Deep-Sea Research II 94 (2013) 2–6
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Introduction
An introduction to the Bering Sea Project: Volume II
1. Introduction As one of the most productive marine ecosystems in the world, the Bering Sea is a region particularly sensitive to climate. Seasonal ice cover acts as a major organizing driver, and in winter, geology, latitude, and circulation combine to produce ice cover extending south an estimated 1700 km, that is unmatched elsewhere in the northern hemisphere. In the spring and summer seasons, the retreating ice, longer daylight hours, and nutrient-rich ocean waters forced onto the shallow continental shelf result in intense marine productivity, sustaining nearly half of the U.S. annual commercial fish landings and providing food and cultural value to thousands of coastal and island residents. The predicted major changes in ice cover in the coming decades (Overland et al., 2012) have intensified concern over the future of this economically and culturally important region. In response to these ongoing observations of a changing region, the North Pacific Research Board (NPRB) and the National Science Foundation (NSF) created an important partnership to support the study of how climate change affects the Bering Sea ecosystem from lower trophic level organisms (e.g. plankton) to humans. The “Bering Sea Project” integrates two research programs, the NSF Bering Ecosystem Study (BEST) and the NPRB Bering Sea Integrated Ecosystem Research Program (BSIERP), with substantial inkind contributions from National Oceanic and Atmospheric Administration and the U.S. Fish and Wildlife Service. The program spans the Eastern Bering Sea shelf and slope from the Alaska Peninsula to the border of the U.S. Economic Exclusive Zone with Russia. Over the 6 year program and its ongoing synthesis, the Bering Sea Project has provided new insights into the functioning of the eastern Bering Sea ecosystem, particularly in the northern domain where data sets and temporal coverage have been sparse. The first special volume of DSRII which presented the results of the Bering Sea program included twenty four papers that described new information on this ecosystem, placed new results in their historical context, and assessed their implications for the future of Bering Sea ecosystem as a whole. It coalesced a rich series of new information that explored the ecosystem and the complex linkages of trophic interactions and functions. Each of these papers addressed one or more of the core program hypotheses which guided the field program and ongoing synthesis activities. These hypotheses include (1) physical forcing and its modification by climate affects food availability; (2) ocean conditions structure trophic relationships through bottom–up processes; (3) ecosystem controls are dynamic; (4) location matters; and (5) commercial and subsistence fisheries reflect climate. The papers in the first issue were largely results gained from individual investigator or 0967-0645/$ - see front matter & 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.dsr2.2013.04.023
small study teams, testing these hypotheses and extending their analyses to consider the observed variability that typifies this dynamic system. The papers in this second issue of Deep Sea Research II continue to present new information gained from various projects and data sets, but also extend to include several synthetic results. This issue is organized to reflect these hypotheses, and many papers include comparative results across seasons and domains. This issue also incorporates several papers from parallel studies conducted through related programs in the region including the Ecosystem Studies of Sub-Arctic Seas (ESSAS) Program, which addresses the need to understand how climate change will affect the marine ecosystems of the sub-arctic seas and their sustainability. Finally, we note the ongoing efforts to recognize the complex heterogeneity of the Eastern Bering Sea system and need for tools to support spatially explicit modeling.
2. Physics structure trophic relationships These first two hypotheses of the Bering Sea Program reflect the role of physical environment on ecosystem structure and the complex response of all trophic levels driven by spatial and temporal changes in primary production. A climate-induced change in physical forcing was hypothesized to modify the availability and partitioning of food for all trophic levels through bottom–up processes. Primary production is the dominant source of organic matter on the Eastern Bering shelf as with other productive shelf systems. While a portion of this primary production is consumed in the water column, the rapid onset of primary production experienced in the Eastern Bering Sea in spring and its export to the shallow sediments which underlie much of the region is a hallmark of the system. Using 234Th measures in the water column and sediments. Baumann et al. (2013), examined the export and retention of particles and sediments over a wide range of locations in the eastern Bering Sea. They observed elevated amounts of 234Th in sediments which they attributed to the rapid removal of material following blooms and associated particles in the marginal ice zone during the spring sea-ice retreat. They also found that particles appear to be largely retained on the shelf with little transport to deeper slope/oceanic regions, in contrast to previous models. While much of this material is detrital, some fraction of this vertical export appears to include living material as discussed by Tsukazaki et al. (2013), who showed evidence for the widespread appearance of viable diatom resting cells in bottom sediments across the region. The importance of phytoplankton derived material to the benthos was also documented by Cooper et al. (2013) in early season sampling in the region of St. Lawrence Island. They
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observed low water column chlorophyll values prior to the onset of the spring bloom, but significant sedimentation of chlorophyll containing material. The remineralization of detrital material in sediments showed significant regeneration of ammonium and its release to the water column. They concluded that organic matter recycling is closely linked to areas of increased benthic biomass which in turn leads to preferred areas for feeding by apex diving predators such as the speckled eider. In the Bering Sea large crustacean zooplankters are an important component of the ecosystem and considered an essential element of the trophic link between primary production and fisheries resources. The response of macrozooplankton to climate, however, remains uncertain and led Ohashi and coauthors to use summer samples collected from 1994 through 2009 to examine community structure and composition (Ohashi et al., 2013). Copepod abundance varied dramatically over the period as did biomass, with higher abundance and biomass seen in cold years. These changes were due to alterations of the copepod community between the warm and cold periods. Strong links to primary production and its timing appear to be an important control which in turn has implications for recruitment of fish, such as walleye pollock. Zooplankton grazing on the phytoplankton community, however is not limited to larger macrozooplankton as shown by Sherr et al. (2013) who found significant rates of microzooplankton herbivory in spring with large heterotrophic dinoflagellates and ciliates as the primary consumers of phytoplankton. Microzooplankton grazing was significant in both nonbloom and bloom conditions, and could account for a substantial fraction of phytoplankton growth. These experiments and others point out that multiple consumers may regulate phytoplankton stocks in these polar waters, with microzooplankton playing a significant role in the recycling of materials prior to sediment incorporation. While rapid oscillations in ocean surface conditions have been seen in the eastern Bering Sea over the last 30 years (1st DSRII volume), the impact on benthic processes has not been studied in detail. Gemery et al. (2013) analyzed long-term benthic ostracod assemblages from the northern Bering and the Chukchi Seas, to examine species distributions and the impact of climatic and oceanographic changes. They found evidence that decadal-scale environmental changes were reflected in population distributions which impacted both northern and transitional species. These results suggest that both pelagic and benthic assemblages have been impacted by climatic shifts seen in the region. Esch et al. (2013) investigated broader questions of carbon remineralization in sediments, in particular the role of iron and manganese reduction in sediments and the impact of benthic bioturbation. Their results indicate that Fe oxide reduction is a significant pathway for carbon remineralization in the northern and middle-shelf regions, where organic matter deposition rates and benthic biomass are high. The iron was also implicated as a possible source of bioavailable iron for phytoplankton. In contrast Mn oxide reduction was of minor significance, accounting for no more than 5% of total carbon oxidation in any of the regions. In addition to carbon, sedimentary nitrogen cycling on the shelf was examined by Horak et al., (2013), who quantified benthic fluxes of N2 and dissolved inorganic nitrogen (DIN), together with the extent of coupled nitrification/denitrification. They observed widespread sedimentary denitrification over the shelf which was fueled mostly through coupled nitrification/denitrification. Rates suggested that total nitrogen loss from the Bering Sea shelf was significantly larger than previously estimated. Sediments were not a significant source of remineralized nitrogen returned for primary production over the shelf, further reducing available nitrogen over the ecosystem. While the Bering Sea Project has a strong focus over the eastern Bering shelf, Khen and colleagues expanded the examination to a
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multi-decadal summary of environmental variables observed across the western Bering Sea (Khen et al., 2013). They observed large-scale similarities between the two regions, but also noted differences to the eastern Bering region. Water exchange was seen to be more variable than expected with a slight weakening of vertical exchange over recent years and increased phosphate concentrations. Several of these changes appeared associated with climatic trends and were accompanied by shifts in the fish assemblage. An important component of the overall program is the use of multiscale modeling to integrate observations and link lower trophic processes with fisheries and humans. Those synthesis efforts are underway and the paper by Hermann and colleagues (Hermann et al., 2013) used a multivariate statistical approach to explore the bottom–up and top–down effects of climate change on the spatial structure of the region. Empirical Orthogonal Function analysis was used to extract the emergent properties of a coupled physical/biological hindcast of the Bering Sea for the 36 year period of 1970–2009, which includes multiple episodes of warming and cooling. The model was used to replicate environmental conditions and explore the relationships of temperature and large crustacean zooplankton on the southeastern Bering Sea shelf. Model results were able to replicate the observed relationships among temperature and salinity, as well as the observed inverse correlation between temperature and large crustacean zooplankton on the southeastern Bering Sea shelf.
3. Bottom–up and top–down control The Oscillating Control Hypothesis states that later spring phytoplankton blooms as a result of early ice retreat will increase zooplankton production, thereby resulting in increased abundances of juvenile piscivorous fish (pollock, cod and arrowtooth flounder). The recruitment success of these juvenile fish is initially high, until the point when the adult fish inflict heavy prerecruitment mortality on the larval and juvenile stages and the community is controlled by top–down processes. The third Bering Sea Project hypothesis addresses the influence of bottom–up and top–down control of the Bering Sea ecosystem. Later spring blooms were hypothesized to increase zooplankton abundance and, with successive warm years and delayed blooms, to lead to increased abundance of piscivorous species and switch from a community controlled by bottom–up production to a community controlled by top–down processes. The original premise that warm years would lead to higher recruitment rates and increased abundance of piscivorous species has been shown to be incorrect (Hunt et al., 2011; Coyle et al., 2011), and Bering Sea Project research provided the understanding of why this was the case. Two papers in this volume examine how young pollock accumulate energy reserves and how young pollock must be fat before their first winter for good survival to occur. Siddon et al. devised a conceptual model of energy allocation in walleye pollock from larvae to age-1. Energy densities remained relatively low during the larval phase in spring, consistent with energy allocation to somatic growth and development. Lipid acquisition rates increased rapidly after transformation to the juvenile form with energy allocation to lipid storage leading to higher energy densities in late summer. Siddon et al. (2013) proposed that the time after the end of larval development and before the onset of winter represents a short, critical period for energy storage in age-0 walleye pollock, and that overwinter survival depends on accumulating sufficient stores the previous growing season and consequently may be an important determinant of recruitment success. Heintz et al. (2013) considered the relationship between the condition of young-of-the-year (YOY) pollock in fall and their
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survival to age-1 by characterizing their energy density by season and also the nutritional composition of their prey. They concluded that recruitment to age-1 can be predicted by the condition of YOY pollock prior to their first winter, and that survival is favored by cold conditions in the eastern Bering Sea. The abundance of arrowtooth flounder, a piscivorous flatfish, has been increasing in the Bering Sea, and the third Bering Sea Project hypothesis identified the competitive effect of their increase to negatively affect abundance of their prey and other piscivorous species in the Bering Sea. Wilderbuer et al. (2013) examined whether climate variability and density-dependence affect recruitment of arrowtooth flounder as well as northern rock sole and flathead sole. For arrowtooth flounder, they found that the Arctic Oscillation was an important indicator of arrowtooth flounder productivity, but were not able to identify a more specific physical factor. In contrast, they found that wind-forced, on-shelf transport during spring led to advection of northern rock sole and flathead sole larvae to favorable nursery grounds and coincided with years of good recruitment. They also forecast the future impacts of climate on northern rock sole productivity which gave an unexpected result. IPCC (Intergovernmental Panel on Climate Change) future springtime wind scenarios were used to model the impact of climate change on northern rock sole productivity. Model results indicated that a moderate increase in recruitment might be expected because the current climate change projections favor on-shelf transport. Density-dependence effects were predicted to dampen this increase such that northern rock sole abundance will not be substantially affected by climate change. This demonstrates the importance of considering both physical and biological processes in climate change predictions. Agler et al. (2013) also examined the relationships of climate indices and physical factors on other commercially important species in the Bering Sea. While not a Bering Sea Project focal species, chum salmon are an important subsistence and commercial fishery species in western Alaska. Agler et al. (2013) found that both sea temperature and climate indices were related to chum growth which also was affected by high Asian chum salmon abundance and high Russian pink salmon abundance.
4. Location matters This hypothesis proposes that climate and ocean conditions which influence circulation patterns and domain boundaries will affect the distribution, frequency and persistence of fronts and other preyconcentrating features, and thus the foraging success of marine birds and mammals largely through bottom–up processes. The concern is that climate–ocean changes will displace predictably located, abundant prey necessary for successful foraging by central place foragers such as seabirds and fur seals while nurturing young as well as hot spot foragers dependent on concentrated prey such as baleen whales and walrus. As a result, these central place foragers will shift their diet, foraging locations or rookery locations to optimize foraging opportunities based on differential foraging success. Harding et al. (2013) examined the foraging strategies of thick-billed murres at three colonies. They hypothesized that close proximity of the breeding colony to productive oceanographic features is beneficial for seabird reproduction. Instead, murres in this study exhibited a remarkable degree of plasticity in foraging strategy among nearby breeding colonies, and high breeding performance regardless of colony proximity to productive oceanographic features. In the context of hypothesis four, this result indicates that breeding murres are resilient to a wide range of foraging conditions. Vincenzi and Mangel (2013) modeled the effect of climate-induced changes in the physical environment on another central place forager, the black-legged kittiwake. They examined reproductive tradeoffs these seabirds may
make in the face of variation in environment and energy resources. In their model, they found that tradeoffs in growth rate and nesting duration can be made that compensate for climate variation and thus maintain their potential productivity, at least on the individual level of productivity. Both papers, one using direct evidence and one using modeled scenarios, support the conclusion that these seabird species can adjust their breeding and foraging strategies to compensate for poor foraging conditions and maintain productivity. The next four papers together address the distributions of fish, crab and whale species and how climate variation affects their distributions. Smart et al. (2013) examined vertical distributions of the early life stages of walleye pollock in the southeastern Bering Sea to assess ontogenetic and diel vertical migration in relation to development, area, and prey resources. Eggs occurred deepest in the water column and early juveniles occurred shallowest. Their results suggest that vertical distributions and diel migration potentially are driven by prey availability at sufficient light levels for preflexion larvae to feed and a trade-off between prey access and predation risk for late larvae. Parker-Stetter et al. (2013) assessed forage fish density distributions in late-summer 2006 to 2010 including age-0 pollock, age-0 cod, and capelin. Pollock and cod were most abundant. Age-0 pollock vertical distributional changes occurred between 2006–2007 and 2009–2010. Previous to this assessment, high midwater densities of age-0 pollock had not been observed. These may be related to the increasingly colder water temperatures that occurred during the latter period. Kotwicki and Lauth (2013) used a 30-year time series of bottom fish and crab shelf surveys to examine the effects of the cold pool and population density on spatial distributions. Results clearly show that the size of the cold pool partly drives the short-term interannual variability in patterns of spatial distribution. Despite inclusion of data from the extended cold period lasting from 2006–2010, populations that previously responded with a northward shift during warm periods did not retract during the recent cold period. There continued to be a broad-scale community-wide temporal northward shift over the 30-year time series. Friday et al. (2013) conducted cetacean surveys to describe distribution and estimate abundance on the eastern Bering Sea shelf. Estimates for the Bering Sea Project focal whale species, humpback and fin whales, increased from 2002 to 2010, but it is likely that changes in estimated abundance are due at least in part to shifts in distribution and not just changes in overall population size. Humpback whales were consistently concentrated in coastal waters north of Unimak Pass whereas fin whales were broadly distributed in the outer domain in 2008 and 2010, but sightings were sparse in 2002. The last paper in this section connects fur seals to oceanography by determining how well oceanographic data collected by free-ranging animals compared to those from traditional shipboard vertical sampling. Nordstrom et al. (2013) found similar patterns in the temperature fields produced by ships and instrumented seals despite the differences in sampling frequency and distribution. However, the fur seal dataset was of higher temporal and spatial resolution and could therefore be used to visualize finer detail with less estimated error than ship-derived data, particularly in dynamic areas. Fur seals also collected 4700 additional profiles post-cruise which documented a ≥1 1C warming of the upper 100 m through mid-September, including regions where ship sampling has traditionally been sparse.
5. Commercial and subsistence fisheries, LTK The fifth Bering Sea Project hypothesis addresses the effect of climate change on commercial and subsistence fisheries and the communities that depend on them. The related papers in this
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volume focus on subsistence harvests and Bering Sea coastal communities. Fall et al. (2013) examined harvest surveys spaced approximately twenty years apart including recent surveys during 2008–2010. These surveys documented relatively high and diverse subsistence harvests, consistent with earlier research that demonstrated the continuing economic, social, and cultural importance of subsistence uses of wild resources. So far, as in the past, families and communities have adapted to changing economic, social, and environmental conditions, but the future is less clear if such changes intensify or accelerate. Subsistence harvests typically are depicted in terms of subsistence use areas: the places where harvests and associated travel occur. The first of three papers by Huntington et al. (2013) took another way to consider this interaction by examining seasonal subsistence use areas, lifetime subsistence use areas, and “calorie-sheds,” or the area over which harvested species range. Each perspective offers useful information concerning not only the nature of human-environment interactions, but also the scope for potential conflict with other human activity and the means by which such conflicts could be reduced, avoided, or otherwise addressed. Fienup-Riordan et al. (2013) focused on the coastal community of Emmonak, Alaska and placed the subsistence survey and interview data (like that collected by Fall et al. (2013) in 2013) into an ethnographic and historical context. Taking examples from salmon fishing, seal harvesting, and local understandings of place, they argue that a comprehensive ethnographic approach, including both local and traditional knowledge and cultural history, is essential in understanding contemporary Bering Sea coastal communities. An ethnographic approach could also describe the linkage between people and the Bering Sea, which underlines an overall goal of the Bering Sea Project, to understand the interconnectedness in the system, including humans. The second paper by Huntington et al. (2013) focused on a pair of coastal communities, trying to understand environmental influences on walrus hunting success, combining community and scientific knowledge to tackle this question. Information from
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hunters, harvest monitors, and previous studies suggested that ice concentration and wind were among the environmental factors influencing harvest levels. For the period 1996–2009, they used ice concentrations based on satellite data, wind speed and direction based on a high-resolution atmospheric reanalysis to specify physical conditions each day during spring, and daily walrus harvests provided by U.S. Fish and Wildlife Service records for the villages of Gambell and Savoonga, Alaska on St. Lawrence Island and found that that other factors (e.g., fog, fuel prices, socioeconomic conditions) collectively cause a greater share of variability than ice and wind. Nonetheless, the findings suggest that environmental change is also likely to influence future harvest levels, and that climate models which yield appropriately scaled data on ice and wind around the island may be of use in determining the magnitude and direction of those influences. The final paper by Huntington et al. (2013) surveyed elders, hunters, and fishers from five coastal communities along the eastern Bering Sea to learn what if any changes they observed in this ecosystem. The observations described a complex and dynamic ecosystem with many more responses of change in the south, than the north.
6. Beyond the hypotheses; managing the heterogeneity of the Eastern Bering Sea One challenge of this large research program is the breadth of its geographic scope and the need for consistent and coherent ways of comparing data sets. This is particularly important for a large, heterogeneous area like the eastern Bering Sea shelf. A panel led by Ivonne Ortiz developed a tool for use by Bering Sea Project scientists, which is described in a dataset available in the Bering Sea Project Data Archive (Ortiz et al., 2012). This tool divides the eastern Bering Sea into a spatially explicit set of marine regions with specific boundaries (see Fig. 1). For example, the freshwater influenced, well-mixed, inner domain was separated from the
Fig. 1. Map illustrating the 16 marine regions based on observed physical, environmental, and biotic variables seen across the Eastern Bering Sea Project area. A detailed description of the process used to delineate these areas by consensus panel recommendation is described by Ortiz et al. (2012).
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two-layered (during summer) middle domain. The development of the tool was initiated by the Bering Sea Project modeling group, whose goal was to develop a consensus approach of spatial scales which could be used to compare model predictions to observations. It should be emphasized that the regions were defined strictly in a qualitative way through discussion and general consensus of Bering Sea Project scientists. Although, based on the experience and information available to panelists, it should be considered only a solid starting point for further exploration for Bering Sea system and the models being developed.
Acknowledgments This second issue and broader program has greatly benefited from the contributions of the additional members of the scientific advisory board of the Bering Sea Program (Carin Ashjian, Mike Lomas, Jeffrey Napp and Phyllis Stabeno) and editor Tom Van Pelt, who also provided thoughtful reviews to this introduction. This is best BEST-BSIERP Bering Sea Project publication number 101 and NPRB publication number 424.
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H. Rodger Harvey n Department of Ocean, Earth and Atmospheric Sciences, Old Dominion University, Norfolk, VA 23529, USA E-mail address:
[email protected]
Michael F. Sigler Alaska Fisheries Science Center, National Oceanic and Atmospheric Administration, 17109 Point Lena Loop Road, Juneau, AK 99801, USA E-mail address:
[email protected]
Available online 29 April 2013
n
Corresponding author.