Modern distribution of dinocysts from the North Pacific Ocean (37–64°N, 144°E–148°W) in relation to hydrographic conditions, sea-ice and productivity

Marine Micropaleontology 84-85 (2012) 87–113

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Modern distribution of dinocysts from the North Pacific Ocean (37–64°N, 144°E–148°W) in relation to hydrographic conditions, sea-ice and productivity Sophie Bonnet a,⁎, Anne de Vernal a, Rainer Gersonde b, Lester Lembke-Jene b a Centre de Recherche en Géochimie Isotopique et en Géochronologie (GEOTOP), Université du Québec à Montréal, Case postale 8888, Succursale Centre-Ville, Montréal, Québec, Canada H3C 3P8 b Alfred Wegener Institute for Polar and Marine Research (AWI), Bremerhaven, Germany

a r t i c l e

i n f o

Article history: Received 29 March 2011 Received in revised form 14 November 2011 Accepted 19 November 2011 Keywords: North Pacific Ocean Bering Sea Okhotsk Sea Transfer functions Sea-surface

a b s t r a c t Palynological analyses were performed on 53 surface sediment samples from the North Pacific Ocean, including the Bering and Okhotsk Seas (37–64°N, 144°E–148°W), in order to document the relationships between the dinocyst distribution and sea-surface conditions (temperatures, salinities, primary productivity and sea-ice cover). Samples are characterized by concentrations ranging from 18 to 143816 cysts/cm3 and the occurrence of 32 species. A canonical correspondence analysis (CCA) was carried out to determine the relationship between environmental variables and the distribution of dinocyst taxa. The first and second axes represent, respectively, 47% and 17.8% of the canonical variance. Axis 1 is positively correlated with all parameters except to the sea-ice and primary productivity in August, which are on the negative side. Results indicate that the composition of dinocyst assemblages is mostly controlled by temperature and that all environmental variables are correlated together. The CCA distinguishes 3 groups of dinocysts: the heterotrophic taxa, the genera Impagidinium and Spiniferites as well as the cyst of Pentapharsodinium dalei and Operculodinium centrocarpum. Five assemblage zones can be distinguished: 1) the Okhotsk Sea zone, which is associated to temperate and eutrophic conditions, seasonal upwellings and Amur River discharges. It is characterized by the dominance of O. centrocarpum, Brigantedinium spp. and Islandinium minutum; 2) the Western Subarctic Gyre zone with subpolar and mesotrophic conditions due to the Kamchatka Current and Alaska Stream inflows. Assemblages are dominated by Nematosphaeropsis labyrinthus, Pyxidinopsis reticulata and Brigantedinium spp.; 3) the Bering Sea zone, depicting a subpolar environment, influenced by seasonal upwellings and inputs from the Anadyr and Yukon Rivers. It is characterized by the dominance of I. minutum and Brigantedinium spp.; 4) the Alaska Gyre zone with temperate conditions and nutrientenriched surface waters, which is dominated by N. labyrinthus and Brigantedinium spp. and 5) the Kuroshio Extension-North Pacific-Subarctic Current zone characterized by a subtropical and oligotrophic environment, which is dominated by O. centrocarpum, N. labyrinthus and warm taxa of the genus Impagidinium. Transfer functions were tested using the modern analog technique (MAT) on the North Pacific Ocean (=359 sites) and the entire Northern Hemisphere databases (=1419 sites). Results confirm that the updated Northern Hemisphere database is suitable for further paleoenvironmental reconstructions, and the best results are obtained for temperatures with an accuracy of ±1.7 °C. © 2011 Elsevier B.V. All rights reserved.

1. Introduction Organic-walled dinoflagellate cysts (dinocysts) are commonly used as a proxy for environmental conditions in the upper water column. It is now well established that their modern distribution is determined by hydrographic parameters such as temperature, salinity and the seasonal duration and extent of the sea-ice cover (e.g., Williams, 1977; ⁎ Corresponding author. Tel.: + 1 514 987 4080; fax: +1 514 987 3635. E-mail addresses: [email protected] (S. Bonnet), [email protected] (A. de Vernal), [email protected] (R. Gersonde), [email protected] (L. Lembke-Jene). 0377-8398/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.marmicro.2011.11.006

Harland, 1988; de Vernal et al., 1994, 1997, 2001, 2005; Rochon et al., 1999). The distribution of dinocysts seems also related to productivity and nutrient availability (e.g., Radi and de Vernal, 2008). Although only 10 to 20% of dinoflagellate species produce fossilizable cysts during their life cycle, dinocyst assemblages can be used as a proxy for seasurface conditions in which dinoflagellate populations developed (Taylor and Pollingher, 1987; Fensome et al., 1993, 1996). Contrary to siliceous and calcareous microfossils like diatoms, radiolarians, coccolithophorids and foraminifera, dinocysts that are formed by a highly resistant organic matter (dinosporin) are not affected by dissolution (Dale, 1976; Harland, 1988; Kokinos et al., 1998; Versteegh and Blokker, 2004). Nonetheless, even if dinocysts are usually well preserved

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in marine sediment, it has been demonstrated that some taxa are sensitive to oxidation (Zonneveld et al., 2008, 2010). Dinocyst assemblages constitute a useful proxy for the reconstruction of past sea-surface conditions like temperature, salinity, seasonality, sea-ice cover, and primary productivity (e.g., de Vernal et al., 1994, 1997, 2005; Radi and de Vernal, 2008). Quantitative paleoceanographic and paleoenvironmental reconstructions from transfer functions require large databases representative of diverse environmental conditions (e.g., de Vernal et al., 2005). Most studies conducted on recent dinocyst assemblages, for the development of a reference database, focused on the North Atlantic Ocean (e.g., de Vernal et al., 1994; Rochon et al., 1999) and the marginal Arctic and subarctic seas (e.g., Rochon and de Vernal, 1994; Matthiessen, 1995; Grøsfjeld and Harland, 2001; Kunz-Pirrung, 2001; Mudie and Rochon, 2001; Radi et al., 2001; Voronina et al., 2001; Hamel et al., 2002; Novichkova and Polyakova, 2007; Richerol et al., 2008; Grøsfjeld et al., 2009; Solignac et al., 2009; Bonnet et al., 2010). A few were performed off the northwest coast of Africa (Marret, 1994; Targarona et al., 1999; Bouimetarhan et al., 2009) and off the northeast coast of Brazil (Vink et al., 2000). However, unlike the Atlantic–Arctic regions, the North Pacific Ocean is still poorly documented. Some works were conducted on dinocysts from the western Pacific notably along the north and west coasts of Japan (Matsuoka, 1985, 1987; Kobayashi et al., 1986; Furio et al., 2006), off Korea (Shin et al., 2007; Pospelova and Kim, 2010), in the Philippine Sea (Matsuoka, 1981) and in the Yellow and China Seas (Cho and Matsuoka, 2001; Kawamura, 2004; Wang et al., 2004). Few researches were carried out in the Okhotsk Sea (Miyazono and Minoda, 1990; Selina and Morozova, 2005; Hoppenrath and Selina, 2006; Selina and Orlova, 2009) but they focused on dinoflagellates from the water column and did not document the distribution of dinocysts in marine sediments. There are few other ones about the distribution of dinocyst assemblages off the American and Mexican coasts (16–60°N) in relation with sea-surface salinities and temperatures, upwelling intensity, productivity as well as geochemical parameters such as organic carbon, nitrogen and opal (Radi and de Vernal, 2004; Radi et al., 2007; Pospelova et al., 2008; VásquezBedoya et al., 2008; Krepakevich and Pospelova, 2010; Limoges et al., 2010). The subarctic domain including the Bering Sea was explored by Radi et al. (2001) who documented the modern distribution of dinocysts. Finally, it is relevant to mention that some studies were undertaken in the Southern Hemisphere: the South Atlantic Ocean, off the southwest coast of Africa (Zonneveld et al., 2001; Holzwarth et al., 2007), off the east coast of New Zealand (McMinn and Sun, 1994; Sun and McMinn, 1994; Crouch et al., 2010), off the Chilean coast (Verleye and Louwye, 2010) and in the Southern Ocean (Marret and de Vernal, 1997; Esper and Zonneveld, 2002, 2007). Here, we report on the distribution of dinocyst assemblages from 53 surface sediment samples collected in the northern North Pacific Ocean, including the Okhotsk and Bering Seas (Fig. 1 and Table 1). Sampling sites encompass areas from temperate to subpolar regions and are located from Asian to American coasts (i.e., 37–64°N, 144°E–148°W). We aim at providing an overview of dinocyst taxonomic diversity in the northern North Pacific Ocean and documenting the relationships between the species and sea-surface conditions to North Pacific surface water masses and/or currents. The ultimate objective of this work is to update the North Pacific Ocean database and the Northern Hemisphere reference database for further paleoceanographic and paleoenvironmental reconstructions like in the North Atlantic and Arctic Oceans. 2. Regional setting 2.1. Atmospheric circulation Thermodynamic properties of upper water masses in the North Pacific region are determined by the Pacific/North American pattern

(PNAP), Pacific decadal oscillation (PDO) and Aleutian low (AL). The PNAP was defined by Wallace and Gutzler (1981) as a linear relation of the normalized height anomalies at four centers located near Hawaii (20°N 160°W), over the North Pacific (45°N 165°W), over Alberta (55°N 115°W) and over the Gulf of Mexico (30°N 85°W). Developed by Hare (1996) and Zhang (1996), the PDO presents a similar pattern to El Niño except that its period is longer (20–30 years). Warm PDO phases are associated with cool anomalies of sea-surface temperatures (SSTs) over the central North Pacific and warm SSTs anomalies along the west American coasts (Mantua and Hare, 2002). Although the PNAP and PDO play a key role on ocean–atmosphere exchanges and global climate over the North Pacific, the AL constitutes the main atmospheric pattern. The location and intensity of the AL pressure centers control the regional winter climate and storm trajectories. A measure of the AL strength is provided by the North Pacific index (NPI), which corresponds to the weighted mean sea level pressure from 30 to 65°N and 160°E to 140°W (Trenberth and Hurrell, 1994). A positive value of NPI corresponds to a weak AL. In this case, the AL is split into two centers, one over the northwest Pacific (near the Kamchatka Peninsula) and another over the Gulf of Alaska. The effect on sea-surface conditions is not negligible, for instance, warmer SSTs in the Bering Sea during strong AL are accompanied by a rise in storm frequency (e.g., Overland et al., 1999; Rodionov et al., 2005a, 2005b, 2007). Schwing et al. (2002) have introduced the Northern oscillation index (NOI) as a new climate indicator of the North Pacific–North American area. It is based on the difference between the sea level pressure anomalies over the northeast Pacific and the western tropical Pacific, located near Darwin, Australia. The NOI is positively correlated with SSTs in the central North and South Pacific and negatively on the west coast of Americas. The NOI magnitude tends to be more significant in winter and spring. All these patterns and oscillations are interconnected. For example, Wallace and Gutzler (1981) have established a relationship between the PNAP and AL. Negative values of PNAP are associated with weak AL. Trenberth and Hurrell (1994) found an anti-correlation (R = −0.91) between the PNAP and NPI on a five-month mean for the period 1947–1991. Rodionov et al. (2007) demonstrated that depending upon the PDO and AL strength the northerly winds could modify the air temperature over the Bering Sea. Thus, during a negative PDO phase and a weak AL, a strong relationship between the northerly winds and air temperature is recorded. 2.2. Modern oceanography 2.2.1. North Pacific Ocean The Kuroshio Extension (KuE) is situated in the western Pacific Ocean and represents the eastward extension of the Kuroshio Current (KuC), which originates at 15°N and separates from the Japanese coast at 35°N and 140°E. Near 159°E, the current encounters the Shatsky Rise that slightly deflects the trajectory toward the northeast. Off the Emperor Seamounts (171°E), it becomes wider (150 km) and forms the North Pacific Current (NPC; Qiu, 2000). The transport of this warm and salty water mass is accompanied by an annual heat loss ranging from −50 to − 150 W/m 2 with values reaching up to −450 W/m 2 during wintertime (Da Silva et al., 1994; Qiu, 2000). The KuE system illustrates a large-scale interannual variability that is characterized by an elongated and contracted stage. This bimodal behavior was brought out by altimetry data and results from a nonlinear dynamic induced by wind stress (Qiu, 2000). Moreover, the KuE is also characterized by numerous eddies that modified the seasurface conditions by generating winter SST anomalies and altering the heat budget (Rogachev and Shlyk, 2009a, 2009b). The Subarctic Current (SC) is located north of the KuE–NPC system (42–50°N). Both currents are separated by the Subarctic Frontal Zone (SFZ) that constitutes a permanent and narrow thermal front, from the west to east coast of the North Pacific Ocean. It is located between

S. Bonnet et al. / Marine Micropaleontology 84-85 (2012) 87–113

89

CHUKCHI SEA

SIBERIA

Anadyr River outlet

ALASKA

bs AC

50

31

29

100

30 rin

60°N KC

KA MC HA TK A

ns

AS

KC

7

6

15

22

17

11

ESaC

89 10

Alaska Gyre

40 GULF

OF ALASKA

1000

41

PAPA

2000

SA

3000

8

NORTH PACIFIC OCEAN

SC

43

44

ys

39

36 35

42

fvs

SC

up

AS

Western Subarctic Gyre

bus

Umnak Plateau

ANSC

as

13

Kuril Basin

AB

37

20

krs

ss

500

38

ap

19

50N

14

21

bp

18

M6 cks

AC

33 34

Bowers Ridge 23 Bowers Basin

16

KC

5

Aleutian Basin

OC

Amur River outlet

32

25 24

M4

ESaC

SAKHALIN

4

250 ACC

Bathymetry (m)

OKHOTSK SEA

1

ts

BERING SEA

C

32

f

Arc tic Fro nt

Shirshov Ridge

ks

Yukon River outlet

BS

Tinro Basin

Deryugin Basin

ka at ch n m si Ka Ba

Sh

el

26 KC

50°N

g

WA C

Be

28 27

4000

12

KNOT SC

C

O

5000 45

51

50 49

48 KuE

Subarc 7

NPC

47

NPC

KuC

140°E

160°E

6000

46

JA

PA N

52 KuE

l Zone tic Fronta

40N

Ocean Data View

53

40°N

180°E

6500

160°W

Fig. 1. Location map of the 53 surface sediment samples from the North Pacific Ocean (red circles). Surface currents are represented by black arrows (thin = cold currents and thick = warm currents). The Arctic Front that is associated with the maximum sea-ice extent in winter is indicated by the white dashed line. White stars indicate location of sediment traps (cf. Discussion part). Here, we show the February sea-ice extent based on the period 1979–2005 with a concentration ≥ 15% (NSIDC, 2003; Stroeve and Meier, 2005). The Subarctic Frontal Zone (yellow dashed line) separates the warm and salty water masses from the south to the cold and fresh waters from the north. KuC: Kuroshio Current, KuE: Kuroshio Extension, NPC: North Pacific Current, SC: Subarctic Current, ACC: Alaska Coastal Current, AC: Alaska Current; AS: Alaska Stream, ANSC: Aleutian North Slope Current, BSC: Bering Slope Current, WAC: West Alaska Current, AC: Anadyr Current, KC: Kamchatka Current, OC: Oyashio Current, ESaC: east Sakhalin Current, bs: Bering Strait, up: Unimak Pass, ap: Amutka Pass, as: Amchitka Strait, bp: Buldir Pass, ns: Near Strait, ks: Kamchatka Strait, cks: Chetvertiy Kuril Strait, krs: Kruzenshtern Strait, bus: Bussol Strait, fvs: Friz (De Vries) Strait, ys: Yekaterina Strait, ss: Soya Strait. The map was realized with Ocean Data View 4.3.6 (Schlitzer, 2010).

40 and 44°N in the western and central Pacific, thus separating the cold and fresh water masses to the north from the warm and salty waters to the south. Data from 1968 to 1993 do not show seasonal variations of the SFZ location (Yuan and Talley, 1996). Nevertheless, SSTs vary significantly along the front with amplitudes reaching up to 10.44 °C annually whereas the salinity appears more uniform with an annual variation of 0.23 (Yuan and Talley, 1996). Centered in the Gulf of Alaska, the Alaska Gyre (AG) is mainly controlled by the SC and the Alaska Coastal Current (ACC ~ 1.2 Sv near Kodiak Island; cf. Stabeno et al., 2002). In the Gulf of Alaska, the NPC divides into a northward flow, the Alaska Current (AC) coupled with the ACC, and a southward flow associated with the California Current (CC). The AC–ACC extends westward along the Aleutian and Commander Islands to form the Alaska Stream (AS) which is 100 km wide and centered between 50 and 51°N (e.g., Stabeno et al., 2004). The Kamchatka Current (KC) originates in the Bering Sea. It follows the Siberian and Kamchatka Peninsula coasts and extends into the Oyashio Current (OC), which flows along the Kuril Islands and the Japanese coast. The Oyashio water masses occur until 37°N near 145°E. The region located south of 40°N and east of 146°E is associated with modified Kuroshio water masses. The water transport of the Kamchatka–Oyashio system is essentially determined by the pressure gradient related to the halocline depth along the continental slope (e.g., Stabeno et al., 1994; Yasuda, 1997). 2.2.2. Bering Sea The Bering Sea is regarded as a transitional basin between the Arctic and Pacific Ocean. It is delimited to the north by the Bering Strait

(45 m deep and 85 km wide), surrounded by the Siberia and the Kamchatka Peninsulas in the northwest, Alaska in the northeast and the Commander and Aleutian Islands in the south. The basin is supplied continuously by freshwater from the Anadyr (Siberia) and Yukon (Alaska) Rivers. The Bering Sea is characterized by a wide shallow continental shelf and three deep basins (Aleutian, Kamchatka and Bowers Basins) separated by the Shirshov and Bowers Ridges (Roden, 1995; Fig. 1). It is also characterized by high productivity on the continental shelf and is the origin of the name “Green Belt” given by Springer et al. (1996; cf. also Mordy et al., 2005; Sambrotto et al., 2008; http://modis.gsfc.nasa.gov/). The Alaskan Stream (AS) and a part of the ACC–AC penetrate into the Bering Sea through the numerous passes and straits of the Aleutian and Commander Islands. The main ones are, from the east to west (e.g., Stabeno et al., 1999): Unimak Pass (80 m), Amutka Pass (400 m), Amchitka Strait (1000 m), Buldir Pass (500 m), Near Strait (2000 m) and Kamchatka Strait (3600 m). It is worth mentioning that the flows through straits and passes can be bidirectional depending upon tidal currents (e.g., Reed and Stabeno, 1997, 1999; Stabeno et al., 2005). Once inside the Bering Sea, the AS forms the Aleutian North Slope Current (ANSC), which moves eastward and bifurcates northward to form the Bering Slope Current (BSC). A part of the ANSC continues along the Aleutian Islands to reach the Alaskan coast and forms the west Alaska Current (WAC), which flows northward through the Bering Strait. The BSC flows along the continental shelf slope and separates into two branches: one turns eastward and encounters the Anadyr Current that passes through the Bering Strait with the WAC. The other flows westward to form the KC along the Siberia then the Kamchatka Peninsula coasts. The ANSC,

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Table 1 Geographical coordinates, coring devices and water depths of surface sediment samples. The sample number corresponds to the location in Fig. 1. Cruise

Region

R/V Akademik Lavrentyev LV 28 (1998) R/V Marshal Gelovany GE 99 — KOMEX (1999) R/V Marshal Gelovany GE 99 — KOMEX (1999) R/V Marshal Gelovany GE 99 — KOMEX (1999) R/V Akademik Lavrentyev LV 28 (1998) R/V Akademik Lavrentyev LV 28 (1998) R/V Akademik Lavrentyev LV 28 (1998) R/V Akademik Lavrentyev LV 28 (1998) R/V Marshal Gelovany GE 99 — KOMEX (1999) R/V Akademik Lavrentyev LV 28 (1998) R/V Marshal Gelovany GE 99 — KOMEX (1999) R/V Sonne SO202 — INOPEX (2009)

Okhotsk Sea (Deryugin Basin)

Sample Site number

Laboratory Coring number device

Latitude Longitude Water (°N) (°W) depth (m)

1

LV28-34-1

2608-3

Multicore 53.86

146.75

1405

2

GE99-31-3

2654-6

Multicore 54.39

145.92

1600

3

GE99-30-2

2654-5

Multicore 54.40

145.14

1470

4

GE99-12-3

2615-3

Multicore 52.84

144.79

930

5

LV28-4-3

2608-2

Multicore 51.15

145.31

675

6

LV28-41-3

2608-4

Multicore 51.69

149.07

1068

7

LV28-43-3

2608-6

Multicore 51.91

152.27

842

8

LV28-2-2

2608-1

Multicore 48.36

146.03

1286

9

GE99-10-2

2615-4

Multicore 48.30

146.13

1390

10

LV28-61-3

2615-2

Multicore 48.17

146.18

1714

11

GE99-38-3

2615-5

Minicore

49.34

150.50

1100

12 13 14 North Pacific Ocean (off Kamchatka) 15 North Pacific Ocean (Northwest Meiji Drift) 16 17 North Pacific Ocean (Detroit Seamount) 18 North Pacific Ocean (Northest Meiji Drift) 19 North Pacific Ocean (South of central Aleutian trench) 20 R/V Sonne SO202 — INOPEX (2009) Bering Sea (Bowers Ridge) 21 22 23 24 Bering Sea (Central Aleutian Basin) 25 26 Bering Sea (Northern Bering Slope, Pervenets/ 27 Navarin canyons) 28 CCGS Sir Wilfrid Laurier — Bering Sea (Northern Bering Shelf) 29 SLIP (2007) 30 31 Bering Sea (Central Bering Slope) 32 R/V Sonne SO202 — INOPEX (2009) Bering Sea (Unimak Plateau) 33 34 R/V Sonne SO202 — INOPEX (2009) North Pacific Ocean (Southeast of Aleutian trench) 35 36 37 North Pacific Ocean (Patton Seamount) 38 39 40 North Pacific Ocean (Gibson Seamount) 41 North Pacific Ocean (Abyssal Plain) 42 43 North Pacific Ocean (North of Chinook Trough) 44 North Pacific Ocean (East of Southern Emperor Trough) 45 North Pacific Ocean (Hess Rise) 46 47 North Pacific Ocean (West of Ojin Seamount) 48 North Pacific Ocean (Shatsky Rise) 49 50 51 North Pacific Ocean (Abyssal Plain) 52 53

SO202-01 SO202-02 SO202-03 SO202-04 SO202-05 SO202-06 SO202-07 SO202-08 SO202-09 SO202-10 SO202-11 SO202-12 SO202-13 SO202-14 SO202-15 SO202-18 SO202-16 SLIP4 #102 SLIP3 #103 SLIP1 #124 SO202-19 SO202-21 SO202-22 SO202-23 SO202-24 SO202-25 SO202-26 SO202-27 SO202-28 SO202-29 SO202-31 SO202-32 SO202-33 SO202-34 SO202-36 SO202-37 SO202-38 SO202-39 SO201-40 SO201-41 SO202-42 SO202-45

2597-1 2597-2 2597-3 2597-4 2597-5 2597-6 2598-1 2598-2 2598-3 2598-4 2598-5 2598-6 2599-1 2599-2 2599-3 2599-5 2599-4 2458-5 2458-3 2458-1 2599-6 2600-1 2600-2 2600-3 2600-4 2600-5 2600-6 2602-1 2602-2 2602-3 2602-4 2602-5 2602-6 2603-1 2603-2 2603-3 2603-4 2603-5 2603-6 2604-1 2604-2 2604-3

Multicore Multicore Multicore Multicore Multicore Multicore Multicore Multicore Multicore Multicore Multicore Multicore Multicore Multicore Multicore Multicore Multicore Boxcore Boxcore Boxcore Multicore Multicore Multicore Multicore Multicore Multicore Multicore Multicore Multicore Multicore Multicore Multicore Multicore Multicore Multicore Multicore Multicore Multicore Multicore Multicore Multicore Multicore

44.03 46.97 49.61 51.86 52.70 51.90 51.27 50.54 49.66 52.74 53.11 54.05 54.98 56.79 59.51 60.13 60.40 63.03 62.39 62.01 57.65 54.79 54.57 52.17 53.00 54.10 54.64 54.30 54.42 52.03 49.68 45.50 45.08 40.89 38.19 37.77 38.04 38.01 38.00 38.41 38.89 40.29

152.92 156.98 160.38 163.16 164.92 166.49 167.70 170.82 175.16 179.85 178.90 179.09 177.96 178.82 − 179.85 − 179.44 − 179.11 − 173.45 − 174.57 − 175.05 − 175.68 − 170.33 − 168.81 − 160.50 − 157.19 − 152.69 − 150.38 − 149.60 − 148.88 − 148.89 − 152.55 − 158.50 − 174.14 − 177.68 176.70 176.27 169.28 164.45 162.68 160.33 157.63 149.49

5282 4822 5429 5273 3362 3422 2349 3630 5028 1488 2704 2108 1383 3822 3137 1108 548 73 73 80 1751 1911 1478 4613 4565 4588 742 2916 3710 3984 3744 5302 6159 5713 4522 3573 5503 5096 3462 5408 5535 5476

Okhotsk Sea (off Sakhalin)

Okhotsk Sea (Central Basin)

Okhotsk Sea (off Sakhalin)

Okhotsk Sea (Central Basin) North Pacific Ocean (off Kuril Islands)

BSC and KC thus constitute a cyclonic gyre in the Aleutian Basin (Fig. 1). Moreover, eddies generated by wind forcing, strong flows via the eastern passes and straits as well as the topographic barriers affect the upper layer circulation and have an influence on the interannual variability of sea-surface conditions and the regional surface circulation (e.g., Solomon and Ahlnäs, 1978; Overland et al., 1994; Schumacher and Stabeno, 1994; Stabeno et al., 1999).

The major part of the Bering Sea continental shelf is seasonally covered by sea-ice, which extends to the limit of the Arctic Front (Fig. 1). Its formation begins near the Bering Strait in November, reaches its maximum southern extent in March–April and is totally melted in July (Niebauer, 1980, 1983). Inputs from the Anadyr and Yukon Rivers contribute to sea-ice formation by maintaining water column stratification with a cold and fresh surface layer. The interannual variability

S. Bonnet et al. / Marine Micropaleontology 84-85 (2012) 87–113

of sea-ice cover is related to atmospheric circulation (Cavalieri and Parkinson, 1987). For instance, when the AL is located east of the median position, it carries warm Pacific air over the Bering Sea and induces less sea-ice cover (Niebauer and Day, 1989; Niebauer, 1998). During the last decades, the seasonal duration of the sea-ice cover as well as its concentration and extent have diminished drastically, particularly in the southeast part. Stabeno et al. (2007) have proposed processes such as a shift in winter winds, which have resulted in warmer SSTs and thus a shorter sea-ice season, the presence of warmer shelf waters during summer and changes in the AS inflow through the Unimak Pass. 2.2.3. Okhotsk Sea The Okhotsk Sea is separated from the Bering Sea by the Kamchatka Peninsula, which constitutes its eastern boundary (Fig. 1). It is a semienclosed basin surrounded by Siberia to the north and the Sakhalin Island to the west. The connection with the North Pacific water masses takes place through the numerous straits of the Kuril Islands, notably the Chetvertiy Kuril Strait (b500 m), Kruzenshtern Strait (1400 m), Bussol Strait (2300 m), Friz (De Vries) Strait (b500 m) and Yekaterina Strait (b250 m) (Yasuoka, 1967; Talley and Nagata, 1995; Nagata and Lobanov, 1998; Rogachev, 2000). Overall, one major river feeds the Okhotsk Sea in the western part: the Amur River that corresponds to the Russia–China border. The others are located on the Kamchatka Peninsula and contribute about 9% of the total runoff. The total runoff into the Okhotsk Sea is estimated to be 586 km3/year (e.g., Bezrukov, 1960; Rogachev, 2000; Kashiwai and Kantakov, 2009). The eastern part of the Okhotsk Sea is influenced by the KC, which originates from the Bering Sea. The KC enters the Okhotsk Sea via the Chetvertiy Kuril and Kruzenshtern Straits, and flows along the west Kamchatka Peninsula and the Siberian coasts (Fig. 1). Off the Sakhalin Island, the KC forms the east Sakhalin Current (ESaC). Water masses from the Japan Sea penetrate into the Okhotsk Sea via the Tartar (12 m depth and 8 km wide) and Soya Straits (55 m depth and 42 km wide; Fig. 1). However, the main transport takes place through the Soya Strait via the Soya Current, which is driven by the sea level difference between the Japan and Okhotsk Seas (Takizawa, 1982; Ohshima, 1994). Like in the Bering Sea, the KC and ESaC form a cyclonic gyre induced by wind stress in the central basin of the Okhotsk Sea. The SC waters are mixed with those of the ESaC. A part of this flow goes northward and vanishes into the gyre. Another part is deflected to the North Pacific, with the Oyashio Current, via Bussol, Friz (De Vries) and Yekaterina Straits (Talley and Nagata, 1995; Rogachev, 2000; Ohshima et al., 2004; Kashiwai and Kantakov, 2009; Fig. 1). More than two thirds of the Okhotsk Sea is seasonally covered by sea-ice (Fig. 1). Similarly to the Bering Sea, freshwater inputs from the Amur and Kamchatka Peninsula Rivers play a determinant role by contributing to the upper water layer stratification. Sea-ice starts to form in the northwest part, near the Amur River outlet, and then develops toward the center of the basin to reach its maximum extent in February–March. Summertime is marked by ice-free conditions. Formation of sea-ice is mainly controlled by wind stress and variability of in- and outflows of the KC and ESaC (Talley and Nagata, 1995; Kimura and Wakatsuchi, 1999; Kashiwai and Kantakov, 2009; Ohshima et al., 2010). 3. Material and methods 3.1. Sampling and palynological treatments The 53 surface sediment samples analyzed in this study were collected with a multi-corer, mini-corer or box-corer during expeditions of the CCGS Sir Wilfrid Laurier (2007), R/V Akademik Lavrentyev (Biebow and Hutten, 1999), R/V Marshal Gelovany (Biebow et al., 2000) and R/V Sonne (Gersonde and SO-202-INOPEX participants,

91

2010; Table 1; Fig. 1). The surface sediment (0–1 cm) is generally considered to represent recent sedimentation although it may cover the last 10 1 to 10 3 years depending upon the sediment accumulation rates and biological mixing. Sample treatment followed the standard palynological procedure of GEOTOP (de Vernal et al., 1996). Between 1 and 5 cm 3 of wet sediment were sieved between 106 and 10 μm to eliminate the coarse sand, silt and clay particles. The fraction >10 μm was treated four times with warm HCl (10%) and three times with warm HF (48%) to dissolve, respectively, carbonate and silica particles. Treatment with ultrasound (2–3 min) was carried out to defloculate organic matter agglomerates. A small quantity of detergent (Fisherbrand Sparkleen™) was added to the following samples to help disaggregation of fine particles: SO202-32 to 34, 36 to 42, 45, LV28-2-2, LV28-4-3, LV28-34-1, LV28-41-3, LV28-43-3, LV28-61-3, GE99-12-3, GE99-383 and LV28-41-3. The remaining residue was mounted between slide and cover-slide in glycerin gel and observed under a transmitted light microscope with a magnification ranging from 250× to 1000 ×. An average of 181 dinocyst specimens were counted and identified in each sample. This low value is due to low concentrations in most of the samples as well as the water depth of certain sites, which reaches up to 6000 m. In this study, we only used samples with a sum >70 dinocysts (i.e., 38 samples). This threshold value of 70 specimens was selected according to the concentrations and diversity occurring in each sample (cf. Appendix A and Table 2). For statistical analyses, dinocyst assemblages are expressed in relative abundance (i.e., per thousand) and are then log-transformed for upweighting the accompanying taxa, which often have a narrower ecological tolerance than dominant taxa. Concentrations of palynomorphs were calculated using the markergrain method (Matthews, 1969), i.e., by adding one standardized tablet of Lycopodium spores in each sample prior to the treatment (Stockmarr, 1971). This technique provides results with an accuracy of ±10% for a 0.95 confidence interval (de Vernal et al., 1987; Mertens et al., 2009). Only dinocyst results are discussed in this paper. Nonetheless, pollen grains, spores, organic linings of benthic foraminifera and reworked palynomorphs were also counted and identified. Their counts and concentrations are reported in Appendix B. 3.2. Dinocyst nomenclature and taxonomy Dinocyst taxa were identified using the nomenclature of Rochon et al. (1999) and Head et al. (2001). Some species are illustrated from Plates I to V (Appendix C). The assemblages include P. reticulata (cf. Plate I) and Dalella chathamensis (cf. Plate II), which were described by McMinn and Sun (1994) and Marret and de Vernal (1997) in the Southern Ocean. We have also observed Selenopemphix undulata (cf. Plate V), a new species described by Verleye et al. (2011). However, in order to remain consistent with the Northern Hemisphere database, we will continue to identify this taxon as Selenopemphix nephroides (cf. Rochon et al., 1999; Marret and Zonneveld, 2003). In five surface samples from the Okhotsk Sea, we have observed a total of 16 specimens similar to the taxon P. reticulata (cf. Plate I and Appendix A), but having a few distinct characteristics. As with P. reticulata, the specimens have a diameter ranging from 35 to 40 μm, a wall thickness of ≈1.5 μm and a cyst body spherical to subspherical with ornamented surface characterized by two levels of reticulation. The specimens from the Okhotsk Sea possess an inner reticulation with striations more pronounced and complex than the typical P. reticulata described by McMinn and Sun (1994) and Marret and de Vernal (1997). For convenience and with the aim of differentiating this taxon, we have added the term “Okhotsk morphotype” after P. reticulata. This designation is informal and will be used throughout the text. Some taxa such as Impagidinium japonicum and I. velorum (cf. Plate II and III) were identified according to the nomenclature of Bujak (1984), Bujak and Matsuoka (1986) and Matsuoka (1987). Cysts of Echinidinium karaense (cf. Plate IV) described in Head et al. (2001) as well as Echinidinium

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Table 2 List of dinocyst taxa included in the Northern Hemisphere reference database as well as the grouping used for transfer functions. Heterotrophic taxa are indicated by an asterisk and ✓ corresponds to taxa used for each database. Taxa

Code

cf. Alexandrium tamarense type cyst Achomosphaera sp. Ataxiodinium choane Bitectatodinium tepikiense Bitectatodinium spongium Impagidinium aculeatum Impagidinium pallidum Impagidinium paradoxum Impagidinium patulum Impagidinium sphaericum Impagidinium strialatum Impagidinium plicatum Impagidinium velorum Impagidinium japonicum Impagidinium spp. Lingulodinium machaerophorum Nematosphaeropsis labyrinthus Operculodinium centrocarpum sensu Wall & Dale 1966 Operculodinium centrocarpum sensu Wall & Dale 1966 — short processes Operculodinium centrocarpum– Arctic morphotype Operculodinium israelianum Operculodinium cf. janduchenei Operculodinium centrocarpum– morphotype cezare Polysphaeridium zoharyi Pyxidinopsis reticulata Pyxidinopsis reticulata–Okhotsk morphotype Spiniferites septentrionalis Spiniferites membranaceus Spiniferites delicatus Spiniferites elongatus Spiniferites ramosus Spiniferites belerius Spiniferites bentorii Spiniferites bulloideus Spiniferites frigidus Spiniferites lazus Spiniferites mirabilis-hyperacanthus Spiniferites type granulaire

Alex Acho Atax Btep Bspo Iacu Ipal Ipar Ipat Isph Istr Ipli Ivel Ijap Ispp Lmac Nlab Ocen

Spiniferites pachydermus Spiniferites spp. Tectatodinium pellitum Cyst of Pentapharsodinium dalei *Islandinium minutum *Islandinium? cezare *Islandinium? brevispinosum *Echinidinium karaense *Brigantedinium spp. *Brigantedinium cariacoense *Brigantedinium simplex *Dubridinium spp. *Protoperidinioids *Lejeunecysta sabrina *Lejeunecysta oliva *Lejeunecysta spp. *Selenopemphix nephroides *Xandarodinium xanthum *Selenopemphix quanta *Cyst of Protoperidinium nudum *Cyst of Protoperidinium stellatum *Trinovantedinium applanatum *Trinovantedinium variabile *Votadinium calvum *Votadinium spinosum *Cyst of Protoperidinium americanum *Quinquecuspis concreta *Cyst of Polykrikos schwartzii *Cyst of Polykrikos sp.–Arctic morphotype

Ocss Oarc Oisr Ojan Ocez Pzoh Pret Preo Ssep Smem Sdel Selo Sram Sbel Sben Sbul Sfri Slaz Smir Sgra Spac Sspp Tpel Pdal Imin Imic Ibre Ekar Bspp Bcar Bsim Dubr Peri Lsab Loli Lspp Snep Xand Squa Pnud Pste Tapp Tvar Vcal Vspi Pame Qcon Psch Parc

Notes

Database with 38 samples of this study (DS-38)

North Pacific database (DS-359)

Northern hemisphere database (DS-1419)

✓ ✓

✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓

✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓

✓

✓

✓

✓

✓

✓ ✓ ✓

✓ ✓ ✓

✓ ✓ ✓

✓ ✓ ✓

✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓

✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓

✓ ✓ ✓ ✓ ✓

✓ ✓ ✓

Grouped with O. centrocarpum sensu Wall & Dale 1966 Grouped with O. centrocarpum sensu Wall & Dale 1966

Grouped with O. centrocarpum sensu Wall & Dale 1966

Grouped with Pyxidinopsis reticulata

✓ ✓

Grouped with Achomosphaera sp.

✓ Grouped with S. membranaceus Grouped with S. ramosus Grouped with S. elongatus

✓ ✓ ✓(grouped with Spiniferites spp.) ✓

Grouped with Brigantedinium spp. Grouped with Brigantedinium spp.

✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓

✓ ✓

✓

✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓

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Table 2 (continued) Taxa

Code

*Cyst of Polykrikos kofoidii *Cyst of cf. Polykrikos kofoidii *Cyst of Polykrikos quadratus

Pkof Pcfk Pqua

*Gymnodinium nolleri *Cyst of Gymnodinium catenatum *Echinidinium aculeatum *Echinidinium granulatum *Echinidinium delicatum *Echinidinium zonneveldiae *Echinidinium transparantum *Echinidinium spp. *Stelladinium bifurcatum Cyst A Tuberculodinium vamcampoea Dalella chathamensis

Gcat Gnol Eacu Egra Edel Ezon Etra Espp Sbif Cysa Tvam Dcha

Notes

Database with 38 samples of this study (DS-38)

North Pacific database (DS-359)

Northern hemisphere database (DS-1419)

✓

✓ ✓ ✓

Grouped with Cyst of Polykrikos sp. Arctic morphotype

Grouped with Echinidinium granulatum Grouped with Echinidinium transparantum

✓ ✓ ✓ ✓ ✓

✓

✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓

*: heterotrophic taxa. ✓: taxa used in databases.

aculeatum, E. transparantum, E. delicatum and E. granulatum (cf. Plate IV) described by Zonneveld (1997) were also observed. For statistical analyses, some taxa were grouped due to their morphological similarities or uncertain identification at species level (cf. Table 2). This is the case with Spiniferites elongatus and S. frigidus. Unidentified Brigantedinium specimens, Brigantedinium simplex and B. cariacoense were merged as Brigantedinium spp. Furthermore, P. reticulata–Okhotsk morphotype was grouped with P. reticulata. 3.3. Environmental data Modern hydrographic and sea-ice data from the sample sites were compiled from the World Ocean Atlas 2001 (WOA01; Conkright et al., 2002) and provided, respectively, by NODC (2001) and NSIDC (2003). Compilations of SSTs (WOA01; Stephens et al., 2002) and SSSs (WOA01; Boyer et al., 2005) were made from measurements performed between 1900 and 2001 within a radius of 30 nautical miles around the sites. Sea-ice data were compiled from measurements from 1953 to 2003 according to a one-degree longitude and latitude grid scale. Sea ice is expressed as the number of months per year with a concentration ≥50%. Primary productivity data were provided by the Aqua MODIS satellite for the period 2002–2005 with a spatial resolution of 4.63 km 2 (http://modis.gsfc.nasa.gov/index.php/; Radi and de Vernal, 2008). 3.4. Statistical analyses We have used three different databases for statistical treatments (cf. Table 2; Fig. 2). The first one includes 38 sites and 30 taxa (DS-38). The second one groups the North Pacific samples including those of this study for a total of 359 sites and 61 taxa (DS-359). The third one corresponds to the Northern Hemisphere database that includes 1419 sites and 67 taxa (DS-1419). Multivariate analyses were performed on DS-38 with CANOCO software (Ter Braak and Šmilauer, 2002a; http://www.pri.wur.nl/uk/ products/canoco/). We applied a Detrended Correspondence Analysis (DCA) in order to determine the type of distribution, unimodal or linear according to the length of the first gradient, expressed in standard deviation unit (SD). DCA yielded a first gradient of 3.275 SD implying a unimodal distribution of dinocyst percentages (Table 3). Thereafter, we used a direct method with the Canonical Correspondence Analysis (CCA; Ter Braak and Šmilauer, 2002a, 2002b). We performed CCA analyses with the dinocyst taxa and 13 environmental parameters, which include the water depth, SSTs and SSSs in winter and summer, February and August, seasonal duration of the sea-ice cover and primary productivity in February and August and throughout the year

(Table 4). A forward selection was applied to diminish the set of environmental variables that could explain variations in the species distribution. These results are explained in terms of marginal and conditional effects. Marginal effect represents an environmental parameter taken individually then ranked by its variance, whereas conditional effect ranks a parameter according to the importance of the other ones. Finally, a Monte Carlo permutation test (reduced model with 499 unrestricted randomizations) was done to analyze the statistical significance level (i.e., p-value ≤ 0.05) of the relationship between species and environmental variables (Ter Braak and Šmilauer, 2002a, 2002b). We tested transfer functions for quantitative reconstructions of past sea-surface conditions in the North Pacific Ocean based on dinocyst assemblages. The selected approach is the Modern Analog Technique (MAT), which provides results more reliable than those of calibration techniques (cf. Peyron and de Vernal, 2001; Guiot and de Vernal, 2007, 2011; Bonnet et al., 2010). We used the R software (http://www.r-project.org/), with scripts adapted from PPPbase (http://www.imep-cnrs.com/pages/3pbase.htm/). MAT is based on the similarity degree between fossil and modern spectra and assumes that fossil assemblages developed in environmental conditions comparable to their modern analogs. We made validation tests using a set of 5 analogs and by splitting each database into verification (1/6) and calibration (5/6) datasets from which the root mean square error of prediction (RMSEP) and the root mean square error (RMSE) are respectively calculated (cf. Guiot and de Vernal, 2007). The reliability of transfer functions is given by the coefficient of correlation (R 2) between observed and estimated values. Accuracy is provided by the RMSE that corresponds to the standard deviation of the difference between observed and estimated values from the calibration dataset. We tested the approach on DS-359 and DS-1419 (Fig. 2). DS-1419, available at http://www.geotop.ca/, constitutes the reference database updated by Radi et al. (2001, 2007), Radi and de Vernal (2004), Pospelova et al. (2008); Vásquez-Bedoya et al. (2008), Bonnet et al. (2010) and Limoges et al. (2010).

4. Results 4.1. Dinocyst concentrations and assemblages Dinocyst concentrations of the 53 surface sediment samples analyzed are highly variable. They range from 18 to 143 816 cysts/cm 3 with a mean of 6443 cysts/cm 3. The lowest values correspond to sites located in the open oceanic realm whereas the highest ones are recorded in coastal and neritic areas (Fig. 3 and Appendix A).

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Database n=38 (DS-38)

+

Database n=359 (DS-359)

+

+

Database n=1419 (DS-1419)

180° W

20° N

50 100

40° N

250 500

60° N 750 1000 1250

90° W

90° E

1500 2000 2500 3000

Bathymetry (m)

80° N

3500 4000 4500 5000 5500 w

ta

a nD

Vie

ea

Oc

6000 6500

0° Fig. 2. Location map of surface sediment samples included in the Northern Hemisphere dinocyst reference database (i.e., DS-1419 sites). The different databases used in this study are also represented (i.e., DS-359 and DS-38). The map was realized with Ocean Data View 4.3.6 (Schlitzer, 2010).

Dinocyst assemblages include 19 cysts produced by autotrophic dinoflagellates and 13 by heterotrophic ones. The occurrence of many taxa is occasional and only 15 taxa were counted on a regular basis (Fig. 3). Dinocysts belonging to the genus Echinidinium were mostly recovered from the Okhotsk and Bering Seas. Autotrophic taxa occur mainly along the KuE, NPC and SC. Heterotrophic taxa are located along the ACC–AC, AS, KC, OC, in the Okhotsk Sea but their maximum abundance is recorded in the Bering Sea (Fig. 4). Their distribution is linked to the concentrations of chlorophyll-a (cf. http://modis.gsfc.nasa.gov/). The Okhotsk Sea is characterized by the dominance of O. centrocarpum and Brigantedinium spp. whereas the Bering Sea is marked by the dominance of I. minutum and Brigantedinium spp. In the North Pacific Ocean samples, O. centrocarpum, N. labyrinthus, P. reticulata and Brigantedinium spp. dominate. Some species such as P. reticulata and I. minutum show a south to north latitudinal gradient, respectively, along the KC–OC (sites 12 to 18) and the continental slope of the Bering Sea (sites 26 to 34). N. labyrinthus

Table 3 Results of DCA analysis for the first four axes. Axes Eigenvalues Lengths of gradient

1

2 0.489 3.275

Cumulative percentage variance Of species data 32.2

0.096 1.572

38.4

3

4 0.055 1.27

42

0.044 1.56

44.9

Total inertia 1.521

also exhibits a longitudinal gradient along the KuE, NPC and SC (sites 41 to 53). 4.2. Multivariate analysis CCA results from DS-38 (Figs. 5 and 6) point out that amongst the 13 environmental variables selected, 6 are statistically significant with a p-value lower than 5% (Table 5a) and that all parameters selected are intercorrelated. Only the first two axes were taken into consideration owing to their statistical weight representing, respectively, 29% and 11.1% of the species variance. Axes 3 and 4 can be considered insignificant since they represent less than 5.8% of the species variance (Table 5b). The first ordination axis explains 47% of the canonical variance (Figs. 5c, 6 and Table 5b) and is positively correlated with August and summer SSTs (R2 =0.90), primary productivity in February (R2 =0.81), February and winter SSTs (R2 =0.83), February and winter SSSs (R2 >0.76), August and summer SSSs (R2 >0.64), water depth (R2 =0.71) and annual primary productivity (R2 =0.51). Primary productivity in August (R2 = −0.42) and sea-ice (R2 =−0.27) are negatively correlated with axis 1 (Fig. 5c and Table 5c). The second ordination axis represents 17.8% of the canonical variance (Figs. 5c, 6 and Table 5c). None of the environmental variables we compiled seem to be correlated with this axis. Based on the CCA ordination diagram, we can differentiate three different dinocyst groups. Each one reflects specific hydrographic and trophic conditions in the North Pacific Ocean (Fig. 5c): Group 1 forms a cluster of heterotrophic taxa (Echinidinium spp., I. minutum, Selenopemphix quanta, cysts of Polykrikos spp.,

1.92 1.94 1.59 − 0.27 − 0.62 1.40 − 0.89 1.55 1.59 0.58 1.69 1.25 1.25 0.41 1.12 1.50 1.25 1.60 − 2.20 1.04 − 0.57 − 0.21 0.09 − 0.19 − 0.72 − 0.70 − 0.28 − 0.82 − 0.31 − 0.32 − 0.54 − 0.28 0.39 0.06 0.13 − 0.24 − 0.04 − 0.08 − 0.21 − 0.99 − 0.16 − 0.53 156.58 8.58 12.25 168.78 202.16 179.72 215.79 228.79 228.79 228.79 231.23 227.54 213.23 180.98 188.04 187.86 206.71 226.55 220.37 220.37 193.56 1.86 0.00 0.00 1.40 1.40 2.20 1.72 1.40 1.86 1.86 2.00 1.34 0.48 0.48 0.16 0.00 0.00 0.00 0.00 0.00 0.00 32.56 32.33 32.33 32.22 32.49 33.01 33.08 32.83 32.83 32.83 33.09 33.18 33.18 33.18 33.18 33.18 33.18 33.18 33.25 33.25 33.25 −1.50 −1.47 −1.47 −2.02 −1.27 −1.52 −0.49 −0.35 −0.35 −0.35 −0.20 0.94 1.18 1.81 1.98 2.65 2.56 3.03 2.98 3.19 2.81 LV28-34-1 GE99-31-3 GE99-30-2 GE99-12-3 LV28-4-3 LV28-41-3 LV28-43-3 LV28-2-2 GE99-10-2 LV28-61-3 GE99-38-3 SO202-02 SO202-03 SO202-04 SO202-05 SO202-06 SO202-07 SO202-08 SO202-10 SO202-11 SO202-12 1 2 3 4 5 6 7 8 9 10 11 13 14 15 16 17 18 19 21 22 23

1405 1600 1470 930 675 1068 842 1286 1390 1714 1100 4822 5429 5273 3362 3422 2349 3630 1488 2704 2108

−1.72 −1.65 −1.65 −2.10 −2.02 −1.04 −0.43 −1.58 −1.58 −1.58 −0.55 0.90 1.34 1.84 1.52 2.16 2.26 2.53 2.88 3.06 2.73

9.97 12.78 12.15 10.44 8.15 12.53 11.69 13.14 13.46 13.60 12.04 10.92 11.01 11.80 10.47 10.50 9.70 10.18 9.18 9.62 9.00

10.87 10.97 9.95 9.95 10.57 11.80 9.73 10.30 10.52 10.34 9.02 10.31 8.51 11.38 10.23 10.27 9.14 9.24 8.58 8.89 8.34

32.49 32.26 32.26 32.17 31.52 33.02 33.05 32.74 32.74 32.74 33.03 33.06 33.06 33.08 33.35 33.28 33.18 33.18 33.27 33.25 33.25

32.29 31.99 31.21 30.75 32.10 32.62 32.71 32.26 32.16 32.16 32.47 32.72 32.65 32.82 32.77 32.85 32.77 32.97 32.83 32.91 32.84

32.50 31.79 31.49 29.74 31.65 32.62 32.73 32.20 32.15 32.14 32.54 32.67 32.68 32.82 32.99 32.86 32.78 32.89 32.97 32.99 32.96

55.00 0.00 0.00 0.00 0.00 52.00 49.50 62.14 62.14 62.14 69.72 63.25 60.00 56.00 57.18 62.91 74.91 89.67 86.73 86.73 73.17

188.50 17.16 24.51 309.58 356.14 233.50 252.62 298.62 298.62 298.62 389.48 481.56 368.64 317.92 318.43 352.25 378.25 413.42 403.82 403.82 352.08

CCA Axis 2 (17.8% of the canonical variance) CCA Axis 1 (47% of the canonical variance) Annual productivity MODIS (gC/m2/year) Productivity August MODIS (gC/m2) Productivity February MODIS (gC/m2) Duration of sea-ice cover (month/year) Salinity summer Salinity August Salinity winter Salinity February Temperature summer (°C) Temperature August (°C) Temperature winter (°C) Temperature February (°C) Water depth (m) Site Sample number

Table 4 Environmental parameters and scores of CCA analysis (axes 1 and 2) for the 38 surface sediment samples used in statistical analyses. Sea-surface conditions provided correspond to the surface (i.e., water depth of 0 m), winter and summer values are, respectively, averages from January to March and from July to September.

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Brigantedinium spp. and S. nephroides), which are primarily associated with productivity in August and secondarily by sea-ice cover. This group includes all the sites located north of the SC characterized with mesotrophic–eutrophic water masses. Group 2 is characterized by temperate to tropical autotrophic taxa including Impagidinium patulum, I. aculeatum, I. japonicum, I. paradoxum, I. sphaericum, D. chathamensis and Spiniferites mirabilis-hyperacanthus. CCA illustrates a strong correlation with high SSTs and SSSs. Group 2 sites take place on the KuE-NPC trajectory. Group 3 includes temperate to polar autotrophic species such as S. elongatus-frigidus, Spiniferites ramosus, cysts of P. dalei as well as the cosmopolitan taxon O. centrocarpum. Maximum weighting of this group occurs along the AS, KC–OC and ESaC. 4.3. Regional distribution Based on the relative abundances of dinocyst taxa (Fig. 3) and CCA results (Fig. 5a), we can differentiate five assemblage zones which can be associated with currents and water masses as follows (cf. also Fig. 4). They correspond to the Okhotsk Sea (zone I), the Western Subarctic Gyre (zone II), the Bering Sea (zone III), the Alaska Gyre (zone IV) and the NPC–KuE (zone V). The ordination diagram representing all the sites (Fig. 5b) illustrates clearly the oceanic provinces and how regions affected by gyres form a cluster in the diagram center. 4.3.1. Okhotsk Sea This zone includes sites situated along Sakhalin Island (n°1 to 5) and influenced by the freshwater plume from the Amur River. It is characterized by relatively high concentrations ranging from 1279 to 143 816 dinocysts/cm 3 with a mean of 27 382 dinocysts/ cm 3 (Appendix A). Assemblages are dominated by O. centrocarpum reaching up to 85% except for the site LV28-43-3 where Brigantedinium spp. and I. minutum composed, respectively, 30% and 55% of the assemblage. Most accompanying taxa are autotrophic. They include P. reticulata, S. elongatus-frigidus and Spiniferites spp. Heterotrophic species such as I. minutum and Echinidinium spp. occur at some sites. 4.3.2. Western Subarctic Gyre This zone is restricted to the northeast part of the North Pacific and is under the influence of cold to temperate waters of AS, KC and OC. It differs from the Okhotsk Sea by very low concentrations, ranging from 80 to 632 dinocysts/cm 3 and averaging 252 dinocysts/cm 3 (Appendix A). It is marked by the occurrence of N. labyrinthus, cysts of P. dalei, I. minutum, Echinidinium spp., P. reticulata, S. elongatus-frigidus, Spiniferites spp. and Brigantedinium spp. A subzone (IIa), corresponding to an AS gateway across the Commander and Aleutian Islands, can be distinguished. It is marked by a higher dinocyst concentration (4287 dinocysts/cm3) and the exclusive occurrence of heterotrophic species: Brigantedinium spp. (40%), E. karaense (29%), E. granulatum (13%) and Islandinium? cezare (9%). Assemblages of this zone are linked to the position of the western AL centre. 4.3.3. Bering Sea This zone records dinocyst concentrations averaging 2878 dinocysts/ cm3 (Appendix A). The Bering Sea zone is associated with very high primary productivity and shows elevated proportions of heterotrophic taxa with the co-dominance of I. minutum (up to 67%) and Brigantedinium spp. (up to 58%). Accompanying taxa include O. centrocarpum, S. elongatusfrigidus and cysts of P. dalei. N. labyrinthus, P. reticulata, E. karaense, E. granulatum, I.? cezare and S. nephroides occur mostly at the Bowers Ridge sites. The three sites located on the continental shelf (29, 30 and 31; Fig. 1) are

96 S. Bonnet et al. / Marine Micropaleontology 84-85 (2012) 87–113

Fig. 3. Dinocyst assemblages from the North Pacific Ocean, showing total counts, concentrations and regional zonation (cf. Fig. 5a).

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Fig. 3 (continued).

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Fig. 4. Map showing the proportions of autotrophic and heterotrophic taxa for each surface sample as well as the five regional zones determined by the dinocyst assemblages. The map was realized with Ocean Data View 4.3.6 (Schlitzer, 2010).

directly influenced by the freshwater plume from the Anadyr River. They are characterized by elevated percentages of O. centrocarpum (up to 36%) and low percentages of Brigantedinium spp. (b10%). 4.3.4. Alaska Gyre This zone shows dinocyst concentrations averaging 199 dinocysts/ cm 3 (Appendix A). Assemblages are co-dominated by N. labyrinthus (up to 92%) and Brigantedinium spp. (up to 80%). They are characterized by the occurrence of P. reticulata, Impagidinium pallidum, Impagidinium spp., O. centrocarpum, S. elongatus-frigidus, cysts of P. dalei and Echinidinium spp. I. minutum is absent from this zone. 4.3.5. NPC–KuE This zone encompasses an east–west transect from the Gulf of Alaska to off the Japanese east coast, which is under the influence of temperate to tropical water masses of SC, KuE and NPC. Dinocyst concentrations are low, averaging 120 dinocysts/cm 3, but the assemblages show relatively high species diversity with the occurrence of 15 autotrophic taxa. This zone is characterized by the co-dominance of O. centrocarpum (up to 58%) and N. labyrinthus (up to 73%), which shows a longitudinal gradient with a decrease from 73 to 3% from sites 43 to 53, respectively. The most prominent feature of this zone is the occurrence of temperate to tropical species typical of oligotrophic-mesotrophic environments: I. aculeatum (up to 35%), I. patulum (up to 14.5%), I. japonicum (up to 11.4%), I. sphaericum (up to 8.5%), I. paradoxum (up to 7.3%), I. velorum (up to 5.4%), S. mirabilis-hyperacanthus (1 to 26% from sites 48 to 52, respectively), P. reticulata (up to 19%), D. chathamensis (up to 3.4%) and I. pallidum (up to 10%). Heterotrophic taxa are absent from the assemblages. 5. Discussion 5.1. Taphonomic processes Amongst the numerous taphonomic processes that can affect dinocysts, preservation (i.e., oxidation) and transport (i.e., direction

and strength of oceanic currents) constitute the most significant parameters in the marine environment. Apart from cyst production, which is highly variable from area-to-area and year-to-year, assemblages in surface sediments depend also upon sedimentary processes. 5.1.1. Preservation of dinocysts Zonneveld et al. (1997) have suggested that oxygen concentrations ([O2]) in bottom water masses could affect dinocysts selectively. It turns out that certain taxa belonging to the order Peridiniales (i.e., Brigantedinium spp. and Echinidinium spp.) are more sensitive to oxidation than the Gonyaulacales like Impagidinium spp., O. centrocarpum and N. labyrinthus, which are classified as resistant (Zonneveld et al., 2001, 2007). Despite low concentrations, our samples illustrate a relatively high species diversity. With the exception of some sites in the North Pacific (sites 43 to 53; cf. Fig. 6), Brigantedinium spp. is always present (mean of 30%; reaching up to 80%) and specimens belonging to the genus Echinidinium occur sporadically, mainly in the Bering Sea (sites 22 to 34; cf. Fig. 6). We think that the absence of heterotrophic dinocysts at certain sites is linked to the ecological conditions and low cyst production since it corresponds to sites characterized by oligotrophic– mesotrophic water masses of the KuE–NPC–SC system. Another significant factor to take into account, as shown by the CCA (cf. Fig. 5c and Tables 5a, c), is the water depth that attains up to 6000 m. Depending upon the water depth and [O2], cysts could be oxidized before reaching the seafloor. However, the [O2] in the North Pacific realm records low values, around 1 ml/l at 1000 m and 3 ml/l below 3500 m depth (Garcia et al., 2010). Moreover, in all the surface samples, dinocysts were not damaged or corroded and no other sign of degradation was observed suggesting good conditions for organic-walled cyst preservation. 5.1.2. Transport Transport is equally a key variable, which has to be considered especially in the deep North Pacific Ocean, where the probability of lateral displacements is high. Sinking of fine biogenic particles occurs usually with fecal pellets and amorphous aggregates such as marine snow (Alldredge and Gotschalk, 1988; Heiskanen, 1993; Turner,

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Fig. 5. a) Scores of CCA axes 1 and 2 for each site. A regional zonation is also established based on CCA results and dinocyst assemblages (cf. Fig. 3). b) CCA ordination diagram representing the score of each site according to axes 1 and 2. c) Ordination diagram resulting from the CCA analysis for the first two principal axes. Autotrophs are represented in red and heterotrophs in green. The length and orientation of each arrow determine the environmental variable importance in the dinocyst distribution. Taxon acronyms are indicated in Table 2 and the environmental ones in Table 5a.

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Fig. 5 (continued).

2002). Some studies were done on sediment traps/water samples with diatoms (Onodera and Takahashi, 2009), radiolarians (Okazaki et al., 2003), silicoflagellates (Takahashi, 1989; Onodera and Takahashi, 2005), planktonic foraminifera (Eguchi et al., 2003; Asahi and Takahashi, 2007) and other microplankton (Komuro et al., 2005) at several stations distributed over the North Pacific Ocean (cf. Fig. 1). The main objective of these studies was to determine the production rates in relation to temporal variability and oceanographic conditions. They indicate, for instance, at stations 40 N, AB and SA (cf. Fig. 1) that the variability in fluxes and faunal compositions of silicoflagellates, planktonic foraminifera and diatoms is mostly determined by changes in water mass properties related to atmospheric oscillations, and not by transport (Onodera and Takahashi, 2005; Asahi and Takahashi, 2007; Onodera and Takahashi, 2009). Also, the study of Eguchi et al. (2003) led to the conclusion that there is no exchange between the subarctic and subtropical water masses since the planktonic foraminifera assemblages and fluxes are distinct from one site to another. Nevertheless, at station KNOT (cf. Fig. 1), the study of Komuro et al. (2005) demonstrates that diatoms analyzed in water and sediment traps were laterally transported from the Okhotsk Sea to the West Subarctic Gyre via the Oyashio Current and the numerous eddies occurring in this area. In the Okhotsk Sea, Okazaki et al. (2003) suggested that lateral transport and focusing could explain high concentrations of radiolarians at sites M4 and M6 (cf. Fig. 1). Likewise, it might explain the high dinocyst concentrations at sites 4 (108150 cysts/cm3) and 5 (143816 cysts/m 3, cf. Fig. 1 and Appendix A). Additionally, the absence or very low concentrations of reworked marine palynomorphs like acritarchs and pre-Quaternary dinocysts even at sites 4 and 5 support the idea that lateral transport is negligible in surface samples we analyzed (cf. Appendix B.2). 5.2. Ecological taxa distribution 5.2.1. Operculodinium centrocarpum According to the data compilations of Rochon et al. (1999) and Marret and Zonneveld (2003), assemblages dominated by high percentages of O. centrocarpum are commonly found in cold to temperate

and mesotrophic to eutrophic environments. This agrees with other studies performed in upwelling areas by Holzwarth et al. (2007) and Radi et al. (2001, 2007), respectively, in the Benguela area, on the continental shelf of the Bering Sea and the fjords of the southwest coast of Vancouver Island. In addition, O. centrocarpum constitutes a cosmopolitan taxon in the northeastern Atlantic Ocean and its distribution is closely related to the Gulf Stream and the North Atlantic Drift (cf. also Rochon et al., 1999). In the updated database DS-1419 (Fig. 7a, b), its optimum is recorded between −2 and 15 °C in winter and −2 and 18 °C in summer with salinities ranging from 30 to 35 in winter and from 28 to 35 in summer. It appears that the occurrence of sea-ice is not a limiting parameter. The 38 samples of this study are included in the range of DS-1419. However, the updated database also shows that O. centrocarpum is tolerant to an oligotrophic environment as observed by Radi and de Vernal (2004), Pospelova et al. (2008) and Bouimetarhan et al. (2009), respectively, in the Gulf of Alaska, off the west coast of the United States and Africa. 5.2.2. Nematosphaeropsis labyrinthus Nematosphaeropsis labyrinthus is considered to be a cosmopolitan taxon in the North Atlantic Ocean developing in a wide range of SSTs (0 to 8 °C in winter and 0 to 15 °C in summer) and SSSs (18 to 36 in winter and 27 to 36 in summer), in a mesotrophic environment as well as in neritic and oceanic domains (e.g., Rochon et al., 1999; Marret and Zonneveld, 2003; Fig. 7a, b). Its distribution is similar to that of O. centrocarpum except that N. labyrinthus has a more stenohaline behavior (i.e., optimum at 35). Also, in this study, N. labyrinthus occurs exclusively at open ocean sites. The 38 samples added to the Northern Hemisphere database enlarge the domain of distribution for SSTs (up to 12 °C in winter and 20 °C in summer; cf. Fig. 7a, b). In the northern Pacific, its distribution permits Okhotsk and Bering Sea water masses to be distinguished from the rest of the North Pacific Ocean. 5.2.3. Pyxidinopsis reticulata Pyxidinopsis reticulata is present in all the samples except for sites located on and along the continental shelf of the Bering Sea and two

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200 m

1000 m

5000 m

CCA axis 1 47% of the canonical variance

3 1.5 0.3 -0.3 -1.5 -3

200 m

1000 m

5000 m

CCA axis 2 17.8% of the canonical variance

2.5 1.25 0.25 -0.25 -1.25 -2.5

Fig. 6. Geographical distribution of CCA axes 1 (top) and 2 (bottom). Isobaths correspond to 200, 1000 and 5000 m water depths.

sites in the Okhotsk Sea (n°4 and 5). Even though its distribution is mainly located in the Southern Ocean, it was also identified off the Oregon and Californian coasts (cf. Pospelova et al., 2008). Interestingly, it has not been recorded yet in regions with a seasonal sea-ice cover. In our surface samples, however, it occurs at sites where up to 2 months/year are recorded (mean of 5%; cf. Fig. 7a, b; McMinn and Sun, 1994; Marret and de Vernal, 1997; Marret and Zonneveld, 2003; Esper and Zonneveld, 2002, 2007; Crouch et al., 2010). Its distribution is associated with wide ranges of SSTs (−2 to 16 °C in winter and 7 to 25 °C in summer), SSSs (30 to 36 in winter and summer)

and productivity (oligotrophic to eutrophic conditions). Its occurrence in DS-38 corresponds to SSTs ranging from 0 to 5° in winter and 7 to 12 °C in summer. 5.2.4. Genus Impagidinium Taxa from the genus Impagidinium are represented in high proportions only in the southern part of the North Pacific Ocean. They are restricted to the KuE–NPC–SC system and assemblages obtained are consistent with other studies in the Arabian Sea (Zonneveld, 1997), the Southern Ocean (Esper and Zonneveld, 2002; Crouch et al., 2010)

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Table 5 a) Ranking of each environmental parameter according to their marginal and conditional effects resulting from the forward selection and Monte Carlo permutation. The statistical significance is indicated by the p-values and λ corresponds to the eigenvalue. b) Results of CCA analysis including the species and canonical variances. c) Intra-set correlation between environmental parameters and the first four axes. a) Marginal effects

Conditional effects

Variable

λ

Variable

λ

p-Value

AUG_SST S_SST W_SST FEB_SST FEB_SSS FEB_MODIS W_SSS AUG_SSS WD S_SSS AN_MODIS AUG_MODIS ICE

0.40 0.40 0.36 0.36 0.34 0.34 0.30 0.27 0.27 0.23 0.16 0.12 0.09

AUG_SST FEB_SST WD S_SST ICE S_SSS AUG_SSS AN_MODIS AUG_MODIS FEB_SSS W_SSS FEB_MODIS W_SST

0.40 0.12 0.09 0.06 0.04 0.04 0.04 0.03 0.03 0.02 0.03 0.02 0.02

0.002 0.002 0.002 0.018 0.036 0.150 0.058 0.288 0.288 0.474 0.390 0.490 0.718

b) Axes

1

2

Eigenvalues 0.441 Species–environment 0.957 correlations Cumulative percentage variance Of species data 29 Of species–environment 47 relation

3

0.168 0.828

40.1 64.8

4 0.089 0.913

45.9 74.3

0.058 0.877

Total inertia 1.521

49.7 80.5

c) Environmental parameters

Axis 1

Axis 2

Axis 3

Axis 4

WD FEB_SST W_SST AUG_SST S_SST FEB_SSS W_SSS AUG_SSS S_SSS ICE FEB_MODIS AUG_MODIS AN_MODIS

0.7106 0.8332 0.8393 0.912 0.9058 0.822 0.765 0.7167 0.6464 − 0.2754 0.8128 − 0.4238 0.5104

0.194 − 0.2793 − 0.2513 0.028 − 0.0091 − 0.1058 − 0.0928 − 0.1411 − 0.1201 − 0.0254 − 0.1828 − 0.0358 − 0.2941

− 0.1978 −0.179 −0.1583 0.1036 0.1611 −0.2173 −0.3343 −0.3174 −0.4417 0.408 −0.174 −0.1283 0.0209

− 0.3535 − 0.1519 − 0.15 0.1744 0.0713 − 0.0522 − 0.0329 − 0.1865 − 0.0808 0.4662 − 0.1005 −0.5186 − 0.1698

AUG_SST: sea-surface temperature in August, FEB_SST: sea-surface temperature in February, W_SST: sea-surface temperature in winter, S_SST: sea-surface temperature in summer, AUG_SSS: sea-surface salinity in August, FEB_SSS: sea-surface salinity in February, W_SSS: sea-surface salinity in winter, S_SSS: sea-surface temperature in summer, AN_MODIS: annual primary productivity, FEB_MODIS: primary productivity in February, AUG_MODIS: primary productivity in August, ICE: duration of the sea-ice cover, WD: water depth.

and along the west Canadian–American coasts (Radi and de Vernal, 2004; Pospelova et al., 2008). According to Rochon et al. (1999) and Marret and Zonneveld (2003), I. aculeatum, I. patulum, I. sphaericum and I. paradoxum present similar distribution patterns with an occurrence in oligotophic and tropical to temperate environments. The updated database DS-1419 confirms this distribution and the samples we have added are included in the same ranges of sea-surface conditions. Nevertheless, I. aculeatum, I. patulum and I. paradoxum that were not recorded in sea-ice areas have percentages reaching up to 10% in zones where the sea-ice occurs up to 2 months/year (cf. Fig. 7a, b). Impagidinium pallidum differs from the other Impagidinium species since it is characteristic of subpolar–polar water masses. The compilations of Rochon et al. (1999), Marret and Zonneveld (2003) and Matthiessen et al. (2005) indicate that high abundances of this

taxon are constrained in this specific environment. In the Northern Hemisphere, it was observed in low percentages in the Gulf of Alaska (b4%; Radi and de Vernal, 2004) and along the American coast (b1%; Pospelova et al., 2008). In the Southern Hemisphere, in spite of high proportions (35%) at a few sites from the Southern Ocean (Marret and de Vernal, 1997), its represents no more than 7% of assemblages (Esper and Zonneveld, 2002; Crouch et al., 2010; Verleye and Louwye, 2010). Its occurrence in the northern North Pacific completes the database DS-1419 and corresponds to SSTs between 2 and 12 °C in winter and 8–24 °C in summer. It is also associated with a variable range of sea-ice cover ranging from 0 to 12 months/year (cf. Fig. 7a, b). Other species like I. japonicum and I. velorum are long-ranging, i.e., from Pliocene–Pleistocene to Eocene–Pliocene sediments, respectively. I. japonicum was identified by Matsuoka (1983) in central Japan and by Bujak (1984), Bujak and Matsuoka (1986) and Matsuoka and Bujak (1988) in the Bering Sea. So far, I. japonicum has not been reported yet from modern sediments. From an ecological point of view and based on this study, we can assume that its distribution is restricted to an open oceanic environment with a salinity optimum at 33, a sea-ice cover up to 1 month/year, oligotrophic–mesotrophic (250–350 gC/m 2/ year) and temperate (15–20 °C in winter and 18–22 °C in summer) conditions (cf. Fig. 7a, b). I. velorum was identified for the first time by Bujak (1984) and Matsuoka and Bujak (1988) in the Bering Sea, mainly along the AS. In contrast to I. japonicum, it was observed sporadically in surface sediment samples from the Southern Ocean (McMinn and Sun, 1994) and the Arabian Sea (Zonneveld, 1997). Nevertheless, Crouch et al. (2010) have studied modern sediments from the same area as McMinn and Sun (1994) and they did not report this species in their assemblages. It thus confirms that I. velorum is a rare taxon occurring at localized sites with salinity and productivity conditions similar to those of I. japonicum (cf. Fig. 7a, b). 5.2.5. Dalella chathamensis So far, D. chathamensis was found in modern sediments from the Southern Hemisphere including the Benguela region (Holzwarth et al., 2007) and the Southern Ocean (McMinn and Sun, 1994; Marret and de Vernal, 1997; Crouch et al., 2010), as well as in the Northern Hemisphere, off the American coast (Pospelova et al., 2008). In DS1419, D. chathamensis occurs where salinity ranges from 33 to 35 and where winter and summer temperatures range from 10 to 13 °C and from 17 to 22 °C, respectively. It seems to be associated with open oceanic and oligotrophic–mesotrophic (250–350 gC/m 2/year) conditions without sea-ice cover (cf. Fig. 7a, b). 5.2.6. Islandinium minutum and Islandinium? cezare The highest percentages of I. minutum and Islandinium? cezare are commonly associated with polar–subpolar regions seasonally covered by sea-ice and having a low productivity (Rochon et al., 1999; Head et al., 2001; Mudie and Rochon, 2001; Kunz-Pirrung, 2001; Marret and Zonneveld, 2003; Richerol et al., 2008; Solignac et al., 2009; Bonnet et al., 2010; Fig. 7a, b). Their distribution in the northern North Pacific is similar with optimum SSTs and SSSs between −2 and 0 °C, 33 to 35 in winter and −2 and 6 °C, 30–35 in summer. I.? cezare is found in an area with strong seasonal SST and SSS fluctuations (cf. Marret and Zonneveld, 2003). In the North Pacific Ocean, these taxa are present in low abundances in certain upwelling zones along the west American coasts (Kumar and Patterson, 2002; Radi and de Vernal, 2004; Radi et al., 2007; Pospelova et al., 2010; Price and Pospelova, 2011). However, at the regional scale of the Bering Sea, our results show that their distribution is more closely related to productivity since they develop in the “Green Belt” area, along the continental slope. We also notice low percentages or the absence of these taxa at sites located in the Aleutian Basin (n°21 to 25) and corresponding to mesotrophic conditions, which is in agreement with Radi et al. (2001).

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Fig. 7. Relationship between the percentages of some dinocyst taxa (cf. Discussion part) found in the North Pacific Ocean and the (a) summer SSTs and SSSs (b) as well as the sea-ice cover and MODIS primary productivity for DS-38, DS-359 and DS-1419.

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Fig. 7 (continued).

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Fig. 7 (continued).

5.2.7. Echinidinium granulatum Very low abundances of E. granulatum are recorded at some sites located near the Amur River outlet. This taxon is normally associated with high productivity environments under the influence of river discharges (Zonneveld, 1997; Marret and Zonneveld, 2003; Holzwarth et al., 2007; Vásquez-Bedoya et al., 2008; Bouimetarhan et al., 2009; Limoges et al., 2010). Yet, sea-surface data show low salinities along Sakhalin Island involving the Amur River plume influence. It is likely that this species thrives only in regions influenced by river inputs. E. granulatum occurs preferentially between 12 and 28 °C in winter and at 30 °C in summer. It characterizes mesotrophic to eutrophic environments (from 150 to 600 gC/m 2/year) with ice-free conditions

and a salinity ranging from 33 to 35 (cf. Fig. 7a, b). Marret and Zonneveld (2003) have described this species as subtropical to tropical since it was found in the Arabian Sea (Zonneveld, 1997), the west coast of Mexico (Vásquez-Bedoya et al., 2008; Limoges et al., 2010) and Africa (Zonneveld et al., 2001; Bouimetarhan et al., 2009) as well as off the coasts of Brazil (Vink et al., 2000). Data from the northern North Pacific broaden the ecological affinity of this taxon to temperate environments as it was identified, in addition to this study, off the west coasts of the United States (Pospelova et al., 2008) and Canada (Radi and de Vernal, 2004; Radi et al., 2007; Krepakevich and Pospelova, 2010; Pospelova et al., 2010; Price and Pospelova, 2011).

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b)

Annual primary productivity (MODIS; gC/m2)

Duration of the sea-ice cover (months/year) 100

100 DS-1419 DS-359 DS-38

% Operculodinium centrocarpum

90 80

70

60

60

50

50

40

40

30

30

20

20

10

10 0

% Nematosphaeropsis labyrinthus

0

2

4

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8

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100

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80

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70

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10

10 0

% Pyxidinopsis reticulata

0

100

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400

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0

100

200

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0

100

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0

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0

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0

0 2

4

6

8

10

12

70

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10 0

0 0

% Impagidinium aculeatum

80

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0 0

% Impagidinium patulum

90

2

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25

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20

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15

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10

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5

5

0

0 0

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Fig. 7 (continued).

S. Bonnet et al. / Marine Micropaleontology 84-85 (2012) 87–113

Fig. 7 (continued).

107

108

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Fig. 7 (continued).

5.3. Evaluation of transfer functions The CCA demonstrates that the assemblage composition of this study is strongly related to environmental conditions and particularly to seasonal SSTs. In order to ensure the accuracy and reliability of dinocyst transfer functions to reconstruct paleoenvironments in the North Pacific realm, we performed validation tests with MAT on the North Pacific Ocean (DS-359) and the Northern Hemisphere databases (DS-1419). Results from DS-359 and DS-1419 are illustrated in Figs. 8–9 and show that the best reconstructions are obtained for winter and summer SSTs with a R 2 > 0.95 and RMSE b 1.73 °C. The

salinity data exhibit a scattered distribution below 29 in winter and 27 in summer due to inputs of freshwater by rivers and sea-ice melting. Sea-ice reconstructions also show a scattered distribution which reflect its interannual variability. Validation tests were previously performed by Radi et al. (2007), Pospelova et al. (2008) and Radi and de Vernal (2008) on datasets including 123, 188 and 287 sites from the Northeastern Pacific and the Bering Sea, respectively. By comparing the results of the DS-359 to the previous ones, we obtain better reconstructions for SSTs. The coefficient of correlation of SSSs is slightly lower due to the larger dispersal of values at sites located near fluvial discharges. The annual primary

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109

Fig. 8. Results of validation tests performed with MAT on the North Pacific Ocean database (DS-359). Calibration and validation datasets as well as DS-38 are also illustrated.

productivity is not as well reconstructed with a R 2 of 0.70 in this study, whereas Radi et al. (2007), Pospelova et al. (2008) and Radi and de Vernal (2008) have a R2 > 0.90. Since previous databases integrated a narrower range of productivity values, the reconstructions of DS-359 appear less accurate. Furthermore, the RMSEP is also larger (67.37 gC/m2 in this study and 27.97 gC/m2 in Radi et al., 2007), which points to more equivocal relationships between productivity and dinocyst assemblages at the scale of the North Pacific Ocean. Reconstructing paleoenvironments from cores located in the North Pacific Ocean is challenging given the rarity of surface sediment from this area and the wide range of sea-surface conditions. So far, solely three papers were published. de Vernal and Pedersen (1997) and Marret et al. (2001) reconstructed sea-surface conditions from

a core located in the Gulf of Alaska for the last 23 and 430 kyrs. They applied MAT with a Northern Hemisphere database including 439 sites and that comprised an underrepresented North Pacific database. However, they obtained satisfying results with reliable analog distances. Conversely, Pospelova et al. (2006) reconstructed environments from a core located off the west American coast (Santa Barbara Basin) for the last 40 kyrs. They also applied MAT with a Northern Hemisphere database including 1054 sites. Results showed some non-analog situations and analogs with large distances. Hence the importance to improve the number of surface sediment samples all over the North Pacific Ocean, and particularly, from the oceanic realm and semi-enclosed basins like the Japan, China and Yellow Seas.

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Fig. 9. Results of validation tests performed with MAT on the Northern Hemisphere database (DS-1419). Calibration and validation datasets as well as DS-38 and DS-359 are also illustrated.

6. Conclusion This study fills the gap in the dinocyst distribution from the North Pacific realm and particularly, by integrating deep-sea sites. The analyses of the 53 surface sediment samples provide an overview of the high taxonomic diversity in the North Pacific Ocean compared to the North Atlantic. Furthermore, this work improves our knowledge on the ecological range of certain taxa such as Impagidinium spp., E. granulatum, and notably those that were presumed to be restricted

to the Southern Ocean (e.g., P. reticulata and D. chathamensis). Samples from the Okhotsk Sea contained a species similar to P. reticulata but presenting some morphological differences. We named it, in an informal way, P. reticulata–Okhotsk morphotype. The results of CCA showed that dinocyst assemblages are closely related to the North Pacific water masses despite the numerous currents, eddies and atmospheric oscillations affecting the surface. Indeed, we identified a regional zonation corresponding to the Okhotsk Sea, the Western Subarctic Gyre, the Bering Sea, the Alaska

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Gyre and the NPC–KuE. The CCA demonstrated also that SST constitutes a key variable in dinocyst distribution owing to the influence of the warm NPC–KuE system across the Pacific Ocean. The 38 samples of this study were added to the North Pacific database, raising the number of sites to 359 sites. Validation tests performed with MAT on the Northern Hemisphere reference database confirm that all environmental parameters are well reconstructed. However, the best scores are obtained for temperatures with a R2 >0.95 and a RMSE b 1.73 °C. Finally, this study improved the database for transfer functions, which can be used for further paleoenvironmental reconstructions in the North Pacific Ocean. Nevertheless, the density of reference data from the North Pacific is still low, and it is essential to keep ameliorating the database in order to obtain results with the same quality as those of the North Atlantic Ocean. Supplementary materials related to this article can be found online at doi:10.1016/j.marmicro.2011.11.006 Acknowledgments This study is a contribution to the international INOPEX (Innovative NOrth Pacific EXperiment) project funded by the German Ministry of Education and Science (Bundesministerium für Bildung und Forschung) and led by the Alfred Wegener Institute for Polar and Marine Research (Bremerhaven, Germany). This is also a Past4Future contribution n°15. The research leading to these results has received funding from the European Union's Seventh Framework programme (FP7/20072013) under grant agreement no 243908, "Past4Future. Climate change - Learning from the past climate. Additional financial support was provided by the Fonds Québécois de la Recherche sur la Nature et les Technologies (FQRNT) and the Natural Sciences and Engineering Research Council of Canada (NSERC). We wish to thank the Captain of the German ship R/V Sonne, Lutz Mallon, as well as the crew members for their remarkable work, their support for the sampling and their good humor. We are also grateful to Maryse Henry (Geotop-UQAM) for her help in the laboratory and the management of the Northern Hemisphere dinocyst reference database, Taoufik Radi (Geotop-UQAM) for the dinocyst taxonomy in the North Pacific Ocean and Charles Gobeil for providing samples from the Bering Sea (SLIP#1, #2, #4). We appreciate comments and suggestions from the regional editor, Richard Jordan, and the three reviewers: Arun Kumar, Vera Pospelova and Fabienne Marret. References Alldredge, A.L., Gotschalk, C., 1988. In situ settling behavior of marine snow. Limnology and Oceanography 33 (3), 339–351. Asahi, H., Takahashi, K., 2007. A 9-year series of planktonic foraminifer fluxes and environmental change in the Bering Sea and the central subarctic Pacific Ocean, 1990–1999. Progress in Oceangraphy 72, 343–363. Bezrukov, P.L., 1960. Bottom sediments of the Okhotsk Sea. Trudy IO AS USSR 32, 15–95. Biebow, N., Hutten, E., 1999. Cruise Report KOMEX I and II: RV Professor Gagarinsky Cruise 22, RV Akademik MA Lavrentyev Cruise 28. GEOMAR Report n°82 188 pp. Biebow, N., Luedmann, T., Karp, B., Kulinich, R., 2000. Cruise reports: Komex V and VI. GEOMAR Report n°88 296 pp. Bonnet, S., de Vernal, A., Hillaire-Marcel, C., Radi, T., Husum, K., 2010. Variability of seasurface temperature and sea-ice cover in the Fram Strait over the last two millennia. Marine Micropaleontology 74, 59–74. Bouimetarhan, I., Marret, F., Dupont, L., Zonneveld, K., 2009. Dinoflagellate cyst distribution in marine surface sediments off West Africa (17–6°N) in relation to seasurface conditions, freshwater input and seasonal coastal upwelling. Marine Micropaleontology 71 (3–4), 113–130. Boyer, T., Levitus, S., Garcia, H., Locarnini, R., Stephens, C., Antonov, J., 2005. Objective analyses of annual, seasonal, and monthly temperature and salinity for the world ocean on a 1/4 degree grid. International Journal of Climatology 25, 931–945. Bujak, J.P., 1984. Cenozoic dinoflagellate cysts and acritarchs from the Bering Sea and Northern North Pacific, DSDP Leg 19. Micropaleontology 30 (2), 180–212. Bujak, J.P., Matsuoka, K., 1986. Taxonomic reallocation of cenozoic dinoflagellate cysts from Japan and the Bering Sea. Palynology 10, 235–241. Cavalieri, D.J., Parkinson, C.L., 1987. On the relationship between atmospheric circulation and the fluctuations in the sea ice extents of the Bering and Okhotsk seas. Journal of Geophysical Research 92 (C7), 7141–7162.

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