Quaternary International 387 (2015) 58e71
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Correlation of marine and coastal terrestrial records of central California: Response to paleoceanographic and paleoclimatic change during the past 19,000 years Mary McGann U.S. Geological Survey, 345 Middlefield Road, Menlo Park, CA 94025, USA
a r t i c l e i n f o
a b s t r a c t
Article history: Available online 20 March 2015
New benthic foraminiferal census data combined with previously published planktic foraminiferal and pollen data from the continental margin off central California provide a unique opportunity to document concurrent paleoceanographic and paleoclimatic changes in the region during the late Quaternary. All three datasets were evaluated in gravity core S3-15G, collected at a depth of 3491 on the western levy of the Monterey Fan (36 23.530 N, 123 20.520 W). Accelerator mass spectrometry radiocarbon dates and the ratio of the planktic foraminiferal species Neogloboquardrina pachyderma (Ehrenberg) to Neogloboquadrina incompta (Cifelli) provide a good age-depth model for the last 19,000 years, covering the last glacial, BøllingeAllerød, Younger Dryas, and Holocene intervals. Separate Q-mode cluster analyses of the hemipelagic as well as mixed (combined hemipelagic and turbiditic) mud samples grouped the benthic foraminiferal fauna into two clusters reflecting faunal adaptation to changing climatic conditions during the Pleistocene and Holocene. R-mode cluster analysis also differentiated glacial (Uvigerina senticosa and Globobulimina auriculata) and interglacial (Melonis pompilioides and Gyroidina planulata) faunas. A general trend of slightly increasing oxygen in the deep sea is suggested from the Pleistocene to Holocene based on the reduction in abundance of G. auriculata and increased frequency of M. pompilioides. Q-mode cluster analysis of the planktic foraminifera illustrates a change in the surface water from a glacial subpolar fauna in the Pleistocene to a transitional fauna in the Holocene, whereas the pollen record separated into three clusters, two of Pleistocene age (glacial and transitional) and one in the Holocene (interglacial), reflecting the terrestrial floral adaptation in the California Coast Ranges of central California to the warmer climate in the Holocene. Decoupling is evident between the benthic and planktic foraminiferal and terrestrial floral responses to changing oceanographic and climatic conditions. The floral response leads the surface-dwelling fauna by several millennia, and is followed by the deepdwelling benthic foraminiferal fauna a millennium later. © 2015 Elsevier Ltd and INQUA. All rights reserved.
Keywords: Climate Foraminifera Monterey Fan Pollen California Coast Ranges Late Quaternary
1. Introduction During May and June 1978, a geophysical and sediment sampling cruise (USGS cruise S3-78-SC) embarked off central California to investigate the characteristics and growth patterns of Monterey Fan, and the sediment transport processes associated with it. Core S3-15G was one of the longest and best preserved of the deep-sea cores obtained during the cruise, and therefore was selected for detailed quantitative analyses of benthic foraminifera, planktic foraminifera, and pollen. The availability of census data for these
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sediment constituents provides a unique opportunity to compare the microfaunal response to changing paleoceanographic conditions in the deep ocean and surface waters, as well as the concurrent terrestrial response to climate change in the California Coast Ranges of central California during the late Quaternary. The census counts and analysis of the planktic foraminiferal record have been previously reported in Brunner and Ledbetter (1989), whereas the pollen data are presented in McGann (2015). The following is a synthesis of the microfaunal and pollen analysis for core S3-15G. Included are new observations on simultaneous faunal variability between deep- and surface-water foraminifera and inferred climatic changes based on the foraminiferal records. Additionally, the marine paleoceanographic and terrestrial
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climate records during the late Quaternary time period are correlated based on paired foraminiferal and pollen datasets. 2. Setting 2.1. Regional submarine geomorphology and recovery of core S315G Submarine canyons play an important role in transporting sediment to deep-sea fans and are found along the slopes of most continental margins (Garfield et al., 1994; Paull et al., 2003). Monterey Canyon, off central California (Fig. 1), receives more than 400,000 m3 of sand and organic-rich material transported from the littoral zone each year (Paull et al., 2003). The trail of sand down the axis of the canyon demonstrates that it is the major conduit for sediment transport from the continental shelf to Monterey Fan (Greene and Hicks, 1990; Greene et al., 2002; Fildani and Normark, 2004; Paull et al., 2005). Presently, Monterey Fan has an area of active fan growth that extends more than 300 km from the base of the central California continental slope (Normark and Hess, 1980). This deep-sea turbiditic deposit constitutes the largest submarine fan off California (Normark, 1970a, 1999; Hess and Normark, 1976; Normark et al., 1984; EEZ-SCAN 84 Scientific Staff, 1986) and is one of the most extensive found offshore the contiguous United States (Greene and Hicks, 1990). Further discussion of Monterey Fan morphology and evolution can be found in Fildani et al. (1999), Normark (1999), Fildani and Normark (2004), and summarized in McGann (2014). As the sand is carried down Monterey Canyon toward the fan, it is generally restricted to the channel except for rare overbank transport. However, because of the volume of sediment being transported downslope and the length of time over which this process occurs, the fan valley is characterized by extensive levee development, the largest of which is the western levee (Normark, 1970a, 1970b; Hess and Normark, 1976; Normark et al., 1984). Gravity core S3-15G, 4.72 m in length, was recovered by the R/V Sea Sounder (USGS cruise S-3-78-SC) 18 km from the crest of the western levee of the Monterey Fan Valley (36 23.530 N, 123 20.520 W; Fig. 1). It was obtained at a depth of 3491 m, approximately 135 km southwest of Santa Cruz. S3-15G is a mud-
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dominated deep-sea core, consisting of hemipelagic mud (Bouma, 1962) interspersed with overbank turbiditic mud and rare finegrained sand deposits. The hemipelagic and turbiditic muds are easily distinguished by color, appearing lighter and darker, respectively, as is often seen in deep-sea deposits (Howell and Normark, 1982; Piper and Normark, 1983; Brunner and Normark, 1985; Normark and Damuth, 1997). 2.2. Oceanography Hydrographic depth profiles acquired 15 times between 2003 and 2005 off central California in the vicinity of S3-15G (Fig. 1) provide data showing the variability in temperature, salinity, and dissolved oxygen in the water column from the surface to a depth of 3500 m (Fig. 2). As reported by Robison et al. (2010), the data show that temperature declines from 14.0 C at the surface to about 1.5 C at 3500 m, salinity increases from 32.9 psu to 34.65 psu, and oxygen decreases from 5.55 ml/L at the surface to about 0.25 ml/L at a depth of 700e800 m, and then increases to 9.5 ml/L at the bottom. These oceanographic parameters reflect the water masses of the region. The dominant surficial water mass off central California is the southward-flowing California Current, which constitutes the eastern limb of the North Pacific gyre and is restricted to the upper 200 m over the continental shelf (Hickey, 1979). The California Current is composed of subarctic water and, therefore, is characterized by cool temperature, low salinity, and a high concentration of dissolved oxygen (Reid et al., 1958; Robinson, 1976; Hickey, 1979, 1998; Simpson et al., 1984). Below the California Current is the poleward-flowing California Undercurrent (Cannon et al., 1975), which is comprised of Equatorial Pacific Water, and is characterized by warm and saline water with low oxygen content (Pickard, 1964; Cannon et al., 1975). Unlike the California Current, the California Undercurrent is seasonally variable in location, depth and intensity (Sverdrup and Fleming, 1941; Hickey, 1979), but usually becomes fully developed off central California between the depths of 200 and 500 m (Wickham, 1975). North Pacific Intermediate Water (Reid and Mantyla, 1978) underlies the California Undercurrent at depths from 500 m to about 1000 m and is characterized by cool, low-salinity, and oxygen-
Fig. 1. Map of Monterey Canyon off central California with the location of core S3-15G and the site of the average 3500-m hydrographic depth profile from Robison et al. (2010). Image courtesy of Monterey Bay Aquarium Research Institute.
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Fig. 2. Average 3500 m hydrographic depth profile of temperature, salinity, and oxygen based on 15 ROV dives from 2003 to 2005 off central California near the S3-15G core site (after Robison et al., 2010). Benthic foraminiferal biofacies after Ingle (1980); E-IS ¼ estuarine to inner shelf; OS ¼ outer shelf; depth range for lower bathyal (2000e4000 m) and abyssal (>4000 m) biofacies not to scale. Water masses in bold.
depleted water (Pickard, 1964; Reid and Mantyla, 1978). The reduced oxygen concentration (<0.5 ml/L) is due to the degradation of organic matter in the highly productive surface waters where strong seasonal upwelling exists, as well as the presence of poorly ventilated intermediate-water (van Geen et al., 1996; Cannariato and Kennett, 1999; Hendy and Pederson, 2005). The result is the development of an extensive oxygen-minimum zone (OMZ) in the eastern Pacific Ocean (Broenkow and Greene, 1981). Off central California, the OMZ is presently established between depths of about 500 and 1000 m, with the dissolved oxygen content declining to a minimum of about 0.27 ml/L at a depth of 700e750 m (Reid and Mantyla, 1978; Broenkow and Greene, 1981; Robison et al., 2010). A transition zone between North Pacific Intermediate Water and the underlying Pacific Deep Water lies between 1000 and 2000 m in the northeast Pacific Ocean, with the water masses likely mixing vertically within this depth range (Pytkowicz and Kester, 1966). Although oxygen content slowly increases with depth, generally low-oxygen conditions (<1.5 ml/L) prevail off central California at these depths. Pacific Deep Water is located between 2000 and 4000 m and is characterized by cold and very saline water with abundant dissolved oxygen (Sverdrup et al., 1942; Robison et al., 2010). The core site of S3-15G, lying at a depth of approximately 3500 m, is situated within this water mass. 3. Material and methods Fifty-nine mud samples, consisting of 10e20 cm3 of sediment obtained from the undisturbed central portion of the split core, were analyzed for benthic foraminifera. The samples were immersed in a dilute solution of sodium hexametaphosphate buffered to a neutral pH with ammonium hydroxide, and left overnight. Following disaggregation, the samples were sieved through nested 0.063 mm, 0.150 mm, and 1.0 mm screens and then air-dried. Foraminifera 150 mm in size were picked from the matrix, with the goal to obtain a statistically valid 300 specimens per sample (Douglas et al, 1973). If the residue
contained abundant foraminifera, it was split into an aliquot containing approximately 300 foraminifera with the aid of a microsplitter. If fewer than 300 specimens were present, all were picked. The picked benthic foraminifera were mounted on microscope slides and identified. The slides and residues of this study are on file at the U.S. Geological Survey, Menlo Park, California. Of the 59 samples, six were excluded from further analyses because few specimens (<125) were recovered in them and the faunas were not statistically valid (Douglas et al., 1973; Supplementary Table 1). The remaining 53 samples were separated into one of two groups, hemipelagic or turbiditic muds, based on the original sediment color and the abundance of displaced shallow-water foraminifera recovered. Brunner and Normark (1985) suggested that mud samples containing no shallow-water benthic foraminifera were mostly hemipelagic, those with >30% were turbiditic, and those from 1 to 19% were difficult to classify. In this study, samples with fewer than 5% displaced species were arbitrarily considered hemipelagic muds and those with more than 5% were identified as turbiditic muds. The relative species abundances of benthic foraminifera were computed using a sum of total benthic foraminifera in each sample. Once the species counts were converted to frequency data, the census data of the hemipelagic mud and mixed (hemipelagic and turbiditic) mud samples were analyzed separately by Q-mode cluster analyses to describe the relationship between the benthic foraminiferal assemblages, grouping together those samples of similar species composition. The census data of all the mud samples were also analyzed by R-mode cluster analysis to identify those species that commonly occurred together. The samples in both analyses were clustered by a square root transformation of the data, a BrayeCurtis similarity coefficient, and amalgamated by a group averaged linkage strategy. These methods were chosen because they treat all species equally while providing the most realistic grouping of the samples by depth (Clarke and Gorley, 2006). Primer v. 6.1.6, a statistical software package created by Primer-E, Ltd., was used for the cluster analysis (Clarke and Gorley, 2006).
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pachyderma to N. incompta tests in core S3-15G is thought to represent changes in sea surface temperature and is valuable in identifying climatic changes in the overlying surface water over time.
4. Chronology Two methods were used to determine the age of these overbank deposits. First, five samples were used to obtain radiocarbon dates by accelerator mass spectrometry (AMS). Three of the samples were of mixed planktic foraminifera measured by the Lawrence Livermore National Laboratory's Center for Accelerator Mass Spectrometry (CAMS), and two additional samples, one of mixed planktic foraminifera and another of mixed benthic foraminifera, were measured by Beta Analytic. Ages were calculated using the accepted half-life of 14C of 5568 years (Stuiver and Polach, 1977). The radiocarbon ages were obtained by a 14C/12C ratio and then were converted to calibrated calendar ages (cal BP) using the CALIB 7.0.1 program (Stuiver and Reimer, 1993; Stuiver et al., 2005). The calibrated ages are reported in the text as the peak probability ages rounded to the nearest decade for ages <1000 years and to the nearest century for ages >1000 years (Stuiver et al., 2005), although the 2-sigma ranges are also included on Table 1. A reservoir age of 800 years was used for the planktic foraminiferal sample with a radiocarbon age younger than 12,000 years (Southon et al., 1990; Kienast and McKay, 2001), and a 1100-year reservoir age for the two samples older than 12,100 years (Kovanen and Easterbrook, 2002). A 1750-year reservoir age was used for the benthic foraminiferal sample (Mix et al., 1999).
5. Results 5.1. Age models The ratio of N. pachyderma to N. incompta varies significantly in core S3-15G over the last 19,000 years. From 450 to 295 cm, N. pachyderma prevails, suggesting cool, glacial conditions existed off central California (Fig. 3; after McGann and Brunner, 1988). A shift from predominantly N. pachyderma to N. incompta beginning at 295 cm signals the onset of the warmer BøllingeAllerød event (14,600e12,900 BP; Grootes and Stuiver, 1997). This is followed by the Younger Dryas event, a period of climatic cooling (12,900e11,600 BP; Alley et al., 1993; Grootes and Stuiver, 1997; Alley, 2000), reflected in an increase of N. pachyderma from 256 to 243 cm. A return to dominance of N. incompta signals the beginning of the climatic warming of the Holocene (Bandy, 1960). The PleistoceneeHolocene boundary, dated at 11,600 BP (Grootes and Stuiver, 1997), lies between 241 and 212 cm in this core. The lack of precision of this interval is due to spacing of the planktic
Table 1 Radiocarbon ages, calibrated peak probability ages, and 2 sigma ranges for core S3-15G. Accession number
Depth in core S3-15G (cm)
Benthic or planktic foraminifera
Radiocarbon age (14C yr BP)
Beta-399329 Beta-399330 CAMS-21700 CAMS-21701 CAMS-21702
29e34 144e148 241.5e243.5 360e364 448e450
Benthic Planktic Planktic Planktic Planktic
2620 7960 11,180 14,700 17,130
The second method used to provide a biostratigraphic framework for these deposits was the abundance of two planktic foraminifers, left-coiling Neogloboquadrina pachyderma (Ehrenberg) and right-coiling Neogloboquadrina incompta (Cifelli) (previously referred to as right-coiling N. pachyderma; Darling et al., 2006). The ratio of these species varies in relation to surface and near-surface (<100 m; Reynolds and Thunell, 1986; Davis et al., 2014) sea temperature, with dominant N. pachyderma tests indicative of colder conditions (Mix et al., 1999; Taylor et al., 2009). However, changes in sea temperatures may result from several factors, some related to climate change and others independent of it. Included, among others, are variations in the amount of freshwater (riverine) flow and intensity and persistence of upwelling. With the core site situated 135 km from the coast and at lower bathyal depths, riverine input does not appear to be a factor in the S3-15G climate record. In contrast, coastal warming due to climate change may be associated with an increase in coastal winds, which in turn have been shown to intensify upwelling in eastern boundary current systems such as off central California (Bakun, 1990; Sydeman et al., 2014). Since increased abundance of N. pachyderma is associated with upwelling (Naidu and Malmgren, 1996; Ivanova et al., 1999; Davis et al., 2014) whereas N. incompta prefers a relaxation in upwelling (Davis et al., 2014), the ratio of the two species may, in fact, represent changes in upwelling instead of sea surface temperature. However, the recovery of cores containing annually varved sediments near S3-15G (i.e., north off the Russian River and just south of Monterey Bay off Point Lobos; Fig. 2), suggests that upwelling remained a continuous feature in the region from at least 15,000e4700 cal BP (Gardner and Hemphill-Haley, 1986). Therefore, the variability in the ratio of N.
± ± ± ± ±
30 30 110 180 200
Calibrated peak probability (calendar age) (cal yr BP)
2 Sigma range (cal yr BP)
820 8000 12,200 16,400 19,300
732e898 7940e8113 11,856e12,574 15,894e16,969 18,872e19,840
foraminiferal samples analyzed. For the purposes of this study, the mid-point of this interval (226.5 cm) is used as the PleistoceneeHolocene boundary in core S3-15G. Five radiocarbon measurements obtained for core S3-15G suggest the core is a sediment record of late Quaternary age, representing the last ca. 20,000 cal BP A peak probability calibrated age of ca. 19,300 (2 sigma range of 19,840e18,872) cal BP was returned near the bottom of the core at 450e448 cm, ca. 16,400 (16,969e15,894) cal BP at 364e360 cm, ca. 12,200 (12,574e11,856) cal BP at 243.5e241.5 cm, ca. 8000 (8113e7940) cal BP at 148e144 cm, and ca. 820 (898e732) cal BP at a depth of 34e29 cm (Table 1). All five of these ages were in stratigraphic order and corroborate the ages of the climatic events inferred by the variation in the ratio of N. pachyderma to N. incompta. 5.2. Benthic foraminifera One hundred twenty-six species of benthic foraminifera were recovered in the 53 samples from S3-15G (Supplementary Table 1). The species richness varied between 20 and 52 species/sample, with the average lower in the Pleistocene (30 species/sample) than in the Holocene (37 species/sample) sediments. The most abundant species recovered were Uvigerina senticosa Cushman, Globobulimina auriculata (Bailey), and Melonis pompilioides (Fitchel and Moll). Several other species were nearly pervasive and at times, comprised a significant portion of the assemblage. These included Gyroidina planulata Cushman and Renz, Valvulineria araucana (d'Orbigny), Planulina wuellerstorfi (Schwager), Hoeglundina elegans (d'Orbigny), and Oridorsalis umbonatus (Reuss).
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Fig. 3. Downcore ratios of Neogloboquadrina pachyderma (Ehrenberg) to Neogloboquadrina incompta (Cifelli) in core S3-15G, after McGann and Brunner (1988). Radiocarbon ages reported as calibrated years before 1950 (cal BP; in bold and italics) and include both the calibrated peak probability age and 2 sigma range. Ages of the PleistoceneeHolocene boundary, and the Younger Dryas and BøllingeAllerød events (in BP), based on Alley et al. (1993), Grootes and Stuiver (1997), and Alley (2000). Ages are estimated for the middle Holocene dry period (Thompson, 1992; Quade et al., 1998; Grayson, 2000; Benson et al., 2002; Mensing et al., 2013) and the Medieval Climate Anomaly (Stine, 1994; Mann, 2002; Cronin et al., 2003; Kleppe et al., 2011).
Nineteen hemipelagic mud samples were analyzed in S3-15G (Supplementary Table 1). Q-mode cluster analysis grouped them into two distinct clusters (Fig. 4) in which the samples are stratigraphically homogeneous. One cluster amalgamated those samples from the bottom of the core at 470e466 cm to 384.5e382.5 cm as well as the uppermost sample (24e20 cm), and the other joined those from 263e261 cm to 75-72 cm. Q-mode cluster analysis of all 53 hemipelagic and turbiditic mud samples from core S3-15G also grouped them into two distinct clusters with samples in stratigraphic order, but here the separation is more precisely defined. The first cluster combined all the samples from the bottom of the core at 470e466 cm to 272e270 cm, and the second, those samples from 263e261 cm to 24e20 cm (Fig. 5). R-mode cluster analysis of the 53 mud samples grouped the dominant or pervasive species into four clusters and one outlier (Fig. 6). The remainder of the clusters added on the rare species. 6. Discussion 6.1. Benthic foraminifera Benthic foraminifera are abundant and widespread in the marine realm, yet the spatial distribution of individual taxa are restricted and easily recognized. The ranges of these local species, taken cumulatively, comprise faunal associations (i.e., biofacies) that mirror the unique environmental conditions in which the species reside, including water mass characteristics (Zalesny, 1959; Bergen and O'Neil, 1979), sedimentology (Lankford and Phleger, 1973; Echols and Armentrout, 1980; Quinterno and Gardner, 1987; McGann, 2002), and availability of oxygen and organic matter flux (Altenbach and Sarnthein, 1989; Gooday and Turley, 1990; Jorissen, 1999). Based on the compilation of benthic foraminiferal depth distributions from past studies in the northeastern Pacific, the species living off central California may be assigned to seven biofacies (Ingle, 1980; McGann, 2014). As shows in Fig. 2, these biofacies are estuarine to inner shelf (0e50 m), outer shelf (50e150 m), upper
bathyal (150e500 m), upper middle bathyal (500e1500 m), lower middle bathyal (1500e2000 m), lower bathyal (2000e4000 m), and abyssal (>4000 m). In turn, the presence of these biofacies in marine deposits identifies the sediments as in-situ or displaced (or both), and if allochthonous, their origination site and possible mode of transport (i.e., staged or full-canyon transport; McGann, 2014). Although it is often assumed that turbidites originate in the upper canyons on the slope below the shelf break where enough relief exists to set the sediment in motion when the continental shelf can no longer accommodate the sediment supply (Paull et al., 2005; Piper and Normark, 2009; Covault, 2011), benthic foraminiferal evidence from the turbiditic sand deposits in S3-15G demonstrate that the source area can be as shallow as estuarine or the continental shelf (McGann, 2014). The core site of S3-15G, located at 3491 m water depth, is situated on the lower slope of the continental margin off central California and is represented by the in-situ lower bathyal biofacies (Ingle, 1980; Van Morkhoven et al., 1986; Finger et al., 2007) that resides in Pacific Deep Water. This biofacies is dominated by U. senticosa and M. pompilioides. Some of the dominant faunal constituents of the overlying lower middle bathyal biofacies (1500e2000 m; Ingle, 1980; Corliss, 1991) occur in lower abundance in these deeper waters as well, including G. planulata, Gyroidina gemma Bandy, Gyroidina altiformis Stewart and Stewart, Pullenia bulloides (d'Orbigny), V. araucana, P. wuellerstorfi, G. auriculata, O. umbonatus, Hoeglundina elegans (d'Orbigny), Cibicidoides kullenbergi (Parker), and Melonis barleeanus (Williamson). According to Corliss (1991), the microhabitat preference of several of these deep-sea benthic foraminifera is epifaunal (0e1 cm; C. kullenbergi, H. elegans, and P. wuellerstorfi), whereas P. bulloides is shallow infaunal (0e2 cm) and G. auriculata has the morphology typical of a deep infaunal species (>4 cm). 6.1.1. Q-mode cluster analysis of the hemipelagic muds Q-mode cluster analysis of the benthic foraminiferal hemipelagic mud samples (Fig. 4) segregated them into two groupings, Cluster BFHM1 (Benthic Foraminiferal Hemipelagic Mud
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Fig. 4. Q-mode cluster diagram of benthic foraminiferal relative frequency abundance in 19 hemipelagic mud samples from core S3-15G. The samples are listed by depth in core (cm) and were grouped into two associations. BFHM1 ¼ Benthic Foraminiferal Hemipelagic Mud Association 1; BFHM2 ¼ Benthic Foraminiferal Hemipelagic Mud Association 2.
Association 1) and Cluster BFHM2 (Benthic Foraminiferal Hemipelagic Mud Association 2), reflecting the benthic foraminiferal faunal adaptation to changing oceanographic conditions in the deep sea off central California during the late Quaternary. With the exception of the sample at 24e20 cm that clustered in BFHM1, these clusters are considered to reflect glacial (Pleistocene) and interglacial (Holocene) climates, respectively, based on the position of the PleistoceneeHolocene boundary in this core. However, due to the limited data available, the timing of the PleistoceneeHolocene faunal adaptation is not well defined, having occurred somewhere over about 120 cm of the core (~383e263 cm; ca. 17,000e13,000 cal BP). Cluster BFHM1 represents the fauna endemic to the lower bathyal zone during the Pleistocene. As shown in Fig. 7, this
Fig. 5. Q-mode cluster diagram of benthic foraminiferal relative frequency abundance in 53 hemipelagic and turbiditic (i.e., mixed) mud samples in core S3-15G. The samples are listed by depth in core (cm) and were grouped into two associations. BFMM1 ¼ Benthic Foraminiferal Mixed Mud Association 1; BFMM2 ¼ Benthic Foraminiferal Mixed Mud Association 2.
biofacies includes dominant G. auriculata (mean ¼ 44%) and U. senticosa (mean ¼ 25%) (Supplementary Table 1). The minor constituents are Karreriella grammostomata (Galloway and Wissler) (mean ¼ 5%), M. pompilioides (mean ¼ 4%), G. planulata (mean ¼ 3%), and P. wuellerstorfi (mean ¼ 3%). A similar fauna occurs again near the top of the core (24e20 cm), explaining why this sample is associated with BFHM1. Cluster BFHM2 grouped together species that adapted to the Holocene climatic conditions at lower
Fig. 6. A. R-mode cluster diagram of benthic foraminiferal species in 53 hemipelagic and turbiditic (i.e., mixed) mud samples in core S3-15G. The order of the species names is provided on the left. B. Detail of the dominant or pervasive species that grouped into four associations [Glacial (dominant), Glacial (minor), Interglacial (dominant), and Interglacial (minor)] and one outlier (Transitional). The remainder of the clusters added on the rare species.
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Fig. 7. Relative frequency abundance of the most prominent benthic foraminifera and benthic foraminiferal cluster analysis associations plotted with depth in core S3-15G. Calibrated ages (in bold and italics) include the peak probability ages and 2 sigma ranges. The trend lines indicating the general abundance pattern of the two most abundant foraminifera (Uvigerina senticosa and Globobulimina auriculata) are shown as grey lines. BFHM1 ¼ Benthic Foraminiferal Hemipelagic Mud Association 1; BFHM2 ¼ Benthic Foraminiferal Hemipelagic Mud Association 2; BFMM1 ¼ Benthic Foraminiferal Mixed Mud Association 1; and BFMM2 ¼ Benthic Foraminiferal Mixed Mud Association 2.
bathyal depths. U. senticosa now dominates the biofacies (mean ¼ 30%) (Fig. 7) and M. pompilioides is also a significant species (mean ¼ 19%), whereas G. auriculata dropped significantly in abundance to an average of only 8%. Minor constituents include H. elegans (mean ¼ 6%), G. planulata (mean ¼ 6%), and P. wuellerstorfi (mean ¼ 3%). The presence of U. senticosa in the lower bathyal biofacies is indicative of cool water and as with the genus Uvigerina in general, may be associated with high surface water productivity and increased input of organic matter (Corliss et al., 1986; Burke et al., 1993). M. pompilioides has been shown to be a water massdependent species (Corliss, 1983; Kurihara and Kennett, 1988), with a preference for cool, oxygenated bottom water (Sharma and Mazumdar, 1996). According to Kaiho (1994), both Uvigerina and Melonis are suboxic (0.1e1.5 ml/L) indicators. In contrast, G. auriculata is associated with dysoxic (0.1e0.3 ml/L) environments or is infaunal in high-oxygen (>2 ml/L) bottom water (Kaiho, 1994). Abundant U. senticosa in both Cluster BFHM1 and Cluster BFHM2, and M. pompilioides in BFHM2, indicates cool water prevailed at lower bathyal depths during the Pleistocene and Holocene off central California. The significant decrease in abundance of G. auriculata from the Pleistocene to the Holocene and increased abundance of M. pompilioides in the Holocene may be a response to a slight increase in oxygen in the deep-sea in the Holocene. The association of sample 24e20 cm with BFHM1 suggests a possible return to Pleistocene conditions toward the end of the Holocene at lower bathyal depths off central California. 6.1.2. Q-mode cluster analysis of the combined hemipelagic and turbiditic muds In an effort to more precisely identify the timing of the faunal adaptation to changing climatic conditions from the Pleistocene to Holocene, Q-mode cluster analysis was also used on the census counts recovered in the turbiditic muds as well as those of the hemipelagic muds, increasing the sample size from 19 to a more statistically robust 53 samples. Turbiditic muds may contain
upslope foraminifera that are entrained in the flow and eventually are transported to the site of deposition. These muds may also incorporate hemipelagic sediment as they move down channel and over the levee (Brunner and Normark, 1985). In addition, bioturbation can mix turbiditic and hemipelagic mud after deposition, adding the in-situ fauna to those that have been displaced (Griggs et al., 1969). Because the turbiditic muds in S3-15G include only 5e10% displaced shallow-water species in addition to the endemic lower bathyal fauna (McGann, 2014), the faunas they contain primarily reflect environmental conditions at the core site and can be useful environmental indicators if the displaced species are excluded. This is in contrast to the turbiditic sands in S3-15G, where as much as 39% of the fauna in laminated turbiditic sand (Td) units and 75% of cross-bedded turbiditic sand (Tc) units may be allochthonous (McGann, 2014), making them inappropriate for climatic reconstruction. As with the cluster analysis of only the hemipelagic mud samples, utilizing both hemipelagic and turbiditic (i.e., mixed) muds defined two groupings (Fig. 5): Cluster BFMM1 (Benthic Foraminiferal Mixed Mud Association 1) and Cluster BFMM2 (Benthic Foraminiferal Mixed Mud Association 2). The separation of the two associations is now less than 10 cm apart in the core, rather than 120 cm using the hemipelagic muds alone. The species composition of the mixed mud Cluster BFMM1 (470e270 cm; ca. 20,000e13,000 cal BP) is similar to the hemipelagic mud Cluster BFHM1 in that U. senticosa (mean ¼ 30%) and G. auriculata are still dominant, although the latter dropped somewhat in abundance (mean ¼ 27%) (Fig. 7; Supplementary Table 1). The minor constituents include V. araucana (mean ¼ 4%) and P. wuellerstorfi (mean ¼ 3%), as well as G. gemma, G. planulata, and M. pompilioides that occasionally comprise a significant portion (~5e10%) of the biofacies. This faunal association is thought to represent the glacial (Pleistocene) faunal adaptation. The mixed mud cluster BFMM2 (263e20 cm; ca. 13,000e100 cal BP) is also comparable to the hemipelagic mud Cluster BFHM2, representing the interglacial (Holocene) faunal
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shift. Once again, U. senticosa dominates (mean ¼ 24%) the faunal association, whereas other significant species include M. pompilioides (mean ¼ 14%), G. auriculata (mean ¼ 12%), and G. planulata (mean ¼ 5%), and V. araucana and P. wuellerstorfi are now rare. Interestingly, in this cluster analysis, the sample from 24 to 20 cm now groups with the interglacial samples. In the mixed mud faunal record, the shift in dominance by the low oxygen-indicating species G. auriculata in the Pleistocene to dominance of the oxygen-preferring species M. pompilioides in the Holocene again suggests a possible increase in oxygen at lower bathyal depths from the Pleistocene to Holocene off central California, comparable to the conclusions for the hemipelagic mud samples. In contrast, intermediate water analyzed from the Farallon Escarpment, 93 km northeast of the core site, shows a decrease in dissolved oxygen from the Pleistocene to Holocene, reflecting increased surface productivity and intensity of North Pacific Intermediate Water as the source of the water mass changed from the Sea of Okhotsk to the tropical east Pacific (McGann, 2011). This paleoceanographic change also has been noted elsewhere along California and Oregon in intermediate water (Dean and Gardner, 1998; Kienast et al., 2002; Ivanochko and Pedersen, 2004). 6.1.3. Benthic foraminifera R-mode cluster analysis The R-mode cluster analysis of all 53 mud samples (Fig. 6A) separated the dominant and minor, but pervasive, species of glacial
the Interglacial (minor) Association are M. barleeanus, P. salisburyi, C. kullenbergi, Eggerella bradyi (Cushman), Valvulinera laevigata Phleger and Parker, G. barbata (Cushman), Pyrgo depressa (d'Orbigny), Pyrgo murrhina (Schwager), Lagena striata (d'Orbigny), Lagena hispidula Cushman, Chilostomella ovoidea Reuss, H. elegans, and Buliminella tenuata Cushman. The R-mode cluster analysis clearly differentiated a glacial and interglacial fauna. Dominated by U. senticosa and G. auriculata, the lower bathyal water in the glacial period appears to have been less oxygenated than the interglacial period that was dominated by M. pompilioides, G. planulata, and U. senticosa, but remained cool throughout the last ca. 20,000 cal BP. 6.2. Planktic foraminifera Based on the published results during an earlier investigation by Brunner and Ledbetter (1989), 17 species of planktic foraminifera were recovered in S3-15G (Table 2). The dominant species were N. pachyderma, N. incompta (referred to as right-coiling N. pachyderma), Globigerina bulloides d'Orbigny, Turborotalita quinqueloba (Natland) (referred to as Globigerina quinqueloba), and Globigerinita uvula (Ehrenberg). The planktic foraminiferal record is comprised of 14 samples between 450 and 150 cm in S3-15G. So few specimens were encountered below and above these horizons, respectively, that they were considered barren zones (Fig. 3).
Table 2 Planktic foraminiferal census counts (relative frequency abundance) for core S3-15G. Data modified from Brunner and Ledbetter (1989) (i.e., left-coiling Neogloboquadrina pachyderma ¼ Neogloboquadrina incompta and Globigerina quinqueloba ¼ Turborotalita quinqueloba). Species
Depth in core S3-15G (cm) 150e152 165e167 193e195 200e202 220e222 241e243 256e257 270e272 280e282 288e290 300e302 352e354 428e430 448e450
Globigerina bulloides 1.1 Globigerinita uvula 46.4 Neogloboquadrina 21.4 incompta Neogloboquadrina 17.2 pachyderma Turborotalita 12.7 quinqueloba Other species 1.1 Unidentified 0.3 Total specimens 379
11.8 24.6 10.7
4.6 25.7 17.4
3.7 9.7 28.7
33.8 27.0 17.6
0.5 14.7 8.5
0.7 54.1 15.7
5.8 9.7 31.6
2.3 33.5 6.5
0.0 29.5 2.3
5.9 4.1 14.1
3.8 47.0 1.0
1.1 54.6 0.9
3.6 44.4 5.3
2.5
1.2
2.1
14.9
37.9
17.1
23.5
11.9
56.8
70.0
15.3
21.5
39.8
42.2
46.3
55.1
0.0
37.1
11.3
26.5
37.3
9.1
4.4
22.0
8.1
6.6
0.5 7.8 448
2.9 2.0 350
0.7 0.0 703
5.4 1.4 74
0.0 1.3 224
0.7 0.3 292
1.6 1.3 310
2.3 6.2 260
0.0 2.3 44
1.5 0.0 340
4.2 6.6 287
13.2 0.6 469
0.0 0.3 304
and interglacial periods (Fig. 6B) from the remainder of the rare species. The Glacial (dominant) Association includes two species, G. auriculata and U. senticosa, which occurred together in the Pleistocene and dominated the benthic foraminiferal assemblages (Fig. 7). The less abundant species at this time [the Glacial (minor) Association] include G. altiformis, G. gemma, P. bulloides, P. wuellerstorfi, K. grammostomata, Cassidulina minuta Cushman, and O. umbonatus. In the late Pleistocene and early Holocene, V. araucana is one of the more abundant species (Fig. 7) and is identified in the R-mode cluster analysis as an outlier (i.e., Transitional Outlier; Fig. 6B). During the interglacial period, M. pompilioides and G. planulata dominate the assemblage along with U. senticosa (i.e., note the nearly vertical trend line of this species throughout the Pleistocene and Holocene in Fig. 7), whereas the abundance of G. auriculata declines substantially (i.e., a decreasing trend line upcore in Fig. 7) until ca. 1000 cal BP when it increases again. For this reason, the Rmode cluster analysis grouped together M. pompilioides and G. planulata (Fig. 6B), defined here as the Interglacial (dominant) Association. The minor species in the interglacial period making up
6.2.1. Planktic foraminiferal Q-mode cluster analysis Q-mode cluster analysis of the census counts were reported in Brunner and Ledbetter (1989) but were rerun here in order to isolate the data for S3-15G from a larger data set and to use a similarity coefficient (BrayeCurtis) consistent with the other analyses in this study. The analysis separated the samples into two clusters, PF1 (Planktic Foraminiferal Association 1) and PF2 (Planktic Foraminiferal Association 2), and two outliers (Fig. 8). Cluster PF1 includes those samples from 450 to 288 cm with the addition of two others (257e256 and 152e150 cm). Brunner and Ledbetter (1989) considered all of these to be subarctic faunas except the one at 290e288 cm that they thought was a dissolution fauna. Their subarctic fauna is characterized by high frequencies of N. pachyderma, with lesser abundances of T. quinqueloba and G. uvula, whereas their dissolution fauna has similar species but the specimens are corroded and the samples have lower than average foraminiferal numbers. N.pachyderma is a dissolution resistant morphotype (Parker and Berger, 1971; Malmgren, 1983; Reynolds and Thunell, 1986) that prefers colder water (6e8 C) of the subpolar to polar regions (Bandy, 1972; Kennett, 1976; Keller, 1978;
M. McGann / Quaternary International 387 (2015) 58e71
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nearby off central California (planktic assemblage PFI of Gardner et al., 1988; planktic Cluster E of McGann, 2011). Cluster PF2 grouped the samples from 280 to 165 cm. Brunner and Ledbetter (1989) classified these samples as having a transitional assemblage, except for the sample from 243 to 241 cm that they considered an outlier. Their transitional assemblage has high frequencies of T. quinqueloba and G. uvula and low frequencies of N. pachyderma. The two remaining outliers at 222e220 cm and 302e300 cm were classified by Brunner and Ledbetter (1989) as representing upwelling and dissolution faunas, respectively. The upwelling fauna at 222e220 cm has high frequencies of G. bulloides and G. uvula. G. bulloides is another highly solution-resistant taxon (Berger, 1968; Thunell and Honjo, 1981) but is eurythermal (5e26 C) with an affinity for high food availability (Ortiz et al., 1995; Field, 2004), such as that associated with spring upwelling (Thunell and Reynolds, 1984; Reynolds and Thunell, 1985; Sautter and Thunell, 1989, 1991). Cluster PF2 species are thought to represent slightly warmer, transitional conditions and have been reported off central California in the vicinity of the Russian River (38 25.510 N, 123 47.770 W; planktic assemblage PFII of Gardner et al., 1988) and the Farallon Escarpment (3713.40 N, 12314.60 W; planktic Cluster D of McGann, 2011). Based on the position of the PleistoceneeHolocene boundary in S3-15G, Cluster PF1 shows the faunal response to glacial (Pleistocene) conditions in the surface waters off central California and Cluster PF2 shows the interglacial (Holocene) response. The clusters separate into glacial (450e288 cm; ca. 20,000e14,100 cal BP) and interglacial (282e150 cm; ca. 14,100e5000 cal BP) faunas at about 285 cm. 6.3. Pollen record and Q-mode cluster analysis
Fig. 8. Q-mode cluster diagram of planktic foraminiferal relative frequency abundance in 14 hemipelagic mud samples in core S3-15G. The samples are listed by depth in core (cm) and were grouped into two associations and two outliers. PF1 ¼ Planktic Foraminiferal Association 1; PF2 ¼ Planktic Foraminiferal Association 2.
Coulbourn et al., 1980; Sautter and Thunell, 1989) with high nutrient content and a poorly developed thermocline (Reynolds and Thunell, 1986). G. uvula also prefers cold water of both the subarctic (Brunner and Ledbetter, 1989) and subantarctic (Boltovskoy et al., 2000). T. quinqueloba is eurythermal (5e26 C) and common during diatom blooms (Sautter and Thunell, 1991; Kincaid et al., 2000), with the highest fluxes of the species occurring early during the onset of upwelling (Kincaid et al., 2000). In this present study, the species associated with Cluster PF1, with elements of both the subarctic and dissolution faunas of Brunner and Ledbetter (1989), are considered to represent cool, subarctic conditions. A similar cool-water indicating fauna has been reported
The response of the terrestrial flora to changing climatic conditions in the California Coast Ranges of central California during the late Quaternary is presented in McGann (2015). Pinus (pine), Sequoia (redwood), Quercus (oak) and high-spine Asteraceae (composites) were the most abundant pollen types recovered from S3-15G, whereas Abies (fir), Amaranthaceae (coastal strand vegetation), Rhamnaceae [most likely Ceanothus thyriflorus Eschscholtz (blue brush) and Rhamnus californicus Eschscholtz (coffeeberry)], Notholithocarpus densiflora (Hooker and Arnott) (tanoak), Alnus (alder), Poaceae (grass), Salix (willow), low-spine Asteraceae (composites), Artemisia (sagebrush), and Eriogonum (buckwheat) were minor constituents of the pollen record. Q-mode cluster analysis divided the pollen record into three groupings, Cluster P1 (Pollen Association 1), Cluster P2 (Pollen Association 2), and Cluster P3 (Pollen Association 3), two of which are Pleistocene in age and the third is Holocene (Fig. 9). Cluster P1 (472e381 cm; ca. 20,000e17,000 cal BP) is characterized by very abundant Pinus and rare Abies pollen, reflecting environmental conditions during the last glacial maximum. Overlying this is Cluster P2 (381e226.5 cm; ca. 17,000e11,600 cal yr BP) containing a pollen assemblage indicative of a transitional climatic regime with decreasing Pinus and Artemisia, and increasing abundance of Sequoia and Alnus. The algae Pediastrum and dinoflagellates are also common and are attributable to increased nutrient-rich coastal runoff. Cluster P3 (226.5e0 cm; ca. 11,600 cal BP to the present) is characterized by decreasing Pinus pollen and increasing Sequoia, Quercus, and composites, reflecting changes in vegetation during the climatic warming of the Holocene. Two brief drier periods are also represented in this pollen zone, one from ca. 150e125 cm (ca. 8000e6400 cal BP) that correlates with the middle Holocene dry period (Thompson, 1992; Quade et al., 1998; Grayson, 2000; Benson et al., 2002; Mensing et al., 2013), and another in the late Holocene (ca. 22e20 cm; ca. 800e700 cal BP), coincident with the droughts
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Fig. 9. Correlation and chronology of deep marine, surface marine, and terrestrial floral records in S3-15G based on the frequency abundance of benthic foraminifera, planktic foraminifera, and pollen, respectively. Separate Q-mode cluster analyses defined nine associations: BFHM1 and BFHM2 ¼ Benthic Foraminiferal Hemipelagic Mud Associations 1 and 2; BFMM1 and BFMM2 ¼ Benthic Foraminiferal Mixed Mud Associations 1 and 2; PF1 and PF2 ¼ Planktic Foraminiferal Associations 1 and 2; P1, P2, and P3¼ Pollen Associations 1, 2 and 3. Stippled areas represent drier periods.
associated with the Medieval Climate Anomaly (ca. 1200-750 cal BP; Stine, 1994; Cronin et al., 2003; Kleppe et al., 2011; ca. 1100-700 cal BP in Mann, 2002). 6.4. Correlation of marine and terrestrial response to climate change A comparison of the concurrent records of the bottom-dwelling benthic foraminifera in the deep sea, surface-dwelling planktic foraminifera, and marine pollen show asynchronous responses to changing paleoceanographic conditions and terrestrial climate during the late Quaternary off central California (Fig. 9). In the lower ~200 cm of S3-15G (BFMM1, 472e265 cm; ca. 20,000e13,000 cal BP), the lower bathyal benthic foraminiferal assemblage represents the faunal adaptation to the cold oceanographic conditions of the last full glacial interval. In the surface water, the planktic foraminifer N. pachyderma far outnumbers N. incompta (472e295 cm; Fig. 3; ca. 20,000e14,600 cal BP), indicating cold-water (glacial) conditions as well. The character of the terrestrial pollen record changes first, responding to the onset of climatic warming as continental deglaciation began. The pollen assemblage changes from a glacial, Pinusdominated flora (P1) to a transitional flora with increasing Sequoia and Alnus (P2) near a depth of 381 cm (ca. 17,000 cal BP) in S3-15G. The surface-dwelling planktic foraminifera are next to respond, as their glacial assemblage (PF1) (“subarctic” of Brunner and Ledbetter, 1989) is replaced by an interglacial fauna (PF2) (“transitional” of Brunner and Ledbetter, 1989) at 285 cm (ca. 14,100 cal BP), signifying the beginning of warmer surface paleoceanographic conditions. Similarly, the shift from dominance of cool water-indicating N. pachyderma to warm water-indicating N. incompta at this time suggests the onset of deglaciation (BøllingeAllerød; 14,600e12,900 BP). Finally, based on the cluster analysis of the mixed hemipelagic and turbiditic muds, it is not until about 265 cm (13,000 cal yr BP) that the benthic foraminiferal assemblage shows a response to changing paleoceanographic
conditions in the deep sea (BFMM2). A decoupling of the planktic and benthic foraminiferal responses to climate change, with the surface water response leading the bottom water by several millennia, was noted nearby in North Pacific Intermediate Water on the Farallon Escarpment (McGann, 2011) as well, whereas a correlation of a terrestrial floral record from Clear Lake, CA and the adjacent marine record off central California over the past 20,000 years found a complex record suggesting a disequilibrium mode that lasted from about 15,000 to 5000 years ago (Gardner et al., 1988). Both the planktic foraminiferal and pollen records are more sensitive to the environmental changes than are the benthic foraminifera in the deep sea. At the end of the Pleistocene, the planktic record shows several shifts in the ratio of N. pachyderma to N. incompta between 295 and 212 cm (Fig. 9), interpreted to represent the onset of deglaciation already noted (BøllingeAllerød; 295e256 cm; 14,600e12,900 BP), a short glacial advance (the Younger Dryas; 256e243 cm; 12,900e11,600 BP), and the re-establishment of deglaciation at the PleistoceneeHolocene boundary (ca. 226.5 cm; 11,600 BP). These faunal trends have been noted in planktic foraminiferal faunas in cores elsewhere off California and Oregon (Gardner et al., 1988; Mathewes et al., 1993; Mix et al., 1999; Barron et al., 2003; McGann, 2011). In contrast, the benthic foraminiferal assemblage does not appear to shift significantly over this time period. Likewise, alterations in the pollen record during the Holocene interglacial suggesting a middle Holocene drier period and the Medieval Climate Anomaly are not evident in the planktic or benthic foraminiferal marine records. Extensive dissolution characterizes the planktic foraminiferal record in S3-15G from 150 to 0 m (Brunner and Ledbetter, 1989) and the benthic foraminiferal record in the core-top sediments (0e4 cm) as well. This interval of intense carbonate dissolution during the late Holocene has been reported nearby off central California (Brunner and Normark, 1985; ca. 5000 cal BP to present in Gardner et al., 1988; Brunner and Ledbetter, 1989; McGann, 2011)
M. McGann / Quaternary International 387 (2015) 58e71
and elsewhere in the Pacific Ocean (Keir and Berger, 1985, and references therein). 7. Conclusions Use of benthic and planktic foraminiferal and pollen records from a deep-sea core obtained at about 3500 m water depth from the western levee of Monterey Canyon has documented a dramatic change in the microfauna off central California and flora of the California Coast Ranges of central California over the last 19,000 years. The benthic and planktic foraminiferal faunas reflect the deep-sea and shallow-marine response to changing paleoceanographic conditions, respectively, whereas the pollen responds to changing terrestrial climate. Distinct glacial and interglacial assemblages were identified in all three records. The shallow-marine record is more sensitive to climate change than that of the deep-sea, however, in that the short deglaciation event (BøllingeAllerød) and subsequent climatic cooling (Younger Dryas) at the end of the Pleistocene are evident. Even more sensitive yet is the terrestrial floral record, with a pronounced transitional fauna apparent between the glacial and interglacial intervals, as well as a middle Holocene drier period and the Medieval Climate Anomaly evident. Clearly, all three records are asynchronous, with the terrestrial floral response occurring several millennia before the surfacemarine waters, followed by the deep-sea a millennium later. Acknowledgements I thank the late William Normark (USGS) for making core S315G available for study, Christina Gutmacher (USGS) for aiding in the core description, and Charlotte Brunner (University of Southern Mississippi) for helping with the core description as well as the design and implementation of the investigation. Radiocarbon dates were kindly provided by Michaele Kashgarian of Lawrence Livermore National Laboratory's Center for Accelerator Mass Spectrometry and the staff of Beta Analytic. This manuscript greatly benefited by reviews provided by Eileen Hemphill-Haley (Humboldt State University), Scott Ishman (Southern Illinois University Carbondale), and Charles Powell, II and Scott Starratt (USGS). Appendix A. Supplementary data Supplementary data related to this article can be found at http:// dx.doi.org/10.1016/j.quaint.2015.01.037. References Alley, R.B., 2000. The Younger Dryas cold interval as viewed from central Greenland. Quaternary Science Reviews 19, 213e226. Alley, R.B., Meese, D.A., Shuman, C.A., Gow, A.J., Taylor, K.C., Grootes, P.M., White, J.W.C., Ram, M., Waddington, E.D., Mayewski, P.A., Zielinski, G.A., 1993. Abrupt increase in Greenland snow accumulation at the end of the Younger Dryas event. Nature 362, 527e529. http://dx.doi.org/10.1038/362527a0. Altenbach, A.V., Sarnthein, M., 1989. Productivity record in benthic foraminifera. In: Berger, W.H., Smetacek, V.S., Wefer, G. (Eds.), Productivity of the Ocean: Present and Past. Wiley, Chichester, pp. 255e269. Bakun, A., 1990. Global climate change and intensification of coastal ocean upwelling. Science 247, 198e201. http://dx.doi.org/10.1126/science.247.4939.198. Bandy, O.L., 1960. The geologic significance of coiling ratios in the foraminifer Globigerina pachyderma (Ehrenberg). Journal of Paleontology 34, 671e681. Bandy, O.L., 1972. Origin and development of Globorotalia (Turborotalia) pachyderma (Ehrenberg). Micropaleontology 18, 294e318. Barron, J.A., Heusser, L., Herbert, T., Lyle, M., 2003. High-resolution climatic evolution of coastal northern California during the past 16,000 years. Paleoceanography 18, 20-1e20-14. http://dx.doi.org/10.1029/2002PA000768. Benson, L., Kashgarian, M., Rye, R., Lund, S., Paillet, F., Smoot, J., Kester, C., Mensing, S., Meko, D., Lindstrom, S., 2002. Holocene multidecadal and multicentennial droughts affecting Northern California and Nevada. Quaternary Science Review 21, 659e682.
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