Shifting Patterns of Life in the Pacific Arctic and Sub-Arctic Seas

MA04CH04-Grebmeier ARI 3 November 2011 13:42

Shifting Patterns of Lifein the Pacific Arctic andSub-Arctic SeasJacqueline M. GrebmeierChesapeake Biological Laboratory, University of Maryland Center for Environmental Science,Solomons, Maryland 20688; email: [email protected]

Annu. Rev. Mar. Sci. 2012. 4:63–78

First published online as a Review in Advance onSeptember 19, 2011

The Annual Review of Marine Science is online atmarine.annualreviews.org

This article’s doi:10.1146/annurev-marine-120710-100926

Copyright c© 2012 by Annual Reviews.All rights reserved

1941-1405/12/0115-0063$20.00

Keywords

Arctic ecosystem structure, benthic carbon cycling, poleward transitions,biodiversity

Abstract

Recent changes in the timing of sea ice formation and retreat, along withincreasing seawater temperatures, are driving shifts in marine species com-position that may signal marine ecosystem reorganization in the PacificArctic sector. Interannual variability in seasonal sea ice retreat in the north-ern Bering Sea has been observed over the past decade; north of the BeringStrait, the Chukchi Sea ecosystem has had consistent earlier spring sea iceretreat and later fall sea ice formation. The latitudinal gradient in sea icepersistence, water column chlorophyll, and carbon export to the sedimentshas a direct impact on ecosystem structure in this Arctic/sub-Arctic complex.Large-scale decadal patterns in the benthic biological system are driven bysea ice extent, hydrographic forcing, and export production that influencesbenthic processes. Shifts in species composition and northward faunal rangeexpansions indicate a changing system. The shifting patterns of life andchange in key biological processes have the potential for a system-wide re-organization of the marine ecosystem.

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INTRODUCTION

The Arctic Ocean is experiencing changes in seasonal sea ice extent and retreat as well as increasedocean temperatures and freshwater content (Stroeve et al. 2007, Polyakov et al. 2010, Steele et al.2010). Reductions in sea ice cover have been particularly significant in the marginal seas of theAlaskan and Russian continental shelves, including the northern Bering and Chukchi Seas (Steeleet al. 2008). Emerging observations indicate that these changes are driving shifts in marine speciescomposition and carbon cycling. These changes may signal ecosystem reorganization because theobserved sea ice changes are critical driving factors for biological processes and marine ecosystemstructure. Biological observations include changing composition and range extensions of benthicfauna as prey coincident with more northern migration of marine mammals into the Pacific Arctic(Grebmeier et al. 2010).

Thus, a fundamental research question is, how else will the marine ecosystem respond to therapid sea ice loss that is occurring now in the Arctic? The seasonal ice zones support ecosystemsthat are influenced by ice algae and/or by early stabilization of the water column by melting seaice, which initiates a spring bloom. The timing and location of this pulse of primary productionand associated grazing by zooplankton over both shallow shelves and deep regions have a directinfluence on the energy pathway connecting the water column to the underlying sediments. Theshort food chains characteristic of polar regions can have large cascading impacts on higher trophicorganisms, such as seabirds, seals, walrus, and whales, particularly if they are ice-obligate species orundergo large migrations. Thus, the marine ecosystems in polar regions will likely respond throughboth short-term population changes and long-term restructuring with continued sea ice retreat.

These reductions are enhanced by increased heat fluxes that enter the Arctic Ocean throughthe Bering Strait (Shimada et al. 2006; Woodgate et al. 2006, 2010) and inhibit fall sea ice growth(Steele et al. 2008). These recent changes in sea ice extent are likely to have dramatic impactson ecosystem productivity over the shallow continental shelves of the Arctic Ocean, and perhapsthe deep Arctic Basin. Arrigo et al. (2008), for example, have estimated significant increases inprimary production across the Arctic Ocean over the past few years based on a satellite-derivedprimary production algorithm and observed reductions in sea ice extent, although nutrient levelswill likely influence the extent of production regionally (Grebmeier et al. 2010).

BIOLOGICAL SYSTEM CONNECTIONS TO CLIMATE FORCING

The detection of biological changes in the Bering Strait region (e.g., Grebmeier et al. 2010) coin-cides with recent observations of larger-scale Arctic environmental changes in water temperature,hydrography, and sea ice regimes (Overland & Stabeno 2004, Stroeve et al. 2007, Steele et al.2010). These ecosystem changes on the shallow shelves of the northern Bering and Chukchi Seasare directly linked to systems to the north (Arctic Ocean) and south (Bering Sea/Pacific Ocean).The nutrient-rich Pacific water enters the western side of the Pacific Arctic sector as Anadyr Waterthat moves northward into the Chukchi Sea, while the fresher, less nutrient-rich Alaska CoastalWater enters the eastern side; a mixture of Bering Shelf Water occurs in between, in the ChukchiSea (Figure 1; Weingartner et al. 1998, 2005; Pickart et al. 2010). We are only now understandingthe seasonal processes in the northern Bering and Chukchi ecosystem using retrospective and fieldmeasurements of sea ice extent, the water column, and benthic areas.

Primary and Secondary Production

The northern Bering and Chukchi Seas are among the most productive marine ecosystems inthe world and act as important carbon sinks, particularly during May and June when seasonal

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0

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Siberia

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Atlantic WaterAtlantic Water

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SiberianCoastal Current

Figure 1Schematic of general current patterns in the Pacific Arctic sector. Modified from data presented inWeingartner et al. (2005) and Pickart et al. (2010).

sea-ice-associated phytoplankton blooms occur throughout the region (Springer et al. 1996, Leeet al. 2007, Gradinger 2009). Spring sea ice melt and breakup strongly drive this production byenhancing light availability in the water column, enabling stratification and stabilization of thewater column to maintain nutrients in surface waters. It is widely recognized that recent changesin sea ice seasonality in the northern Bering and Chukchi Seas have significant impacts on springphytoplankton production. In addition, modeling identifies the impacts of retreating North Pacificmarginal sea ice biomes on chlorophyll content as one of the four most important key responsesof global ocean ecosystems to climate warming (Sarmiento et al. 2004). Significant declines in seaice cover throughout the region are already apparent (Figure 2), with the Chukchi Sea showingthe largest sea ice retreat.

In the northern Bering Sea, surface phytoplankton blooms and peaks in chlorophyll a concen-trations coincide with the onset of sea ice degradation and begin to decline within approximatelytwo weeks of the peak of photosynthetic activity (Cooper et al. 2011). Earlier sea ice breakup inthe northern Bering and Chukchi Seas is therefore likely to directly affect the timing and intensityof phytoplankton blooms. With earlier sea ice breakup, although the sea ice melt still enablesthe stratification and trapping of nutrients in surface waters, sunlight may not yet be sufficient

www.annualreviews.org • Shifting Patterns of Life in the Pacific Arctic 65

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≤–0.15 –0.12 –0.09 –0.06 –0.03 0

Shifts in chlorophyll a concentrations (mg m–3 per year)0.03 0.06 0.09 0.12 ≥0.15

180° 160° W 140° W160° E180° 160° W 140° W160° E

≤–15 –12 –9 –6 –3 0

Shifts in sea ice persistence (days per year)3 6 9 12 ≥15

55° N

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Arctic OceanArctic Ocean

Chukchi SeaChukchi Sea BeaufortBeaufortSeaSea

Arctic OceanArctic Ocean

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Arctic Ocean

a

AlaskaSiberia

Bering SeaBering Sea Bering SeaBering SeaBering Sea

0 200Distance (km)

Chukchi Sea BeaufortSea

Arctic Ocean

b

AlaskaSiberia

Bering Sea

Chukchi Sea BeaufortSea

Figure 2Shifts in (a) annual sea ice persistence and (b) chlorophyll a concentrations between 2003 and 2009. Sea ice persistence is based on dailypassive microwave sea ice concentrations using a threshold of 15% (data available from the University of Hamburg; http://www.ifm.zmaw.de), and chlorophyll a concentrations are based on monthly Aqua Moderate Resolution Imaging Spectroradiometer (MODIS)satellite products (data available from NASA; http://oceancolor.gsfc.nasa.gov). Figure updated and modified from Grebmeier et al.2010, courtesy of Karen Frey.

enough to induce as intense a bloom (Clement et al. 2004), suggesting a potential lowered overallproductivity. Alternatively, however, earlier sea ice breakup may cause overall increases in primaryproduction, as observed across the Arctic Ocean by Arrigo et al. (2008) and suggested regionallyby recent changes in surface chlorophyll levels (Figure 2).

For secondary production, the dominant zooplankton in the Pacific sector have distinct pop-ulations. The large Pacific copepod Neocalanus cristatus, the medium-size copepod Neocalanusflemingeri, and the small copepod Calanus marshallae are the dominant copepods in the Bering Seaand are advected northward in the Anadyr Water (west), Bering Shelf Water (center), and AlaskaCoastal Water (east) (Lane et al. 2008, Llinas et al. 2009, Hopcroft et al. 2010). Common shelfcopepods include Pseudocalanus sp. and Oithona sp., particularly in the middle shelf waters of theChukchi Sea. At the northern end of the Pacific downstream region over the outer Chukchi con-tinental shelf and slope are Calanus hyperboreus (an Atlantic species), Calanus glacialis (also found inthe Bering and Chukchi Seas), and Metridia longa. However, in spite of population growth over theseason, these zooplankton populations do not consume a majority of new organic carbon (Ashjianet al. 2005, Campbell et al. 2009). Notably, the location and biomass of zooplankton make them

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http://www.ifm.zmaw.de

http://www.ifm.zmaw.de

http://oceancolor.gsfc.nasa.gov


an important prey base for bowhead whales, which can be indicators of regional hot spots in thePacific sector, such as around Barrow, Alaska (Ashjian et al. 2010; Moore et al. 2010a,b).

Studies by Coyle et al. 2007 indicate that elevated seawater temperatures cause an increase inzooplankton grazing compared with colder temperatures. Similarly, a recent comparative zoo-plankton synthesis study in the Chukchi Sea by Matsuno et al. (2011) evaluated zooplankton pop-ulations between the 1991–1992 period (high sea ice coverage) and the 2007–2008 period (low seaice coverage). Although zooplankton species composition was similar between the two decades,zooplankton abundance and biomass were higher in the 2007–2008 period than in the 1990s, likelyowing to the reduced sea ice conditions in the 2000s. This positive effect on zooplankton popula-tions as sea ice extent is reduced suggests that continued sea ice retreat will enhance the invasionnorthward of larger Pacific water species because these species growth rates are directly influencedby warming seawater. However, when sea ice returns in midfall, it is unlikely that these speciescan overwinter in the ice-covered seas. In addition, the seasonality of zooplankton populations—especially the timing of population increases and decreases in the region—will directly influenceexport production of organic carbon to the underlying benthos. Also, the appearance of morerapidly growing southern species is likely to have a negative impact on Arctic zooplankton speciescharacteristic of the Chukchi Sea; thus, the potential to switch from a benthic to pelagic-dominatedsystem is intimately tied to the seasonality of zooplankton community development.

Export Production: Decadal Sediment Oxygen Uptake as Carbon Supply

Recent studies of zooplankton in the Chukchi and Beaufort Seas indicate that they are not foodlimited and that only a small proportion of the total primary production is consumed by themesozooplankton and microzooplankton combined during both spring and summer (Campbellet al. 2009). These results support the regional high export production settling to the benthosand maintaining the high underlying benthic populations (Dunton et al. 2005, Grebmeier et al.2006a). Portions of the southeast Chukchi Sea and the northern Chukchi Sea around BarrowCanyon are known for high primary production (Hill & Cota 2005), and low grazing pressure inthe water column provides a high food base for underlying benthic communities; this is also thecase in the northern Bering Sea south of the Bering Strait (Grebmeier & Barry 2007).

Sediment community oxygen consumption can provide an overall indicator of carbon sup-ply to the benthos (Cooper et al. 2002, 2009; citations in Grebmeier et al. 2006a). Decadalmeasurements indicate spatially explicit areas of high pelagic-benthic coupling between seasonalwater column carbon-production processes and underlying benthic carbon-transformation pro-cesses, either through sediment oxygen uptake (Figure 3) or benthic infaunal biomass (Figure 4),both of which provide footprints in the sediments of persistent ecosystem events (updated fromGrebmeier et al. 2006a). As stated above, the limited impact of zooplankton grazing overall in thisregion results in a benthic-dominated system that supports large populations of seabirds and marinemammals (Lovvorn et al. 2009; Moore 2008, 2010). However, a recent decline in primary produc-tion in the northern Bering Sea in 2007 compared with the 1980s (Lee et al. 2011) coincides withapparent declining carbon supply to the underlying sediments (Grebmeier et al. 2006b) as well as adramatic shift in benthic biomass and community composition in the region (see sidebar, ClimateImpacts on Biological Response in the Northern Bering Sea, updated from Grebmeier et al. 2006b).

Benthic Infaunal Biomass and Population Structure

Bivalves, amphipods, polychaetes, and sipunculids dominate infaunal community structure in thePacific sector, and their biomass acts as an integrator of export carbon reaching the underlying


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a 1984–1988

c 2000–2010b 1990–1999

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Predicted sedimentcommunity oxygen consumption

(mmol O2 m–2 per day)

28–32

32–36

36–53

24–28

20–24

16–20

12–168–12

4–80–4

0 200 400

Nautical miles

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Figure 3Decadal distribution of sediment community oxygen consumption—an indicator of carbon supply to the benthos—in the Pacific Arcticregion measured using shipboard sediment incubation experiments. Black dots identify the station locations. Modified from datapresented and referenced in Grebmeier et al. 2006a, including unpublished data through 2010. Data available from citations inGrebmeier et al. 2006a, with many benthic data sets available at the following data archives under the benthic section: http://www.eol.ucar.edu/projects/sbi (phase I, Dunton, Grebmeier & Maidment component; and phase II, Grebmeier & Cooper component)and http://www.eol.ucar.edu/projects/best (Grebmeier & Cooper component).

sediments (Feder et al. 2005, 2007; Grebmeier 2006a). When evaluating the available data on adecadal basis, we see large-scale patterns. The highest benthic biomass is maintained in portionsof the Gulf of Anadyr and southwest of St. Lawrence Island, in the central region of the ChirikovBasin north of St. Lawrence Island, in the southern Chukchi Sea, and at the head of BarrowCanyon (Figure 4). The high-biomass regions in the Gulf of Anadyr and southern ChukchiSea are dominated by bivalves: Tellinidae (Macoma calcarea), Nuculanidae (Nuculana radiata),and Nuculidae (Ennucula tenuis) (Figure 7), all of which are common food of the Pacific walrus(Odobenus rosmarus; Sheffield & Grebmeier 2009) and spectacled eider (Somateria fischeri; Lovvornet al. 2009). The central Chirikov Basin just south of the Bering Strait is dominated by amphipods:Ampeliscidae (Ampelisca macrocephala and other Ampelisca spp., which are common food of the

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c 1990–1999 d 2000–2010

a 1970–1974 b 1984–1988

0 200 400

Nautical miles

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Predicted benthic biomass (g C m–2)

70–150

40–70

30–40

20–30

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Figure 4Decadal distribution of total station infaunal benthic biomass in the Pacific Arctic region measured using a 0.1-m2 van Veen grab. Blackdots identify the station locations. Modified from data presented and referenced in Grebmeier et al. 2006a, including unpublished datathrough 2010. Data available from citations in Grebmeier et al. 2006a, with many benthic data sets available at the following dataarchives under the benthic section: http://www.eol.ucar.edu/projects/sbi (phase I, Dunton, Grebmeier & Maidment component; andphase II, Grebmeier & Cooper component) and http://www.eol.ucar.edu/projects/best (Grebmeier & Cooper component).

California gray whale, Eschrichtius robustus), with some areas near the coast dominated by bivalves(Tellinidae and Nuculanidae).

A variety of other benthic fauna inhabit sediments underlying more coastal waters surroundingthe central high-biomass regions in both the Chirikov and southern Chukchi regions (Figure 7).These fauna include sand dollars (Echinarachniidae), polychaetes (Nephtyidae and Maldanidae),


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CLIMATE IMPACTS ON BIOLOGICAL RESPONSE IN THE NORTHERN BERING SEA

Threatened spectacled eiders (Figure 5) overwinter in the open areas of sea ice south of St. Lawrence Island in thenorthern Bering Sea and feed on productive bivalve populations in the region. In this shallow shelf water system,these diving sea ducks consume three species of bivalves (family Tellinidae, Macoma calcarea; family Nuculanidae,Nuculana radiata; and family Nuculidae, Ennucula tenuis) that all have high cascade potential and transfer efficienciesto higher trophic organisms (Grebmeier & Barry 2007). In addition, recent evidence of seasonal ocean acidificationin cold bottom water (Fabry et al. 2009, Mathis et al. 2011) indicates the potential for seasonally low-pH shelf waterto dissolve bivalve shells in this region. An important characteristic of this ecosystem is the development (extent andduration) of a cold pool (<0◦C) resulting from winter ice formation, which is critical to benthic infauna because itlimits benthic fish and epibenthic predators. With recent seawater warming and variability in sea ice retreat, declinesin clam populations (Figure 6) coincident with dramatic declines in diving sea ducks have occurred (Lovvorn et al.2009). In addition, walrus—which are cosmopolitan and focus on hot spots of benthic prey—have been observedattacking spectacled eiders (Lovvorn et al. 2010), providing yet another stress to predator-prey interactions.

sea anemones (Anthozoa), and gastropods (Muricidae, Montacutidae, Trochidae, and Turridae).By comparison, bivalves (Tellinidae and Nuculanidae), sipunculids (Sipunculidae), amphipods(Ampeliscidae and Lysianassidae), isopods (Idoteidae), and polychaetes (Maldanidae and Nepthyi-dae) dominate benthic biomass in the northern Chukchi Sea. Notably, the highest benthic biomassoccurs at the head of Barrow Canyon, where bivalves (Mytilidae: Musculus sp.) and sipunculids(Sipunculidae: Golfingia sp.) are dominant by biomass owing to the large load of organic carbon

Figure 5Flock of spectacled eiders in the winter polynya south of St. Lawrence Island. Courtesy of Matthew Sexson.

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100

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*

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Figure 6Decline in the dominant nuculanid bivalve Nuculana radiata at five time-series sites in the northern BeringSea as part of the Distributed Biological Observatory initiative (Grebmeier et al. 2010). Although notstatistically significant, beginning in 2003 (dashed line) there is a general trend upward in biomass of thesmaller nuculid bivalve (Ennucula tenuis), which is not a preferred prey item for spectacled eiders.

that transits northward from the Chukchi Sea system, along with high spring primary productionin the region (Hill & Cota 2005, citations in Grebmeier et al. 2006a).

Research findings suggest that climate change will influence the standing stock of benthicspecies and that the transition zone between sub-Arctic and Arctic waters in the Pacific regionmay be moving northward in the Bering Sea (Grebmeier et al. 2006a,b; Bluhm et al. 2009). In theclassic ecosystem configuration, export production in the northern Bering Sea is dominated bythe direct, nearly ungrazed deposition of phytoplankton, which maintains the high productivityof the underlying benthic communities, which are in turn key prey for benthic feeding specialistssuch as diving sea ducks, bearded seals, walrus, and gray whales (Grebmeier & Barry 2007).

Time-series sites embedded in larger clustered communities (based on faunal composition andbiomass) in the northern Bering and Chukchi Seas indicate a latitudinal change, with the largestdecline to the south and north of St. Lawrence Island at the interface with the Arctic proper, northof the Bering Strait. For example, biological changes include a decrease in overall benthic biomassof the dominant bivalve fauna south of St. Lawrence Island (sidebar; Grebmeier & Dunton 2000,Lovvorn et al. 2003, Grebmeier et al. 2006b, Lovvorn et al. 2009) and of amphipods north ofthe island in the Chirikov Basin (Moore et al. 2003, Coyle et al. 2007). The declining extentof amphipod populations in the Chirikov Basin and the northern range extension of gray whalefeeding sites to as far north as Barrow, Alaska (Moore et al. 2003, Moore 2008), are among theindications that a larger spatial-scale ecosystem change is underway.

BIOLOGICAL RESPONSE: NORTHWARD ADVECTION, MIGRATIONS,AND BIODIVERSITY IMPACTS

These recent observations of seasonal ice reductions are also driving shifts in marine speciescomposition in other ways that signal large-scale ecosystem reorganization (Huntington & Moore2008). Potential biological impacts that require focused evaluation include (a) shifts in species


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Amphipoda

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Figure 7Decadal distribution of dominant benthic infaunal taxa by benthic biomass in the Pacific Arctic region measured using a 0.1-m2 vanVeen grab. Colored dots identify the dominant taxa at each station location: Amphipoda (magenta), Bivalvia (brown), Echinoidea( green), Polychaeta ( yellow), Sipunculidea ( purple), and others (blue). Modified from data presented and referenced in Grebmeier et al.2006a, including unpublished data through 2010. Data available from citations in Grebmeier et al. 2006a, with many benthic data setsavailable at the following data archives under the benthic section: http://www.eol.ucar.edu/projects/sbi (phase I, Dunton, Grebmeier& Maidment component; and phase II, Grebmeier & Cooper component) and http://www.eol.ucar.edu/projects/best (Grebmeier &Cooper component).

composition and abundance, (b) northward range expansions, and (c) changes in species growthrates and productivity at key trophic levels. Some examples of ecological change are an increasednorthward distributional shift of fish and invertebrates in the Bering Sea (Mueter & Litzow 2008),penetration of Pacific clams into the Chukchi Sea (Sirenko & Gagaev 2007), and movementof Pacific zooplankton into the Beaufort Sea (Nelson et al. 2009). As an example of ecosystem

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response, declines in dominant clam populations in the northern Bering Sea have been observedconcomitantly with dramatic declines in numbers of spectacled eiders, the threatened diving seaducks that consume the clams (Grebmeier et al. 2006b, Lovvorn et al. 2009). In addition to lessfood, higher energy losses due to increased open-water conditions are additional stress factors forthe eiders on their overwintering grounds (Lovvorn et al. 2009).

The advective inflow shelves of the Pacific and Atlantic sectors are key locations for the potentialtransport of sub-Arctic species into Arctic regions (Carmack & Wassmann 2006, Grebmeieret al. 2006b, Weslawski et al. 2011). Bluhm et al. (2009) suggest that water temperature is amain factor limiting the distribution of Pacific species to the north and that range expansion ofthese species into the Chukchi Sea could occur with continued warming. Warming seawater andnorthward extension of sub-Arctic species are likely to bring increased biological competition.These interactions could potentially lead to a decrease in the abundance of cold-water Arcticspecies that cannot adapt quickly to rising seawater temperatures (Bluhm et al. 2009, Weslawskiet al. 2011, Somero 2012), which will ultimately affect biodiversity (Bluhm et al. 2011).

Biological responses to climate forcing can occur at multiple levels in the marine food web:lower trophic plankton are intimately connected to atmospheric and seawater changes, which cancascade to successive levels in the food web and ecosystem in both predictable ways (e.g., changinggrowth rates and trophic interactions) and nonlinear ways (e.g., change in life history and predator-prey events; Wassmann et al. 2011). Biological and ecosystem change is being documented in thePacific Arctic sector, ranging from primary through secondary production to higher trophic levelsof fish, seabirds, and marine mammals. A shift in species size and composition at the lower trophiclevel can cascade quickly to impact higher trophic predators. For example, Li et al. (2009) havedocumented declines in phytoplankton cell size in the Canada Basin with increased stratification,seawater temperatures, and freshwater content. For a benthic example, a shift from larger Nuculanaradiata bivalves to smaller Ennucula tenuis bivalves has also occurred in the northern Bering Sea(Lovvorn et al. 2009; also see sidebar and Figure 6). Limited numbers of commercially fishedspecies historically seen in the southern Bering Sea (e.g., walleye pollock, Pacific cod, and Beringflounder) are now observed in the Beaufort Sea together, as are commercial-sized snow crabs(Rand & Logerwell 2010). In addition to the gray whale range extension discussed above, they arenow known to feed on both water column and benthic crustaceans, which may reflect a food webshift (Moore 2010). Walrus, which use sea ice as a resting platform between feeding bouts and aredependent on dense populations of benthic fauna as prey, have been seen more regularly and inunprecedented numbers on both U.S. and Russian beaches because sea ice now retreats entirelyoff the continental shelf in late summer (Fischbach et al. 2009, Jay et al. 2011). This has majorimplications for the long-term stability of walrus populations, because many shallow-water feedingareas on the vast continental shelf are well offshore, and so are only accessible while seasonal seaice is present. Likewise, polar bears have tended to move their denning habitats from sea ice toland (Fischbach et al. 2007), and observations of long-distance swims in open water and drowningmortality have increased (e.g., Monnett & Gleason 2006).

CONCLUSIONS

As seasonal sea ice continues to retreat and seawater warms, we can expect continued biologicalresponse at various scales that will ramify through the Arctic ecosystem. The combination of rangeexpansions and/or changes to community composition along with changes in the timing of lifehistory events provides indications of a Pacific Arctic/sub-Arctic ecosystem in transition.

Multiple efforts are being planned to track biological and ecosystem trends in a changingArctic environment, including the Circumpolar Biodiversity Monitoring Program (CBMP), an


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international effort of the Arctic Council that proposes an international network of ma-rine transect lines and process studies to track biodiversity status and trends throughout thefood web (Gill et al. 2011). Coincidently, international members of the Pacific Arctic Group(http://pag.arcticportal.org) have developed a Distributed Biological Observatory (DBO) oflatitudinally placed transect lines and stations in the Pacific sector of the Arctic to evaluate bio-geographic boundaries of Pacific versus Arctic species (Grebmeier et al. 2010; further informationat http://www.arctic.noaa.gov/dbo) that has cross-linked study lines with the planned CBMPeffort in the region. The DBO, initiated in 2010, was developed as a change-detection array com-posed of latitudinal transects and stations from the northern Bering Sea to the Barrow Arc that areoccupied by both national and international partners as part of multiple ship programs. The DBOconcept also incorporates standard environmental, chemical, and biological measurements (type,abundance, and biomass) of both water column and benthic prey coincident with observations ofmarine mammals and seabirds that consume these prey. Transects and stations are focused onhigh biological diversity, high biomass, and regions with high potential for change, with samplescollected seasonally owing to the shared ship opportunities (spring to fall). National and interna-tional coordination for time-series measurements as well as focused studies at key locations at thetransition between the sub-Arctic and Arctic will be essential to evaluate the status and trends ofthe drivers and responders influencing the shifting patterns of life in both the Pacific sector andits connectivity to the pan-Arctic regions.

SUMMARY POINTS

1. Sea ice type, duration, and extent are critical driving factors for biological processes andmarine ecosystem structure.

2. Any changes to the hydrography of the Arctic/sub-Arctic, by either warming seawatertemperatures or reduced sea ice extent, will have a major influence on the timing andspatial extent of primary and secondary production.

3. Climate warming can directly impact pelagic-benthic coupling and transformation pro-cesses in the sediments on the shallow shelves of the northern Bering and Chukchi Seas aswell as, ultimately, the productivity of benthic ecosystems that support diving sea ducksand marine mammals in the Pacific sector.

4. Biological studies at various scales are essential when evaluating ecosystem health andidentifying select sites for time-series sampling. Notably, these sites should be embeddedin periodic larger-spatial-scale process studies to understand ecosystem status and trends.

5. Potential biological impacts with climate change are shifts in species composition andabundance, northward range expansions, and changes in species growth rates and pro-ductivity at key trophic levels.

FUTURE ISSUES

1. Placement of time-series biophysical transect lines and mooring arrays at key regions inboth the Pacific and Atlantic sectors is essential to track biological response to physicalforcing factors in a changing Arctic/sub-Arctic connection.

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http://pag.arcticportal.org

http://www.arctic.noaa.gov/dbo


2. Advection is a key process influencing the transport of pelagic life stages of plankton andbenthic organisms from the sub-Arctic and Arctic through the Bering Strait. Current di-rection, temperature, and salinity measurements are important parameters to understandthis process.

3. Studies of growth rates of key organisms in changing temperature and salinity regimescoincident with inorganic carbon acquisition experiments are required to determine ratemeasurements for evaluating production, competition, and predation impacts.

4. Experimental studies on key water column and benthic species exposed to more acidicwaters under various scenarios of ocean acidification are needed.

5. Development of biophysical coupled models for select species—from phytoplanktonthrough benthos and higher trophic organisms—along with key process rate measure-ments are essential to evaluate ecosystem response to a rapidly changing Arctic.

6. With the ongoing seasonal sea ice decline, it is essential to include time-series observa-tions of lower- and higher-trophic-level prey and predator species as well as key biologicalprocesses in a comprehensive Arctic observing network that includes biological, chemical,and physical components.

DISCLOSURE STATEMENT

The author is not aware of any affiliations, memberships, funding, or financial holdings that mightbe perceived as affecting the objectivity of this review.

ACKNOWLEDGMENTS

Support for this synthesis effort and research has been provide by the U.S. National ScienceFoundation, National Oceanic and Atmospheric Administration, Fish and Wildlife Service, NorthPacific Research Board, and Bureau of Ocean Management, Regulation, and Enforcement, andby the Shell Exploration and Production Company.

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Impacts of Climate Change on the Ecosystems and Chemistry of the Arctic Pacific Environment(ICESCAPE): http://www.espo.nasa.gov/icescape

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MA04-FrontMatter ARI 16 November 2011 9:36

Annual Review ofMarine Science

Volume 4, 2012 Contents

A Conversation with Karl K. TurekianKarl K. Turekian and J. Kirk Cochran � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 1

Climate Change Impacts on Marine EcosystemsScott C. Doney, Mary Ruckelshaus, J. Emmett Duffy, James P. Barry, Francis Chan,

Chad A. English, Heather M. Galindo, Jacqueline M. Grebmeier, Anne B. Hollowed,Nancy Knowlton, Jeffrey Polovina, Nancy N. Rabalais, William J. Sydeman,and Lynne D. Talley � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �11

The Physiology of Global Change: Linking Patterns to MechanismsGeorge N. Somero � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �39

Shifting Patterns of Life in the Pacific Arctic and Sub-Arctic SeasJacqueline M. Grebmeier � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �63

Understanding Continental Margin Biodiversity: A New ImperativeLisa A. Levin and Myriam Sibuet � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �79

Nutrient Ratios as a Tracer and Driver of Ocean BiogeochemistryCurtis Deutsch and Thomas Weber � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 113

Progress in Understanding Harmful Algal Blooms: Paradigm Shiftsand New Technologies for Research, Monitoring, and ManagementDonald M. Anderson, Allan D. Cembella, and Gustaaf M. Hallegraeff � � � � � � � � � � � � � � � � 143

Thin Phytoplankton Layers: Characteristics, Mechanisms,and ConsequencesWilliam M. Durham and Roman Stocker � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 177

Jellyfish and Ctenophore Blooms Coincide with Human Proliferationsand Environmental PerturbationsJennifer E. Purcell � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 209

Benthic Foraminiferal Biogeography: Controls on Global DistributionPatterns in Deep-Water SettingsAndrew J. Gooday and Frans J. Jorissen � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 237

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MA04-FrontMatter ARI 16 November 2011 9:36

Plankton and Particle Size and Packaging: From Determining OpticalProperties to Driving the Biological PumpL. Stemmann and E. Boss � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 263

Overturning in the North AtlanticM. Susan Lozier � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 291

The Wind- and Wave-Driven Inner-Shelf CirculationSteven J. Lentz and Melanie R. Fewings � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 317

Serpentinite Mud Volcanism: Observations, Processes,and ImplicationsPatricia Fryer � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 345

Marine MicrogelsPedro Verdugo � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 375

The Fate of Terrestrial Organic Carbon in the Marine EnvironmentNeal E. Blair and Robert C. Aller � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 401

Marine Viruses: Truth or DareMya Breitbart � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 425

The Rare Bacterial BiosphereCarlos Pedros-Alio � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 449

Marine Protistan DiversityDavid A. Caron, Peter D. Countway, Adriane C. Jones, Diane Y. Kim,

and Astrid Schnetzer � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 467

Marine Fungi: Their Ecology and Molecular DiversityThomas A. Richards, Meredith D.M. Jones, Guy Leonard, and David Bass � � � � � � � � � � � � 495

Genomic Insights into Bacterial DMSP TransformationsMary Ann Moran, Chris R. Reisch, Ronald P. Kiene, and William B. Whitman � � � � � � 523

Errata

An online log of corrections to Annual Review of Marine Science articles may be found athttp://marine.annualreviews.org/errata.shtml

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Documents

Shifting Patterns of Life in the Pacific Arctic and Sub-Arctic Seas