the other two sites. Laboratory cultures of E. huxleyi display the range of compositions observed in these time series, but only if grown over a wide range of temperatures (8-25°C, PRAHLet al., 1988). Because the observed range of u3k7values observed in the overall data set implies very little variation in growth temperature, we infer that the observed behavior for ME/K37 in trap particles results from spatial and temporal variations in the assemblage of prymnesiophyte species contributing to the vertical alkenone flux. Nonetheless, the inference of a seasonal change in species assemblage is not proven by these data. Preferential degradation of alkenoates and alkenones also must be considered
Prymnesiophyteproductivityin the northeastPacificOcean
2069
when variations in ME/K37 values are explained. Preferential degradation may not control the sediment trap observations for ME]K37, but it could be important in the longer term sedimentary geochemistry of these biomarkers. ME/K37 values of average trap particles decrease along the transect and are -3-fold (Nearshore), 4-fold (Midway) and 10-fold (Gyre) lower than values recorded in underlying surface sediments (-0.25, Table 1). If the particle flux measured in the trap series accurately represents the average annual input to underlying surface sediment, then alkenoates must be preserved more efficiently than alkenones at some early stage in the sedimentary process. A l k e n o n e unsaturation patterns a n d trap-sediment comparisons
For each sediment trap time series, an annual uk7 value was calculated by averaging the sum of all individual measurements weighted for the quantity of total alkenones collected in respective cups. These values were converted into estimates of average annual water temperature recorded by the alkenones transported through 1000 m water depth using the calibration equation for uk7 versus temperature. The estimates are essentially the same for Nearshore and Midway (-10°C) and somewhat lower for Gyre (8.7°C). Average water temperatures estimated from uk7 measurements for underlying surface sediments at corresponding sites are - I ° C warmer than the trap-based temperatures for Nearshore and Midway and -3.3°C warmer for Gyre (Table 1). We consider the large temperature difference in the trap-sediment comparison for Gyre real and provide a geochemical explanation. The percentage of the annual alkenone flux through 1000 m water depth preserved in underlying sediments declines steeply along the transect from 22% at Nearshore to <1% at Gyre (Table 2). Extensive degradation of alkenones produced during the high flux period in late spring (cup 5, Table 1) is required to eliminate >99% of the presumed sedimentary input at Gyre. uk7 from this trap interval is noticeably lower than at all other times (Fig. 2A and B). Consequently, if the fraction of total flux surviving burial were disproportionately lower during the time period represented by cup 5, uk7 values preserved in sediments would appear higher than the weighted annual average for traps. This mechanism does not require selective degradation of the more Table 2. TOC and alkenone preservational efficiencies estimated by comparison of average annual trap (I000 m water depth)flux with surface sediment (0--1 cm) accumulation rate at the Nearshore (2712 m water depth), Midway (3111m water depth) and Gyre (3680m waterdepth) sites
Traps TOC (~g cm-2 y-l) Nearshore Midway Gyre Aikenones (ng cm-2 y-l) Nearshore Midway Gyre
470 230 110 150 110 140
Sediments % Preserved* 130 50 3.4 33 11 0.35
28 22 3.1 22 10 0.25
*Preservational efficiencydefinedby ratio of sediment accumulation rate to trap flux,expressedas a percentage.
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unsaturated alkenones per se, although that would be the apparent effect on the integrated alkenone composition preserved in sediments. Although such a mechanism is yet only hypothetical, it would also account for the less pronounced, but similar temperature offset in trap-sediment comparisons for Nearshore and Midway. Relationship o f alkenone unsaturation to hydrographic conditions
Two NOAA weather buoys monitoring sea-surface temperature (SST) hourly are moored close to the multitracers sampling transect. One mooring is landward of Nearshore on the continental shelf break (No. 46027), and the other is roughly equidistant between Midway and Gyre (No. 46002) (Fig. 1). The annual SST record for the buoy at the continental shelf break (Fig. 2A), shows cold water (10-12°C) at the surface throughout the year with signs of episodic, wind-induced upwelling events. Such upwelling events driven by strong northerly winds occur frequently in coastal regions above -40°N, in the northeast Pacific Ocean from late spring to fall (HICKEY, 1989 and references therein). The record for the weather buoy farthest from land (Fig. 2B) shows a smoother annual cycle of summertime heating and stability versus wintertime cooling and deep mixing expected in regions of the northeast Pacific Ocean remote from the influence of coastal upwetling. SST comparable to the uniform water temperature (10-12°C) estimated by U~7 in sedimentary materials collected along the -500 km sampling transect are detected at both weather buoys throughout the winter to early spring (Fig. 2A and B). Similar SST estimates (PRAHL et al., 1988) are obtained from the alkenone record preserved in sediments located 440-550 km farther north on the Washington margin (Fig. 1). Although u3k7 values recorded in sediments correspond to the coldest seasonal SST, it does not follow that the prymnesiophyte species are only productive in winter to early spring in this region. Our sediment trap data show appreciable alkenone flux throughout the year at all three sites (Fig. 2C). SST warms to -18°C in summer at offshore sites such as Gyre (Fig. 2B). Therefore, the consistent u3k7 temperature estimates in the summer trap samples from Gyre suggest that alkenone flux derives from productivity in colder, subsurface waters within the euphotic zone. Figure 3 displays a typical depth profile for water temperature and chlorophyll fluorescence in late summer at Gyre. The upper water column is thermally stratified as expected by inference from the annual SST record for the offshore weather buoy (Fig. 2B). Chlorophyll fluorescence is low and constant throughout the surface mixed layer and underlain by a pronounced subsurface chlorophyll maximum (SCM) in the upper thermocline. The water temperature at the SCM is -12°C, close to the U~7-predicted temperature of trap particles collected at this time of year (Table 1). This correspondence suggests that alkenone production during periods of offshore stratification in the northeast Pacific Ocean occurs at the SCM rather than in the surface mixed layer. The key alkenone producer in today's ocean, E. huxleyi, biosynthesizes the carotenoid 19'-hexanoyloxyfucoxanthin as a major accessory pigment which enhances photosynthetic effectiveness in the spectral interval 500-550 nm (Haxo, 1985). These wavelengths are among the most penetrative in seawater, comprising much of the residual spectrum deep in the euphotic zone (PARSONSet al., 1984). Thus, E. huxleyi and perhaps other alkenone producers are suited for growth in the low light regime of the SCM. Figure 3 also displays a depth profile for nitrate in the thermally stratified offshore water column in summer to early fall. The SCM is situated at the top of the nitricline. Conditions for alkenone
Prymnesiophyteproductivityin the northeastPacificOcean r (oc)
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.....
Fluorescence (rel. units) - - 5 10 15 20 0
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.
.
.
.
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.
.
.
.
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.
.
.
.
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Fig. 3. Profiles for water temperature, chlorophyll fluorescence and nitrate concentration measuredwithdepth beneath the sea-surfaceat Gyrcin September 1989. production may be optimum within the SCM because the algal source is adapted for photosynthesis under low ambient light, and because nutrients such as nitrate, virtually absent in the surface mixed layer, are replete at this depth. The association of the SCM with the top of the nitricline is a common feature in many open ocean environments, at least during some portion of the year (LONGHURSTand HARRISON, 1989). The euphotic zone in such settings has been modelled as a two-layered biological system: an upper oligotrophic layer and a lower eutrophic layer (DoGDALEand GOERING, 1967; COALE and BRULAND, 1987; SMALL et al., 1987). The upper layer corresponds to the surface mixed layer and is characterized by relatively high rates of primary productivity but low rates of sedimentary export ("new production"). Low new production results because of tight coupling between trophic levels within the upper layer and, consequently, efficient biological recycling. The lower stratified layer encompasses the SCM and is characterized by reduced rates of primary productivity but higher new production than above because of less efficient biological recycling. Alkenone data from the sediment trap time series are consistent with a two-layered biological system in stratified offshore waters of the northeast Pacific Ocean. The correspondence between predicted algal growth temperature and measured water temperature at the SCM and a maximum in alkenone concentration at the SCM (AMTHOR, unpublished data) shows at least circumstantially that a prymnesiophyte biomass contributing to the SCM is photosynthetically viable and influences the vertical TOC flux to the seafloor. Some fraction of the alkenone content of Nearshore, Midway and Gyre sediments derives from prymnesiophyte production in upwelled waters and/or in stratified waters at the base of the euphotic zone (Table 1). Such contribution to the record certainly complicates the relationship between atmospheric pCO2 and the isotopic composition (613C) of alkenones preserved in underlying sediments from this region because the inorganic carbon fraction fixed photosynthetically in these waters is not equilibrated with
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F.G. PRArILet al.
the atmosphere. If future molecular isotopic analyses reveal in cores from the northeast Pacific a systematic trend between 6 values and sediment age (e.g. JASPERand HAYES, 1990), a more complex process than direct coupling with atmospheric pCO2 changes must be invoked to explain the observation.
Water column-surface sediment comparisons for alkenones TOC and alkenone accumulation rates (Table 1) were calculated from the product of respective concentrations in surface (0-1 cm) sediment from Nearshore, Midway and Gyre and average sedimentation rate estimated for each site (see Experimental Methods). Accumulation rates for both TOC and alkenones show an offshore decrease. TOC accumulation decreases by a factor of 30, much more than the 4-fold decrease in TOC flux observed in trap particles collected at 1000 m water depth. Alkenone accumulation rates along the transect exhibit an even greater contrast to the trap fux, being 100 times lower at the Gyre site than at the Nearshore site. Average annual fluxes measured by traps showed virtually no difference between sites. Consequently, the ratio of alkenone to TOC in surface sediments decrease from -260 at Nearshore, 210 at Midway to 100/~g gC -1 at Gyre (Table 1). If supply is the dominant factor controlling the TOC and alkenone content of sediments, our data imply a 2.5-fold offshore decrease in prymnesiophyte productivity relative to total primary productivity. Because this trend is opposite to that of the trap data, such an interpretation is most likely wrong.
Dependence of alkenone preservation on sedimentary conditions We have determined the TOC and alkenone preservational efficiency at each site from comparison of sediment accumulation rate with average annual trap flux (Table 2). Preservational efficiency for both properties is highest and roughly equivalent (-25%) at Nearshore and declines disproportionately seaward. The low estimates of TOC and alkenone preservation at Gyre (3.1 and 0.25%) are similar to those previously documented for the central equatorial Pacific (Manop site C) where accumulation rates for TOC (3.6/~g cm -2 y-1) and alkenones (0.33 ng cm -2 y-~) in surface sediments (4287 m water depth) represented - 2 . 1 % and 0.65 % of corresponding annual flux measured 500 m above bottom (PRAHLet al., 1989). We must explain: (1) why the two reference points, 1000 m traps and surface sediments, infer different offshore trends for the prymnesiophyte to total phytoplankton assemblage; and (2) why calculated TOC and alkenone preservationai efficiencies vary between Nearshore, Midway and Gyre. Either the sediment traps poorly sampled the average TOC and alkenone input to underlying sediments or diagenetic effects operating at the seafloor selectively altered the sediment records of these properties. The former possibility is a perennial criticism levied against all sediment trap studies (e.g. LEE et al., 1988) and cannot be dismissed. But observations from further geochemical examination of sediments accumulating at these locations and reference to current literature show that diagenesis is a key consideration in explaining both inquiries. The total aluminum and manganese content of sediments at Nearshore, Midway and Gyre reveals an offshore gradient in redox conditions at the seafloor, Surface sediments from box cores collected at all three sites contain 7-8 weight per cent of aluminum (multitracers, unpublished data), which is similar to the average abundance of AI in shales
Prymnesiophyte productivity in the northeast Pacific Ocean
Mn Enrichment Foctor 5 10 15 20 25
0 . .
5
10
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2073
.
.
i
,
.
.
.
i
.
.
.
.
i
.
.
.
.
i
.
.
.
.
if----,i
c-
o. 25 ID
a
~ 3O-
c~ 35. 40, 45. 5O
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Fig. 4. Profiles displaying enrichment factors for reducible manganese with depth in box cores from Nearshore, Midway and Gyre. The Mn-enrichment factor is defined by the ratio of Mn/Al values measured in a given sediment interval to the Mn/A1 value for average shale (0.011; TUREKIANand W E D E P O L , 1961). Both elements were measured by instrumental neutron activation analysis (Multitracers, unpublished data).
and other crustal rocks (8% by weight, TUREKIANand WEDEPOL, 1961). This indicates that crustally eroded aluminosilicates are the major components of bulk surface sediment at all sites. We have normalized the downcore Mn/A1 values to the Mn/A1 composition of average shale (0.011; TUREKIANand WEDEPOL, 1961) in order to define how reducible manganese content varies with sediment depth at each site (Fig. 4). Nearshore sediments show virtually no Mn-enrichment above crustal abundance at all sediment depths, indicating suboxic, Mn-reducing conditions extend to the water-sediment interface. Midway sediments display a 25-fold enrichment near the surface decreasing to near crustal abundance by 7 cm depth. Thus, these sediments are suboxic and Mn-reducing at a shallow depth beneath the water-sediment interface. Gyre sediments are enriched 10-15-fold above the crustal abundance for Mn throughout the core and must be oxic over the - 5 0 cm depth range penetrated by box coring. We suggest that contrasting redox conditions lead to differences in alkenone relative to TOC preservation. Alkenones, like TOC, are susceptible to degradation in sediments under the complete range of redox conditions. Examination of an organic-rich turbidite interval deposited on Madeira Abyssal Plain (MAP) revealed - 8 5 % loss of alkenones from the record as a consequence of aerobic degradation (PRAHL e t al., 1989). Alkenone degradation was - 3 0 % greater than that of TOC. This result does not conflict with the much greater aerobic degradation of alkenones relative to TOC at Gyre and in the central equatorial Pacific. Differences in depositional context can explain the discrepancy. The trap-sediment comparisons have assessed the impact of aerobic degradation on alkenones and TOC in fresh organic debris arriving for the first time at the seafloor. The MAP study, on the other hand, assessed the secondary impact of aerobic degradation on alkenones and TOC that had already survived destruct,ion in passage through a water-sediment interface in the source region for the turbidite.
2074
F . G . PRAnL et al.
The estimates of preservational efficiency from the trap-sediment comparisons support the following viewpoint. Alkenones are at least as reactive as TOC in sediments under the complete span of anaerobic to aerobic sedimentary conditions. Preservation for both properties declines in slower accumulating, more oxidizing sediments, but alkenones degrade preferentially to TOC along such a gradient. Thus, even if the blend of alkenone and TOC introduced to the bottom were the same at two sites, the concentration of alkenone (/gC) would be lower in slower accumulating, more oxidizing sediments. Assuming the sediment trap time series provided reasonable measures of the average alkenone to TOC composition raining into sediments at Nearshore, Midway and Gyre, the assessed dependence of preservational efficiency on sedimentary conditions at the seafloor emphasizes an important geochemical point. Diagenetic processes occurring at the seafloor complicate our ability to hindcast even relative changes in prymnesiophyte productivity from the sediment record of alkenone accumulation rate. This problem is well-recognized in relating TOC accumulation rate to primary productivity (EMERSONand HEDrES, 1988 and references therein). Properties such as alkenone flux and concentration normalized to TOC may still provide valuable clues for palaeoceanographic reconstruction assuming a regular relationship exists between organic preservation and sedimentary conditions, the relationship can be defined by empirical means and this relationship is used in the data interpretation. CONCLUSIONS
Geochemical analysis of sediment trap particles collected in time series have clarified productivity patterns for alkenone producers in the northeast Pacific Ocean. The productivity of these phytoplankton occurs throughout the year but displays a conspicuous seasonal pattern. Yet unspecified oceanographic conditions associated with the spring transition from deep winter mixing to episodic upwelling near the coast and stratification in more remote oceanic locations are conducive to regional-scale blooms of alkenone producers. The amplitude of the blooms above the background productivity for the rest of the year increases offshore. The integrated annual productivity for these organisms, on the other hand, appears independent of setting, despite an increasing seaward importance of seasonality. In contrast, the integrated annual TOC flux infers that total primary productivity declines significantly offshore. Thus, alkenone producers contribute increasingly to total primary productivity along the offshore gradient. The growth temperature inferred for alkenone producers throughout the year is 10-12°C. The narrow range corresponds well with sea-surface temperature in winter to spring throughout this region, sea-surface temperature in the vicinity of the shelf-break during the summer to fall period of favorable upwelling winds, and water temperature at the subsurface chlorophyll maximum in more offshore regions during the summer to fall period of stratification. Comparison of sediment trap results with corresponding information for underlying surface sediment has identified distinct strengths and limitations of using alkenones for purposes of reconstructing palaeoceanographic conditions in the northeast Pacific Ocean. The alkenones are quite sensitive to degradation in early diagenetic processes. The extent of degradation depends upon the sedimentary setting and challenges our usage of downcore records of alkenone content to assess even relative changes in prymnesiophyte productivity through time. Alkenone unsaturatiota patterns (UkT) recorded in sediments correspond with water temperature at the sea-surface in the winter-spring season, even
Prymnesiophyte productivity in the northeast Pacific Ocean
2075
though biomarker flux to the seabed is not restricted to this period of the year. Contributions from prymnesiophytes living within a subsurface chlorophyll maximum dominate alkenone flux during periods of thermal stratification in more offshore regions. Comparative studies of suspended particulate materials collected seasonally with depth in the euphotic zone, vertically transported particulate materials collected in sediment trap time series and surface sediments are needed to identify what fraction of the alkenone record preserved in open ocean sediments derives in general from productivity at subsurface depths in the euphotic zone. Acknowledgements--We thank C. Moser and P. Kalk for technical assistance in various aspects of field work, K. Brooksforce, P. Collier and B. Conard for preparation of sediment trap materials for chemical analysis and conducting the LECO analyses and P. A. Wheeler for the use of nitrate data. This research was supported by funds from NSF grants OCE 860936 (JD), 8911688 (RWC), 9000517 (FGP) and 9000945 (ML). NSF support (07831-01) for the core repository at Oregon State University is also gratefully acknowledged.
REFERENCES BRASSELLS. C., G. EGLINTON,I. T. MARLOWE,U. PFLAUMANNand M. SARNTHEIN(1986) Molecular stratigraphy: a new tool for climatic assessment. Nature, 320, 129-133. COALE K. H. and K. W. BRULAND (1987) Oceanic stratified euphotic zone as elucidated by 234Th:23Su disequilibria. Limnology and Oceanography, 32,189-200. DUGDALE R. C. and J. J. GOERING (1967) Uptake of new and regenerated forms of nitrogen in primary productivity. Limnology and Oceanography, 12, 196-206. EMERSONS. R. and J. I. HEDGES(1988) Process controlling the organic carbon content of open ocean sediments. Paleoceanography, 3, 621-634. HAXO F. T. (1985) Photosynthetic action spectrum of the coccolithophorid, Emiliania huxleyi (Haptophyceae): 19'hexanoyloxyfucoxanthin as antenna pigment. Journal of Phycology, 21,282-287. HICKEYB. M. (1989) Patterns and processes of circulation over the Washington continental shelf and slope. In: Coastal oceanography of Washington and Oregon, M. R. LANDRYand B. M. HXCKEY,editors, Elsevier, Amsterdam, pp. 41-115. Homo S. and H. OKADA(1974) Community structure of coccolithophores in the photic layer of the mid-Pacific. Micropaleontology, 20, 209-230. JASPERJ. P. and J. M. HAVES(1990) A carbon isotope record of CO2 levels during the late Quaternary. Nature, 347,462-464. LEE C., S. G. WAKEHAMand J. J. HEDGES(1988) The measurement of oceanic particle flux--are "swimmers" a problem? Oceanography, 1, 34-36. LONGHURST A. R. and W. G. HARRISON (1989) The biological pump: profiles of plankton production and consumption in the upper ocean. Progress in Oceanography, 22, 47-123. LYLE M., F. G. PRAHL and M. A. SPARROW(1992) Upwelling and productivity changes inferred from a temperature record in the central equatorial Pacific. Nature, 355,812-815. LYLE M., R. ZAHN,F. G. PRAHL,J. DYMOND,R. W. COLLIER,N. PISIASand E. StJESS (1992) Paleoproductivity and carbon burial across the California Current: the multitracers transect, 42°N. Paleoceanography, 7,251272. MARLOWEI. T., S. C. BRASSELL,G. EGLINTONand J. C. GREEN(1990) Long-chain alkenones and alkyl alkenoates and the fossil coccolith record of marine sediments. Chemical Geology, 88,349-375. MCCAFFREYM. A., J. W. FARRINGTONand D. J. REPETA(1990) The organic geochemistry of Peru margin surface sediments: I. A comparison of the C37 alkenone and historical E1 Nino records. Geochimica et Cosmochimica Acta, 54, 1671-1682. PARSONS T. R., M. TAKAHASHIand B. HARGRAVE(1984) Biological oceanographic processes, 3rd Edition, Pergamon Press, Oxford, 330 pp. PRAHL F. G., G. DELANGE, M. LVLE and M. A. SPARROW(1989) Post-depositional stability of long-chain alkenones under contrasting redox conditions. Nature, 341,434--437. PRAHL F. G., L. A. MUEHLHAUSENand D. L. ZAHNLE (1988) Further evaluation of long-chain alkenones as indicators of paleoceanographic conditions. Geochimica et Cosmochimica Acta, 52, 2303-2310.
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PRAHL F. G., L. MUEHLHAUSENand M. LYLE (1989) An organic geochemical assessment of oceanographic conditions at MANOP site C over the past 26,000 years. Paleoceanography, 4,495-510. PRAHLF. G. and S. G. WAKEHAM(1987) Calibration of unsaturation patterns in long-chain ketone compositions for palaeotemperature assessment. Nature, 33tl, 367-369. SANCETFAC. (1992) Comparison of phytoplankton in sediment trap time series and surface sediments along a productivity gradient. Paleoceanography, 7,183-194. SIKES E. L., J. W. FARRINGTONand L. D. KEIGWlN (1991) Use of the alkenonc unsaturation ratio U3k7 to determine past sea surface temperatures: core-top SST calibrations and methodology considerations. Earth and Planetary Science Letters, 104, 36~,7. SMALLL. F., G. A. KNAUERand M. D. TUEL (1987) The role of sinking fecal pellets in stratified euphotic zones. Deep-Sea Research, 34, 1705-1712. SOUTAR A., S. A. KLING, P. A. CRILL, E. DUFFRIN and K. W. BRULAND (1977) Monitoring the marine environment through sedimentation. Nature, 266, 136-139. SUESS E. (1980) Particulate organic carbon flux in the oceans--surface productivity and oxygen utilization. Nature, 288, 260-263. TAPPANH. (1980) Thepaleobiology of plant protists. W. H. Freeman, San Francisco, 1028 pp. TUREKIANK. K. and K. H. WEDEPOL(1961) Distributions of the elements in some major units ofthc earth's crust. Bulletin of the Geological Society of America, 72, 175-192. VOLKMANJ. K., G. EGLINTON,E. D. S. CORNERand J. R. SARGENT(1980) Advances in organic geochemistry 1979, A. G. DOUGLASand J. R. MAXWELL,editors, Pergamon Press, Oxford, pp. 219-227. WELIRV K., E. SUESS, C. A. UN~ERER, P. MULLERand K. FISCHER (1983) Problems with accurate carbon measurements in marine sediments and particulate matter in seawater. Limnology and Oceanography, 28, 1252-1259.
0967-0637/93 $6.00 + 0.00 © 1993 Pergamon Press Ltd
A biomarker perspective on prymnesiophyte productivity in the northeast Pacific Ocean F. G . PRAHL,* R . B . COLLIER,* J. DYMOND,* M . LYLE* a n d M . A . SPARROW*
(Received 13 July 1992; in revisedform 28 December 1992; accepted 6 January 1993) Abstract--Long-chain alkenones derived from prymnesiophyte algae were analysed in 1-year sediment trap time series (September 1987-1988) from three sites along a 630 km offshore transect at -42°N in the northeast Pacific Ocean. Biomarker flux monitored at 1000 m water depth was evident throughout the year at all sites and showed a consistent seasonal maximum in late spring which increased in amplitude with distance offshore. The integrated annual biomarker flux was constant along the transect, despite differences in seasonality between sites. Alkenone unsaturation patterns were remarkably uniform throughout the time series, reflecting an algal growth temperature of 10.6 _+ 1.1°C. This value corresponds to regional water temperature at the seasurface in winter. It recurs in seasonal upwelling near the coast and at the depth of the subsurface chlorophyll maximum offshore during seasons of stratification. These biomarker observations, interpreted in view of trap data for total organic (TOC) and inorganic carbon and ancillary hydrographic information, help to clarify seasonal productivity patterns for alkenone-producing prymnesiophytes in the northeast Pacific Ocean. Sediments accumulating with distance offshore along the sampling transect change from suboxic and Mn-reducing at the water-sediment interface to aerobic throughout the depths penetrated by box coring. Comparison of alkenone and TOC accumulation rates in surface (0-1 cm) sediments with corresponding annual fluxes integrated by the trap time series, shows that the fraction of both properties accounted at the seafloor is highest and similar under sub-oxic conditions (-25%), and declines steeply and disproportionately as aerobic conditions are encountered farther offshore. Only 0.25 and 3.1% of the annual inventory for alkenones and TOC in traps are accountable in surface sediments from the slowest accumulating, most oxidizing site farthest offshore. Despite major loss of biomarker to early diagenesis, surface sediments and trap particles display consistent alkenone unsaturation patterns. Results from this study provide a necessary background for palaeoceanographic reconstruction of the northeast Pacific Ocean from stratigraphic analysis of alkenone abundances, unsaturation patterns and isotopic compositions in sediment cores.
INTRODUCTION A SEPaES o f l o n g - c h a i n ( C 3 7 , C 3 8 , C 3 9 ) , p r i m a r i l y di- a n d t r i - u n s a t u r a t e d a l k e n o n e s , w a s d i s c o v e r e d in o r g a n i c - r i c h s e d i m e n t s f r o m t h e B l a c k S e a a n d W a l v i s B a y , a n d s u b s e q u e n t l y w a s d o c u m e n t e d w i d e l y in o c e a n s e d i m e n t s (BRASSELL et al., 1986). T h e c o c c o l i t h o p h o r i d Emiliania huxleyi h a s b e e n i d e n t i f i e d as a s o u r c e o f this s e r i e s (VOLKMAN et al., 1980). S y s t e m a t i c e x a m i n a t i o n o f p h y t o p l a n k t o n c u l t u r e s h a s r e v e a l e d t h a t E. huxleyi is n o t t h e e x c l u s i v e s o u r c e . H o w e v e r , t h e a l k e n o n e s r e m a i n r e s t r i c t e d
*College of Oceanic and Atmospheric Sciences, Oregon State University, Corvallis, OR 97331, U.S.A. 2061
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taxonomically to only a few genera within the class Prymnesiophyceae and are considered biomarkers of such phytoplankton (MARLOWEet al., 1990). Alkenone compositions in living cells of E. huxleyi have two unique attributes. Unsaturation patterns within the series provide a well-behaved index (uk7 = [C37:2]/([C37:2 ] -k- [C37:3]) of algal growth temperature, and total alkenone content of the cell is relatively constant independent of growth condition (PRAHL et al., 1988). Both characteristics suggest these compounds play some role in cell membrane architecture and processes, although their specific physiological function remains unknown. Because of these attributes, long-chain alkenones have now been explored in a palaeoceanographic context on a variety of geological time scales to assess changes in productivity (e.g. PRAHL et al., 1989), sea-surface temperature (SST) (e.g. BRASSELLet al., 1986; McCAFFREYet al., 1990; SIKESet al., 1991; LYLEet al., 1992) and pCO2 in the atmosphere (JASPERand HAYES, 1990). Various factors limit environmental interpretation in such applications. These biomarkers are susceptible to degradation in sedimentary processes (PRArILet al., 1989), and the dependence of degradation on depositional setting is poorly understood beyond a qualitative level. Consequently, it is not yet possible to separate effects of productivity and diagenesis on the sediment record for alkenone content. Despite major losses of total alkenone content, unsaturation patterns appear to be insensitive to diagenetic alteration (PRAHL et al., 1989; McCAFFREYet al., 1990). Therefore, the sedimentary u3k7 record provides a potentially accurate measure of algal growth temperature in the overlying water column. However, the relationship between average growth temperature recorded by uk7 and mean SST remains unclear because the productivity patterns for alkenone-producers in the oceans are poorly understood. Finally, the possibility of appreciable alkenone flux to sediments from production in upwelled waters or waters at subsurface depths within stratified euphotic zones (LONGHURSTand HARRISON, 1989) challenges the utility of uk7 and 613C measurements on alkenones as reliable proxies of SST or atmospheric pCO2, respectively. This paper presents results from alkenone analyses of trap-collected particles and underlying surface sediments from three sites along an offshore transect at 42°N, in the northeast Pacific Ocean (Fig. 1). The data are from a one-year sediment trap deployment at 1000 m water depth in which samples were collected at approximately bimonthly intervals. The time series identifies when alkenone-producers are productive at each site and how the seasonality of productivity varies spatially in t-his region. We use U~7 values and contemporary hydrographic data to constrain the depth of alkenone production at each site. Also, we are able to estimate alkenone preservation at each location by comparing the annual integrated flux through 1000 m water depth with accumulation rates in underlying surface sediments. These results illuminate the strengths and limitations of using alkenone analyses for palaeoceanographic reconstruction of the northeast Pacific Ocean. EXPERIMENTAL METHODS Sample collection
All samples analysed in this study were collected in the first year of Multitracers, a project designed to monitor changes in particle flux and sediment accumulation across a gradient in primary productivity associated with the California Current System (LYLEe t
Prymnesiophyte productivity in the northeast Pacific Ocean
2063
I I I
47*
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/
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200 t
130 °
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Fig. 1. Map showing the region in the northeast Pacific Ocean where the three sampling sites (Nearshore, Midway, Gyre) are situated (solid diamonds)• The location of two NOAA weather buoys (No. 46027: 41.8°N, 124.2°W;No. 46002: 42.5°N, 130.4°W)is also indicated (open boxes). Solid circles depict sites farther north along the continental margin off Washington state where the alkenone composition of surface sediment has been previously reported (PRAIJLet al., 1988).
al., 1992). Particle flux was defined at three sites in the northeast Pacific Ocean by samples from sediment traps moored at 1000 m water depth. The three sites (Nearshore, Midway and Gyre) are situated -120, 270 and 630 km, respectively, off the coast of northern California along 42°N (Fig. 1). Each trap was equipped with six sampling cups that opened and closed sequentially at approximately bimonthly intervals over the one-year deployment time of each mooring (22 September 1987-16 September 1988). Trap construction was a modification of a previous design (SoUTARet al., 1977) and featured all plastic and fiberglass materials, a 2:1 height to diameter cone with 0.5 m 2 collecting area, and a honeycomb baffle at the mouth of the cone to limit turbulence and minimize particle sampling bias. Box cores were collected at Nearsfiore (2712 m water depth), Midway (3111 m water depth) and Gyre (3680 m water depth) on the deployment cruise (W8709A) for the sediment trap moorings using a 25 x 25 cm standard box corer. Gravity and piston cores penetrating the Late Pleistocene also were recovered from these sites at the same time. Sedimentation rates established by 6180 stratigraphy and 14Cdates for the cores averaged -20, 10 and 1.3 cm ky -1, respectively (LYLEet al., 1992). Chemical analyses Subsamples of particles collected in each sediment trap cup and surface (0-1 cm) box core sediments from the three sites were analyzed for long-chain alkenone content and
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composition, total organic (TOC) and inorganic (CaCO3) carbon content (Table 1). Lipid fractions enriched in long-chain alkenones and structurally related alkenoates (MARLOWE et al., 1990) were isolated from samples of freeze-dried trap particles and wet surface sediments and analysed by published methods (PRAHLand WAKEHAM,1987; PRAHLet al., 1989). All conditions for alkenone analysis by capillary gas chromatography were the same as previously described except for the use of a fused silica column (0.25 ktm film thickness, 30 m length × 0.32 mm i.d.;J&W Scientific) containing a methylsilicone (DB-1) rather than phenylmethylsilicone (DB-5) bonded phase. Selection of the DB-1 bonded phase improved resolution of the diunsaturated C36 methyl ester (ME) from the C37:2 methyl ketone, but merged the diunsaturated C36 ethyl ester (EE) with the C3s:3 ethyl ketone (PRAHL et al., 1988). TOC and CaCO3 content of trap particles and sediments were determined sequentially on each sample using a LECO analyser and the wet chemical technique of WEENSYet al. (1983). RESULTS AND DISCUSSION Seasonal fluxes o f alkenones
The vertical flux of alkenones through 1000 m water depth showed a common seasonal pattern at Nearshore, Midway and Gyre (Table 1). Fluxes were lowest in the fall to late winter period (cups 1-3), increased in early spring (cup 4) at Gyre, followed by a pronounced maximum in late spring (cup 5, mid-April to mid-June) at all three sites, then declined in summer to the levels observed at corresponding sites at the start of the time series (Fig. 2C). Although the timing of the peak in alkenone flux was synchronous at the three sites, the amplitude increased significantly offshore along the transect. Alkenone flux measured in cup 5 was ~ 2 x (Nearshore), ~ 6 x (Midway) and ~20x (Gyre) greater than that for the average of the other cups. These results imply that alkenone-producers are productive over the entire year, and oceanographic conditions extant during the latespring are conducive to a large-scale, synchronized bloom for these primary producers throughout the northeast Pacific Ocean. TOC and CaCO3 flux also varied seasonally in the trap series (Table 1). The coccolithophorid Emiliania huxleyi (Homo and OKADA,1974), an important primary producer in the ocean over the past -270 ky (Thai'AN, 1980), is a key representative of the alkenoneproducing prymnesiophytes living in today's ocean. Therefore, significant correlation between TOC, CaCO3 and alkenone flux might be expected. If the complete data set for the time series is considered, however, the correlation between TOC and alkenone flux (r 2 = 0.17) or between CaCO 3 and alkenone flux (r 2 = 0.014) is poor. Omitting all data for cup 5, TOC and CaCO3 fluxes correlate reasonably well with alkenone flux (r 2 = 0.75 and 0.67, respectively). Either alkenone-producers in surface waters are only minor contributors to the vertical flux of TOC and CaCO3 at these sites (SANCErrA, 1992), or decomposition and dissolution in the upper 1000 m decouple TOC and CaCO3 from the alkenones. Interestingly, no such decoupling occurred between the TOC and CaCO3 flux. These two properties are strongly correlated in the overall data set (r 2 = 0.67). We believe that alkenone-producing phytoplankton are only minor contributors to TOC and CaCO3 flux. The study of laboratory cultures (PRArlLet al., 1988) has shown that the alkenone content of E. huxleyi is constant (1.2 + 0.28 pg cell-l), independent of growth conditions, and constitutes a large percentage of total cellular organic carbon
N/A N/A N/A N/A N/A
340 0.87 0.00 0.44 11.9
0.68 0.19 0.053 18
270 0.97 0.04 0.44 11.8
295 0.98 0.00 0.42 11.2
0.21 0.098 0.019 N/A
1.9 0.47 0.11 30
200 1.09 0.12 0.45 12.2
320 0.92 0.13 0.42 11.2
0.9 0.25 0.07 21
8.5 1.1 0.33 68
12.8 1.3 0.43 140
Cup 2 10/25-12/24
400 0.96 0.00 0.40 10.5
0.36 0.90 0.025 10
290 1.02 0.09 0.43 11.6
6.4 1.9 0.25 72
180 0.85 0.12 0.42 11.3
25.8 2.1 0.67 120
Cup 3 12/24-2/22
560 1.06 0.00 0.38 10.0
2.6 0.75 0.13 74
290 1.12 0.17 0.42 11.2
8.7 2.0 0.35 100
240 1.12 0.23 0.37 9.8
20.7 2.8 0.69 170
Cup 4 2/22--4/22
2020 1.02 0.02 0.33 8.4
2.5 0.36 0.34 680
830 1.07 0.03 0.33 8.5
4.1 0.90 0.40 330
550 0.94 0.02 0.33 8.6
5.5 1.0 0.51 280
Cup 5 4/22~5/21
260 0.99 0.00 0.36 9.3
0.93 0.44 0.090 23
410 0.99 0.03 0.42 11.3
1.6 0.37 0.15 63
515 1.07 0.01 0.39 10.4
6.4 1.0 0.27 140
Cup 6 6/21-9/16
*K37/K3s: ratio of total C37-C38alkenone abundance; ME/K37: ratio of C 36 methyl alkenoate to total C 37 alkenone abundance. tWater temperature estimate from the calibration equation uk7 = 0.034 × T + 0.039 (PRAHLet al., 1988). :~Integrated annual average for time series.
Fluxes Mass (mg cm -2 )~-1) CaCO 3 (mg cm -2 y 1) TOC (mg cm -2 y - l ) Alkenones (ng cm -2 y-l) Compositions Atkenones (,ug gC- 1) K37]K38 ME/K37 U3k7 T (°C)*
Gyre
Fluxes Mass (mg cm -2 ),-1) CaCO3 (mg cm -2 y-l) TOC (mg cm -2 y) Alkenones (ng cm -2 y-l) Compositions Alkenones (,ug gC- l) K37/K3s ME/K37 Uak7 T(°C)
Midway
Fluxes Mass (mg cm -2 y-l) CaCO3 (mg cm -2 y - l ) TOC (mg cm -2 y - l ) Alkenones (ng cm -2 y - 1) Compositions Alkeuones ~ g gC -1 ) K37/K38* ME/K37* U~7 T(°C)t
Nearshore
Cup 1 9/22-10/25
100 1.18 0.24 12.0
1190 1.02 0.02 8.7
0.0034 0.35
0.6
11.4
9.9
1.3 0.44 0.11 140
210 1.16 0.24
470 1.05 0.06
0.050 11
3.8
11.1
10.1
3.96 1.00 0.23 110
260 1.14 0.26
0.13 33
7.0
Sediment
320 1.00 0.09
12.8 1.54 0.47 150
Ave:~
TOC, CaCO 3 and alkenone data from analysis of sediment trap particles collected in time series (22 September 1987 - 16 September 1988) at 1000 m water depth and of underlying surface (0-1 cm) sediments from three sites in the northeast Pacific Ocean (Nearshore, Midway and Gyre; Fig. 1)
Sampling periods
Table 1.
© P~
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o ~r
2066
F.G. PRAHLet
al.
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i
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15
lo.
5 2O
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15
, !
.
i' I
.
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•
•
.
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•
. . . . . .
"~600
~
.
.
.
.
.
.
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..... Nay
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....... May
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Sept
Julian Day (since 1987) Fig. 2. Water temperature estimates from the analysis of alkenone unsaturation patterns (ok7) in the sediment trap time series for the Nearshore (A), Midway (B) and Gyre (B) sites are compared with the annual records for sea-surface temperature (SST) monitored hourly at 1 m water depth at two NOAA weather buoys located at the shelf break (No. 46027) and a more remote offshore site (No. 46002) (Fig. 1). Panel (C) displays the record for total alkenone flux in each sediment trap time series. The specific time intervals between 22 September 1987 and 16 September 1988 for each sampling cup in the sediment trap time series are defined in Table 1.
(8.0 + 2.9%). Alkenone concentrations normalized to T O C in sediment trap particles from the time series range from ~200 to 2000/~g gC -1 (Table 1). Using the ratio of concentrations measured in sediment trap particles to that expected for the living biomarker source suggests that alkenone producers contribute only 0.25-2.5% to the observed T O C fluxes. This estimate of source contribution to T O C is accurate only if the
Prymnesiophyteproductivityin the northeast PacificOcean
2067
fixed proportion of alkenone to organic carbon observed in the living algal cell is not disrupted significantly in the production of sedimentary particles. Nonetheless, the low estimates obtained by this exercise are maximum contributions, unless alkenones are more labile than cellular organic carbon during early sedimentation processes. The latter possibility seems unlikely at present (VOLgMAN et al., 1980), although it cannot be discounted yet on full experimental grounds. Annual fluxes of alkenones
An annual alkenone flux through 1000 m water depth at each site was calculated by averaging the time weighted individual fluxes (Table 1). The range of annual flux along this transect was 100-150 ng alkenone cm-2 y-1, close to constant. In contrast, the average annual fluxes for TOC and CaCO3 (Table 1) both decreased steadily offshore, -4-fold along the transect. Alkenone concentration reconstructed for average trap particles varied from 320 #g gC-1 at Nearshore through 470 #g gC-1 at Midway to 1190 #g gC-1 at Gyre. Thus, annual export productivity for alkenone-producing prymnesiophytes appears relatively constant over a wide spatial range in the northeast Pacific Ocean and comprises an increasing fraction of primary productivity seaward. Such inferences about prymnesiophyte productivity assume that alkenones are degraded similarly in the upper water column at all three sites, and that alkenone, TOC and CaCO3 fluxes measured in sediment traps relate directly to primary productivity in surface waters (e.g. SUESS, 1980). These assumptions seem credible but are equivocal and require more rigorous examination. Seasonal variations in alkenone unsaturation patterns
Alkenone unsaturation patterns were defined by measurement of U3k7in all samples collected in the sediment trap time series. Values range from 0.33 to 0.45, averaging 0.40 _+ 0.04 in the complete data set (n = 17, Table 1) and show that the composition of the alkenone series has remarkable uniformity in this region of the ocean. Unsaturation patterns in the aikenone series are related to the growth temperature of the prymnesiophyte source (BgASSELLet al., 1986). Laboratory study of a single strain of E. huxleyi has shown the relationship between U3k7and growth temperature is linear (U3k7 = 0.034 X T + 0.039, r 2 = 0.994) over the range 8-25°C (PRAHLet al., 1988). PRAHLand WAKEnAM (1987) and SIKES et al. (1991) tested this calibration equation in the field and concluded it provides realistic estimates of the water temperature associated with prymnesiophyte growth over a large geographic range of ocean conditions. Consequently, uk7 measures in the sediment trap time series were converted to water temperature estimates (Table 1), assuming the calibration equation also applies to the alkenoneproducing biomass in the northeast Pacific Ocean. The observed range of uk7 (0.33-0.45) corresponds to water temperatures between 8.4 and 12.1°C, averaging 10.6 + 1.1°C (n = 17). Inspection of the data (Fig. 2A and B) reveals that the recorded water temperature is not constant but follows a common seasonal pattern at Nearshore, Midway and Gyre. The lowest estimates (-8.5°C) were from trap particles collected in late spring (cup 5), the period corresponding to maximum alkenone flux at each site (Fig. 2C). A purely diagenetic process cannot explain the similarities between each time series. Despite substantial degradation of total alkenones in sedimentary processes, the unsaturation
2068
v.G. PRAHLet al.
pattern in this biomarker series, once set, appears insensitive to alteration (e.g. PRAHLet al., 1989). The consistently low temperature estimate for cup 5 at all three sites more likely requires a biological explanation, For example, the prymnesiophyte assemblage contributing to alkenone flux may change systematically throughout the year and unsaturation patterns in species predominant during the productivity event in late spring could respond somewhat differently to temperature than suggested by the calibration equation for a single strain of E. huxleyi. The observation also might be explained biologically without invoking violation of the uk7 versus temperature calibration, however. The oceanographic process triggering the large-scale productivity event for alkenone producers throughout the region (Fig. 2C) may have distinctive hydrographic characteristics as reflected accurately by lower apparent growth temperature. A case is made in the following discussion for biological rather than geochemical factors controlling the uk7-based temperature record in trapped particles. Evidence for biological control on seasonal variations in unsaturation patterns
The alkenones occur as a series of C37, C3s and C39 homologues and are often accompanied by structurally related C36 methyl and ethyl alkenoates (MARLOWEet al., 1990 and references therein). Evidence for a seasonal shift in the prymnesiophyte species contributing to the alkenone record in trap particles is potentially imbedded in the overall composition of the biomarker series. Various compositional properties of the biomarker series were examined for this reason. Values for the proportion of total C37--C3s aikenones, monitored in each time series (K37/K38 values, Table 1), range from 0.85 to 1.12 but show no coherent seasonal variation within or between time series. The weighted annual average for K37/K3s is virtually indistinguishable at each site (-1.02, Table 1). If the prymnesiophyte species controlling alkenone flux change seasonally or differ between sites, it is not discerned by K37/K38 measurements. Values for this property measured in sediment trap particles and underlying sediments from the northeast Pacific Ocean (Table 1) are lower than those reported for a single strain of E. huxleyi grown in laboratory culture (PRAHL et al., 1988), but the difference is small and considered insignificant. Methyl and ethyl alkenoates structurally related to the aikenones were typical of lipid compositions isolated from many of the trap samples and all surface sediments. Values for the proportion of C36:2 methyl alkenoate (ME) (PRAHLet al., 1988) to total C37 alkenones were monitored in each time series (ME/K37 , Table 1) and display different temporal trends among sites. An abrupt shift occurs at Nearshore from high ME/K37 values in cups 1-4 (0.12-0.23) to low values in the remaining series (0.011-0.023). At Gyre, ME/K37 values as low or lower than those in cup 5-6 of Nearshore occur throughout the year. The situation at Midway is intermediate between the other two sites. Laboratory cultures of E. huxleyi display the range of compositions observed in these time series, but only if grown over a wide range of temperatures (8-25°C, PRAHLet al., 1988). Because the observed range of u3k7values observed in the overall data set implies very little variation in growth temperature, we infer that the observed behavior for ME/K37 in trap particles results from spatial and temporal variations in the assemblage of prymnesiophyte species contributing to the vertical alkenone flux. Nonetheless, the inference of a seasonal change in species assemblage is not proven by these data. Preferential degradation of alkenoates and alkenones also must be considered
Prymnesiophyteproductivityin the northeastPacificOcean
2069
when variations in ME/K37 values are explained. Preferential degradation may not control the sediment trap observations for ME]K37, but it could be important in the longer term sedimentary geochemistry of these biomarkers. ME/K37 values of average trap particles decrease along the transect and are -3-fold (Nearshore), 4-fold (Midway) and 10-fold (Gyre) lower than values recorded in underlying surface sediments (-0.25, Table 1). If the particle flux measured in the trap series accurately represents the average annual input to underlying surface sediment, then alkenoates must be preserved more efficiently than alkenones at some early stage in the sedimentary process. A l k e n o n e unsaturation patterns a n d trap-sediment comparisons
For each sediment trap time series, an annual uk7 value was calculated by averaging the sum of all individual measurements weighted for the quantity of total alkenones collected in respective cups. These values were converted into estimates of average annual water temperature recorded by the alkenones transported through 1000 m water depth using the calibration equation for uk7 versus temperature. The estimates are essentially the same for Nearshore and Midway (-10°C) and somewhat lower for Gyre (8.7°C). Average water temperatures estimated from uk7 measurements for underlying surface sediments at corresponding sites are - I ° C warmer than the trap-based temperatures for Nearshore and Midway and -3.3°C warmer for Gyre (Table 1). We consider the large temperature difference in the trap-sediment comparison for Gyre real and provide a geochemical explanation. The percentage of the annual alkenone flux through 1000 m water depth preserved in underlying sediments declines steeply along the transect from 22% at Nearshore to <1% at Gyre (Table 2). Extensive degradation of alkenones produced during the high flux period in late spring (cup 5, Table 1) is required to eliminate >99% of the presumed sedimentary input at Gyre. uk7 from this trap interval is noticeably lower than at all other times (Fig. 2A and B). Consequently, if the fraction of total flux surviving burial were disproportionately lower during the time period represented by cup 5, uk7 values preserved in sediments would appear higher than the weighted annual average for traps. This mechanism does not require selective degradation of the more Table 2. TOC and alkenone preservational efficiencies estimated by comparison of average annual trap (I000 m water depth)flux with surface sediment (0--1 cm) accumulation rate at the Nearshore (2712 m water depth), Midway (3111m water depth) and Gyre (3680m waterdepth) sites
Traps TOC (~g cm-2 y-l) Nearshore Midway Gyre Aikenones (ng cm-2 y-l) Nearshore Midway Gyre
470 230 110 150 110 140
Sediments % Preserved* 130 50 3.4 33 11 0.35
28 22 3.1 22 10 0.25
*Preservational efficiencydefinedby ratio of sediment accumulation rate to trap flux,expressedas a percentage.
2070
F.G. P~I~Let al.
unsaturated alkenones per se, although that would be the apparent effect on the integrated alkenone composition preserved in sediments. Although such a mechanism is yet only hypothetical, it would also account for the less pronounced, but similar temperature offset in trap-sediment comparisons for Nearshore and Midway. Relationship o f alkenone unsaturation to hydrographic conditions
Two NOAA weather buoys monitoring sea-surface temperature (SST) hourly are moored close to the multitracers sampling transect. One mooring is landward of Nearshore on the continental shelf break (No. 46027), and the other is roughly equidistant between Midway and Gyre (No. 46002) (Fig. 1). The annual SST record for the buoy at the continental shelf break (Fig. 2A), shows cold water (10-12°C) at the surface throughout the year with signs of episodic, wind-induced upwelling events. Such upwelling events driven by strong northerly winds occur frequently in coastal regions above -40°N, in the northeast Pacific Ocean from late spring to fall (HICKEY, 1989 and references therein). The record for the weather buoy farthest from land (Fig. 2B) shows a smoother annual cycle of summertime heating and stability versus wintertime cooling and deep mixing expected in regions of the northeast Pacific Ocean remote from the influence of coastal upwetling. SST comparable to the uniform water temperature (10-12°C) estimated by U~7 in sedimentary materials collected along the -500 km sampling transect are detected at both weather buoys throughout the winter to early spring (Fig. 2A and B). Similar SST estimates (PRAHL et al., 1988) are obtained from the alkenone record preserved in sediments located 440-550 km farther north on the Washington margin (Fig. 1). Although u3k7 values recorded in sediments correspond to the coldest seasonal SST, it does not follow that the prymnesiophyte species are only productive in winter to early spring in this region. Our sediment trap data show appreciable alkenone flux throughout the year at all three sites (Fig. 2C). SST warms to -18°C in summer at offshore sites such as Gyre (Fig. 2B). Therefore, the consistent u3k7 temperature estimates in the summer trap samples from Gyre suggest that alkenone flux derives from productivity in colder, subsurface waters within the euphotic zone. Figure 3 displays a typical depth profile for water temperature and chlorophyll fluorescence in late summer at Gyre. The upper water column is thermally stratified as expected by inference from the annual SST record for the offshore weather buoy (Fig. 2B). Chlorophyll fluorescence is low and constant throughout the surface mixed layer and underlain by a pronounced subsurface chlorophyll maximum (SCM) in the upper thermocline. The water temperature at the SCM is -12°C, close to the U~7-predicted temperature of trap particles collected at this time of year (Table 1). This correspondence suggests that alkenone production during periods of offshore stratification in the northeast Pacific Ocean occurs at the SCM rather than in the surface mixed layer. The key alkenone producer in today's ocean, E. huxleyi, biosynthesizes the carotenoid 19'-hexanoyloxyfucoxanthin as a major accessory pigment which enhances photosynthetic effectiveness in the spectral interval 500-550 nm (Haxo, 1985). These wavelengths are among the most penetrative in seawater, comprising much of the residual spectrum deep in the euphotic zone (PARSONSet al., 1984). Thus, E. huxleyi and perhaps other alkenone producers are suited for growth in the low light regime of the SCM. Figure 3 also displays a depth profile for nitrate in the thermally stratified offshore water column in summer to early fall. The SCM is situated at the top of the nitricline. Conditions for alkenone
Prymnesiophyteproductivityin the northeastPacificOcean r (oc)
2071
.....
Fluorescence (rel. units) - - 5 10 15 20 0
t
~. 20
.
.
.
.
a
.
.
.
.
I
.
.
.
.
i
/ i i
40
. . . . . ~'h
O
.'" 60
t (
._/
80 ..~........:............................ 0.0
1.0 2.0 3.0 NO3 - ( / z M ) . - - .
4.0
Fig. 3. Profiles for water temperature, chlorophyll fluorescence and nitrate concentration measuredwithdepth beneath the sea-surfaceat Gyrcin September 1989. production may be optimum within the SCM because the algal source is adapted for photosynthesis under low ambient light, and because nutrients such as nitrate, virtually absent in the surface mixed layer, are replete at this depth. The association of the SCM with the top of the nitricline is a common feature in many open ocean environments, at least during some portion of the year (LONGHURSTand HARRISON, 1989). The euphotic zone in such settings has been modelled as a two-layered biological system: an upper oligotrophic layer and a lower eutrophic layer (DoGDALEand GOERING, 1967; COALE and BRULAND, 1987; SMALL et al., 1987). The upper layer corresponds to the surface mixed layer and is characterized by relatively high rates of primary productivity but low rates of sedimentary export ("new production"). Low new production results because of tight coupling between trophic levels within the upper layer and, consequently, efficient biological recycling. The lower stratified layer encompasses the SCM and is characterized by reduced rates of primary productivity but higher new production than above because of less efficient biological recycling. Alkenone data from the sediment trap time series are consistent with a two-layered biological system in stratified offshore waters of the northeast Pacific Ocean. The correspondence between predicted algal growth temperature and measured water temperature at the SCM and a maximum in alkenone concentration at the SCM (AMTHOR, unpublished data) shows at least circumstantially that a prymnesiophyte biomass contributing to the SCM is photosynthetically viable and influences the vertical TOC flux to the seafloor. Some fraction of the alkenone content of Nearshore, Midway and Gyre sediments derives from prymnesiophyte production in upwelled waters and/or in stratified waters at the base of the euphotic zone (Table 1). Such contribution to the record certainly complicates the relationship between atmospheric pCO2 and the isotopic composition (613C) of alkenones preserved in underlying sediments from this region because the inorganic carbon fraction fixed photosynthetically in these waters is not equilibrated with
2072
F.G. PRArILet al.
the atmosphere. If future molecular isotopic analyses reveal in cores from the northeast Pacific a systematic trend between 6 values and sediment age (e.g. JASPERand HAYES, 1990), a more complex process than direct coupling with atmospheric pCO2 changes must be invoked to explain the observation.
Water column-surface sediment comparisons for alkenones TOC and alkenone accumulation rates (Table 1) were calculated from the product of respective concentrations in surface (0-1 cm) sediment from Nearshore, Midway and Gyre and average sedimentation rate estimated for each site (see Experimental Methods). Accumulation rates for both TOC and alkenones show an offshore decrease. TOC accumulation decreases by a factor of 30, much more than the 4-fold decrease in TOC flux observed in trap particles collected at 1000 m water depth. Alkenone accumulation rates along the transect exhibit an even greater contrast to the trap fux, being 100 times lower at the Gyre site than at the Nearshore site. Average annual fluxes measured by traps showed virtually no difference between sites. Consequently, the ratio of alkenone to TOC in surface sediments decrease from -260 at Nearshore, 210 at Midway to 100/~g gC -1 at Gyre (Table 1). If supply is the dominant factor controlling the TOC and alkenone content of sediments, our data imply a 2.5-fold offshore decrease in prymnesiophyte productivity relative to total primary productivity. Because this trend is opposite to that of the trap data, such an interpretation is most likely wrong.
Dependence of alkenone preservation on sedimentary conditions We have determined the TOC and alkenone preservational efficiency at each site from comparison of sediment accumulation rate with average annual trap flux (Table 2). Preservational efficiency for both properties is highest and roughly equivalent (-25%) at Nearshore and declines disproportionately seaward. The low estimates of TOC and alkenone preservation at Gyre (3.1 and 0.25%) are similar to those previously documented for the central equatorial Pacific (Manop site C) where accumulation rates for TOC (3.6/~g cm -2 y-1) and alkenones (0.33 ng cm -2 y-~) in surface sediments (4287 m water depth) represented - 2 . 1 % and 0.65 % of corresponding annual flux measured 500 m above bottom (PRAHLet al., 1989). We must explain: (1) why the two reference points, 1000 m traps and surface sediments, infer different offshore trends for the prymnesiophyte to total phytoplankton assemblage; and (2) why calculated TOC and alkenone preservationai efficiencies vary between Nearshore, Midway and Gyre. Either the sediment traps poorly sampled the average TOC and alkenone input to underlying sediments or diagenetic effects operating at the seafloor selectively altered the sediment records of these properties. The former possibility is a perennial criticism levied against all sediment trap studies (e.g. LEE et al., 1988) and cannot be dismissed. But observations from further geochemical examination of sediments accumulating at these locations and reference to current literature show that diagenesis is a key consideration in explaining both inquiries. The total aluminum and manganese content of sediments at Nearshore, Midway and Gyre reveals an offshore gradient in redox conditions at the seafloor, Surface sediments from box cores collected at all three sites contain 7-8 weight per cent of aluminum (multitracers, unpublished data), which is similar to the average abundance of AI in shales
Prymnesiophyte productivity in the northeast Pacific Ocean
Mn Enrichment Foctor 5 10 15 20 25
0 . .
5
10
E 15 "~ 20
2073
.
.
i
,
.
.
.
i
.
.
.
.
i
.
.
.
.
i
.
.
.
.
if----,i
c-
o. 25 ID
a
~ 3O-
c~ 35. 40, 45. 5O
e - .e o. • . t R o a ~
Fig. 4. Profiles displaying enrichment factors for reducible manganese with depth in box cores from Nearshore, Midway and Gyre. The Mn-enrichment factor is defined by the ratio of Mn/Al values measured in a given sediment interval to the Mn/A1 value for average shale (0.011; TUREKIANand W E D E P O L , 1961). Both elements were measured by instrumental neutron activation analysis (Multitracers, unpublished data).
and other crustal rocks (8% by weight, TUREKIANand WEDEPOL, 1961). This indicates that crustally eroded aluminosilicates are the major components of bulk surface sediment at all sites. We have normalized the downcore Mn/A1 values to the Mn/A1 composition of average shale (0.011; TUREKIANand WEDEPOL, 1961) in order to define how reducible manganese content varies with sediment depth at each site (Fig. 4). Nearshore sediments show virtually no Mn-enrichment above crustal abundance at all sediment depths, indicating suboxic, Mn-reducing conditions extend to the water-sediment interface. Midway sediments display a 25-fold enrichment near the surface decreasing to near crustal abundance by 7 cm depth. Thus, these sediments are suboxic and Mn-reducing at a shallow depth beneath the water-sediment interface. Gyre sediments are enriched 10-15-fold above the crustal abundance for Mn throughout the core and must be oxic over the - 5 0 cm depth range penetrated by box coring. We suggest that contrasting redox conditions lead to differences in alkenone relative to TOC preservation. Alkenones, like TOC, are susceptible to degradation in sediments under the complete range of redox conditions. Examination of an organic-rich turbidite interval deposited on Madeira Abyssal Plain (MAP) revealed - 8 5 % loss of alkenones from the record as a consequence of aerobic degradation (PRAHL e t al., 1989). Alkenone degradation was - 3 0 % greater than that of TOC. This result does not conflict with the much greater aerobic degradation of alkenones relative to TOC at Gyre and in the central equatorial Pacific. Differences in depositional context can explain the discrepancy. The trap-sediment comparisons have assessed the impact of aerobic degradation on alkenones and TOC in fresh organic debris arriving for the first time at the seafloor. The MAP study, on the other hand, assessed the secondary impact of aerobic degradation on alkenones and TOC that had already survived destruct,ion in passage through a water-sediment interface in the source region for the turbidite.
2074
F . G . PRAnL et al.
The estimates of preservational efficiency from the trap-sediment comparisons support the following viewpoint. Alkenones are at least as reactive as TOC in sediments under the complete span of anaerobic to aerobic sedimentary conditions. Preservation for both properties declines in slower accumulating, more oxidizing sediments, but alkenones degrade preferentially to TOC along such a gradient. Thus, even if the blend of alkenone and TOC introduced to the bottom were the same at two sites, the concentration of alkenone (/gC) would be lower in slower accumulating, more oxidizing sediments. Assuming the sediment trap time series provided reasonable measures of the average alkenone to TOC composition raining into sediments at Nearshore, Midway and Gyre, the assessed dependence of preservational efficiency on sedimentary conditions at the seafloor emphasizes an important geochemical point. Diagenetic processes occurring at the seafloor complicate our ability to hindcast even relative changes in prymnesiophyte productivity from the sediment record of alkenone accumulation rate. This problem is well-recognized in relating TOC accumulation rate to primary productivity (EMERSONand HEDrES, 1988 and references therein). Properties such as alkenone flux and concentration normalized to TOC may still provide valuable clues for palaeoceanographic reconstruction assuming a regular relationship exists between organic preservation and sedimentary conditions, the relationship can be defined by empirical means and this relationship is used in the data interpretation. CONCLUSIONS
Geochemical analysis of sediment trap particles collected in time series have clarified productivity patterns for alkenone producers in the northeast Pacific Ocean. The productivity of these phytoplankton occurs throughout the year but displays a conspicuous seasonal pattern. Yet unspecified oceanographic conditions associated with the spring transition from deep winter mixing to episodic upwelling near the coast and stratification in more remote oceanic locations are conducive to regional-scale blooms of alkenone producers. The amplitude of the blooms above the background productivity for the rest of the year increases offshore. The integrated annual productivity for these organisms, on the other hand, appears independent of setting, despite an increasing seaward importance of seasonality. In contrast, the integrated annual TOC flux infers that total primary productivity declines significantly offshore. Thus, alkenone producers contribute increasingly to total primary productivity along the offshore gradient. The growth temperature inferred for alkenone producers throughout the year is 10-12°C. The narrow range corresponds well with sea-surface temperature in winter to spring throughout this region, sea-surface temperature in the vicinity of the shelf-break during the summer to fall period of favorable upwelling winds, and water temperature at the subsurface chlorophyll maximum in more offshore regions during the summer to fall period of stratification. Comparison of sediment trap results with corresponding information for underlying surface sediment has identified distinct strengths and limitations of using alkenones for purposes of reconstructing palaeoceanographic conditions in the northeast Pacific Ocean. The alkenones are quite sensitive to degradation in early diagenetic processes. The extent of degradation depends upon the sedimentary setting and challenges our usage of downcore records of alkenone content to assess even relative changes in prymnesiophyte productivity through time. Alkenone unsaturatiota patterns (UkT) recorded in sediments correspond with water temperature at the sea-surface in the winter-spring season, even
Prymnesiophyte productivity in the northeast Pacific Ocean
2075
though biomarker flux to the seabed is not restricted to this period of the year. Contributions from prymnesiophytes living within a subsurface chlorophyll maximum dominate alkenone flux during periods of thermal stratification in more offshore regions. Comparative studies of suspended particulate materials collected seasonally with depth in the euphotic zone, vertically transported particulate materials collected in sediment trap time series and surface sediments are needed to identify what fraction of the alkenone record preserved in open ocean sediments derives in general from productivity at subsurface depths in the euphotic zone. Acknowledgements--We thank C. Moser and P. Kalk for technical assistance in various aspects of field work, K. Brooksforce, P. Collier and B. Conard for preparation of sediment trap materials for chemical analysis and conducting the LECO analyses and P. A. Wheeler for the use of nitrate data. This research was supported by funds from NSF grants OCE 860936 (JD), 8911688 (RWC), 9000517 (FGP) and 9000945 (ML). NSF support (07831-01) for the core repository at Oregon State University is also gratefully acknowledged.
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