Ecosystem Dynamics of the Pacific-Influenced Northern Bering

Progress in Oceanography Progress in Oceanography 71 (2006) 331–361 www.elsevier.com/locate/pocean

Ecosystem dynamics of the Paciﬁc-inﬂuenced Northern Bering and Chukchi Seas in the Amerasian Arctic

Jacqueline M. Grebmeier a,*, Lee W. Cooper a, Howard M. Feder b, Boris I. Sirenko c

a Marine Biogeochemistry and Ecology Group, Department of Ecology and Evolutionary Biology, 10515 Research Dr., Building A, Suite 100, The University of Tennessee, Knoxville, TN 37932, USA b Institute of Marine Science, University of Alaska Fairbanks, Fairbanks, Alaska 99775, USA c Zoological Institute, Russian Academy of Sciences, Universitetskaya emb., 1, St.-Petersburg, 190034, Russia

Abstract

The shallow continental shelves and slope of the Amerasian Arctic are strongly influenced by nutrient-rich Pacific waters advected over the shelves from the northern Bering Sea into the Arctic Ocean. These high-latitude shelf systems are highly productive both as the ice melts and during the open-water period. The duration and extent of seasonal sea ice, seawater temperature and water mass structure are critical controls on water column production, organic carbon cycling and pelagic–benthic coupling. Short food chains and shallow depths are characteristic of high productivity areas in this region, so changes in lower trophic levels can impact higher trophic organisms rapidly, including pelagic- and benthic-feeding marine mammals and seabirds. Subsistence harvesting of many of these animals is locally important for human consumption. The vulnerability of the ecosystem to environmental change is thought to be high, particularly as sea ice extent declines and seawater warms. In this review, we focus on ecosystem dynamics in the northern Bering and Chukchi Seas, with a more limited discussion of the adjoining Pacific-influenced eastern section of the East Siberian Sea and the western section of the Beaufort Sea. Both primary and secondary production are enhanced in specific regions that we discuss here, with the northern Bering and Chukchi Seas sustaining some of the highest water column production and benthic faunal soft-bottom biomass in the world ocean. In addition, these organic carbon-rich Pacific waters are peri- odically advected into low productivity regions of the nearshore northern Bering, Chukchi and Beaufort Seas off Alaska and sometimes into the East Siberian Sea, all of which have lower productivity on an annual basis. Thus, these near shore areas are intimately tied to nutrients and advected particulate organic carbon from the Pacific influenced Bering Shelf-Ana- dyr water. Given the short food chains and dependence of many apex predators on sea ice, recent reductions in sea ice in the Pacific-influenced sector of the Arctic have the potential to cause an ecosystem reorganization that may alter this benthic-oriented system to one more dominated by pelagic processes. Ó 2006 Elsevier Ltd. All rights reserved.

Regional terms: USA; Arctic; Russia; Northern Bering Sea; Chukchi Sea

Keywords: Ecosystem dynamics; Pelagic–benthic coupling; Benthos

* Corresponding author. Tel.: +1 865 974 2592; fax: +1 865 974 7896. E-mail address: [email protected] (J.M. Grebmeier).

1. Introduction

The seasonally ice-covered Bering and Chukchi Sea shelves are among the largest continental shelves in the world. Pacific water with high nutrient levels upwells onto the shelf of the northern Bering Sea and influences planktonic and benthic foodwebs as well as sediment community dynamics throughout this region. Mean current flow of Pacific-derived water is northward into the Arctic Ocean over most of the year (Woodgate et al., 2005). Sea-ice production, extent, and duration are critical for influencing annual primary production of ice algae and phytoplankton, as well as water mass formation. Current direction and speed influence subsequent organic carbon transport through the system. Annual primary production estimates (based on a 120 day growing season) for the region range from <50 to 800 g C mÀ2 yÀ1 (Springer and McRoy, 1993; Springer et al., 1996; Sakshaug, 2004; Hill and Cota, 2005), with ice-edge production proportionally more important in regions of limited open water production (Ambrose et al., 2005; Lovvorn et al., 2005). While zooplankton can significantly graze both phytoplankton and microheterotrophs, ultimately limiting export production, zooplankton grazing and the microbial loop in the nutrient-rich, offshore Pacific waters in the northern Bering and Chukchi Seas have less of an impact on overall organic carbon cycling than in nutrient-limited, nearshore Alaska Coastal waters (Walsh et al., 1989; Sakshaug, 2004). The net result of these factors, specifically the extremely high primary production over shallow shelves and relatively low grazing pressure, is that more organic carbon settles to the seafloor where it supports a rich benthic food web. Generally, in shallow arctic regions with high water column production, there are tight coupling and strong spatial linkages of water column organic carbon production and deposition to the underlying sediments. These patterns of abundant benthic carbon supply and high biomass of long-lived benthic fauna in cold Arctic waters are dominant characteristics in these productive Pacific-influenced ecosystems. Although cold temperatures limit migratory fish populations in these northern regions (Alton, 1974), a limited number of fish species, including Arctic cod (Boreogadus saida) and to a lesser extent Bering flounder (Hippoglossoides robustus) and saffron cod (Eliginus gracilis) have important trophic roles as food for many marine mammals and seabirds (Frost and Lowry, 1980; Bradstreet and Cross, 1982; Springer et al., 1987; Gil- lispie et al., 1997; Wyllie-Echeverria et al., 1997). Various ice-associated seals, including ribbon, ringed and spotted, migrate seasonally with the sea ice and feed pelagically (Simpkins et al., 2003). In addition, migratory bowhead whales in the western Beaufort Sea are also known to feed opportunistically on zooplankton advected northward from the northern Bering Sea (Moore and Laidre, 2006). The high benthic standing stocks on these northern shelves also support key benthic-feeding apex predators, including Pacific walrus (Odobenus rosmarus divergens), gray whales (Eschrichtius robustus), and bearded seals (Erignathus barbatu; Sheffield et al., 2001; Moore et al., 2003; Simpkins et al., 2003; Feder et al., 2005). These benthic-feeding marine mammals and seabirds (e.g. the spectacled eider, Somateria fischeri) provide relatively higher regional pre- dation pressure than fishes (Feder and Jewett, 1978; Grebmeier et al., 1995; Lovvorn et al., 2003; Moore et al., 2003; Simpkins et al., 2003). Our objective in this review is to summarize published and other available data documenting the marine ecosystem in the northern Bering and Chukchi Seas. In many respects, the northern Bering Sea is more clo- sely connected in hydrographic characteristics to the Arctic Chukchi Sea to its north than to the southern Bering Sea. An Arctic–subarctic temperature front separates the northern and southern sectors of the Bering Sea, and that front appears to be moving northward, with potential for a restructuring of the ecosystem (Overland and Stabeno, 2004; Grebmeier et al., 2006). Sea-ice algal production is important in the more extensively ice-covered continental shelves of the northern Bering and Chukchi Seas, with meso- and macro-zooplankton populations having a relatively smaller overall role in organic carbon cycling relative to other regions of the Arctic (Walsh et al., 1989, 2005; Walsh and Dieterle, 2004). There is an increased importance of benthic populations and processes progressing from south to north on these shallow, Paci- fic-influenced continental shelves. From an ecosystem perspective, benthic foodwebs play a significant role in influencing trophic dynamics and organic carbon cycling on these productive Amerasian Arctic shelves and, therefore, are a major focus of this review. J.M. Grebmeier et al. / Progress in Oceanography 71 (2006) 331–361 333

2. General review format, methods, and data selection criteria for Geographic Information System (GIS) analysis

Major biological patterns of organic carbon production, export, and utilization in the northern Bering and Chukchi Sea regions vary widely (Table 1), with large ranges observed in annual primary production, particulate organic carbon (POC) export, macroinfaunal biomass, sediment community oxygen consumption (SCOC), and organic carbon deposition. Low temperatures limit rates of zooplankton growth and reproduction during the winter and early spring, so new production during the spring is not heavily grazed and instead settles rapidly to the underlying sediments (Springer et al., 1996; Coyle and Pinchuk, 2002). Although we have spatial information on seasonal water column phytoplankton biomass and production, only limited data are available for zooplankton population biomass and production in this region (Sakshaug, 2004). That limits detailed review of this ecosystem component. By contrast to zooplankton, much more data are available on underlying benthic populations and sediments including short- and long-term benthic organic carbon transformation processes. Export of POC from the upper ocean and out of the euphotic zone to the benthos is controlled by the magnitude of primary production and the degree of organic carbon recycling in the water column (Wassmann et al., 2004). Spatial comparisons of water column production and benthic standing stock and indicators of benthic production demonstrate linkages to overlying water column processes (Grebmeier and Cooper, 1995; Grebmeier and Dunton, 2000; Grebmeier and Barry, in press). A number of interdisciplinary oceanographic cruises have been undertaken in the northern Bering and Chukchi Seas over the last two decades, with more limited studies in the East Siberian and Beaufort Seas. Many of these cruises collected both water column and benthic parameters as part of an ecosystem approach, and we have chosen a subset of these data sets for this review (Table 2). For our analysis, we utilized those cruises, listed in Table 2, where both water column chlorophyll-a (chl-a) and sediment measurements were made with similar analytical procedures. This analysis allows us to develop a broad-scale, ecosystem-level understanding of this Pacific-influenced system in the Amerasian Arctic. Water column chlorophyll data were used that were determined using standard oceanographic methods (Cooper et al., 2002). Total SCOC rates, inclusive of macro, meio, and microfauna (microbes), as well as chemical cycling, were obtained from shipboard incubation experiments conducted at in situ temperatures (Grebmeier and Cooper, 1995; Devol et al., 1997; Clough et al., 2005; Grebmeier and Barry, in press; see Table 2). These rates were then converted to carbon respiration rate units using a respiratory quotient of 122 moles of C respired per 175 moles of O2 consumed (Pilson, 1998; Moran et al., 2005). This molar ratio assumes that most sediment respiration is due to macrobenthic infauna, an assumption supported by previous data (Grebmeier and McRoy, 1989) and that rates of microbial anoxic respiration are low (Kirchman et al., 2005). We consider this assumption reasonable for the shelf and upper slope, although it is less applicable to lower slope and basin sediments where benthic faunal abundance was low. Note also that the SCOC data represent minimum values for sediment carbon mineralization, because they do not include the contribution from anaerobic processes that accompany sediment carbon mineralization, previously found to average 25% of the total rate (Grebmeier and McRoy, 1989; Devol et al., 1997). Finally, mmol C was converted to mg C weight based on the formula that 1 mole of carbon equals 12 g of carbon. Benthic population studies were undertaken with 0.1 m2 van Veen grabs and the 0.25 m2 OKEAN grab used primarily by Russian scientists (e.g., Sirenko and Koltun, 1992). Both have a good record of documenting the population structure and biomass of macrofaunal communities (Feder et al., 1994a, 2005, in press; Sto- ker, 1978, 1981; Grebmeier et al., 1989; Sirenko and Koltun, 1992; Grebmeier and Cooper, 1995). By contrast, a smaller published suite of studies have used small subcores from box cores for documenting sediment exchange processes, but because of the large biomass of individual macrofaunal organisms, small core-based studies cannot be expected to adequately sample for biomass. Recent studies as part of the Western Arctic Shelf-Basin Interactions (SBI) project have investigated the differences between quantitative grabs and coring collections, and these results indicate that biomass in the Chukchi Sea and extending into the Arctic Ocean can only be adequately estimated from cores taken on the lower slope and in deep basin regions where infaunal populations are low (R. Pirtle-Levy and J. Grebmeier, unpublished data). Due to bioturbation in shelf sediments that quickly mixes surface materials, van Veen grabs can also be used to estimate certain sediment characteristics. For example, collections made with cores and grabs at the same locations are not statistically different for materials deposited to shelf surface sediments, including 137Cs (Cooper et al., 1998) and in most cases sedimentary chlorophyll (Pirtle-Levy, 2006). 334

Table 1 Summary of organic carbon production and export, benthic macroinfaunal biomass, sediment community oxygen consumption and tracers in the Paciﬁc-inﬂuenced regions of the Amerasian Arctic a Region Depth Annual primary POC Sediment community oxygen Macroinfaunal Sediment Sediment Sediment CPE Citations 331–361 (2006) 71 Oceanography in Progress / al. et Grebmeier J.M. À2 (m) production (g C export (g C consumption (mmol O2 m biomass (g wet wt. TOC (%) Chl-a (mg (Chl+ Phaeo; mÀ2 yÀ1 ) mÀ2 yÀ1 ) dÀ1 ) [mg C mÀ2 dÀ1 ] mÀ2 )[gCmÀ2 ] mÀ2 ) (mg mÀ2 ) Northern 30–80 250–470 44 (over 1–40 [ < 1–335] 38–756 [1–30] <0.5–1.5 10–1500 9–46 1, 2, 3, Bering Sea 96 d) Table 2 Southern 50–100 80–840b 166 (over 1–40 [ < 1–335] 85–1800b [1–100a] <0.5–2.5 10–50 nd 1, 2, 4, Chukchi Sea 365 d) Table 2 East Siberian 30 25–40 nd 1–22 [ < 1–184] 1–530 [1–20] 0.5–1.5 10–30 nd 5, 6, Table 2 Sea Northern 50–200 70–430c 3–13 (over 3–40c [25–335] 1–2800c [1–100c] <0.5–2.0 8–19 4–42 7, 8, 9, Chukchi 100 d) Table 2 Sea-shelf Northern 200– <50 1–9 (over <3 [ < 25] 1–270 [1–12] 1.0–2.0 2–15 1–11 4, 5, 8, 9 Chukchi 2000 100 d) Table 2 Sea-slope Western 50–2000 30–70 4–9 1–15 [ < 1–125] <50–680 [1–20] 1.0–2.0 10–30 nd 4, 5, 7, 8, Beaufort Sea Table 2 (shelf and slope) Arctic Basin >2000 <20 <10 <5 [ < 42] 1–200 [ < 2] 1.0–1.5 <5 nd 4, 5, 7, 8, Table 2 BC = upper Barrow Canyon, POC = particulate organic carbon, TOC = total organic carbon, Sed chl-a = sediment chlorophyll-a, CPE = chl pigment equivalents, nd = no data. Note that citations for annual primary production, POC export and sediment Chl-a are included in this table, whereas citations for summary values of all other sediment parameters are found in Table 2. Conversion values for SCOC and macroinfaunal biomass are in Section 2, methods. a Citations: 1Springer and McRoy, 1993; 2Springer et al., 1996; 3Fukuchi et al., 1993; 4Wassmann et al., 2004, 5Sakshaug, 2004; 6Petrova et al., 2004; 7Hill and Cota, 2005; 8Cooper et al., 2005b; 9Moran et al., 2005. Table 2 includes detailed citations for benthic parameter summary values presented in this current table and visually in the GIS maps. b High value in ‘‘hot-spot region’’ in southeastern Chukchi Sea. c High value for upper Barrow Canyon (BC) only. J.M. Grebmeier et al. / Progress in Oceanography 71 (2006) 331–361 335

Table 2 Listing of research cruises by year, month, ship, cruise designator, region, and associated references for data used for all GIS station maps produced in the northern Bering, Chukchi and portions of the East Siberian and Beaufort Seas for this paper Year Month Ship Cruises Regions References 1974–1979 July–Sept. See reference Various Bering, cf. Dunton et al. (2005) Beaufort Seas 1970–74 Jan.–Oct. Jan.–Feb. 1970 USCG icebreaker Stoker70– Bering, Stoker (1978, 1981) and cf. Dunton Northwind, Mar.–April 1971 USCG 74 Chukchi et al. (2005) icebreaker Glacier, Feb.–Mar. 1972 Seas USCG icebreaker Burton Island, July–Sept. 1973 RV Acona and RV Alpha Helix, June–July 1974 RV Alpha Helix 1985–1988 June–Oct. See reference Various Bering, cf. Dunton et al. (2005) (ISHTAR Chukchi data reports) Seas 1984 June RV Alpha Helix HX059 Northern Grebmeier et al. (1988, 1989) and Bering Sea Grebmeier and McRoy (1989) and cf. Dunton et al. (2005) 1985 July–Aug. RV Alpha Helix HX073, Northern Grebmeier et al. (1988, 1989), Bering, Grebmeier and McRoy (1989) and cf. Chukchi Dunton et al. (2005) Seas RV Alpha Helix HX074 1986 July–Sept. RV Alpha Helix HX085 Northern Grebmeier et al. (1988, 1989), Feder Bering, et al. (1994a,b, in press) and cf. Chukchi Dunton et al. (2005) Seas RV Oceanographer OC862 RV Oceanographer OC863 1987 July–Sept. RV Surveyor NO871 Chukchi Feder et al. (1991a, in press) and cf. Seas Dunton et al. (2005) RV Surveyor SU872 1988 Aug.–Sept. MV Akademik Korolev (BERPAC- AK47 Bering, Grebmeier (1993), Cooper et al. 1988) Chukchi (2002), cf. Dunton et al. (2005) and Seas Grebmeier and Cooper, 2006 1990 June RV Alpha Helix (SLIPP-90) HX139 Northern Grebmeier et al. (1995), Cooper et al. Bering Sea (1998, 2002) and cf. Dunton et al. (2005) 1992 Aug.–Sept. RV Alpha Helix HX165 Chukchi, Devol et al. (1997), Cooper et al. Beaufort (1998) and Grebmeier, unpublished Seas data 1993 June RV Alpha Helix (SLIPP-93) HX171 Northern Cooper et al. (1998, 2002), Grebmeier Bering Sea and Dunton (2000) and cf. Dunton et al. (2005) 1993 Aug. USCGC Polar Star Polar Chukchi Cooper et al. (1998) Star93 Sea, Arctic Ocean 1993 Aug.–Sept. MV Okean (BERPAC-1993) Okean93 Bering, Cooper et al. (1998, 2002), Grebmeier Chukchi and Dunton (2000), cf. Dunton et al. Seas (2005) and Grebmeier and Cooper (in press) 1994 May–June RV Alpha Helix (SLIPP-94) HX177 Northern Cooper et al. (1998, 2002), Grebmeier Bering Sea and Dunton (2000) and Grebmeier and Cooper, unpublished data (continued on next page) 336 J.M. Grebmeier et al. / Progress in Oceanography 71 (2006) 331–361

Table 2 (continued) Year Month Ship Cruises Regions References 1994 July–Aug. USCGC Polar Sea AOS94 Chukchi Clough et al. (2005) Sea, Arctic Ocean 1995 Aug. RV Alpha Helix HX189 Chukchi Cooper et al. (1998), Reed (1998), cf. and East Dunton et al. (2005), Grebmeier and Siberian Barry (in press) and Grebmeier and Sea Cooper, unpublished data 1996 June USCGC Polar Sea Polar Sea96 Chukchi Clough et al. (2005) Sea 1998 June–July USCGC Polar Sea Polar Sea98 Chukchi Clough et al. (2005) Sea 1998 July CCGS Sir Wilfrid Laurier (BSEO-98) SWL1998 Bering, Grebmeier et al. (2006) and Chukchi Grebmeier, unpublished data Seas 1998 Aug. RV Alpha Helix (SLIPP-98) HX214 Northern Cooper et al. (2002) and Grebmeier Bering Sea and Cooper, unpublished data 1999 April USCGC Polar Sea (SLIPP-99/ Polar Sea99 Northern Cooper et al. (2002) and Grebmeier spring) Bering Sea and Cooper, unpublished data 1999 July CCGC Sir Wilfrid Laurier (BSEO- SWL1999 Bering, Grebmeier et al. (2006), Grebmeier 99) Chukchi and Cooper, unpublished data Seas 1999 Aug. RV Alpha Helix (SLIPP-99/summer) HX224 Northern Cooper et al. (2002) and Grebmeier Bering Sea and Cooper, unpublished data 2000 July CCGS Sir Wilfrid Laurier (BSEO-00) SWL2000 Bering, Grebmeier and Barry (in press), Chukchi, Grebmeier et al. (2006) and Beaufort Grebmeier and Cooper, unpublished Seas data 2001 March–April USCGC Polar Star (SLIPP-01) Polar Star01 Northern Simpkins et al. (2003) and Grebmeier Bering Sea and Cooper, unpublished data 2001 July CCGS Sir Wilfrid Laurier (BSEO-01) SWL2001 Bering, Grebmeier and Barry (in press), Chukchi Grebmeier et al. (2006) and Seas Grebmeier and Cooper, unpublished data 2002 May–June USCGC Healy (SBI-02/spring) HLY0201 Chukchi, Cooper et al. (2005b), cf. Dunton Beaufort et al. (2005), Grebmeier and Barry Seas, Arctic (in press) and Grebmeier and Ocean Cooper, unpublished data 2002 July–Aug. USCGC Healy (SBI-02/summer, HLY0203 Chukchi, Cooper et al. (2005b), Dunton et al. Beaufort (2005), Grebmeier and Barry (in Seas, Arctic press), Grebmeier et al. (2006) and Ocean Grebmeier and Cooper, unpublished data CCGS Sir Wilfrid Laurier (BSEO-02) SWL2002 2003 July CCGS Sir Wilfrid Laurier (BSEO-03) SWL2003 Bering, Grebmeier and Barry (in press), Chukchi Grebmeier et al. (2006) and Seas Grebmeier and Cooper, unpublished data 2004 May–June USCGC Healy (SBI-04/spring) HLY0402 Chukchi, Grebmeier and Barry (in press), Beaufort Grebmeier et al. (2006) and Seas, Arctic Grebmeier and Cooper, unpublished Ocean data July–Aug. CCGS Sir Wilfrid Laurier (BSEO-04) SWL2004 July–Aug. USCGC Healy (SBI-04/summer) HLY0403 RV Khromov (RUSALCA-2004) RUSALCA04

AOS94 = Arctic Ocean Section1994, BERPAC = Joint US-USSR Bering & Chukchi Seas Expeditions, BSEO = Bering Strait Environ- mental Observatory, ISHTAR = Inner Shelf Transfer and Recycling project, MV = Marine Vessel, RUSALCA = Russian-American Long-term Census of Marine Life project, SLIPP = St. Lawrence Island Polynya Project, USCG=US Coast Guard, USCGC = USCG Cutter, RV = Research Vessel. J.M. Grebmeier et al. / Progress in Oceanography 71 (2006) 331–361 337

One other consideration for determining which data we would compare was the method for converting to biomass from preserved macrofauna. We present here infaunal benthic biomass data as both formalin-preserved wet weight and as carbon dry weight values, the latter obtained with carbon conversion values determined by Stoker (1978) and also used by Grebmeier et al. (1989). This conversion allows removal of heavy carbonate test values that can bias the results. These biomass measurement protocols have been widely applied for benthic populations in the Bering and Chukchi Seas (Feder et al., 1994a, in press; Stoker, 1978, 1981; Grebmeier, 1993; Grebmeier et al., 1988, 1995; Grebmeier and Cooper, 1995; Grebmeier and Dunton, 2000; Simpkins et al., 2003). We supplement these analyses with selected Pearson product–moment correlation statistics (SPSSÒ version 11.0.4; http://www.spss.com/). More detailed statistical analyses, including multivariate analyses for subsets of these data, are available in the core literature that we review here. With our data synthesis and analysis framework in place, we provide an overview of the general trophic structure in the water column and sediments and of organic carbon export production as interpreted through sediment community metabolism and tracers. Due to the dominance of benthic food webs in the region, we use spatial patterns in benthic biomass and community structure as indicators of focused organic carbon deposition and recycling sites based on composite, averaged data. Spatial analysis of data was accomplished using a geographical information system (ArcGIS; ESRIÒ ArcInfo versions 8.3 and 9.1; http://www.esri.com) that includes modeling tools to convert sampled field data into continuous maps. These procedures allowed us to obtain a more synoptic view of patterns over a large sampling area. Our spatial analyses were created by first loading measured, averaged point data for a specific parameter into a geodatabase in ArcCatalog software, creating a feature class. A map template was then opened in ArcMap, and the feature class data were added to the map via an open Geostatistical Analyst layer. The map layer to be analyzed with the geostatistical analyst subroutine was then highlighted and the ESRI’s Geostatistical Wizard software launched. The input data for the specified parameter were then chosen and the attribute to be interpolated selected. Inverse Distance Weighting is the interpolation method that we used. It is a deterministic technique using surrounding measurements to calculate the interpolated surface, and sample data closest to the unmeasured areas contrib- ute proportionally more to the interpolation than sample data located far away. All data points are, however, included in the interpolation without statistical manipulation of the data beyond the default settings of the software. The interpolated layer was then created, a scale selected to best illustrate the data, with the subsequent map exported and saved using Adobe Illustrator graphics software (Adobe Systems, Inc.; http://www.a- dobe.com). Additional details on the methodology for generating the maps are provided in Pirtle-Levy (2006).

3. General ecosystem processes and patterns

3.1. Circulation, hydrography and sea ice cover

The key water mass types of this region are defined primarily by seasonally varying salinity in the spring and summer, with more saline (>32.5), nutrient-rich Anadyr Water (AW) transiting northward on the western side of the northern Bering and Chukchi Seas with fresher (<31.8), more nutrient-limited Alaska Coastal Water (ACW) flowing northward on the eastern side of the northern Bering and Chukchi Seas (Fig. 1; Gre- bmeier et al., 1988; Weingartner et al., 2005; Walsh et al., 2005). South of Bering Strait, in the open water season, a third water mass of intermediate salinity (31.8–32.5), Bering Shelf Water (BSW), lies between AW and ACW. A strong frontal system develops during the open-water period between the nutrient-rich BSW offshore water and the nutrient-depleted ACW near the Alaska coastline (Coachman et al., 1975; Gre- bmeier et al., 1988). As these waters flow north through Bering Strait, the AW and BSW mix to form a modified Bering Sea Water that we term Bering Shelf-Anadyr Water (BSAW) following the nomenclature of Grebmeier et al. (1988) and Feder et al. (2005, in press). Recent results from the SBI project have documented key hydrographic and biological characteristics of Pacific water at the Arctic shelf-basin boundary following its transit over the outer shelf and slope areas of the Chukchi and Beaufort Seas into the Arctic Basin (Pickart et al., 2005; c.f. Grebmeier and Harvey, 2005). Finally, the East Siberian Sea northwest of Bering Strait is influenced by freshwater flow from the Kolyma River, sea ice melt, and limited inflow of Anadyr water westward through Long Strait (Reed, 338 J.M. Grebmeier et al. / Progress in Oceanography 71 (2006) 331–361

Beaufort East Sea Beaufort Gyre (surface) 70˚ N Siberian Barrow Canyon Atlantic Water (subsurface) Sea Siberian Coastal Current Chukchi Alaska Coastal Water Wrangel I. Sea Barrow Bering Shelf Water Icy Cape Bering Shelf Anadyr Water (Bering Sea Water) Aleutian North Slope, Bering Slope & Anadyr Waters Pt. Hope Alaskan Stream 65˚ N September Ice Edge Maximum & Minimum Extent Kotzebue March Ice Edge Maximum & Minimum Extent Chukotka Sound Peninsula Bering Gulf of Strait Anadyr Yukon River Norton Sound St. Lawrence I. 60˚ N

55˚ N Bering Sea

Aleutian Islands Gulf of Alaska

180˚ 175˚ W170˚ W 165˚ W 160˚ W 155˚ W

Fig. 1. Schematic of water mass type and sea ice extent in the northern Bering, Chukchi, eastern East Siberian and western Beaufort Seas (modiﬁed from map provided by Tom Weingartner and Seth Danielson, University of Alaska Fairbanks).

1998; Mu¨nchow et al., 1999; Weingartner et al., 1999; Petrova et al., 2004). Although the net flow is from the East Siberian Sea eastward into the Chukchi Sea (Fig. 1), periodic current reversals allow Pacific-water to move westward into the East Siberian Sea and to influence both productivity and organic carbon deposition to the sediments on the western side of the region (Mu¨nchow et al., 1999; Petrova et al., 2004). The Bering Strait Complex (Anadyr Strait, Shpanberg Strait, and Bering Strait) in the northern Bering Sea and southern Chukchi Sea is the sole connection between the Pacific and Arctic Oceans. Pacific water inflow through this complex is an important source of heat, freshwater, nutrients, and Pacific fauna into the Arctic Ocean (Aagaard and Carmack, 1989; Cooper et al., 1997; Shimada et al., 2005, 2006; Woodgate and Aagaard, 2005; Woodgate et al., 2005), as well as fluxes of organisms and organic carbon (Grebmeier, 2003; Walsh and Dieterle, 2004; Walsh et al., 1989, 2005; Grebmeier et al., 2006). When normalized to the salinity of Atlantic Water, the inflow through Bering Strait provides 40% of the total freshwater input to the Arctic Ocean (Woodgate and Aagaard, 2005). In addition, shelf transformation processes substantially modify the physical and biogeochemical properties of Pacific Ocean waters as they cross the Chukchi shelf. Episodic flows can then transport organic material (plankton, particulates, nutrients) offshore into the basin (via eddies, filaments, jets, downwelling) or from the deep basin (upwelling) onto the shelf, both in canyons and along the shelf break (Ashjian et al., 2005; Codispoti et al., 2005). For the Chukchi and Beaufort regions current transport from the shelves to slope and deep basins occurs primarily through Barrow and Herald canyons (Codispoti et al., 2005; Grebmeier and Harvey, 2005; Weingartner et al., 2005), with subsequent transport into the basin via currents flowing eastward along the continental slope, eddies generated along the slope, and/or by the effects of surface wind-forcing (Pickart et al., 2005). These seawater and particulate organic carbon exchanges are critical for maintaining the thermohaline and ecosystem structure of the Arctic Ocean, and because of their high nutrient and biological content, they are key components of the Arctic Ocean’s organic carbon budget. These processes may have important impacts on Arctic shelf and basin ecology and community composition (e.g., transport of large bodied copepods from the basin onto the shelves; S. Smith, personal communication). Moreover, changes in the quantity and properties of the Pacific waters entering the Arctic Ocean are likely to have far-reaching consequences, possibly even impacting the meridional overturning circulation of the global ocean (Peterson et al., 2006). J.M. Grebmeier et al. / Progress in Oceanography 71 (2006) 331–361 339

The recent, well-documented reduction in sea ice distribution in the Pacific sector (thickness and extent) is likely to influence regional and global climate through changes in surface albedo, salt, heat and nutrient budgets, and restructuring of the marine ecosystem. The seasonal northward retreats of sea ice in 2002–2005 were the most extreme in the satellite image record (Meier et al., 2005; Stroeve et al., 2005). Recent data also indicate that the position of the seasonal ice edge in this region directly responds to warming from inflowing waters coming through Bering Strait (Shimada et al., 2006). Anomalous spring and summer shifts in productivity on the Bering Sea shelf are linked to decadal-scale atmospheric/sea ice/oceanographic processes, but probably also reflect long-term climate change in the western Arctic (Stabeno and Overland, 2001; Overland and Stabeno, 2004). The shallow and dynamic northern Bering Strait region appears to be responding directly to changes in climate forcing (Overland and Wang, 2005). Some of the environmental changes recently observed in this region include ocean warming, reduced benthic organic carbon supply and standing stocks, and a northward shift in fish and benthic-feeding marine mammal populations (Grebmeier et al., 2006).

3.2. Primary production, ice algae and suspended biomass

The Pacific-influenced northern Bering and Chukchi Seas, the eastern portion of the East Siberian Sea and the western portion of the Beaufort Sea support both ice-covered and open water primary production. How- ever, ice algal production over these shelves is not so important proportionally as in other regions of the Arctic (Sakshaug, 2004), and Gosselin et al. (1997) estimated that ice algal production only made up to 3% of the total primary production occurring in Arctic shelf areas. Ice algal production rates in the northern Chukchi outer shelf and slope are relatively low (5–10 g C mÀ2 yrÀ1; Gosselin et al., 1997; Wheeler et al., 1996)compared to water column phytoplankton production that averages 80–90 g C mÀ2 yÀ1 over the northern Chukchi shelf, excluding upper Barrow Canyon (430 g C mÀ2 yÀ1; Springer and McRoy, 1993; Springer et al., 1996; Hill and Cota, 2005; Table 1). Low annual primary production occurs in the coastal waters of the Chukchi, Beaufort and East Siberian Seas (20–70 g C mÀ2 yÀ1; Sakshaug, 2004). The highest water column primary production occurs further south in the nutrient-rich areas of the northern Bering and southern Chukchi Seas, averaging 470 g C mÀ2 yÀ1 (Table 1; Springer et al., 1996; Sakshaug, 2004; Hill and Cota, 2005). Maximum primary production, ranging up to 840 g C mÀ2 yÀ1, has been calculated in the southern Chukchi Sea (Table 1; Springer and McRoy, 1993). Observations also indicate that shelf-break upwelling and shelf basin exchange are enhanced in canyons (Macdonald et al., 1987; Grebmeier and Harvey, 2005; Hill and Cota, 2005). These exchange processes could be important to biological production; Carmack et al. (this issue) hypothesize that nutrient supply, rather than light (which is influenced by snow and ice cover), limits primary productivity on Arctic shelves. Hence, nutrient supply from the Pacific inflow, along with stratification, upwelling, and vertical mixing are all key factors influencing organic carbon cycling processes on the Pacific-influenced Amerasian shelves. Sea ice algae provide a highly concentrated food source for the planktonic foodwebs in spring, with sea ice primary production and biomass high on the shelf and low over the slope and basin on an annual basis (Cota et al., 1991; Ambrose et al., 2001; Ambrose et al., 2005; Hill and Cota, 2005; McMahon et al., 2006). Increases in water column primary production from May through late summer are driven by the extent of open water area, not by an increase in sea surface temperature. The majority of the high production over the northern Bering and Chukchi shelves, including sea ice and planktonic diatoms, either falls through the shallow water column unconsumed to the benthos (Cooper et al., 2002; Ambrose et al., 2005), or, when it reaches the shelf break, is transported eastward along the shelf break in the prevailing currents or is transported by episodic physical mechanisms into the basin (Bates et al., 2005; Moran et al., 2005). Water mass structure in the northern Bering Sea influences the high primary productivity maintained in the spring and summer in the offshore waters of the Bering Strait region and extending into the Chukchi Sea (Springer and McRoy, 1993; Walsh et al., 2005; Table 1). Even with horizontal transport, there are significant spatial patterns and statistical correlations of integrated water column chlorophyll standing stock (Fig. 2) and underlying sediment community oxygen consumption (SCOC), the latter an indicator of carbon supply to these shallow shelf sediments (Fig. 3, Table 3). A 20-year spatial composite of integrated water column chlorophyll shows the influence of eutrophic AW to the west, producing a chlorophyll-rich water 340 J.M. Grebmeier et al. / Progress in Oceanography 71 (2006) 331–361

Fig. 2. Integrated chlorophyll-a (mg mÀ2) in the northern Bering, Chukchi, eastern East Siberian and western Beaufort Seas for the period April–September 1976–2004 (updated from Dunton et al., 2005 with additional data; references listed in Table 2). Chlorophyll-a analysis followed methods outlined in Cooper et al. (2002). column as well as an organic carbon export to the underlying sediments. By comparison, the spring bloom in the ACW to the east is not maintained through the summer via nutrient upwelling; thus, the coastal system becomes nutrient-limited in the summer and the overall integrated chlorophyll level is lower, as is SCOC. J.M. Grebmeier et al. / Progress in Oceanography 71 (2006) 331–361 341

À2 À1 Fig. 3. Sediment community oxygen consumption (mmol O2 m d ) for the northern Bering, Chukchi, eastern East Siberian and western Beaufort Seas for the period 1984–2004 (references listed in Table 2). Methodology for data sources identiﬁed by lead authors on the ﬁgure can be found in Grebmeier and McRoy (1989), Devol et al. (1997) and Clough et al. (2005).

3.3. Zooplankton and the Microbial loop

Dominant zooplankton populations vary south to north from the northern Bering Sea to the Arctic basin, and they directly or indirectly support higher trophic levels. These larger animals include water column-feeding marine mammals, such as bowhead whale, Balaena mysticetus, ice-associated seals (spotted, Phoca largha, 342 J.M. Grebmeier et al. / Progress in Oceanography 71 (2006) 331–361

Table 3 Pearson product-moment correlations (with 1-tailed probability estimates) of infaunal benthic biomass (g C mÀ2) and sediment À2 À1 community oxygen consumption (SCOC; mmol O2 m d ) to environmental parameters, as well as between environmental parameters: integrated chlorophyll-a, Int chl-a (mg mÀ2), sediment chlorophyll-a, sed chl-a (mg mÀ2), total organic carbon, TOC (%), depth (m), sediment carbon isotope, d13C (per mil), % P5 phi (silt and clay) Parameter correlation Correlation coefficient (r) Count (n) Probability Benthic biomass, SCOC 0.582 348 <0.001** Benthic biomass, depth À0.176 766 <0.001** Benthic biomass, d13C 0.225 188 <0.001** SCOC, Int chl-a 0.207 260 <0.001** SCOC, TOC À0.108 339 0.023* SCOC, Depth À0.344 347 <0.001** SCOC, d13C 0.173 96 0.046* SCOC, % silt/clay À0.179 296 <0.001** Int chl-a, Sed chl-a 0.572 324 <0.001** Int chl-a, TOC 0.164 402 <0.001** Int chl-a, depth À0.095 434 0.024* Int chl-a, d13C À0.518 111 <0.001** Sed chl-a, depth À0.144 406 0.002* Sed chl-a,%P 5phi À0.225 342 <0.001** TOC, depth 0.152 578 <0.001** TOC, d13C 0.133 187 0.035* TOC, % P 5phi 0.623 477 <0.001** * Significant correlation at p 6 0.05. ** Significant correlation at p 6 0.01.

ringed, Phoca hispida, and ribbon, Phoca fasciata) and seabirds (e.g., multiple species of alcids and kittiwakes) which take advantage of the productive nature of the water column in this region. Zooplankton population biomass is low under the sea ice during winter, when there is minimal primary production and very low temperatures, e.g. <1 °C(Lovvorn et al., 2005). When the sun returns to the Bering Strait region in the spring and ice begins to retreat, a large episodic pulse of organic carbon from an ice-edge bloom occurs, plus a subsequent open water bloom, all of which sinks to the bottom to feed the underlying benthos without being significantly grazed by zooplankton (Coyle and Cooney, 1988; Grebmeier et al., 1988; Grebmeier and Dunton, 2000; Coyle and Pinchuk, 2002). Springer et al. (1989) described the general zooplankton community in the northern Ber- ing and southern Chukchi Seas in relation to water mass type. Oceanic species, including the large Pacific copepods Neocalanus cristatus and Neocalanus plumchrus, along with smaller Eucalanus bungii and Metridia pacifica dominated the herbivorous zooplankton, with larvaceans (Oikopleura sp.) important in the summer, all occurring in the high salinity AW. By comparison, the BSW located between AW and the nearshore ACW (Fig. 1) was dominated by the subarctic herbivorous copepod Calanus marshallae, with the low salinity nearshore waters dominated by the smaller Pseudocalanus spp. and Acatia longiremis. Although the oceanic copepod species do not significantly graze the available standing biomass in these high productivity waters, the shelf and nearshore zooplankton in ACW can more effectively utilize the limited production, thus retaining much of the in situ production in the upper water column and making the underlying sediments food-limited for benthic fauna. In the northern Chukchi Sea, Calanus marshallae is dominant in the outer shelf regions, along with the larger arctic species Calanus glacialis, in addition to the Atlantic-species Calanus finmarchicus found in Arctic Basin waters (Plourde et al., 2005; Lane et al., 2006; S. Smith, personal communication). The regional spatial patterns of zooplankton coincide with an elevated abundance of Calanus glacialis/marshallae in Pacific water transiting the Chukchi Sea, along the shelf break, and extending down Barrow Canyon (Ashjian et al., 2005; Moran et al., 2005; Plourde et al., 2005). Recent studies indicate that reproduction and production of Calanus glacialis and Calanus marshallae in this region are tightly linked to spring and summer primary production (Plourde et al., 2005), with greater egg production over the Chukchi shelf and shelf break than in the deep J.M. Grebmeier et al. / Progress in Oceanography 71 (2006) 331–361 343

Arctic Basin. Rates of mesozooplankton processes (e.g., reproduction, grazing) are enhanced in the upper slope environment where shelf-derived and basin-derived zooplankton merge and where mesoscale physical processes (upwelling, eddies) are most significant (Ashjian et al., 2005; Plourde et al., 2005). Heterotrophic protists are ubiquitous over the Chukchi Sea, and at times attained a high biomass during the SBI studies. They were found to be an important food resource for zooplankton both in shelf and basin waters (Andersen, 1988; Sherr et al., 1997; E. Sherr and B. Sherr, personal communications). Although heterotrophic protists may have significant grazing impacts on phytoplankton, the grazing impacts of mesozooplankton on phytoplankton have been found to be minimal (R. Campbell, C. Ashjian, E. Sherr and B. Sherr, unpublished data). It is known that mesozooplankton grazing impacts are primarily dependent on zooplankton biomass, which increases in the summer on the outer shelf and slope of the Chukchi Sea (Plourde et al., 2005), but mesoplankton grazing is still low compared to other Arctic shelf regions. Findings from the SBI project indicate that mesozooplankton prey preferences change seasonally, with ice algae preyed upon under ice-cover and microzooplankton preyed upon preferentially during the summer (Plourde et al., 2005; E. Sherr, personal communication). Thus, high primary production and low zooplankton grazing result in strong pelagic–benthic coupling that supports very high infaunal benthic biomass in this shelf system (Grebmeier et al., 1988; Dunton et al., 2005; Grebmeier and Barry, in press). By contrast to the throughflow of nutrient-rich Pacific water over the northern Bering Sea to the slope of the Chukchi Sea, the East Siberian Sea is influenced strongly by freshwater flow from the Kolyma River as well as other Russian rivers further to the west. Extensive sea ice cover and limited, periodic inflow of waters of Pacific origin westward through Long Strait all influence the more Arctic, low productivity nature of this region (Mu¨nchow et al., 1999; Khim et al., 2003; Petrova et al., 2004). Few data for zooplankton are available for the East Siberian Sea, but we expect that small, neritic species are most likely to be those present under the influence of runoff, with some oceanic species being carried in by AW entering the East Siberian Sea through Long Strait from the Chukchi Sea. The microbial loop in the northern Bering and Chukchi shelf waters is relatively weak compared to other continental shelves and bacterial recycling directly consumes only a small fraction of primary production (Walsh et al., 1989; Rich et al., 1997; Cota et al., 1996; Kirchman et al., 2005). Past water column studies indicate that substrate concentration (e.g., dissolved organic matter, DOM), not temperature, drives microbial production in the Bering Strait region and across to the Canadian Basin (Rich et al., 1997; Kirchman et al., 2005). This key finding is at variance with water column metabolism studies at lower latitudes, where temperature is more important than organic carbon supply (Cota et al., 1996; Hopkinson et al., 2001). These results suggest that very high primary production within Pacific water overlying shallow (<100 m) continental shelves coincides with a microbial loop that is less efficient in recycling organic carbon in the water column.

3.4. Organic carbon export and sediment consumption

If a seasonal phytoplankton bloom develops slowly, zooplankton populations may have sufficient time to respond numerically and graze a significant fraction of the production (Coyle and Pinchuk, 2002). Such communities with strong coupling between primary production and zooplankton grazers can be termed ‘‘retention systems’’ (Wassmann, 1998), meaning that there is a large proportion of organic carbon recycling in the upper water column. In these systems the timing of production and subsequent micro- and meso-zooplankton growth, along with microbial transformations, can reduce the fraction of primary production exported to the sediments, thereby limiting benthic populations and benthic carbon cycling. In contrast, if an episodic phytoplankton bloom is more typical, such as occurs in the northern Bering Sea and in the southern Chukchi Sea under the influence of high nutrient AW, zooplankton populations are only coupled weakly to changes in production, recycling in the water column will be low and the fraction of primary production exported high. In these ‘‘export systems’’ much of the organic matter will sink to the benthos, allowing for enhanced benthic processing of organic carbon (Grebmeier and Barry, in press). Only one published study has utilized anchored sediment traps to directly measure POC export in the northern Bering Sea. Fukuchi et al. (1993) deployed a fixed trap array in the northern Bering Sea and determined a mean POC flux of 462 mg C mÀ2 dÀ1, which was consistent with nearly simultaneous estimates of SCOC by Grebmeier and McRoy (1989) that resulted in a benthic organic carbon uptake value of 464 mg 344 J.M. Grebmeier et al. / Progress in Oceanography 71 (2006) 331–361

CmÀ2 dÀ1 at the same site. Together, these two studies indicate a tight relationship between organic carbon export and benthic oxygen uptake (converted to C-uptake for this discussion – see methods section) in the northern Bering Sea (Grebmeier, 1993; Grebmeier et al., 1995; Grebmeier and Barry, in press). Moving farther north, Moran et al. (1997) calculated a POC export flux using the thorium method for a site in the productive southern Chukchi Sea and determined a vertical POC export of 458 mg C mÀ2 dÀ1. By comparison recent thorium export and floating sediment trap studies in the northern Chukchi Sea and extending into the Arctic Basin (excluding Barrow Canyon) have indicated variable export over the outer shelf to basin zone that increased from spring (<1–91 mg C mÀ2 dÀ1) to summer (10–367 mg C mÀ2 dÀ1; Moran et al., 2005; Lalande et al., in press). Export values range from highest on the outer shelf to lowest in the deep basin. The highest export rates for both these two studies occurred in Barrow Canyon and increased from spring (1–508 mg C mÀ2 dÀ1) to summer (136–796 mg C mÀ2 dÀ1; Moran et al., 2005; Lalande et al., in press). Export fluxes measured in the western Beaufort Sea in summer using the thorium method ranged from 119 to 134 mg C mÀ2 dÀ1 (Moran et al., 2005). Spatial patterns of SCOC identify regions of organic carbon deposition throughout the Pacific-influenced shelf region and can be used as a surrogate for variations of export production in the region (Grebmeier and Barry, in press). Specific ‘‘hot-spots’’ of high SCOC values include the regions southwest of St. Lawrence Island, in the Chirikov Basin north of St. Lawrence Island, in the southern Chukchi Sea and at the head À2 À1 of Barrow Canyon (Fig. 3). SCOC measurements ranged from 10 to 40 mmol O2 m d (84–335 mg C À2 À1 À2 À1 m d ) in the northern Bering Sea south and north of St. Lawrence Island to 20–50 mmol O2 m d (167–418 mg C mÀ2 dÀ1) in the southern Chukchi Sea and upper Barrow Canyon. SCOC values decline to À2 À1 À2 À1 1–10 mmol O2 m d (8–84 mg C m d ) on the outer Chukchi and western Beaufort shelves, with the À2 À1 À2 À1 lowest values from 0.1 to 5 mmol O2 m d (<1–42 mg C m d ) on the northern Chukchi and western Beaufort slope and Arctic basin regions. The lower SCOC rates nearshore in the northern Bering, Chukchi, East Siberian, and western Beaufort Seas, except Barrow Canyon, indicate reduced organic carbon export and deposition to the benthos (Grebmeier and Barry, in press). These values of SCOC are comparable in range to export production determined from both the thorium method and sediment traps. For example, the high SCOC in the southern Chukchi Sea and upper Barrow Canyon ‘‘hotspots’’, is consistent with export flux rates determined by the thorium method, although lower than those measured using the floating sediment trap method in the summer period. When SCOC is greater than the water column export production, it suggests the import of organic carbon from upstream productive zones. The lower SCOC observed on the outer Chukchi and Beaufort shelves is similar to export flux determined by the thorium and floating sediment trap methods for this region in spring, but only for some areas during the summer. Moran et al. (2005) evaluated this seasonal disparity between export production and SCOC and concluded that whereas most of the organic carbon descending to the sediments in spring is utilized by benthic processes, approximately 20% of the summer export production is instead exported off the shelf and unavailable for benthic carbon cycling in the summer. Past studies also indicate that sediment respiration in this region is dominated by benthic macrofauna and that rates of microbial anoxic respiration are low by comparison (Blackburn, 1987; Grebmeier and McRoy, 1989; Henriksen et al., 1993; Devol et al., 1997; Clough et al., 2005; Grebmeier and Barry, in press). The dominance of macrofauna in community respiration is assumed for the shelf and upper slope of the Pacific-influenced waters, though for the deep slope and basin meiofauna and microfauna become proportionally more important as benthic macrofauna diminish (Clough et al., 2005; Pirtle-Levy, 2006). Recent data also indicate that epifaunal animals can increase overall benthic community oxygen consumption and should be considered within total organic carbon budget analyses (Ambrose et al., 2001; Piepenburg et al., 1995; Piepenburg, 2005). Thus, the SCOC rates presented here should be considered minimal values, since they do not include either megafaunal animal impacts or anaerobic processes, both of which would increase total sediment carbon mineralization.

3.5. Indicators of organic carbon supply: benthic biomass, community structure and sediment tracers

Because the focus of this review is on organic carbon processing and ecosystem dynamics on the Pacific- influenced Amerasian shelves, we particularly want to highlight the role of the key infaunal and epifaunal J.M. Grebmeier et al. / Progress in Oceanography 71 (2006) 331–361 345 compartments, in relation to environmental processes. Benthic infaunal biomass can indicate interannually- persistent sites of organic carbon deposition that support substantial benthic communities and food-limited regions with low biomass signatures. Benthic infaunal biomass is a long-term integrator of overlying water column processes and reflects current speed, sediment grain size and food supply (Grebmeier and Barry, 1991, in press). Sediment grain size and total organic carbon (TOC) can be indirect indicators of current transport and sedimentation zones, both influencing the type of benthic fauna occupying a region. Infauna in the northern Bering and Chukchi Seas and the eastern section of the nearshore East Siberian Sea are prey for many epifaunal species, and the numerous epifaunal scavenger–predators present reflect an abundant infaunal food resource. Bivalves, amphipods and polychaetes dominate the infaunal biomass south of St. Lawrence Island in the northern Bering Sea; amphipods and bivalves dominate in the central region between St. Lawrence Island to Bering Strait; and bivalves and polychaetes dominate in the southern Chukchi to the slope region of the Arctic (Fig. 4, Grebmeier and Cooper, 1995; Grebmeier et al., 1995). Sediment grain size is the major factor responsible for determining biodiversity, including which benthic taxa are dominant, and this differs from organic carbon which, as food, drives biomass itself (Grebmeier et al., 1988, 1989). Most offshore sediments in the northern Bering, Chukchi and East Siberian Seas are composed of soft substrates, mud or muddy sand, that are significantly correlated with TOC content (Table 3; Fig. 5; Grebmeier and Cooper, 1994; see also Naidu et al., 2004). Specifically, surface sediment TOC ranged from 0.1% nearshore in sandy sediments to 2.8% in offshore regions of the southwestern Chukchi Sea (Fig. 5). Previous studies indicate that organic carbon content is significantly correlated to silt and clay content in these sediments (Grebmeier and Cooper, 1994; Grebmeier and Cooper, 1995, in press), although grain size is not the sole factor determining sediment organic carbon content. In analysis of 477 surface sediment samples, TOC and the percent fine silt and clay fraction (P5 phi) were highly correlated (r = 0.623, p < 0.001, Table 3), suggesting a direct relationship between the two. For example, sediment TOC and the % silt and clay fraction in surface sediments were both significantly correlated to SCOC (Table 3; Fig. 3) and appear to follow the patterns for integrated chlorophyll concentrations in the water column (Table 3; Fig. 2). These results provide additional support for a tightly coupled water column and benthos in the Pacific-influenced northern continental shelf system. Close to St. Lawrence Island, grain size increase to sand, gravel and rock as a branch of water carried in the Anadyr Current accelerates along the south shore of the island during its transit eastward, then northward once beyond the easternmost point of the island. Sediments in the Chirikov Basin north of St. Lawrence Island are sandy due to high current regimes. The high currents in Bering Strait promote maintenance of gravel, pebbles and rocks, with epifaunal animals being dominant. As these currents move northwestward and reduce speed, fine silt and clay fractions settle from the water column, resulting in increased modes for these particle sizes in the sedimentary spectrum and higher TOC content. The P5 phi grain sizes dominate in Herald Valley and as far west as Wrangel Island. By comparison, grain size coarsens over the shoal areas of the northern Chukchi Sea, especially near the Alaskan coastline (Feder et al., 1994a; J. Grebmeier, unpublished data). Grain size decreases at the edge of the northern Chukchi margins and is dominated by fine silt and clay in the slope and basin regions. As is the case with infauna, the epifauna of the Bering, Chukchi and East Siberian Seas is also influenced by the overlying water mass properties. While Atlantic fauna dominates most of the East Siberian Sea, the Chuk- chi Sea is primarily a habitat for Pacific species, and there is a clear biogeographic boundary in the East Sibe- rian Sea near Long Strait south of Wrangel Island (Sirenko, 2003). The most abundant epifaunal species in the Pacific-influenced Arctic are compiled in Table 4 from field and literature reports. Echinoderms, mainly sea stars, dominate the invertebrate epifaunal biomass in the northeastern Bering and southeastern Chukchi Seas (Feder et al., 2005), differing dramatically from that in the southeastern Bering Sea dominated by crustaceans. This change in biomass dominance from south to north is due to increased food for sea stars, reflecting the absence of large crabs and frequent absence of demersal fishes in the northern regions, many of which use similar food items (Alton, 1974; Feder and Jewett, 1981; Jewett and Feder, 1980, 1981; Feder et al., 2005). Sea stars are also important food competitors of marine mammals. However, sea stars can survive for long periods without food (Feder and Christensen, 1966), whereas marine mammals are much more rapidly impacted by food scarcity. Since sea stars are long-lived, abundant and dominate epifaunal biomass, their biological importance should not be overlooked. Sea stars may function as keystone predators in northern benthic systems 346 J.M. Grebmeier et al. / Progress in Oceanography 71 (2006) 331–361

Fig. 4. Benthic infaunal biomass (g C mÀ2) in the Bering, Chukchi, eastern East Siberian and western Beaufort Seas from 1973 to 2004 (references listed in Table 2). All values are averages of 4–5 samples/station collected with a 0.1 m2 van Veen grab, sieved through 1 mm screens*, with formalin-preserved wet weight biomass converted to dry weight g C biomass following methods outlined in Grebmeier and Cooper, 1995. *Note that a 3 mm sieve screen was used for Stoker (1978, 1981), but his analysis indicated that >90% of the infaunal benthic biomass was collected on the 3 mm screen. where the large crabs and bottom fishes are uncommon. Below we outline dominant faunal type and biomass for three spatial regions from south to north in the Pacific-influenced Arctic sector, combining this with a discussion of trophic dynamics.

3.5.1. Northern Bering Sea High infaunal biomass (Fig. 4) and high SCOC (Fig. 3) are both observed in persistent ‘‘hot-spot’’ zones southwest of St. Lawrence Island (Grebmeier and Cooper, 1995; Grebmeier and Dunton, 2000), emphasizing J.M. Grebmeier et al. / Progress in Oceanography 71 (2006) 331–361 347

Fig. 5. Surface sediment total organic carbon content (%) for the northern Bering, Chukchi, eastern East Siberian and western Beaufort Seas for the period 1976–2004 (references listed in Table 2). Analysis followed methods outlined in Cooper et al. (1998) and Naidu et al. (2004). the signiﬁcant relationship between organic carbon settling to the benthos (indicated by SCOC) and benthic infaunal biomass for the suite of data in this review. Signiﬁcant positive correlations were found for benthic biomass and SCOC, 13C-enrichment, and shallow continental shelf depths (Table 3), all supporting the spatial patterns indicated in the maps (Figs. 2–6). Nuculana radiata and Nucula belloti (=Leionucula tenuis) are cur- rently the dominant bivalves in the region (Grebmeier and Cooper, 1995, in press), although previously the bivalve Macoma calcarea was also dominant (Sirenko and Koltun, 1992). Benthic infaunal biomass ranged from 10 to 20 g C mÀ2 (300–400 g wet wt. mÀ2) on the average (Fig. 4). However, recent studies indicate a 348 J.M. Grebmeier et al. / Progress in Oceanography 71 (2006) 331–361

Table 4 Most abundant epifauna in the northern Bering, Chukchi and East Siberian Seas Dominant Common name Species Northern Bering Chukchi East Siberian Epifauna Sea Sea Sea Porifera Sponge Haliclona gracilis ÀÀ+ Sponge Halichondria panicea + ÀÀ Sponge Phakellia cribrosa À ++ Hydrozoa Hydroid Obelia longissima +++ Anthozoa Soft coral Gersemia fruticosa ÀÀ+ Soft coral Gersemia rubiformis ++À Sea anenome Actinostola callosa ÀÀ+ Sea anenome Epiactis arctica À + À Cirripedia Barnacle Balanus crenatus ++À Amphipoda Amphipod Ampelisca macrocephala ++À Amphipod Anonyx nugax ++À Amphipod Gammarus setosus ÀÀ+ Isopoda Isopod Saduria entomon ÀÀ+ Isopod S. sabini ÀÀ+ Decapoda Snow crab Chionoecetes opilio ++À Crab Hyas coarctatus ++À Helmut crab Telmessus cheiragonus + ÀÀ Hermit crab Labidochirus splendescens À + À Hermit crab Pagurus trigonocheirus + ÀÀ Shrimp Argis lar À + À Gastropoda Whelk Neptunea ventricosa (N. heros in US +++ literature) Whelk N. communis ++À Snail Margarites sp. + ÀÀ Bivalvia Mussel Mytilus trossulus +++ Ectoprocta Bryozoan Alcyonidium disciforme ÀÀ+ Bryozoan A. vermiculare + ÀÀ Holothuroidea Sea cucumber Myriotrochus rinkii À ++ Sea cucumber Ocnus glacialis À ++ Echinoidea Sea urchin Strongylocentrotus pallidus ++À Green sea S. droebachiensis + ÀÀ urchin Sand dollar Echinarachnius parma ++À Asteroidea Sea star Ctenodiscus crispatus +++ Sea star Henricia beringiana ÀÀ+ Sea star Crossaster papposus +++ Sea star Asterias rathbuni (A. amurensis in US ++À literature) Sea star Leptasterias polaris ++À Sea star Urasterias linckii À + À Ophiuroidea Basket star Gorgonocephalus caryi ++À Brittle star Ophiopholis aculeata + ÀÀ Brittle star Ophiura sarsi +++ Ascidiacea Tunicate Chelyosoma inaequale ++À Tunicate Styela coriacea ÀÀ+ Tunicate Pelonaia corrigata À + À Tunicate Rhizomolgula globularis ÀÀ+ Tunicate Boltenia ovifera ++À Tunicate B. echinata ++À References: Derjugin and Ivanov, 1937; Ushakov, 1952; Vinogradova, 1954; Neiman, 1961; Zenkevich, 1963; Feder and Jewett, 1978; Golikov et al., 1994; Shuntov, 2001; Feder et al., 2003, 2005; Sirenko, unpublished data. decline in both organic carbon supply to the benthos (interpreted from SCOC) and bivalve biomass, which has been interpreted as a possible consequence of earlier, seasonal sea ice retreat and warming temperatures (Gre- bmeier and Dunton, 2000; Lovvorn et al., 2003; Grebmeier et al., 2006; J. Grebmeier, unpublished data). J.M. Grebmeier et al. / Progress in Oceanography 71 (2006) 331–361 349

Fig. 6. Distribution of d13C(&) values for organic carbon in surface sediments of the northern Bering, Chukchi, eastern East Siberian and western Beaufort Seas for the period 1984–2004 (references listed in Table 2). Analysis followed methods outlined in Cooper et al. (2002).

These findings are in addition to the apparent shift in dominant bivalve species from Macoma calcarea to Nuculana radiata (Sirenko and Koltun, 1992; Lovvorn et al., 2003; Grebmeier et al., 2006). By comparison, the region north of St. Lawrence Island to Bering Strait is dominated by amphipods (Ampelisca macrocephala, Byblis spp.) and bivalves (Macoma calcarea) living in sandy muds. Recently, there have been declines in these amphipod populations and a shift in gray whale feeding sites from the northern Bering Sea northward to as far as Barrow off the north slope of Alaska (Moore et al., 2003, 2006), supporting the view that a large scale ecosystem change is underway. The high productivity of the Gulf of Anadyr water and the flux of organic carbon to the bottom support a rich infauna and epifauna. In the southwestern region of the Gulf of Anadyr, within sand at a depth less than 50 m, the sand dollar Echinarachnius parma is abundant, while the fine-grained central Gulf supports numer- 350 J.M. Grebmeier et al. / Progress in Oceanography 71 (2006) 331–361 ous omnivorous brittle stars (Ophiura sarsi; see Table 4) as well as a variety of predatory crabs and gastropods (Grebmeier, 1992, 1993; Sirenko and Koltun, 1992). By contrast, the Anadyr Strait to the west of St. Lawrence Island has strong currents and mixed coarse pebbles and rocks dominated by suspension feeders, including sponges, barnacles (Balanus crenatus), and ascidians (Boltenia ovifera and Boltenia echinata). The sea urchin Strongylocentrotus pallidus, often present in regions with strong currents, and Ophiura sarsi are also abundant here. On the soft bottom within the central Gulf of Anadyr common epifauna include snow crabs (Chionoece- tes opilio and Hyas coarctatus), hermit crabs (Pagurus spp.), gastropods (Neptunea ventricosa and Margarites sp.), basket stars (Gorgonocephalus caryi) and brittle stars (Ophiura sarsi). Organic carbon derived from highly productive Anadyr Water passes through Anadyr Strait west of St. Lawrence Island into the Chirikov Basin northward to Bering Strait (Fig. 1) where it supports a rich benthic fauna (Fig. 4; Grebmeier, 1993). Increased bottom currents maintain fine sediments in suspension, resulting in a coarse, sandy sediment that sustains numerous interface-feeding ampeliscid amphipods, a seasonal food source of gray whales (Highsmith and Coyle, 1992). The presence of an abundant infauna (amphipods and bivalves) supports a substantial epifauna (hermit crab Pagurus trigonocheirus, sea star Leptasterias polaris, crangonid shrimp Argis lar, the crabs Hyas coarctatus and Chionoecetes opilio, and the large gastropod Nept- unea hero) in the Chirikov Basin (Feder and Jewett, 1978). A variety of other fauna occur under the more coastal waters surrounding the central high biomass regions of the northern Bering Sea. This fauna includes sea anenomes, sipunculid worms, gastropods, bivalves and sand dollars. It is notable that sand dollars occur at the frontal interface between coastal and offshore waters in various parts of the Gulf of Anadyr, in a band northeast of St. Lawrence Island between BSAW and ACW, and just north of Bering Strait in the southern Chukchi Sea as the grain size changes from coarse gravel to sand (see Fig. 1 for location; Sirenko and Koltun, 1992; Grebmeier et al., 1989; Feder et al., 2005), B. Sirenko, unpublished data). Norton Sound, a large gulf to the east of St. Lawrence Island (Fig. 1), is located under the less productive ACW, but the advection of offshore BSW eastward allows for a substantial level of infaunal and epifaunal populations that support walrus and gray whales (Feder and Jewett, 1978; Jewett et al., 1999). The depth in Norton Sound averages about 20 m, and the region is ice covered during much of the winter-spring. Storms in ice-free periods and strong bottom currents are key factors that influence the sedimentary and biological structure of the area. Small, opportunistic infaunal species dominate the benthic fauna, which reflect the effect of the dynamic environment on these animals. A number of epifaunal species are dominant in Norton Sound but absent or uncommon in the offshore central Chirikov Basin, including red king crab Paralithodes camtsch- atica and predatory sea stars (dominated by Asterias amurensis). Outside Norton Sound and northward, the bottom under the ACW receives food of low quality, comprising a variable mixture of terrigenous and marine organic matter. This results in reduced benthic populations (Feder and Jewett, 1978; Jewett and Feder, 1981). Continuing through Bering Strait, the sediments are replaced by pebble, gravel, and shells (Stoker, 1978, 1981; Grebmeier et al., 1989), and the epifauna in these fast-current areas consist of sponges, the soft coral Gersemia rubiformis, barnacles Balanus crenatus, sea urchins Strongylocentrotus pallidus, basket stars Gorgonocephalus caryi, and the ascidian Boltenia ovifera (Feder et al., 2005; B. Sirenko, unpublished data).

3.5.2. Southern Chukchi Sea The northwestward transit of Pacific water through Bering Strait and northward into the Chukchi Sea, laden with high nutrients and suspended biomass, is a driving factor for the high productivity of the underlying benthos in the southcentral Chukchi Sea. As mentioned in Section 3.1, an oceanic front separates the nutrient-rich BSAW and nutrient-poor ACW in the southern Chukchi Sea. Benthic infaunal biomass is very high in the southern Chukchi Sea (Fig. 4) in association with areas of high water column production (Fig. 2; Springer et al., 1996). These parameters are significantly correlated (Table 3). Previous measurements of SCOC also show persistent patterns of organic carbon flux to sediments in the southern Chukchi Sea (Gre- bmeier and Cooper, 1994; Grebmeier and Dunton, 2000; Fig. 3; Table 3). Substantial infaunal and epifaunal communities are present under the highly productive BSAW water overlying the inner Chukchi shelf. Macro- benthic infaunal biomass in the south-central Chukchi Sea stations ranged from 24 to 59 g C mÀ2 (500–1400 g wet wt. mÀ2), exceeding 117 g C mÀ2 (>3000 g wet wt. mÀ2) at one station, an extremely high value for any- where in the world ocean. In particular, this region includes the ‘‘hot-spot’’ area northwest of Bering Strait, which is dominated by bivalves Macoma calcarea, Nucula belloti, and amphipods (Byblis spp., Anonyx sp.) J.M. Grebmeier et al. / Progress in Oceanography 71 (2006) 331–361 351 and has an average station abundance of 10,000–15,000 individuals mÀ2 and biomass of 40–100 g C mÀ2 (up to 4000 g wet wt. mÀ2; Fig. 4). Unlike the benthic infauna under this productive BSAW system, the benthos to the east in the Chukchi Bight northeast of Bering Strait under ACW, yet outside of Kotzebue Sound, has a variable infaunal community composition and mainly a lower biomass (<10 g C mÀ2, 200 g wet wt. mÀ2; Fig. 4), but with some higher values (12–23 g C mÀ2, 460–820 g wet wt. mÀ2; Feder et al., in press). Infaunal benthic communities in the southern Chukchi Sea are dominated by large numbers of amphipods to the east and bivalves to the west. By comparison, epifauna are dominated by the omnivorous brittle star Ophiura sarsi and a number of predators, such as the sea star Leptasterias polaris that consumes both infauna and epifauna and the large gastropods Neptunea heros and Buccinum spp. that mainly feed on infauna.

3.5.3. Chukchi Bight and Kotzebue Sound Sediments under ACW within the Chukchi Bight and Kotzebue Sound to the east of the southern Chukchi Sea contain fauna that are directly influenced by advection of high quality organic carbon from the more productive offshore waters as the BSAW and ACW mix (Feder et al., in press). This mixed water entering from Bering Strait with its high particulate organic carbon load flows along the Alaska coast into the area, circling counterclockwise in the Kotzebue Sound, then exiting northward along the coast past Pt. Hope (Fig. 1; Feder et al., in press). Carbon and nitrogen isotope signatures of benthic epifauna within Kotzebue Sound and just to the north into the nearshore ACW are similar to values obtained under the ACW in the northeastern Chuk- chi Sea. These values suggest that there are possibly sources of laterally advected, 13C-enriched phytoplankton serving as food for benthic organisms in these nearshore regions (Dunton et al., 1989; Feder et al., 1991a,b, 2005, in press). The organic carbon-rich waters flowing through Bering Strait and eastward into the Chukchi Bight and Kotzebue Sound sustains abundant infauna, particularly the interface-feeding oweniid polychaete Galathowenia oculata (up to 66,200 ind mÀ2) in Kotzebue Sound, the surface-deposit feeding brittle star Diam- phiodia craterodmeta and numerous epifaunal species (Feder et al., 1991a, 2005, in press). In addition, the high allochthonous organic carbon in these inflow waters supports high abundance of Galathowenia oculata (21,000 ind mÀ2) and abundant epifauna on the gravel bottom northward along the coast to Point Hope. This community includes the rapidly growing mussel Mytilus trossulus (up to 2.5 cm in 4 months; Table 4; Feder et al., 2005, in press).

3.5.4. Eastern East Siberian Sea Although the benthos of the East Siberian Sea is only briefly discussed here because of the limited data available, it is clearly different from that of the Chukchi Sea (Tables 1 and 4). It is primarily an Arctic sea, influenced by the Atlantic Ocean and high riverine input (Petrova et al., 2004). It has relatively low salinity and temperature (e.g., Khim et al., 2003; Petrova et al., 2004) that likely cause the observed faunal differences from the Bering and Chukchi Seas (Reed, 1998; Mu¨nchow et al., 1999; J. Grebmeier and B. Sirenko, unpublished data). Although the net flow is from west to east in the nearshore regions of the East Siberian Sea, Paci- fic water does extend though Long Strait south of Wrangel Island to the eastern edge of the area, depending on dominant wind direction (Reed, 1998; Mu¨nchow et al., 1999; Weingartner et al., 1999; J. Grebmeier and B. Sirenko, unpublished data). In the offshore areas, the dominant epifauna includes sea anemones, isopods, amphipods, gastropods, ascidians and sea stars (Table 4).

3.5.5. Central Chukchi Sea Recent studies as part of the USA National Oceanic and Atmospheric Administration (NOAA)-sponsored Russian-American Long-term Census of Marine Life (RUSALCA) program during 2004 (planned for contin- uation in 2008) provided an opportunity for collaborative work in the Russian sector of the Chukchi Sea, which has seen very few prior studies. BSAW apparently becomes nutrient- and phytoplankton-poor during the northward transit, resulting in declining infaunal benthic biomass moving northward from the southern Chukchi Sea ‘‘hot-spot’’ area to the central Chukchi Sea, with infaunal benthic biomass dropping to <10 g CmÀ2 (200–300 g wet wt. mÀ2; Fig. 4, Sirenko and Gagaev, 2005; J. Grebmeier, unpublished data). Benthic infauna in Herald Trough in the central and western Chukchi Sea is dominated by maldanid (Maldane sarsi), lumbrinerid (Nicomache lumbricali) and nephtyid (Nephtys ciliata) polychaetes, brittle stars (Ophiura sarsi) and sipunculids (Golﬁngia margaritacea). An unexpectedly rich assemblage of sedentary epifaunal organisms 352 J.M. Grebmeier et al. / Progress in Oceanography 71 (2006) 331–361

(sponges, soft corals and bryozoans) encrusts both pebbles and manganese nodules in the central Chukchi Sea (Sirenko and Gagaev, 2005). It should be noted that infaunal benthic biomass increases farther north in Her- ald Valley (10–20 g C mÀ2; 200–500 g wet wt.; Fig. 4), which may indicate a hydrographic focusing of high quality organic material into this region. In the USA. sector of the central Chukchi Sea, the hydrographic front between BSAW and ACW oﬀ the Alaska coastline continues to extend northward to just north of Icy Cape (Fig. 1; Grebmeier et al., 1988; Feder et al., 1994a,b).

3.5.6. Northern Chukchi Sea Moving towards the northern Chukchi Sea, nutrient-poor ACW lies inshore of the front, while nutrient- rich BSAW lies to the west and north of the front. Infaunal biomass values are higher north of the front (Fig. 4), which is probably the result of persistent organic carbon deposition to the benthos from carbon advected towards the Alaska coast from offshore waters (Feder et al., 1994a; Fig. 1). The distribution, abundance and biomass of infauna and epifauna in the northeastern Chukchi Sea are related to water mass and current patterns (Feder et al., 1994a). The annual summer return of gray whales that feed on the abundant, benthic amphipods (Ampelisca spp.) along the northern Alaska coast indicates that organic matter is supplied on a long-term basis (Fay, 1982; Feder et al., 1994a). The inshore area north from Icy Cape to Point Barrow, which has a mud, gravel and boulder bottom, con- tains large numbers of epifaunal organisms such as sponges, sea anemones, soft corals (Gersemia rubiformis), barnacles (Balanus crenatus), bryozoans (many species), sea cucumbers and sea urchins (Strongylocentrotus droebachiensis)(MacGinitie, 1955; Table 4). Amphipods (over 100 species) are ubiquitous and abundant on soft bottom and gravel-boulder areas here. Two species of hermit crabs (Labidochirus splendescens and Pagu- rus trigonocheirus) and the crab Hyas coarctatus are common. The gastropods (Buccinum spp.) are common in soft and muddy-gravel bottom. In addition, common echinoderms inshore are the basket star Gorgonoceph- alus caryi and sea stars, while the brittle star Ophiura sarsi and the sea cucumber Psolus sp. are abundant in deep water. Ascidians (mainly Boltenia spp. and Halocynthia aurantium) are extremely abundant on mud- gravel substrates off Barrow. Epifaunal mollusks increase in abundance and biomass northeast of Cape Lisburne (located just north of Pt. Hope, Fig. 1), which suggests a link between biomass and the organic carbon flowing from south to north. The three molluscan groups that occur in large numbers are the surface-deposit feeding bivalve Thyasira gou- ldi, the suspension-feeding scallop Chlamys behringiana, and the large gastropods Neptunea spp. and Buccinum spp. The omnivorous snow crab (Chionoecetes opilio) also had a high abundance in this region (Paul et al., 1997). High mollusk abundance continues along the outer coast northward towards Icy Cape. The coastal area north of Cape Lisburne comprises a gravel-free, sandy substrate with large abundance and biomass of the deposit-feeding sand dollar Echinarachnius parma (Feder et al., 1994a; Ambrose et al., 2001). Although Echinarachnius is mainly a surface-deposit feeder, it can form dense aggregations that may suspension feed in the POC-enriched waters (Ridder and Lawrence, 1982) in the presence of strong currents (Phillips, 1987). Their distribution is similar to the bands of sand dollars under the frontal zone between BSW and ACW along the Alaska coast in the northeastern Bering Sea and just north of Bering Strait (Grebmeier et al., 1989; Feder et al., 1994a; Ambrose et al., 2001; Grebmeier and Cooper, in press; J. Grebmeier, unpublished data). Dominant epifauna on soft sediments in the eastern region of the northern Chukchi Sea include snow crabs (Chionoecetes opilio), crangonid shrimps and mollusks (mainly Neptunea heros, Neptunea ventricosa, Neptunea borealis and the scallop Chlamys behringiana), ophiuroids (mainly Ophiura sarsi), sea stars (Asterias amurensis, Leptasterias polaris) and ascidians (Boltenia, Molgula, Styela and Halocynthia; Table 4). Few bottom-feeding fishes are present in the northern Chukchi Sea, as also noted for the northern Bering Sea and SE Chukchi Sea (Jewett and Feder, 1980; Feder et al., in press). As a consequence, echinoderms are numerous in the northeastern Chukchi Sea (Feder et al., 1994a; Ambrose et al., 2001), including the sand dollar Echinarachnius parma and dense assemblages of ophiuroids, particularly the omnivorous Ophiura sarsi and the suspension-feeding Ophiopholis aculeata. Recent studies indicate that ophiuroids may be more important in the cycling of organic matter in the Arctic than previously thought (Feder et al., 1994a; Piepenburg, 2000, 2005; Ambrose et al., 2001). The abundant large omnivorous gastropods, snow crabs and sea stars in this region probably also play important roles in organic carbon remineralization (Feder et al., 1994b; Paul J.M. Grebmeier et al. / Progress in Oceanography 71 (2006) 331–361 353 et al., 1997; N. Foster, personal communication). Benthic infaunal biomass (excluding upper Barrow Canyon) declines northward over the outer Chukchi shelf. Bivalves and polychaetes dominate the general infaunal community of the northern Chukchi Sea, where average infaunal benthic biomass is 5–15 g C mÀ2 (200–400 g wet wt. mÀ2; Fig. 4). This benthic community structure changes to a Foraminifera-based one on the upper slope (200–1000 m depth), with benthic biomass <5 g C mÀ2 (<200 g wet wt. mÀ2), that extends down into the Canadian Basin (Fig. 4; Pirtle-Levy, 2006;J. Grebmeier, unpublished data). By comparison, upper Barrow Canyon is a ‘‘hotspot’’ region in the NE Chuk- chi Sea, where a rich epifauna of suspension feeders (e.g., sponges, bivalves, barnacles, basket stars and tuni- cates) attached to rocks and cobble and mixed sediments suggests the presence of strong currents (MacGinitie, 1955; Ambrose et al., 2001; J. Grebmeier, unpublished data). In areas with interspersed silt, clay and gravel the suspension-feeding mussel Musculus discors is abundant, with station biomass values up to 100 g C mÀ2 (4000 g wet wt mÀ2; Fig. 4). This enrichment in benthic biomass at the head of Barrow Canyon (Fig. 4) coincides with extremely high SCOC (Fig. 3; Table 3). Observations of black, sulfide-rich muds near the head of Barrow Canyon and other sediment tracers suggest that there is a periodic, downslope transport of organic materials from the shelf to the basin (Grebmeier and Cooper, 1994; Devol et al., 1997; Cooper et al., 2005b). The mud at the bottom of the canyon is covered with tubes of the deposit-feeding polychaete Pista, together with a vast array of other polychaetes and a variety of other infauna and epifauna (MacGinitie, 1955; J. Grebmeier, unpublished data).

3.5.7. Western Beaufort Sea The western portion of the Beaufort Sea, hydrographically downstream of the northward flowing Pacific water, receives advected and locally produced organic carbon as indicated by both higher integrated water column and surface sediment chlorophyll data and more enriched d13C surface sediment values in organic carbon (Figs. 2 and 6, Cooper et al., 2005b. Grebmeier, unpublished data). By comparison, the more riverine-influenced central and eastern Beaufort Sea has lower integrated water column and sediment chlorophyll inventories, and the surface organic carbon is more terrestrially-based as indicated by the more depleted d13C surface sediment values (Figs. 2 and 6, Macdonald et al., 2004; Dunton et al., 2005). This results in locally high infaunal benthic biomass (10–20 g C mÀ2, 200–680 g wet wt mÀ2; Fig. 4) compared to more organic carbon-limited systems to the east in the nearshore Beaufort Sea (<10 g C mÀ2, <200 g wet wt mÀ2; Fig. 4; Dunton et al., 2005).

3.5.8. Spatial patterns of pelagic-benthic coupling Sediment indicators, such as chlorophyll a (chl-a) content and stable carbon isotopes (d13C) can be used to evaluate biological responses to changing ice cover and marine productivity (Grebmeier and Cooper, 1995; Cooper et al., 1998, 2002, 2005b; Clough et al., 2005). Variation in primary production leads to variation in the supply of usable organic carbon to the seabed, influencing benthic faunal patterns and energy turnover (Grebmeier and Barry, in press). Surface sediment chl-a content is an indicator of pelagic-benthic coupling in shallow continental shelves (Cooper et al., 2002), providing an index of recently deposited organic matter to the surface sediments. Seasonal analyses of surface sediment chl-a support a strong coupling of water column production and the underlying benthos in the spring in the northern Bering Sea (Cooper et al., 2002), a finding also confirmed in the northern Chukchi Sea by Ambrose et al. (2005). Chlorophyll inventories in surface sediments decline later in the summer season and over the winter (Cooper et al., 2002). The ‘‘foot prints’’ of chl-a in surface sediments are similar to patterns of the deposition zones indicated by SCOC (Fig. 3) and stable carbon isotopes (Fig. 6). Pearson product-moment correlation analyses indicate significant relationships among these parameters (Table 3). Nearshore regions with limited organic carbon supply to the benthos and faster currents had lower surface sediment chl-a inventories, whereas sediments in the offshore areas had the highest. Although SCOC generally declined toward the eastern margin of the East Siberian Sea, our data from 1995 indicated that organic carbon produced in the water column, primarily as an ice algal bloom, was not neces- sarily being incorporated into the surface sediments or benthic fauna, unlike the Pacific-influenced southern Chukchi Sea, but was being advected offshore across the wide continental shelf towards the Arctic basin (Reed, 1998; Cooper et al., 1998; J. Grebmeier, unpublished data). 354 J.M. Grebmeier et al. / Progress in Oceanography 71 (2006) 331–361

In addition, d13C values and C/N ratios in organic matter in surface sediments can provide information on food quality of the settling organic matter (e.g. Grebmeier et al., 1988; Cooper et al., 2002). Less depleted d13C values and lower C/N ratios in surface sediments occur under the more productive offshore regions of the northern Bering and Chukchi Seas (Fig. 6; modified from Cooper et al., 2002; Naidu et al., 2004; with additional, previously unpublished data sources tabulated in Table 2). In addition, 13C-enrichment observed in secondary benthic consumers, relative to that of zooplankton and water column seston, is consistent with a direct coupling of these consumers to the very high pelagic primary production on the shallow shelf that is minimally grazed before reaching the sea bed (Dunton et al., 1989; Lovvorn et al., 2005; Dunton et al., 2006). Infaunal biomass (Fig. 4) is spatially similar and positively correlated to integrated chl-a (Fig. 2), SCOC (Fig. 3), and to 13C-enrichment in surface sediments (Fig. 6; Table 3). In addition, the feeding methods used by both the infauna and epifauna also reflect the relationship of water–current patterns to the delivery of organic carbon. For example, the numerous predator/scavenger and suspension-feeding taxa highlight the availability of substantial food resources under the mixed ACW in the Chukchi Bight and Kotzebue Sound, as opposed to the low food availability on the bottom under ACW outside the Bight (Feder et al., in press). The absence of large numbers of bottom-feeding demersal fishes increases the availability of benthic infaunal prey for epifaunal predators, such as shrimps, crabs, ophiuroids and sea stars. Although epifauna are important in soft sediments, they are much more dominant life forms on hard substrates, particularly in the coastal regions, straits (Anadyr, Bering, and Long Straits), canyons, and nearshore coastal regions, all under fast currents. Hard substrates in the northern Bering and Chukchi Seas are dominated by sponges, sea anenomes, soft corals, sea urchins, bryozoans, barnacles, brachyuran and hermit crabs, and ascidians. Nearshore embayments off the NW coast of the Chukotka Peninsula, such as Chauna Bay (East Siberian Sea) and Koluchinskaya Bay (Chukchi Sea) are dominated by epifauna including sponges, hydroids, mussels (Mytilus trossulus), and ascidians that are not common in more offshore waters (Table 4; B.Sirenko, personnal communications). More exposed hard substrates of the Chukchi coasts (both off Alaska and Rus- sia) are inhabited mainly by barnacles, basket stars, and mussels (Mytilus trossulus)(Table 4 and references therein; Feder et al., 2003; B. Sirenko, unpublished data).

4. Environmental change and ecosystem structure

The prevalence of southerly winds over the Bering Sea has increased over the past decade, and this change in atmospheric forcing is related to an observed reduction in seasonal sea ice extent and ecosystem change (Overland and Stabeno, 2004; Grebmeier et al., 2006). Biological community structure and organic carbon cycling over the shallow shelves influence the level of organic carbon and recycled nutrients entering the Arctic Basin via shelf-basin exchange mechanisms, such as advective transport, eddy dynamics, and down-canyon material transport. During this period of significant sea-ice retreat, there have been (fortuitously) multiple oceanographic studies in the area as part of the SBI project, the Bering Strait Environmental Observatory (BSEO; http://arctic.bio.utk.edu), RUSALCA, and other programs that have allowed a broad-scale view of the impacts of sea ice retreat upon continental margin dynamics and ecosystem structure. These recent studies provide the comparative basis to evaluate how recent sea ice retreat and water column warming have affected ecosystem structure and the potential for system reorganization. It is important to evaluate the general trophic relationships within a community when developing hypoth- eses for the potential impact of future warming in the Arctic and additional ice retreat. A recent review by Piepenburg (2005) hypothesized that environmental change may alter the sea ice production-to-benthos connection characteristic of productive Arctic shelves to one in which zooplankton grazing and the microbial loop in the water column are more dominant, thus limiting carbon export to the sediments to the detriment of supporting benthic communities. Because of seasonal ice retreat in the Pacific-influenced Amerasian Arctic, this hypothesis is likely to be tested earlier than in other parts of the Arctic. The wide Arctic shelves are key regions for high trophic level consumers, from water-column and demersal fishes to epifaunal predators, benthic-feeding marine mammals and seabirds. A switch in trophic dynamics from a benthic-based to water column-based system would have dramatic impacts on these consumers, such as bearded seal, walrus, gray whales and seabirds. J.M. Grebmeier et al. / Progress in Oceanography 71 (2006) 331–361 355

Because high productivity over wide and shallow shelves is characterized by enhanced seasonal export production (Grebmeier and Barry, in press), we expect that this system is poised to be directly responsive to environmental changes. Some key indicators of major changes are becoming evident. Recent studies in the northern Bering Sea under BSW indicate a declining trend in benthic infaunal biomass from the 1990s through 2000s (Grebmeier and Dunton, 2000; Moore et al., 2003; Grebmeier et al., 2006), both north and south of St. Lawrence Island. The bivalve and amphipod infauna are the benthic prey base for the declining populations of diving seaducks in the northern Bering Sea (Lovvorn et al., 2003) and environmental changes could have significant, more system-wide effects. Recent data do indicate a movement northward of the cold-water barrier that limits crabs and fishes (Gre- bmeier et al., 2006) and a compensatory shift of some benthic-feeding marine mammals farther north into the Arctic (Moore et al., 2003, 2006). However, it is still uncertain whether changes in migratory walrus and gray whale patterns are due to environmental changes affecting prey communities, or whether these larger animals are approaching or exceeding carrying capacity (Lowry et al., 1980; Highsmith and Coyle, 1992; Moore et al., 2003; Grebmeier et al., 2006). Regardless, the unprecedented retreat of seasonal sea ice in recent years suggests that we are in the midst of a climate shift in which the subarctic-to-arctic front in the Bering Sea may be moving northward (Grebmeier et al., 2006). The Chukchi Sea may well be transformed into an ecological extension of the Bering Sea. These observations support previous scenarios of ecosystem shifts from benthic to pelagic dominance of organic matter consumption that could coincide with climate warming (Grebmeier and Dunton, 2000; Stab- eno and Overland, 2001; Carroll and Carroll, 2003; Overland and Stabeno, 2004). Although the northern Bering Sea seems to be undergoing changes in hydrography and in predator-prey relationships, zones of high benthic biomass under the highly productive BSAW in the SE Chukchi Sea do not appear to have changed dramatically in community composition from previous sampling over a 20-year period (Grebmeier et al., 1988; Feder et al., in press; J. Grebmeier and B. Sirenko, unpublished data). In addition, other studies in nearshore, shelf habitats located under the lower productivity ACW in Norton Sound, northern Bering Sea (Hamazaki et al., 2005) and Kotzebue Sound/Chukchi Bight, southern Chukchi Sea (Feder et al., 2005) indicate an increase in epifaunal predators. Although these epifaunal results are at variance with infaunal results in the northern Bering Sea, they may also provide evidence for a changing ecosystem. For example, a warming northern Bering Sea would allow for a northward enhancement of mobile epifauna that are temporally and spatially decoupled from water mass production, although their infaunal prey are not. As adults, infauna cannot migrate to new areas, unlike mobile epifauna, although some infauna can release larvae into the water column for dispersal to new sites which adds complexity to changes in epifaunal population dynamics. Other explanations for a decline of infaunal abundance, while epifaunal abundance remains the same or increases could just be that the studies were done in different places in the northern Bering Sea. Alter- natively, the more oceanic physical-biological processes in the offshore northern Bering and Chukchi Seas could have a more direct impact on benthic infaunal processes compared to the more localized, freshwater- influenced Norton Sound and Kotzebue Sound/Chukchi Bight regions. This spatial variability in infaunal and epifaunal community structure highlights the need for time-series and ecosystem-level studies on these shallow Arctic shelves, including the benthic components, to evaluate biological response to environmental change in these highly productive and efficient, short food chains. What impact changes in shelf productivity in the Pacific-influenced Arctic will have on shelf-basin exchange is uncertain. In a recent review, Piepenburg (2005) suggests that most of the organic carbon produced over the more eutrophic Arctic shelves, such as the northern Bering and Chukchi Seas, actually remains on the shelves and is not transported to the deep basins. On one hand, recent studies support this argument, showing incor- poration of locally produced organic carbon into large plankton and benthic biomass (Springer et al., 1996; Dunton et al., 2005; Plourde et al., 2005; this paper). However, recent data also indicate that outer shelf/slope canyons in the Chukchi Sea are key conduits transporting organic carbon offshore, with surface sediment TOC higher on the slope and basin regions (1–1.5%) compared to the outer continental shelf (<1%; Fig. 5; Grebmeier and Cooper, 1994; Ambrose et al., 2001; Grebmeier and Cooper, 2004; Clough et al., 2005; Cooper et al., 2005b. The high productivity in BSAW supports a large biomass at several trophic levels in this area. The largest benthic populations are on the shelves, where a large percentage of the export production is consumed by the underlying benthos, but recent observations within the SBI program also indicate significant sedimentation of organic carbon to the slope sediments (Cooper et al., 1998, 2005b). In addition, a recent water column study indicates that dissolved organic carbon (DOC) is a significant source of off-shelf organic carbon 356 J.M. Grebmeier et al. / Progress in Oceanography 71 (2006) 331–361 that is transported into the deep basin (Davis and Benner, 2005). In addition to direct runoff of DOC, other work by Cooper et al. (2005a) showed that continental shelf sediments were a significant DOC source. This combination of data support the finding of Moran et al. (2005) that up to 20% of the export production during the summer period is moved off-shelf from the Chukchi Sea into the upper water column of the Canadian Basin. It is not used by the seasonally ice-free shelf trophic system, but instead provides an allocthonous source of organic carbon to the Canadian basin ecosystem which has a longer annual ice cover and lower annual primary production. Ultimately, the potential environmental changes being observed in the Pacific sector could influence the physical and biological connections of the Arctic shelves to the basin, ultimately having large-scale impacts on the overall Arctic system.

5. Summary

The Amerasian shelf system, particularly the northern Bering and southern Chukchi Seas, is one of the most productive regions in the world ocean due to the nutrient-rich Pacific-water overflowing the shallow shelf on its northward transit to the Arctic Ocean. Seasonal sea ice over these shelves allows both sea ice and open water production in the spring and summer coincident with low water temperatures that limit zooplankton production and pelagic organic carbon cycling, resulting in a shunting of organic carbon directly to the sediments. With the record level of ice retreat observed in the early 21st century (ACIA, 2005; Stroeve et al., 2005), the potential for a northward shift of the sub-arctic/arctic boundary is possible, with movement of com- petitive species northward into the warmed environments (Grebmeier et al., 2006). Ultimately, the short food chains and reduction in pelagic–benthic coupling in the region may result in a rapid adjustment from a benthic- to pelagic-based ecosystem at higher trophic levels (Piepenburg, 2005). The ramifications for the benthic feeding marine animals characteristic of this pacific-influenced region (bearded seals, walrus, gray whales, diving sea ducks) are potentially stark, and even pelagic-feeding animals that depend on sea ice, like ring and ribbon seals, bowhead whales, seabirds, and polar bears, may be impacted. Ultimately, there is a critical need for physical, biogeochemical and biological time series studies in selected regions to observe and evaluate the changing Arctic ecosystem to facilitate appropriate societal response.

Acknowledgement

We extend our appreciation to Chirk Chu who has statistically processed almost all of the benthic data sets for cruises from the 1970s onwards. He has been instrumental in analyses of all research cruises discussed here. We also thank Rebecca Pirtle-Levy for preparing ﬁgures and graphics as well as Arianne Balsom, Becky Brown, and Adam Humphrey for laboratory support, along with many past technicians. We thank three anonymous reviewers and the guest editor for constructive comments that helped to improve the quality of the review. Financial support was provided by the US National Science Foundation grants OPP-9910319 (to L. Cooper and J. Grebmeier), OPP-0125082 (to J. Grebmeier and L. Cooper), US National Oceanic and Atmospheric Administration (Cooperative Institute for Arctic Research, UAF 04-0048 to J. Grebmeier) and the Russian Academy of Sciences (B. Sirenko, Russian Foundation for Basic Research and Program Grant N 04-04-49300).

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