Quaternary Science Reviews 82 (2013) 78e92
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Quaternary Science Reviews
journal homepage: www.elsevier.com/locate/quascirev
Biological and climatic consequences of a cold, stratified, high latitude
ocean
James D. Hays a, *, Douglas G. Martinson b, Joseph J. Morley c
a
Columbia University, Lamont Doherty Earth Observatory, P.O. Box 1000 Palisades, New York 10964, USA
Lamont Doherty Earth Observatory, Dept of Earth and Environmental Sciences, Columbia University, USA
c
Lamont Doherty Earth Observatory, USA
b
a r t i c l e i n f o
a b s t r a c t
Article history:
Received 16 August 2012
Received in revised form
16 September 2013
Accepted 24 September 2013
Available online 5 November 2013
The flux from deep- and shallow-living radiolarian assemblages provides evidence of a glacial, high
latitude, cold ocean stratification that increased biological pump efficiency and promoted ocean carbon
sequestration. Greater deep (>200 m) than shallow-living (<200 m) radiolarian assemblage flux characterizes glacial North Pacific (>45 N) sediments with the deep-living Cycladophora davisiana dominant
(>24%). By contrast modern radiolarian flux consists primarily of shallow-living species (C. davisiana
<10%). Clues to the cause of this unusual glacial radiolarian flux come from the presently, strongly
stratified Sea of Okhotsk. Here beneath a thin nutrient depleted mixed layer radiolarian and zooplankton
faunas conform to the sea’s physical stratification with lower concentrations of both in a Cold (1.5 to
1 C) Intermediate Layer (CIL) (20e125 m) and higher concentrations in waters between 200 and 500 m
(Nimmergut and Abelmann, 2002). This biological stratification generates a radiolarian flux echoing that
of the glacial northwest Pacific with C. davisiana 26% of total flux. Widespread C. davisiana percentages
(>20%) in high latitude (>45 ) glacial sediments of both hemispheres is evidence that these oceans were
capped with an Okhotsk-Like Stratification (O-LS). O-LS provides mechanisms to (1) strip nutrients from
surface waters depriving the deep-ocean of preformed nutrients, increasing biological pump efficiency
and (2) deepen carbon re-mineralization increasing deep-ocean alkalinity. Both may have contributed to
lower glacial atmospheric CO2 concentrations. O-LS would also have amplified glacial climatic cycles by
promoting the spread of high latitude sea ice in winter as occurs in the Sea of Okhotsk today, and
reducing gas exchange between ocean and atmosphere in summer.
Ó 2013 Elsevier Ltd. All rights reserved.
Keywords:
Biological pump
Radiolaria
North Pacific
Deep sea cores
Ocean carbon sequestration
Flux
Glacial ocean
Stratification
Pleistocene
Holocene
Sea of Okhotsk
1. Introduction
Positive correlations between temperature and CO2 concentration in ice cores have led to a consensus that atmospheric CO2
variations amplified ice age climate change (Berner et al., 1979;
Petit et al., 1999) but the cause of these variations are poorly understood (Sigman et al., 2010). The partial pressure of atmospheric
CO2 (pCO2) is controlled by the average steady state of ocean surface water pCO2 weighted by area and gas exchange kinetics
(Archer et al., 2000), which in turn varies with temperature and
major nutrient concentrations. Much of the present-day ocean’s
mixed layer is stripped of major nutrients by an efficient biological
pump; however, large areas of the Antarctic, equatorial Pacific and
North Pacific are not. Increased glacial biological pump efficiency in
these areas could cause more complete nutrient utilization and
* Corresponding author. Tel.: þ1 845 351 2451.
E-mail address: [email protected] (J.D. Hays).
0277-3791/$ e see front matter Ó 2013 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.quascirev.2013.09.022
consequent atmospheric CO2 drawdown. The Antarctic Ocean is
especially important, for today its unused nutrients are convected
to the deep-ocean as so called preformed nutrients. Thus atmospheric pCO2 depends on both surface ocean nutrient and deepocean preformed nutrient concentrations. Deeper glacial carbon
re-mineralization could also have lowered atmospheric pCO2 by
triggering deep-ocean alkalinity changes (Broecker and Peng, 1987;
Boyle, 1988).
Increased glacial ocean carbon sequestration is suggested by
lower glacial than Holocene deep-ocean oxygen levels (Thompson
et al., 1990; Francois et al., 1997; Gebhardt et al., 2008; Jaccard et al.,
2009) and more depleted glacial d13C below 2000 m than above
(Herguera, 1992; Keigwin, 1998; Curry and Oppo, 2005). Proxies for
productivity and export, e.g. opal and barium flux, to subarctic
North Pacific sediments do not support increased glacial relative to
Holocene primary productivity (Narita et al., 2002; Kienast et al.,
2004; Haug et al., 2005; Jaccard et al., 2005; Shigemitsu et al.,
2007). So lower North Pacific diatom d15N (increased surface water nitrogen utilization) values in glacial relative to interglacial
J.D. Hays et al. / Quaternary Science Reviews 82 (2013) 78e92
79
Fig. 1. Recent distribution of northern he misphere permafrost (Washburn, 1980 and references therein) and percent C. davisiana in ocean floor sediments (Morley and Hays, 1983;
Morley, 1983; and Pisias personal communication). Holocene high percentages of this species occur only within the Sea of Okhotsk and adjacent Pacific.
sediments, have been attributed to lower upward nutrient flux
caused by increased stratification, rather than higher primary
productivity (Sigman et al., 1999; Galbraith et al., 2008). Glacial
stratification has also been invoked in the Antarctic (Francois et al.,
1997), however the biological consequences of this stratification
are poorly understood in either the Antarctic or North Pacific.
Although organic carbon export is often linked to primary
productivity (Eppley and Peterson, 1979), it can also vary with little
or no primary production change (Boyd and Newton, 1995) because
the quantity of sinking organic carbon is strongly affected by consumer community structure (Michaels and Silver, 1988) that can be
influenced by physical water column properties (Hargrave, 1975;
Gardner et al., 1993). Glacial Ocean cooling has been suggested as
a water column change that could reduce heterotrophic consumption rates and thereby increase biological pump efficiency
relative to today (Matsumoto, 2007).
The remains of shallow (<200 m) and deep-living (>200 m)
organisms can provide information about past depths of organic
carbon respiration but few members of the deep-living community
leave a fossil record. Of those that do, polycystine radiolarians are
the most abundant and diverse group (Kling, 1979; Gowing, 1986;
Takahashi, 1991; Abelmann and Gowing, 1997; Itaki, 2003;
Okazaki et al., 2004; Abelmann and Nimmergut, 2005; Tanaka
and Takahashi, 2005). Radiolarians, as trophic generalists, feeding
on sinking organic detritus and associated microorganisms
including bacteria (Anderson, 1983; Gowing, 1986), respond to
changing organic flux. Because their shells suffer less from dissolution than diatoms (Shemesh et al., 1989; Morley et al., in press)
fossil radiolarians should record production changes at different
levels within the water column.
Shallow-living species (0e200 m) dominate radiolarians
captured by plankton tows (Kling and Boltovskoy, 1995; Tanaka and
Takahashi, 2008) but a deep-living species, Cycladophora davisiana,
dominates Last Glacial Maximum (LGM) high latitude (>45 )
radiolarian faunas of both hemispheres (Hays et al., 1976; Morley
et al., 1982; Morley, 1983; Gersonde et al., 2003). In Holocene
sediments only those of the Sea of Okhotsk approach the high
C. davisiana percentages found in high latitude glacial ocean sediments (Fig. 1). In the Okhotsk water column radiolarian concentrations below 200 m exceed those above, reaching a maximum
between 200 and 500 m, where C. davisiana dominates
(Nimmergut and Abelmann, 2002; Okazaki et al., 2004). This
80
J.D. Hays et al. / Quaternary Science Reviews 82 (2013) 78e92
radiolarian concentration profile is well documented, but its cause
remains controversial. Some attribute high C. davisiana productivity between 200 and 500 m to organic matter advected from
neighboring shelves (Okazaki et al., 2003a) or transported by sea
ice (Okazaki et al., 2003b). Others appeal to favorable intermediate
water properties to enhance production and a possible influence
from overlying stratification (Abelmann and Nimmergut, 2005).
Deep-living radiolarians (>200 m) may also benefit from enhanced
carbon export resulting from reduced respiration in the cold waters
between 20 and 125 m (Hays and Morley, 2004).
Views also diverge on the cause of high C. davisiana percentages
(>20%) in high-latitude glacial sediments. A popular proposal is
that they are a response to well-ventilated Intermediate Water flow
(Nimmergut and Abelmann, 2002; Ohkushi et al., 2003; Abelmann
and Nimmergut, 2005; Matul, 2011). Alternatively it has been
argued they are a product of a cold, highly stratified water column,
similar to that of the modern Sea of Okhotsk (Morley and Hays,
1983; Hays and Morley, 2004). These proposals are testable
because a glacial North Pacific water column, similar to that of the
modern Sea of Okhotsk, would have produced lower shallow-living
flux than its Holocene counterpart while C. davisiana production,
promoted solely by increased intermediate water flow, should not
have influenced shallow-living radiolarian production. This paper
uses a set of radiolarian species that today live dominantly either
above or below 200 m to test these hypotheses. It also documents
for the first time glacial-interglacial changes in the flux of shallowand deep-living radiolarian assemblages and uses this information
to explore the biological and climatic consequences of glacial North
Pacific stratification.
2. Selection of material
Three northwest Pacific cores are selected that have nearly
constant late Pleistocene sedimentation rates (Ninkovich and
Robertson, 1975; Keigwin, 1995) and those rates are sufficiently
high to assure good opal preservation (Broecker and Peng, 1982).
They include a hydraulic piston core, raised from atop Detroit
Seamount (ODP site 883D) and two piston cores from the Pacific
Ocean floor (V20-122, V20-124). Holocene sediments from a Sea of
60°N
55°N
Sea of
Okhotsk
883D
50°N
V32-161
V20-122
V20-124
S
Ja ea
pa of
n
45°N
North
Pacific
40°N
140°E
150°E
160°E
Fig. 2. Location of four sediment cores used in this study, Sea of Okhotsk V32-161,
48.238 N, 149.066 E, 1600 m; deep northwest Pacific cores V20-122, 46.566 N,
161.683 E, 5563 m; V20-124, 45.833 N, 154.5 E, 5534 m; and Detroit Sea Mount 883D,
51.198 N, 167.678 E, 2396 m.
Okhotsk core (V32-161) are also included (Fig. 2). No evidence of
dissolution was observed except in Pleistocene sediments of the
Sea of Okhotsk core. The three Pacific cores are sampled from late
Pleistocene (about 70 ka BP) through Holocene but only the Holocene of the Sea of Okhotsk core (V32-161) because of poor Pleistocene radiolarian preservation (Morley et al., 1991). Species
abundances, the degree to which species are restricted to depths
above or below 200 m and their occurrence in both Sea of Okhotsk
and northwest Pacific sediments, guided the selection of six species
that are grouped into Shallow (<200 m) and Deep (>200 m) Assemblages. The morphological variations of these species are
illustrated in references listed in Table 1. All other species are placed
in an Other Assemblage.
The Shallow Assemblage consists of Spongotrochus glacialis
(Popofsky), Stylochlamydium venustum (Bailey) and their probable
juveniles (Spongodiscidae spp). Stratified plankton tow studies
show that these species live dominantly above 50 m in the Sea of
Okhotsk (Nimmergut and Abelmann, 2002) and above 100 m in the
Antarctic Ocean (Abelmann and Gowing, 1997). They compose
>75% of all radiolarians separated from Recent Bering Sea surface
sediments, raised from <150 m (Blueford, 1983; Wang et al., 2006).
Blueford (1983) refers to these species as “groups” indicating
considerable morphological variation, we also recognize wide
morphological variation (Table 1). In stratified plankton tows
S. venustum is found mostly above 100 m and S. glacialis mostly
above 250 m in the North Pacific (Kling, 1979; Tanaka and
Takahashi, 2008) and other high-latitude seas including the Arctic
Ocean (Hülsemann, 1963; Tibbs, 1967; Kling, 1979; Morley and
Stepien, 1985; Abelmann and Gowing, 1997; Itaki et al., 2003) but
can occur in lower numbers down to 3000 m (Itaki et al., 2003;
Tanaka and Takahashi, 2008). S. venustum is the most abundant
radiolarian in Bering Sea and northwest Pacific Holocene sediments
north of 45 (Ling et al., 1971; Robertson, 1975; Wang et al., 2006).
Tanaka and Takahashi (2005) showed that its flux to Holocene
sediments is greater than its flux to glacial sediments in both the
Bering Sea and northwest Pacific. Both S. venustum and S. glacialis
are residents of polar and sub-polar waters of both hemispheres
Table 1
This table presents a list of references that together illustrates the morphological
variability of the species included in this study. S. venustum, S. glacialis and their
probable juveniles the Spongodiscidae spp. dominate the Shallow Assemblage and
are well illustrated in numerous studies of North Pacific and Antarctic radiolarians.
Similarly C. davisiana and D. hirundo dominate the Deep Assemblage and are likewise widely illustrated. A. micropora and Spongurus sp. are distinctive but much less
abundant and if omitted would not change the conclusions of this paper.
Acanthodesmia micropora (Popofsky), Kruglikova, 1975, p. 84, Fig. 2, (19);
Nimmergut and Abelmann, 2002, p. 470, pl. 2, (7); Hays and Morley, 2004, p.
601, Fig. 7, (c).
Cycladophora davisiana Ehrenberg, Petrushevskaya, 1967, p. 122, Fig. 69, (IeVII);
Tanaka and Takahashi, 2008, p. 69, pl. 3, (7, 8); Hays and Morley, 2004, p. 601,
Fig. 7, (g, h, i); Nimmergut and Abelmann, 2002, p. 469, pl. 1, (9, 10, 11).
Dictyophimus hirundo (Haeckel), Petrushevskaya, 1967, p. 114, Fig. 67, (IeV);
Tanaka and Takahashi, 2008, p. 71, pl. 5 (5, 6, 7); Ling et al., 1971, p. 729, pl. 2,
(8, 9, 10); Nimmergut and Abelmann, 2002, p. 471, pl. 2 (5a, 5b).
Spongodiscidae spp., Tanaka and Takahashi, 2008, p. 68, pl. 2, (5, 6, 7); Okazaki
et al., 2003, p. 204, pl. I (18, 20).
Spongotrochus glacialis (Popofsky), Nigrini and Moore, 1979, p. S117, pl. 15, (2);
Tanaka and Takahashi, 2008, p. 68, pl. 2 (1, 2); Okazaki et al., 2003b, p.204,
plate 1, (21).
Spongurus (?) sp. Petrushevskaya, 1968, p. 49, Fig. 26, (I); Nigrini and Moore,
1979, p. S67, pl. 8, (4); Tanaka and Takahashi, 2008, p. 69, pl. 3 (3); Okazaki
et al., 2003b, p. 204, pl. 1 (23); Ling et al., 1971, p. 727, pl. 1 (6).
Stylochlamydium venustum (Bailey), Boltovskoy and Riedel, 1980, p. 141, pl. 4,
(3); Kruglikova, 1975, p. 84, Fig. 2, (1, 2); Tanaka and Takahashi, 2008, p. 68,
pl. 2 (3);
Ling et al., 1971, p.727, pl. 1 (7, 8); Nimmergut and Abelmann, 2002, p. 469,
pl. 1 (1).
J.D. Hays et al. / Quaternary Science Reviews 82 (2013) 78e92
3. Analytical procedures
Radiolarians, from a known weight of dried sediment, were
washed through a 63 mm screen and collected on microscope slides
(Moore, 1973). At least 300 individuals were counted per slide.
Sediment bulk density of cores V20-122 and V20-124 was estimated by drying (65 C, 4 h), weighing and measuring the volume,
corrected for shrinkage, of a set of 10 rectangular blocks, cut from
the studied segments of each core. Opaline silica, measured using
methods of Mortlock and Froelich (1989), is negatively correlated
with bulk density in these cores (r ¼ 0.9354, level of significance,
a ¼ 104). That is, the Null Hypothesis (r ¼ 0) is rejected (so, r s 0)
accepting a 0.01% chance that this rejection is wrong. We determine
the significance by using the bootstrap. The bootstrap works by
generating synthetic noise series that have the same spectral coloring as the opal data. To do that, we preserve the lowest order
univariate (mean and variance) and bivariate (acvf d autocovariance) statistical moments of the opal series by computing its power spectrum (formally, the power spectral density, PSD) by Fourier
transform of the acvf (the zero frequency of the PSD is the mean,
integral of PSD the variance, and PSD itself is the acvf in the frequency domain). We then transform back to the time domain via
the inverse transform using random phase and correlate each of
these noise series to the bulk density series. We did this for 104
synthetic noise series. A histogram of r-values provides the probability of achieving the r-value we did achieve with the actual
sampled opal series. The probability of getting that r-value
(0.9354) by chance is 1 in 104. The bootstrap method preserves
the important statistical moments including the autocovariance
accounting for the effective degrees of freedom in the series.
This relationship between opal concentration and bulk density
is used to estimate bulk density where direct measurements are
lacking. The bulk densities of sediments from Site 883D are from
Rea et al. (1993).
A 14C date of 5.4 ka BP at 3 cm controls the top age of Detroit
Seamount core 883D and dates of 7.8, 9.3 and 11.2 ka BP at 14, 24
and 44 cm respectively control Holocene rates (Kiefer et al., 2001).
Holocene rates interpolated between these 14C dates range between 4.5 and 10.5 cm/1000 years averaging 7.1 cm/1000 years.
Late Pleistocene time control is provided by 14C dates of, 19.4 and
23.5 ka BP at 107 and 144 cm depths respectively, yielding bulk
accumulation rate between these depths of 9.0 cm/1000 years.
Older time control is provided by the Last Occurrence (LO) of L.
nipponica Nakaseko sakai Morley and Nigrini at 310 cm with an age
of 50 ka BP (Spencer-Cervato et al., 1993), and the MIS 4/5 boundary
(75 ka BP) at 474 cm (Kiefer et al., 2001). These ages yield late
Pleistocene bulk accumulation rates ranging between 6.4 and
10.5 cm/1000 years averaging 6.7 cm/1000 years similar to this
core’s average Holocene rate (Fig. 3). The LO of the diatom species
Proboscia curvirostris (Jouse’) Jordan and Priddle has been extensively dated in North Pacific sediments between 300 and 350 ka BP
(Koizumi and Yamamoto, 2007; Barron and Gladenkov, 1995;
Spencer-Cervato et al., 1993) with most dates closer to 300 ka BP.
Keigwin (1995) correlated the Marine Isotope Stage (MIS) boundaries of site 883D with the orbitally tuned records of Martinson
et al. (1987) and Shackleton et al. (1990). Using the resulting MIS
stage boundary ages he showed that this Site has a nearly constant
sedimentation rate of about 5 cm/1000 years back to the Brunhes/
Matuyama boundary (778 ka BP) (Shackleton et al., 1990; Tauxe
et al., 1996). Using MIS 7/8 and 9/10 boundary ages we calculate
an age of the LO of P. curvirostris in this site of 303,000 yr BP, close to
the widely reported age of 300 ka BP which we will use in this
study. The average sedimentation rate between the LO of
P. curvirostris and the core top is about 6 cm/1000 years suggesting
that the last half of the Brunhes chron at this site has a slightly
higher average sedimentation rate than the earlier half.
A set of sixteen ash layers, identified by their indices of refraction, occur in seven piston cores raised from the Pacific’s floor
southwest of the Detroit Seamount and with each core having a
nearly constant sedimentation rate (Ninkovich and Robertson,
1975). The ages of the ash layers younger than 300,000 yrs BP are
160
140
V20-122
883D
V20-124
120
Age x 103 years
(Kling, 1979; Morley and Stepien, 1985; Abelmann and Gowing,
1997; Tanaka and Takahashi, 2008) but similar forms have been
reported from low latitudes (Renz, 1976; McMillen and Casey,
1978).
The Deep Assemblage consists of four species that stratified
plankton tow collections indicate have depth preferences below
200 m. The cosmopolitan C. davisiana Ehrenberg, is by far the most
abundant member of this assemblage in glacial and Recent sediments. It has been found to be abundant below 150 m and most
abundant between 200 and 500 m in Sea of Okhotsk stratified
plankton tows (Nimmergut and Abelmann, 2002; Okazaki et al.,
2004). Globally it lives primarily below 400 m (Abelmann and
Gowing, 1997; Itaki, 2003; Itaki et al., 2003). Although some researchers recognize several subspecies of C. davisiana, we have
chosen for this study to include all those described by
Petrushevskaya (1967, Fig. 69) as C. davisiana and these have been
shown to be dominantly deep dwellers (>200 m) in the Sea of
Okhotsk (Nimmergut and Abelmann, 2002; Abelmann and
Nimmergut, 2005). Dictyophimus hirundo (Haeckel) is cosmopolitan (Boltovskoy and Riedel, 1980) and most abundant in Okhotsk’s
water column below 400 m (Nimmergut and Abelmann, 2002), and
below 250 m in the subpolar North Pacific (Tanaka and Takahashi,
2008). Acanthodesmia micropora (Popofsky) was caught in deep
1061 m but rarely in shallow 258 m sediment traps in the central
Sea of Okhotsk (Hays and Morley, 2004). Spongurus (?) sp. Petrushevskaya, a cosmopolitan species, occurs primarily below 400 m
in Antarctic waters (Abelmann and Gowing, 1996) and predominantly between 1000 and 3000 m in the North Pacific (Tanaka and
Takahashi, 2008). It has not been reported from the Sea of Okhotsk
but is included here because of its deep-living Antarctic and North
Pacific habitats.
81
100
80
60
40
20
0
0
100
200
300
400
500
600
700
800
Depth in cm.
Fig. 3. Age models for three North Pacific cores. See Table 2 for estimated ages of
volcanic ashes in V20-122, V20-124 and text for other age control.
82
J.D. Hays et al. / Quaternary Science Reviews 82 (2013) 78e92
determined by interpolation between the core tops and the LO of P.
curvirostris. For cores that do not reach the LO of P. curvirostris we
use the interpolated age of the oldest ash layer for control.
Two cores from this set (V20-122 and V20-124), that contain
four of the 16 ash layers, are chosen to supplement data from core
883D. The similarity of the interpolated ages of each of these ash
layers in the selected cores (bold faced type) and five nearby cores
(Table 2) can result only if these cores have nearly constant sedimentation rates. The mean ages of the four ash layers (Table 2)
together with the LO of L. nipponica sakaii (50 ka BP) (V20-122,
240 cm; V20-124, 320 cm) are used to control their Pleistocene
sedimentation rates. This age control generates Pleistocene bulk
sedimentation rates ranging between 5.0 and 6.2 cm/1000 yrs,
averaging 5.5 cm/1000 yrs in V20-122 and between 3.8 and 7.5 cm/
1000 yrs averaging 5.9 cm/1000 yrs in V20-124 (Fig. 3).
The depth to the major deglacial Assemblage’ changes in the
trigger cores of V20-122 and V20-124 is no greater than in their
respective piston cores suggesting that little sediment is missing
from the piston core tops but it is unlikely that these tops have zero
age. Therefore Holocene Assemblage flux is calculated using zero
core top ages and the midpoints of the Holocene/Pleistocene
transitions of C. davisiana percentages (12.5 ka BP) (Fig. 5a and b)
and by extrapolating late Pleistocene rates to the core tops. The
former method yields Holocene bulk sedimentation rates of 2.4
(V20-122) and 3.2 cm/1000 yrs (V20-124) the latter 5.5 and 5.9 cm/
1000 yrs respectively, similar to the Holocene rates of core 883D.
These different estimated Holocene bulk accumulation rates alter
the magnitude but not the direction of Holocene/Pleistocene
Shallow and Deep Assemblage flux changes in both cores.
3.1. Analysis of flux errors
FðXk Þ ¼ FðX1 ; X2 ; X3 Þ ¼ X1 X2 X3
(1)
where X1 ¼ rads./gm.; X2 ¼ bulk density; X3 ¼ sed. rate.
The uncertainty in the individual variables is computed as
follows:
Table 2
Depth to and estimated ages of, four ash layers (AL) in seven northwest Pacific cores.
Cores used in this study are in boldfaced type. Ash layer ages are determined by
linear interpolation, using core tops (zero age) and last occurrence (LO) of the
diatom P. curvirostris at 300,000 yrs. BP (Barron and Gladenkov, 1995; Koitzumi and
Yamamoto, 2007) for time control. For cores that do not reach the LO of P. curvirostris
the interpolated age of the oldest ash layer is used instead. The similarity of individual ash layer ages in multiple cores is evidence these cores have nearly constant
bulk accumulation rates.
Ash layer
(AL)
Core
Depth to AL
base (cm.)
1
V20-122
V20-123
RC14106
V20-124
RC14106
V20-123
V20-124
RC14106
V20-119
V20-120
V20-121
V20-122
V20-123
212
215
204
44.5
42.7
45.3
44 1.3
372
287
63.6
63.8
63 0.6
315
653
539
62.6
111.7
119.8
119
490
520
770
844
132
136
137
145
150
5
8
3.1.2. Bulk density (X2)
This variable is estimated by regressing grams of sediment per
cm3 (bulk density) against grams of opal per grams of sediment
(concentration) of ten samples. For this it is not the error in the
slope we use, but rather the error in predicting the bulk density
from opal concentration. This error is a function of opal concentration, so we estimate a single “representative” error in this prediction by using the error associated with an opal concentration
that is two thirds of the way from the mean concentration to the
highest. The highest opal concentration is large, so this estimate is
conservative.
3.1.3. Sedimentation rate (X3)
Here the deptheage plot of the ash layers in cores V20-122, V20124 and the 14C dates of 883D is fit with a least squares straight line
(consistent with the assumption of a constant sedimentation rate
as justified above). The uncertainty in the slope (the sedimentation
rate) is estimated from calculating the standard error of the slope
(Draper and Smith, 1988).
Because of the nonlinearity in F, we make a first order linear
approximation to its uncertainty (variance) by truncating a Taylor
series expansion to first order. Applying the expectance operator, in
the form of variance, gives:
s2F z
The flux (F) is a nonlinear multivariate product of 3 random
variables (Xk, variables whose exact value we do not know):
2
3.1.1. Radiolarian counts (X1)
Errors associated with how representative a single sample of
sediment is, as well as counting errors. Three counts were made on
each half of a split sample giving 6 estimates that are averaged to
give a single estimate of uncertainty.
Estimated
age ka.
Mean age
116 4
141 9
3 X
3
X
vFðXi Þ vF Xj vX Cov Xi Xj
vX
i mi
j
i¼1 j¼1
(2)
mj
We assume that the 3 random variables are independent (the
number of radiolarians is so small relative to the other sedimentary
components (diatoms, clay and volcanic ash) that any relationship
between X1 and the other variables is considered trivial). Thus the
covariance term (Cov[]) in (2) is 0 whenever, i s j; it only survives
when i ¼ j, reducing covariance to variance giving:
s2F z
3
X
vFðXi Þ vFðXi Þ
Var½Xi vXi mi vXi mi
i¼1
(3)
or, expanded:
s2F z½X2 ðmÞX3 ðmÞ2 Var½X1 þ ½X1 ðmÞX3 ðmÞ2 Var½X2 þ ½X1 ðmÞX2 ðmÞ2 Var½X3 (4)
The uncertainties of each variable (as variance) are combined, as
dictated by Formula (4) to estimate the standard error for each flux
estimate yielding the mean fluxes, their standard error (to first
order) and percent error of the mean flux, all in units of rads/
(cm2 ka) (Table 3).
4. Results
In all three northwest Pacific cores the Deep Assemblage’s percentage of total radiolarians declines during the deglacial (19 ka BP
to 11.5 ka BP) from Pleistocene values of as much as 70% to Holocene values of about 10%. This decline parallels declines of
C. davisiana percentages and d18O of Uvigerina sp. in core 883D
(Figs. 4a and 5a and b). Nearly simultaneously the Shallow
Assemblage rises from about 10% in the late Pleistocene to between
20 and 50% in the Holocene (Figs. 4a and 5a and b). The fact that a
J.D. Hays et al. / Quaternary Science Reviews 82 (2013) 78e92
5.5
Holocene
Holocene
% Shallow
% Deep
δ O Uvigerina sp.
% C. davisiana
a
70
25000
5.5
Late Pleistocene
Late Pleistocene
b
Shallow flux
Deep flux
δ O Uvigerina sp.
5
5
20000
60
Percent
O Uvigerina sp. o/oo
883D
50
4.5
40
4
4.5
15000
4
10000
18
30
883D
20
3.5
5000
3.5
Flux (radiolarians /cm2 1000 years)
80
83
10
0
3
0
10
20
30
40
50
60
0
3
70
0
10
20
30
40
50
60
70
3
Age x 10 year
3
Age x 10 year
Fig. 4. Core 883D, percentages of Deep and Shallow Assemblages and C. davisiana together with d18O of Uvigerina sp. (a) and Deep and Shallow Assemblage flux (b). The Deep
Assemblage constitutes greater than 50% of late Pleistocene total radiolarian flux while the Shallow Assemblage constitutes less than 10%. A reversal of Assemblage dominance
occurs mostly during the deglacial, indicated by vertical lines between 19 and 11.5 ka BP in this figure and Figs. 5 and 6. The Deep Assemblage and C. davisiana percentages follow
variations of d18O of Uvigerina sp.
70
70
a
Percernt
60
Late Pleistocene
Shallow Assemblage %
Deep Assemblage %
C. davisiana %
Holocene
Late Pleistocene
b
V20-122
60
V20-124
50
50
40
40
30
30
20
20
10
10
Percent
Holocene
0
0
0
10
20
30
40
50
60
70
0
10
20
30
40
50
60
70
3
Age x 10 years
Fig. 5. Deep and Shallow Assemblage and C. davisiana percentages of total radiolarian flux for cores V20-122 (a) and V20-124 (b) showing reversals of dominance mostly during the
deglacial.
deep radiolarian assemblage (>200 m) constitutes between 40 and
70% of the glacial radiolarian fauna in these three cores is noteworthy for nowhere in the modern ocean, or in Holocene sediments, have such high percentages of deep-living species been
Table 3
Mean flux (rads/(cm2 ka) of Deep and Shallow Assemblages their standard error
and the percent error of the mean flux. Three counts were made on each of two
halves of a split sample taken from MIS-2 sediments.
833D
V20-122
V20-124
Shallow flux
3389 298 (9%) 2768 197 (7%)
2917 304 (10%)
Deep flux
12,082 1059 (9%) 9864 681 (7%) 10,397 1083 (10%)
reported. This remarkable phenomenon and its cause is the focus of
this paper.
The major flux trends of these Assemblages and their magnitudes are similar in all three cores (Figs. 4b and 6a and b) and
include a rise of Deep Assemblage flux from 70 ka BP to 19 ka BP,
followed by its abrupt decrease during the deglacial. This Deep
Assemblage flux is accompanied by low late Pleistocene Shallow
Assemblage flux followed by an abrupt increase during the deglacial. This latter increase starting about 14 ka BP in 883D, a little
earlier in V20-122 but significantly later in V20-124, lags the
decrease of the Deep Assemblage. The later rise of Shallow
Assemblage flux in Pacific waters near the Sea of Okhotsk (V20124) relative to this rise in open Pacific waters to the east is similar
84
J.D. Hays et al. / Quaternary Science Reviews 82 (2013) 78e92
25000
25000
Late Pleistocene
Flux (radiolarians cm2, 1000 years)
a
Late Pleistocene
b
Shallow flux (A)
Shallow flux (B)
Deep flux (A)
V20-122
20000
Holocene
V20-124
20000
Deep flux (B)
15000
15000
10000
10000
5000
5000
0
0
10
20
30
40
50
60
70
0
10
20
30
40
50
60
70
Flux (radiolarians /cm2, 1000 years)
Holocene
0
3
Age x 10 years
Fig. 6. Holocene and late Pleistocene Shallow and Deep Assemblage flux show similar trends in V20-122 (a) and V20-124 (b). Holocene flux is calculated (1) by using zero core top
ages solid lines (A) and (2) extrapolating Pleistocene rates to the core tops, dashed lines (B).
to that reported for opal flux in these areas (Kohfeld and Chase,
2011).
Calculating the Holocene Deep and Shallow Assemblage flux of
V20-122 and V20-124 by: (1) assuming zero core top ages (Shallow
flux A, Deep Flux A, Fig. 6a and b) or (2) extrapolating Pleistocene
sedimentation rates through the Holocene (Shallow flux B, Deep
flux B, Fig. 6a and b), alters the magnitude but not the direction of
these deglacial trends. The lower Holocene flux of V20-124 than
V20-122 (Fig. 6) is caused by lower radiolarian concentrations not
lower sedimentation rates. The ranges of Total Assemblage flux in
these three cores are similar to the ranges reported by Tanaka and
Takahashi (2005) from piston core ES (49 450 N, 168 190 E).
C. davisiana is the major component of the Deep Assemblage and
its variations dominate temporal changes of this Assemblage. The
time series of the other Deep Assemblage species correlate positively with each other and with C. davisiana indicating a common
response of all Deep Assemblage species to environmental change
(Table 4). Deep and Shallow Assemblage flux are negatively
Table 4
Positive correlations between the time series of all of deep-living species indicate a
common response to environmental change. The positive correlations between
Shallow and Other Assemblages suggests Shallow living species may dominate the
Other Assemblage. The Shallow and Deep Assemblages are negatively correlated.
Core
Species and assemblages
Correlation
coefficient r
p
883D
C. davisiana e D. hirundo
C. davisiana e A. micropora
C. davisiana e Spongurus sp.
Deep and Shallow
Shallow and Other
C. davisiana e D. hirundo
C. davisiana e A. micropora
C. davisiana e Spongurus sp.
Deep and Shallow
Shallow and Other
C. davisiana e D. hirundo
C. davisiana e A. microporav20-122
C. davisiana e Spongurus sp.
Deep and Shallow
Shallow and Other
0.7466
0.6734
0.3848
0.7318
0.2721
0.2171
0.5891
0.4139
0.7091
0.7797
0.7673
0.6205
0.5643
0.1134
0.6311
<0.0001
<0.0001
0.0053
<0.0001
0.0534
<0.152
<0.0001
<0.0047
<0.0001
<0.0001
<0.0001
<0.0001
0.0002
0.4862
<0.0001
V20-122
V20-124
correlated while a generally positive correlation between the Other
and Shallow Assemblages suggests shallow-living species are
important in the Other Assemblage (Table 4).
These radiolarian Assemblage fluxes show no response to the
inferred productivity and d15N maximum that peak around 13 ka BP
during the Bolling-Allerod (Keigwin et al., 1992; Ternois et al., 2001;
Sato et al., 2002; Crusius et al., 2004; Seki et al., 2004; Brunelle
et al., 2007; Kohfeld and Chase, 2011). Higher resolution sampling
of these radiolarian Assemblages during the deglacial is needed to
more thoroughly investigate these relationships.
To compare late Pleistocene and Holocene Assemblage flux and
Assemblage radiolarians/gm. among Pacific and Sea of Okhotsk
cores, average Shallow, Deep, Other and Total Assemblage flux and
their radiolarians/gm. are calculated for MIS-2 (17.5e24.1 ka BP)
and Holocene (0e11.5 ka BP) sediments (Table 5). Holocene
Assemblage fluxes for V20-122 and V20-124 are calculated using
both the low and high bulk accumulation rates discussed above.
The Assemblage flux and their concentrations are more consistent
among cores during MIS-2 than during the Holocene. This may be
due to fewer Holocene than MIS-2 samples, core top age uncertainties or the glacial northwest Pacific was geographically more
uniform than its Holocene counterpart. When using the higher
Holocene bulk sedimentation rates for V20-122 and V20-124
Shallow Assemblage radiolarians/gm and flux increase between
MIS-2 and Holocene by from four times in V20-124 to over 10 times
in V20-122, Other Assemblage flux also increases between MIS-2
and Holocene in all three cores while average Holocene Deep
Assemblage flux falls to less than half its MIS-2 values in all three
cores (Table 5). These large changes of average Shallow and Deep
Assemblage flux between MIS-2 and Holocene that occur in
opposite directions in all three cores cannot be a result of sedimentation rate errors or changes of lithic component accumulations. Rather they must be caused by changes in the flux to the sea
floor of the species components of the Shallow and Deep
Assemblages.
Average Deep Assemblage flux accounts for more than 45% of
MIS-2 Total flux in the three Pacific cores but only 10% of Holocene
Total flux while the Shallow Assemblage constitutes more than 18%
of their Total Holocene flux but less than 10% of MIS-2 total flux. A
scatter plot of these relationships (Fig. 7) produces a cluster of MIS-
J.D. Hays et al. / Quaternary Science Reviews 82 (2013) 78e92
85
Table 5
Average Shallow, Deep, Other and Total Assemblage flux (radiolarians/cm2 1000 years) and radiolarians/gm. of sediment (in bold italicized numerals) for Holocene (0e
11.5 ka BP) and MIS-2 (17.5e24.1 ka BP) sediments of northwest Pacific and Holocene Sea of Okhotsk cores (V32-161). Holocene flux in cores V20-122 and V20-124 is calculated
using bulk sedimentation rates based on zero core top ages (numbers in parentheses) and also using late Pleistocene bulk accumulation rates (numbers in boldfaced type).
Core
Holocene
Shallow
Deep
Other
Total
Shallow
Deep-
Other
Total
V20-122
(6063)
14,404
3119
11,578
2839
(3066)
7089
1036
1693
357
(2452)
5823
1346
4190
958
(2003)
4631
664
4564
965
(17,849)
42,391
9679
15,773
4512
(10,819)
25,020
3615
6057
1315
(26,364)
62,615
14,144
31,541
8309
(15,888)
36,741
5315
12,315
2637
1068
176
13,589
2236
20,388
3351
35,045
5762
1505
335
1631
220
11,785
2637
10,964
1490
13,238
3000
10,419
1421
26,528
5972
23,016
3132
883D
V20-124
V32-161
MIS 2
2 values well separated from a looser cluster of Holocene values.
The Sea of Okhotsk Holocene values plot between but closer to the
MIS-2 cluster. Similar results occur regardless of whether the high
or low Holocene sedimentation rates, discussed above, are used for
cores V20-122 and V20-124. These data provide evidence that the
water column concentration profiles of the Deep and Shallow Assemblages in the Sea of Okhotsk during the Holocene were more
similar to those of the northwest Pacific during MIS-2 than to those
of the northwest Pacific during the Holocene.
It should be noted that while Okhotsk Holocene Shallow
Assemblage flux is similar to that of open Pacific MIS-2 Shallow
Assemblage flux, Okhotsk Holocene Deep, Other and Total Assemblage flux are significantly less than their open Pacific MIS-2
counterparts (Table 5) making the Sea of Okhotsk’s Deep Assemblage flux intermediate between the northwest Pacific’s Holocene
and MIS-2 Deep Assemblage flux. This is surprising considering the
present high productivity of the modern Sea of Okhotsk and the
lower productivity that probably characterized the glacial North
Pacific.
40
Shallow Assemblage flux as % of total flux
883D
35
Holocene
MIS-2
30
C. davisiana dominates Deep Assemblage flux, in the three
northwest Pacific cores, in both MIS-2 (average 63%, range 53e63%)
and Holocene (average 64%, range 53e75%) sediments. The decline
of C. davisana percentages of total flux between MIS-2 and Holocene is caused by both a reduction of C. davisiana flux and an increase of Shallow and Other Assemblage flux. Similarly higher
C. davisiana percentages in Sea of Okhotsk Holocene than northwest Pacific Holocene sediments, are also caused by higher
C. davisiana flux and lower Shallow and Other Assemblage flux in
the former than the latter (Table 5).
From these data the following is inferred:
(1) Similar major trends of Deep and Shallow radiolarian
Assemblage flux in three northwest Pacific cores indicate
that they are robust and have regional significance.
(2) Deep-living radiolarian species dominated total radiolarian
flux to Lateglacial northwest Pacific sediments and were
more dominant in Sea of Okhotsk Holocene than in northwest Pacific Holocene flux.
(3) These data are consistent with the hypothesis that the water
column concentration profiles of the Deep and Shallow Assemblages in the glacial northwest Pacific were more similar
to those of the Holocene Sea of Okhotsk than to those of the
Holocene northwest Pacific.
(4) The major shoaling of northwest Pacific radiolarian production between MIS-2 and Holocene is an important biological
response to deglacial oceanographic changes.
25
V20-122
5. The Sea of Okhotsk, a window on the high latitude glacial
ocean
20
V20-124
V32-161
15
10
V20-124
5
883D
V20-122
0
0
10
20
30
40
50
Deep Assemblage flux as % of total flux
Fig. 7. Average Shallow and Deep Assemblage flux for MIS-2 and Holocene expressed
as percentages of average Holocene and MIS-2 total radiolarian flux. Holocene and
MIS-2 northwest Pacific values are clearly separated with Sea of Okhotsk Holocene
values plotting near northwest Pacific MIS-2 values suggesting similarities between
the environments of these seas.
The Sea of Okhotsk’s biological stratification conforms to its
physical stratification with lower concentrations of both radiolarians and zooplankton in a Cold (1.5 to 1 C) Intermediate Layer
(CIL) (20e125 m) and higher concentrations of both in a subsurface
maximum (Fig. 8, III) between 200 and 500 m (Gorbatenko, 1996;
Nimmergut and Abelmann, 2002). The physical stratification is
caused by extreme winter cooling (mean eastern Siberian January
temperature 45 C (Jones et al., 1986)) and sea ice formation
(Rogachev, 2000; Ogi et al., 2001). Little upward buoyancy flux can
be induced in a column of near freezing seawater (Rooth, 1982;
Winton, 1997; Sigman et al., 2004) so it is prone to stratify as its
surface freshens (Warren, 1983; Winton, 1997). The springesummer pooling of sea ice melt water (51 cm/yr), precipitation and
runoff (37 cm/yr) (Rogachev, 2000) produces a thin (10e20 m) low
salinity mixed layer. Fall-winter mixing is limited to about 100 m
86
J.D. Hays et al. / Quaternary Science Reviews 82 (2013) 78e92
Fig. 8. Annual temperature profile for Bering (panel I) and Okhotsk Seas (panel II). Panel III shows correspondence between low ocean temperatures and low radiolarian and
zooplankton concentrations (a) Polycystine radiolarians, station LV28-3 (AugusteSeptember)(Nimmergut and Abelmann, 2002), (b) zooplankton, Kuril Kamchatka Trench (July)
(Vinogradov, 1970), (c) nekton, Okhotsk Sea summer from Gorbatenko (1996) and (d) temperature (summer), CIL ¼ Cold Intermediate Layer, OUIW ¼ Okhotsk Upper Intermediate
Water, OLIW ¼ Okhotsk Lower Intermediate Water, after Hays and Morley (2004).
forming a permanent Dichothermal or Cold Intermediate Layer
(CIL) between about 20 and 125 m with near zero to subzero
temperatures (Moroshkin, 1968; Kitani, 1973) (Fig. 8, panel II).
Winter sea ice formation and brine rejection in polynyas at the sea’s
northern edge produces dense water that sinks to between150 and
450 m, mixing with Okhotsk Lower Intermediate Water (OLIW), of
Pacific origin, to form Okhotsk Upper Intermediate Water (OUIW)
(Fig. 8 panel III) (Gladyshev, 1998; Martin et al., 1998).
The low radiolarian concentrations above 200 m have been
attributed to strong seasonal contrasts, low surface water salinities
and sea ice cover (Nimmergut and Abelmann, 2002; Okazaki et al.,
2003b; Tanaka and Takahashi, 2005). It is likely that cold CIL temperatures also limit radiolarian production within the CIL, as has
been proposed for Okhotsk zooplankton (Vinogradov, 1970), for
metabolic and reproductive rates decline exponentially with falling
temperature (Arrhenius, 1915; Nelson, 2004). Low numbers of
heterotrophs, with low respiration rates, living within the CIL
should also enhance export through it, benefiting underlying
zooplankton and radiolarians, including C. davisiana (Fig. 8, Panel
III). By contrast a warmer subsurface temperature minimum in the
central Bering Sea (Fig. 8, Panel I) is associated with low C. davisiana
percentages in underlying Holocene sediments (Fig. 1).
The CIL’s minimum temperature (Tmin) is inversely related to the
stability of the stratification for stability reduces summer mixing
preserving low winter temperatures (Kitani, 1973). C. davisiana
percentages, in the summer water column between 200 and 500 m,
J.D. Hays et al. / Quaternary Science Reviews 82 (2013) 78e92
are inversely related to the CIL’s Tmin (Fig. 9) suggesting that
C. davisiana is more sensitive to CIL temperatures and water column
stability than other radiolarians living in that depth range.
C. davisiana percentages in Okhotsk’s Holocene sediments are also
inversely related to the CIL’s Tmin (Fig. 9) connecting these percentages to the CIL’s low temperatures and stable physical
stratification.
Okhotsk’s cold subsurface water, while probably important, is
not sufficient to produce high sedimentary C. davisiana percentages, for water as cold or colder than the Okhotsk CIL underlies the
mixed layer in Antarctic waters today but C. davisiana is generally
less than 5% of Antarctic Holocene radiolarians (Hays et al., 1976;
Gersonde et al., 2003). The thicker Antarctic mixed layer may be
an important difference because in the Okhotsk Sea Shallow
Assemblage species are largely restricted to its upper 50 m
(Nimmergut and Abelmann, 2002) while in the open North Pacific,
where mixed layers are thicker, these same species range through
the upper 100e200 m (Kling, 1979; Tanaka and Takahashi, 2008).
Thin mixed layers may play an important biological role in cold
stratified oceans for they not only limit the space within which
shallow-living species thrive, they also enhance nutrient utilization
(Sverdrup, 1953) and carbon export, the latter because thinner
mixed layers increase the probability of organic particles sinking
through their lower boundaries (Kerr and Kuiper, 1997).
A summer/fall (Sept., Oct., Nov.) C. davisiana flux maxima accounts for most of C. davisiana’s annual flux to a central Okhotsk Sea
(1060 m) sediment trap (Hays and Morley, 2004) and coincides in
this trap with an annual organic carbon flux maximum of 7 mg/m2/
day (Honda et al., 1997). Similar North Pacific and Bering Sea
coincident summer/fall C. davisiana and organic carbon flux maxima (Takahashi, 1995), suggest C davisiana production today is
controlled by seasonal biological rhythms of the North Pacific
Ocean and its marginal seas, i.e. organic carbon export, with high
bacterial numbers, during the late summer heterotrophic phase of
% C. davisiana vs Okhotsk CIL Tmin
35
% C. davisiana core tops
% C. davisiana 200-500m
y = 16.735 - 4.9484x
r = 0.7612
y = 16.668 - 6.2396x
r = 0.65443
30
% C. davisiana
25
20
15
10
5
0
-2.00
-1.00
0.00
1.00
2.00
3.00
CIL Tmin C°
Fig. 9. Sea of Okhotsk C. davisiana percentages versus Tmin of CIL, in summer water
column (200e500 m) (circles), error bars on water column data points represent a 15%
uncertainty that all specimens counted were living (Abelmann and Nimmergut, 2005),
Tmin from Biebow et al. (2003). C. davisiana percentages in Holocene sediments (diamonds) after Morley and Hays (1983), Tmin from CTD and XBT stations each within 80
nautical miles (mean distance of 22 nautical miles) of associated core site (NODC data
base).
87
the plankton cycle (Sorokin and Sorokin, 1999; Nimmergut and
Abelmann, 2002) not factors peculiar to the Sea of Okhotsk.
The high annual organic carbon export to this central Okhotsk
Sea trap of 1.7 g/m2/yr, combined with an organic to inorganic
carbon ratio of 3.4, and a Ca/Si ratio of 0.1 led Honjo and Manganini
(1996) to suggest that this sea is a strong CO2 sink. The biological
utilization of nutrients as they are made available and the consequent stripping of nutrients from the summer mixed layer (Sorokin,
2002) indicates this sea has an efficient biological pump.
In summary, the greater radiolarian flux from below than above
200 m in the Sea of Okhotsk is unusual in modern seas but similar
to that of the glacial northwest Pacific. Both have higher Deep than
Shallow Assemblage flux and C. davisiana percentages >20%. These
data suggest that the glacial northwest Pacific had a physicale
biological stratification similar to that of the Holocene Sea of
Okhotsk.
It should be noted that C. davisiana percentages, of up to 18%,
occur in Recent sediments under upwelling areas (Robson, 1983;
Welling et al., 1992; Jacot Des Combes and Abelmann, 2007) and
other unstratified seas (Itaki, 2003). The cause of these high percentages is not known and needs to be investigated.
6. The glacial ocean viewed through the Sea of Okhotsk
window
Physical factors must have constrained Shallow Assemblage
production in the northwest Pacific during glacial relative to Holocene times because the organic matter that fueled higher Deep
Assemblage production was first available to, but unused by, the
Shallow Assemblage. If well-ventilated intermediate water
(Nimmergut and Abelmann, 2002) or intermediate water charged
with organic matter (Okazaki et al., 2003a) benefited C. davisiana it
should not have been detrimental to overlying shallow-living
species. Also if sea ice transported organic matter (Okazaki et al.,
2003b) benefited either it should have promoted shallow as well
as deep-living species production. The glacial northwest Pacific’s
Shallow and Deep Assemblage flux can best be explained by the
presence of a thin mixed layer and an underlying CIL, similar to that
of the Sea of Okhotsk today. Such a water structure would have
inhibited Shallow and promoted Deep Assemblage production. The
disappearance of this Okhotsk-Like Stratification (O-LS) during the
deglacial, with resulting mixed layer thickening and warming of the
CIL, could explain the decline of the Deep Assemblage, the rise of
the Shallow Assemblage and the resulting fall of C. davisiana percentages. The fact that Sea of Okhotsk Deep Assemblage flux
(Table 5) and Deep and Shallow Assemblage flux as a percent of
total flux (Fig. 7) are intermediate between those of the northwest
Pacific’s Holocene and MIS-2 suggests that northwest Pacific MIS-2
conditions were more severe than Holocene Sea of Okhotsk conditions e.g. colder CIL and more efficient biological pump.
The analogy between the glacial northwest Pacific and Holocene
Okhotsk Sea is marred by the fact that the Holocene Sea of Okhotsk
was highly productive while various proxies suggest the glacial
northwest Pacific was less so (Narita et al., 2002; Kienast et al.,
2004; Seki et al., 2004; Jaccard et al., 2005; Okazaki et al., 2005;
Galbraith et al., 2008). Possible causes of lower glacial than Holocene North Pacific productivity have been much discussed (for a
review see Kohfeld and Chase, 2011). A popular suggestion calls for
increased glacial stratification to reduce nutrient input to the mixed
layer (Sarnthein et al., 2004; Sigman et al., 2004; Jaccard et al.,
2005; Brunelle et al., 2007, 2010). Yet the Sea of Okhotsk’s strong
stratification does not prevent Ekman pumping of nutrient rich
thermocline waters into its thin mixed layer causing high seasonal
productivity that fully utilizes nutrients as they are provided
(Sorokin, 2002). So lower North Pacific diatom d15N values in glacial
88
J.D. Hays et al. / Quaternary Science Reviews 82 (2013) 78e92
Fig. 10. LGM C. davisiana percentages suggest Okhotsk-Like Stratification existed at that time north of the present position of the Pacific Polar Front (Belkin et al., 2002). The
geographical continuity between permafrost and O-LS suggests both were responses to cold winter air. Glacial permafrost distribution (Svendsen et al., 2004; Washburn, 1980 and
references there in) and C. davisiana percentages; Atlantic data (Morley, 1983), Pacific data (Sachs, 1973; Robertson, 1975; Morley and Hays, 1983; Morley and Robinson, 1986;
Morley et al., 1982; Ohkushi et al., 2003; Tanaka and Takahashi, 2005; N. Pisias personal communication and Morley personal communication).
relative to interglacial sediments (Sigman et al., 1999; Galbraith
et al., 2008) may not have been caused only by stratification
limiting upward nutrient flux. Alternatively the glacial relative to
Holocene supply of silica to the glacial North Pacific and Sea of
Okhotsk thermocline may have been reduced (Gorbarenko et al.,
2004; Seki et al., 2004; Okazaki et al., 2005; Kohfeld and Chase,
2011). Today mixing in the Kurile Island region brings nutrient
rich water from the deep Pacific to and above North Pacific Intermediate Water (NPIW) contributing to Sea of Okhotsk and North
Pacific productivity (Tsunogai, 2002; Sarmiento et al., 2004).
Because this mixing occurs well below the surface, nutrient ratios
are not reset by sea surface biological processes and retain high Si/N
ratios. In glacial times the apparently nutrient depleted water mass
above 2000 m (Herguera et al., 1992; Keigwin, 1998; Matsumoto
et al., 2002) was probably ventilated in the far North Pacific
(Duplessy et al., 1988; Keigwin, 1998) or Bering Sea (Matsumoto
et al., 2002; Ohkushi et al., 2003; Gorbarenko et al., 2010;
Horikawa et al., 2010). Because cooling the North Pacific today
would further stabilize it (Warren, 1983), it is likely that in glacial
time such ventilation occurred through brine rejection in high
latitude polynyas as in the Sea of Okhotsk today (Gorbarenko et al.,
2010). During ventilation sea surface biological activity would have
reset upwelled nutrient ratios, depleting silica relative to nitrate as
occurs in the Antarctic today (Sarmiento et al., 2004). Glacial North
Pacific Intermediate water depleted of silica in a similar way could
have lowered glacial relative to Holocene opal flux in the northwest
Pacific and Sea of Okhotsk (Okazaki et al., 2005; Brunelle et al.,
2007; Kohfeld and Chase, 2011). The deglacial initiation of deep
mixing in the northwest Pacific should have caused a simultaneous
Holocene increase in diatom production throughout the North
J.D. Hays et al. / Quaternary Science Reviews 82 (2013) 78e92
Pacific not just in the northwest Pacific and Sea of Okhotsk, yet this
may not have been the case for the northeast Pacific (Kohfeld and
Chase, 2011). Because the northwest Pacific and Sea of Okhotsk
are beneficiaries of nutrients supplied directly by upwelled North
Pacific Deep Water while the northeast Pacific receives nutrients
via the NPIW, the latter’s history may be different (Tsunogai, 2002).
The strong dissolution of diatom and radiolarian tests in the glacial
sediments of core V32-161 indicates the deep waters of this sea
were more under saturated in silica in glacial than Holocene times
(Van Cappellen and Qui, 1997; Rickert et al., 2002). A similar degree
of dissolution does not occur in northwest Pacific glacial sediments.
In any event it is possible that the glacial northwest Pacific and
Holocene Sea of Okhotsk could have had similar physical biological
stratifications but differing silica supply mechanisms and consequent opal flux values.
Cold winter air masses and resultant extensive sea ice cause
Okhotsk’s physical stratification today. There is ample evidence of
air colder than today’s eastern Siberian winter air across northern
continents at the LGM (Atkinson et al., 1987; Cuffey et al., 1995;
Isarin et al., 1998; Severinghaus et al., 1998; Isarin and Bohncke,
1999; Denton et al., 2005). North Pacific sea ice rafted detritus
from this time, a consequence of cold winter air, extends to about
45 N (Conolly and Ewing, 1970; Kent et al., 1971). Conditions
therefore were in place for O-LS to form and the C. davisiana percentages north of the 20% line in Fig. 10 are evidence that it did. This
line follows the trend of today’s North Pacific Polar Front that
separates water with a summer subsurface minimum to the north
from water without or with a weakly developed subsurface minimum to the south (Belkin et al., 2002). For O-LS to develop north of
the 20% line today would only require a thinning of the mixed layer
and cooling the subsurface minimum (CIL).
While summer temperatures play a major role in ice sheet
growth and decay (Denton et al., 2005) cold winter temperatures
and their duration control the development of permafrost (Nelson
and Outcalt, 1987) and O-LS. The geographical continuity of glacial
permafrost and O-LS (Fig. 10) is consistent with their mutual
dependence on long cold winters. Modeling experiments suggest
that reduced northern summer insolation, in response to orbital
variations, cooled northern continents producing vegetative albedo feed-backs that promoted further cooling and associated
cold winter air masses (Harrison et al., 1995; Gallimore and
Kutzbach, 1996; Ganopolski et al., 1998; Notoro and Liu, 2007,
2008). This cold winter air could have engendered permafrost
on land as well as O-LS on northern seas and the climatic feedbacks that accompany them. If so, O-LS formation and destruction
could have been as abrupt as changes of the seasonal winter air
that controls it.
Widespread high C. davisiana percentages in Antarctic Ocean
LGM sediments south of the Polar Front (Hays et al., 1976; Gersonde
et al., 2003) result from a combination of higher C. davisiana flux
and lower flux of other radiolarians (Hays et al., 1976) likely
signaling the presence of O-LS in this region as well. Radiolarian
assemblage data therefore supports inferences of North Pacific and
Antarctic stratification based on increased glacial relative to interglacial surface water nitrate utilization (lower d15N) (Francois et al.,
1997; Sigman et al., 1999; Brunelle et al., 2007, 2010; Galbraith
et al., 2008). Phosphate (Elderfield and Rickaby, 2000) and silica
data (De La Rocha et al., 1998) however suggest that the glacial
Antarctic was not highly stratified. Low nitrate concentrations also
characterize Okhotsk’s thin mixed layer (Sapozhnikov et al., 1999;
Arzhanova and Naletova, 1999; Sorokin, 2002), so high latitude
glacial O-LS obviates the need for iron fertilization (Martin, 1990) to
lower glacial, relative to Holocene, surface water nitrate concentrations. Relative to the Holocene this glacial stratification would
have deepened organic carbon re-mineralization by radiolarians
89
and other plankton (Fig. 8, panel III). This potential for O-LS to
reduce shallow carbon re-mineralization combined with a general
glacial ocean cooling (Matsumoto, 2007) provides a mechanism for
high latitude oceans to efficiently transfer carbon to the deep ocean.
Glacial high latitude oceans capped with O-LS had the potential
to amplify glacial cycles by: 1) promoting the spread of sea ice, as
occurs in the Sea of Okhotsk today where the CIL insulates sea ice
from underlying warmer water allowing its spread to the shores of
Hokkaido (45 N) (Bulgakov, 1965), a low-latitude extreme for
modern sea ice, and a latitude similar to that of the southern limit
of glacial North Pacific sea ice rafted detritus (Conolly and Ewing,
1970; Kent et al., 1971). Glacial sea ice expansion combined with
strong summer stratification (Fig. 8, panel II) could have reduced
glacial CO2 transfer from ocean to atmosphere (Stephens and
Keeling, 2000) relative to today; 2) increasing high latitude biological pump efficiency through full utilization of surface water
nutrients, depriving the deep-ocean of preformed nutrients and
lowering atmospheric CO2 concentrations (Sigman et al., 2010); 3)
triggering ocean alkalinity changes by deepening carbon remineralization further lowering atmospheric pCO2 (Broecker and
Peng, 1987; Boyle, 1988). The deglacial transition from dominantly deep to dominantly shallow radiolarian production may
reflect the change from deep to shallow organic carbon remineralization envisaged by Boyle (1988). If so it should lead
alkalinity induced changes in atmospheric pCO2 by about 2500
years (Broecker and Peng, 1987).
This model of the high latitude glacial ocean makes several
testable predictions. The causal relationship between O-LS and sea
ice predicts a consistent relationship between maximum winter sea
ice extent and high sedimentary C. davisiana percentages, although
their low latitude limits need not be the same. Opal flux peaks in
Southern Ocean cores (Anderson et al., 2002) should be accompanied by shallow-living radiolarian flux peaks signaling reduced
Southern Ocean stratification. The deglacial decline of C. davisiana
percentages should coincide with or lead the rise of atmospheric
pCO2.
7. Conclusions
1. The deepening of northwest Pacific glacial relative to Holocene
radiolarian production records an important change of this
oceans consumer community structure. A similar preference for
deep-living radiolarians and zooplankton occurs in today’s Sea
of Okhotsk where cold ocean stratification (O-LS) reduces
shallow-relative to deep-living radiolarian production giving
rise to the dominance of the deep-living C. davisiana. C. davisiana
percentages (>20%) in high latitude (>45 ) LGM sediments of
both hemispheres suggest these seas were capped with O-LS.
2. The physical and biological structure of glacial high latitude
ocean stratification presented here has several potential climatic
feedbacks; a) it promotes winter sea ice spread by insulating sea
ice from warmer underlying water; b) its thin mixed layer fully
utilizes surface water nutrients enhancing biological pump efficiency, and low respiration rates within the CIL deepen carbon
re-mineralization, both of which could aid CO2 transfer from
atmosphere to ocean in summer; c) the summer stratification
may have reduced CO2 return to the atmosphere;
3. O-LS and its biological consequences rest on two fundamental
properties of Earth’s climate system; a) the non-linearity of
seawater’s equation of state that promotes cold ocean stratification; b) the exponential relationship between temperature
and heterotrophic metabolic and reproductive rates that limit
the rate of organic carbon re-mineralization within cold near
surface waters (CILs).
90
J.D. Hays et al. / Quaternary Science Reviews 82 (2013) 78e92
Acknowledgements
We are grateful to Aaron Putnam, Dorothy Peteet, O. Roger
Anderson, Michael Sarnthein, Taro Takahashi, Maureen Raymo
and Wallace Broecker for reading the manuscript and offering
useful suggestions. We are especially grateful to Ray Sambrotto,
and Arnold Gordon for helpful discussions during manuscript
preparation and for useful comments on multiple drafts of this
paper. We are also grateful for the constructive suggestions of four
anonymous reviewers. We appreciate the expert assistance of
Maureen McAuliffe Anders during final manuscript preparation
and are grateful to Nick Pisias for unpublished C. davisiana data.
We thank the Ocean Drilling Program and its successor IODP for
collecting and archiving the drill core used. The piston cores are
archived at the Lamont-Doherty Earth Observatory of Columbia
University whose core repository is supported by funds from
National Science Foundation Grant OCE09-62010. This work was
supported with funds through the Cooperative Institute for
Climate Applications and Research (CICAR) under award number
NA030AR4320179 from the National Oceanic and Atmospheric
Administration, U.S. Department of Commerce. The statements,
findings, conclusions, and recommendations are those of the authors and do not necessarily reflect the views of the National
Oceanic and Atmospheric Administration or the Department of
Commerce. This paper bears Lamont Doherty Earth Observatory
contribution number 7735.
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