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Comparison of Near-bottom Fish Densities Show Rapid Community and Population Shifts in Bering and Barents Seas

J. T. Thorson1, M. Fossheim2, F. J. Mueter3, E. Olsen4, R. R. Lauth1, R. Primicerio5, B. Husson2, J. Marsh3, A. Dolgov6,7,8, and S. G. Zador1

1Alaska Fisheries Science Center, NOAA, Seattle, WA, USA
2Institute of Marine Research, Tromsø, Norway
3College of Fisheries and Ocean Sciences, University of Alaska Fairbanks, Juneau, AK, USA
4Institute of Marine Research, Bergen, Norway
5University of Tromsø, Tromsø, Norway
6Polar Branch of the Federal State Budget Scientific Institution "Russian Federal Research Institute of Fisheries and Oceanography" (PINRO), Murmansk, Russia
7Federal State Educational Institution of Higher Education "Murmansk State Technical University" (FSEI HE MSTU), Murmansk, Russia
8Tomsk State University, Tomsk, Russia

Highlights

  • The northern edge of distribution for fishes associated with the Bering Sea shelf (e.g., walleye pollock and Pacific cod) shifted northward from 2010 to 2017/18.
  • The spatial distribution of boreal fishes in the Barents Sea in 2017 resembles their distribution in 2012, showing a northward shift relative to their previous distribution in 2004.
  • In both Bering and Barents Seas, recent shifts are associated with changes in bottom water temperature and loss of sea ice.
  • Density estimates for individual species show that responses vary among species, and boreal species can maintain high densities in southern habitats even during shifts in the northward edge of distribution.

Introduction

Marine populations are expected to remain within their preferred thermal conditions, and therefore to shift their spatial distributions to track changes in ocean temperatures (Pinsky et al. 2013). Many different indicators show changes in Arctic physical conditions, with an increased rate of change from 2005 to present day (Overland et al. 2019). Given these rapid physical changes and expected responses of marine populations to changing thermal conditions, the spatial distribution of Arctic and subarctic fish communities will likely be a sensitive indicator for contemporary and ongoing Arctic climate change.

Here we present changes in the fish communities of the Bering and Barents Seas during 2017/18 relative to baseline conditions 10-15 years earlier. This involves mapping shifts in the spatial distribution of boreal (southern) and Arctic (northern) fish communities in each ecosystem, as well as identifying indicator species associated with each community. The Bering Sea has shown substantial and rapidly warming ocean temperatures and associated decreases in the thickness and extent of sea ice from 1982 to 2019, with pronounced changes occurring since 2014, while the sea surface temperature trends in the Barents Sea are varied both spatially and seasonally (see essay Sea Surface Temperature). Fish populations in both the Bering and Barents Seas are expected to expand into new areas in a warming climate if certain pre-conditions are met, including suitable bottom topography, water temperatures, salinities and distance to spawning grounds (Hollowed et al. 2013). The patterns and rates of documented shifts are species-specific and tend to follow temperature gradients (Pinsky et al. 2013), although observed shifts have trailed behind and are sometimes poorly correlated with the actual rates of climate shifts (Alabia et al. 2018).

Bering Sea community shifts

On the shallow Bering Sea shelf, the summer distribution of fishes and invertebrates living near the sea floor (i.e., demersal fishes) is tied to the extent of the cold pool (bottom temperatures < 2°C) as determined by the southern extent of sea ice during the preceding winter (Mueter and Litzow 2008). Until recently, there was a general expectation that sea ice would continue to persist throughout the winter over the shallow northern Bering Sea and Chukchi Sea shelf, limiting the northward expansion of boreal species (Stabeno et al. 2012). However, latent heat from the warm conditions of summer 2016, combined with less sea-ice formation in the 2017 winter, resulted in an extensive but narrow cold pool on the eastern Bering Sea shelf during summer 2017 (see essay Recent Warming in the Bering Sea). This created a wide corridor within the shallow continental shelf for species to move northward, as observed with dramatic increases of Pacific cod, Gadus macrocephalus, walleye pollock, G. chalcogrammus and several flatfish species into the northern Bering Sea (Stevenson and Lauth 2019). A delayed freeze-up in the Chukchi Sea and unusual southerly winds resulted in near-complete lack of sea ice in the northern Bering Sea the following winter, in 2018. Maximum sea-ice extent subsequently reached the lowest levels on record in 2019 (see essay Recent Warming in the Bering Sea).

We identify shifts in distribution for four assemblages in the eastern and northern Bering Sea (Fig. 1), and also identify indicator species that are associated with each assemblage (Table 1). Boreal groundfish were observed again in the northern Bering Sea during the 2018 summer (Duffy-Anderson et al. 2019; Stabeno et al. 2019). Although shifts in these large, abundant species are more apparent, Arctic taxa tend to be more sensitive to habitat changes. Arctic cod (Boregadus saida) in particular can serve as a sentinel species that responds quickly to changes in temperature and ice extent (Alabia et al. 2018; Marsh and Mueter 2019). Changes in individual species result in community-level changes (Fig. 1) that reflect a transition from a 'Northern Shelf' (Arctic) community dominated by relatively few, smaller and less abundant species with Arctic affinities to a community dominated by larger boreal species. In particular, the Arctic and northern shelf community is represented by butterfly sculpin, Hemilepidotus papilio, and Bering flounder, Hippoglossoides robustus (see Table 1 for full list), and this community retreated northward from 2010 to 2018. This Arctic community was then replaced by the southern shelf community represented by northern rock sole, Lepidopsetta polyxystra, and sturgeon poacher, Podothecus accipenserinus (i.e., comparing the spatial distribution of light and dark blue in Fig. 1).

Map of major fish assemblages identified in the eastern Bering Sea
Fig. 1. Major fish assemblages identified in the eastern Bering Sea, including two boreal assemblages on the southern shelf (light blue) and in the outer shelf/slope region (green), as well as a mixed Norton Sound (light green) and an Arctic / northern shelf assemblage (dark blue). Contours denote -1°C (black) and 3°C (red) isotherms of bottom temperature. Assemblages are based on Ward's minimum variance clustering of pairwise Bray-Curtis distances among 1463 hauls sampled during summer trawl surveys. Bray-Curtis distances were computed from fourth-root transformed catch-per-unit-effort (kg/ha) of 44 common demersal fish and macroinvertebrate species.

Table 1. Indicator species associated with each of four fish communities in the Bering Sea; shifts in spatial distribution for these communities are mapped in Fig. 1. Species are shown that have a statistically significant association (p < 0.001) for each community, following methods in Dufrêne and Legendre (1997). Only species for which specificity exceeds 0.5 and group fidelity exceeds 0.2 are shown.
Community Species
  Scientific Name Common Name
Boreal: outer shelf / slope Atheresthes evermanni Kamchatka flounder
  Atheresthes stomias arrowtooth flounder
  Lycodes brevipes shortfin eelpout
  Hippoglossoides elassodon flathead sole
  Hemitripterus bolini bigmouth sculpin
  Icelus spiniger thorny sculpin
  Chionoecetes bairdi tanner crab
  Bathyraja interrupta sandpaper skate
  Glyptocephalus zachirus rex sole
  Reinhardtius hippoglossoides Greenland halibut/turbot
  Leptagonus frenatus sawback poacher
Boreal: southern shelf Lepidopsetta polyxystra Northern rock sole
  Podothecus accipenserinus sturgeon poacher
  Paralithodes camtschaticus red king crab
Norton Sound Eleginus gracilis saffron cod
  Myoxocephalus jaok plain sculpin
  Platichthys stellatus starry flounder
  Limanda proboscidea longhead dab
  Gymnocanthus pistilliger threaded sculpin
  Telmessus cheiragonus helmet crab
  Lumpenus fabricii slender eelblenny
Arctic: northern shelf Hemilepidotus papilio butterfly sculpin
  Liparis gibbus variegated snailfish
  Limanda sakhalinensis Sakhalin sole
  Hippoglossoides robustus Bering flounder
  Boreogadus saida Arctic cod
  Lycodes raridens marbled eelpout
  Myoxocephalus verrucosus warty eelpout

Barents Sea community shifts

In the Barents Sea, the warming ocean temperatures and retraction of the sea ice was concurrent with a northeastward displacement of Arctic fish (Fig. 2). This region includes three communities: Arctic (represented by Arctic cod, Boreogadus saida and bigeye sculpin, Triglops nybelini), boreal (represented by haddock, Melanogrammus aeglefinus and saithe, Pollachius virens) and a transition community (see Table 2 for full list of species associated with each community). The decreasing extent of Arctic water masses was associated with a northward shift in the transition zone separating Arctic and boreal fish communities from 2004 to 2012 (Fossheim et al. 2015a,b). During these years, the southern (boreal) fish community gradually expanded northward while the northern (Arctic) community retracted (Fossheim et al. 2015a,b). In 2017 the Arctic fish communities continued to have a displaced spatial distribution similar to 2012; there was neither a recovery to previous distributions (like 2004), nor a further displacement (beyond 2012). The boreal community includes large-bodied generalist feeders. These species took advantage of favorable conditions in the Barents Sea, both by increasing in abundance (demography) and by expanding their distribution (behavior). By contrast, many Arctic species are small-sized bottom-associated specialists and their spatial distribution has retracted to smaller areas in the northeast. We hypothesize that new areas for boreal species opened as Arctic waters warmed and primary and secondary production increased (see essay Arctic Ocean Primary Productivity). These changes likely favored the boreal generalists competitively over the arctic specialists. In some cases, the larger predatory species (i.e., boreal fish) might also exert feeding pressure on the smaller benthivore species (i.e., Arctic fish).

Map of major fish assemblages identified in the Barents Sea
Fig. 2. Major fish assemblages identified in the Barents Sea, showing a boreal (dark green), mixed (light green) and Arctic (blue) assemblage. Fish assemblage classification of 1199 hauls, sampled during summer trawl surveys, was based on log transformed catch-per-unit-effort data for 66 demersal fish taxa. The classification was obtained using linear discriminant functions trained on 2004 fish assemblages identified via Ward's minimum variance clustering of Bray-Curtis dissimilarities.

Table 2. Indicator species associated with each of three estimated fish communities in the Barents Sea; shifts in spatial distribution for these communities are mapped in Fig. 2. See Table 1 caption for details.
Community Species
  Scientific Name Common Name
Boreal Melanogrammus aeglefinus Haddock
  Micromesistius poutassou blue whiting
  Sebastes mentella deepwater redfish
  Amblyraja radiata thorny skate
  Sebastes norvegicus golden redfish
  Trisopterus esmarkii Norway pout
  Anarhichas minor spotted wolffish
  Pollachius virens saithe
Mixed Leptoclinus maculatus daubed shanny
  Lumpenus lampretaeformis snakeblenny
  Triglops murrayi moustache sculpin
Arctic Triglops nybelini bigeye sculpin
  Boreogadus saida Arctic cod
  Liparidae spp. snailfish spp.
  Reinhardtius hippoglossoides Greenland halibut/turbot
  Icelus spp. sculpin spp.

Single-species analyses

We next illustrate these same patterns for individual, large-bodied species in each region. For walleye pollock and Pacific cod in the eastern Bering Sea, northward shifts in distribution are clearly apparent between bottom-trawl surveys occurring first in 2010 and repeated in 2017 and 2018 (Fig. 3a-f). Hotspots of increased density for Pacific cod are apparent south of St. Lawrence Island (63° N -170° W) and for walleye pollock along the limits of the Russian exclusive economic zone near the Bering Strait (64° N -172° W) in 2017/18. The locations of these hotspots along the northern portion of the Bering Sea have contributed to a rapid northward shift in the population centroid for these and other commercially important species (e.g., northern rock sole, Lepidopsetta polyxystra, see Stevenson and Lauth (2019)). Distribution shifts in the Barents Sea are also apparent by comparing densities of Atlantic cod and haddock in the summer bottom-trawl survey from 2003 with surveys in 2017/18 (Fig. 3g-l). For example, Atlantic cod show increased densities in the central Barents Sea (75° N 35° E) while haddock show increased densities near Bear Island (75° N 19° E). These species-specific results show that the areas with the greatest changes vary from species to species. These results also show that northward shifts can occur even while population densities for boreal species remain high within the southern portion of their range, e.g., elevated estimates of walleye pollock density near Unimak Island (65° N -165° W) in 2010 and 2018 (Fig. 3a,c).

Visualization of density estimates for fish in the eastern and northern Bering Sea shelf
Fig. 3. Visualization of density estimates for Pacific cod and walleye pollock in the eastern and northern Bering Sea (EBS) shelf in 2010, 2017 and 2018 (a-f), and Atlantic cod and haddock in Barents Sea (BS) summer survey in 2003, 2017 and 2018 (g-l); see colorbar in bottom row for each species, with units of natural-logarithm of biomass per area. Years are chosen to show the first year with sampling data spanning the full spatial domain, as well as the two most recent years available at the time of analysis. Estimates are generated using a spatio-temporal delta-model (Thorson 2019) applied to all years of data for each species individually, and predicting density within the footprint of the survey (EBS) or for all locations within 20 km of any survey observation (BS). We estimate density at 500 modeled locations, which are distributed in proportion to the spatial area being estimated, and using bilinear interpolation to predict densities between modeled locations. The models for the EBS shelf estimate the magnitude of first-order autoregression among years in the spatio-temporal term.

Consequences for Arctic ecosystems

In the Bering Sea, the expansion of nearshore ('Norton Sound') and southern shelf species into the northern Bering Sea is likely to have profound effects on the benthic ecology of the northern Bering Sea, due to an increase in demersal fish biomass by several orders of magnitude (Stevenson and Lauth 2019). The observed high densities of fish in Bering Strait suggest that boreal species may shift their summer feeding migrations into the Chukchi Sea, which has also shown large decreases in summer sea-ice extent (see essay Sea Ice). Movement northward into the Chukchi Sea highlights the need for additional fisheries surveys north of Bering Strait, ongoing monitoring of benthic ecosystem components in the northern Bering and Chukchi seas, as well as synthesis of data from the western portion of the Bering Sea within Russian waters. In the Barents Sea, fish communities shifted rapidly from 2004 to 2012, and then remained relatively stable from 2012 to 2017. Increasing water temperatures opened new feeding habitats in the Barents Sea for Atlantic cod and haddock. So far, these species have been benefiting from the effects of climate change on the Barents Sea. These recent bottom-trawl surveys suggest that the spatial distributions of fish communities in the Barents Sea are stable for the moment at a new state, associated with warmer waters, less sea ice, and northward displacement of boreal species. However, different processes drive density changes in leading (northern) and trailing (southern) edges of species distribution (Pinsky et al. 2020), and contemporary warming could still result in future (lagged) changes. We encourage further comparison between climate-driven distribution shifts for these Atlantic and Pacific gateways to the Arctic. In particular, we note the importance of separating mechanisms occurring on the leading (northward) edges where populations are colonizing new habitats, relative to trailing (southward) edges where populations are likely to be extirpated from existing habitat given future warming.

Acknowledgments

We thank the many scientists who have contributed to these long-term surveys of the eastern and northern Bering Sea, and the Barents Sea. We also thank L. Britt, L. Barnett, E. Yasumiishi, and three anonymous reviewers for comments on an earlier draft.

References

Alabia, I. D., J. G. Molinos, S. -I. Saitoh, T. Hirawake, T. Hirata, and F. J. Mueter, 2018: Distribution shifts of marine taxa in the Pacific Arctic under contemporary climate changes. Divers. Distrib., 24, 1583-1597, https://doi.org/10.1111/ddi.12788.

Duffy-Anderson, J. T., and Coauthors, 2019: Responses of the northern Bering Sea and southeastern Bering Sea pelagic ecosystems following record-breaking low winter sea ice. Geophys. Res. Lett., 46(16), 9833-9842, https://doi.org/10.1029/2019GL083396.

Dufrêne, M., and P. Legendre, 1997: Species assemblages and indicator species: The need for a flexible asymmetrical approach. Ecol. Monogr., 67, 345-366, https://doi.org/10.1890/0012-9615(1997)067[0345:SAAIST]2.0.CO;2.

Fossheim, M., R. Primicerio, E. Johannesen, R. B. Ingvaldsen, M. M. Aschan, and A.V. Dolgov, 2015a: Climate change is pushing boreal fish northwards to the Arctic: The case of the Barents Sea. Arctic Report Card 2015, M. O. Jeffries, J. Richter-Menge, and J. E. Overland, Eds., https://www.arctic.noaa.gov/Report-Card.

Fossheim, M., R. Primicerio, E. Johannesen, R. B. Ingvaldsen, M. M. Aschan, and A.V. Dolgov, 2015b: Recent warming leads to a rapid borealization of fish communities in the Arctic. Nat. Climate Change, 5, 673-677, https://doi.org/10.1038/nclimate2647.

Hollowed, A. B., and Coauthors, 2013: Projected impacts of climate change on marine fish and fisheries. ICES J. Mar. Sci., 70, 1023-1037, https://doi.org/10.1093/icesjms/fst081.

Marsh, J. M., and F. J. Mueter, 2019: Influences of temperature, predators, and competitors on polar cod (Boreogadus saida) at the southern margin of their distribution. Polar Biol., https://doi.org/10.1007/s00300-019-02575-4.

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Overland, J. E., M. Wang, and J. E. Box, 2019: An integrated index of recent pan-Arctic climate change. Environ. Res. Lett., 14, 035006, https://doi.org/10.1088/1748-9326/aaf665.

Pinsky, M. L., B. Worm, M. J. Fogarty, J. L Sarmiento, and S. A. Levin, 2013: Marine taxa track local climate velocities. Science, 341, 1239-1242.

Pinsky, M. L., R. L. Selden, and Z. J Kitchel, 2020 (in press): Climate-driven shifts in marine species ranges: Scaling from organisms to communities. Annu. Rev. Mar. Sci., 12, https://doi.org/10.1146/annurev-marine-010419-010916.

Stabeno, P. J., E. V. Farley Jr., N. B. Kachel, S. Moore, C. W. Mordy, J. M. Napp, J. E. Overland, A. I. Pinchuk, and M. F. Sigler, 2012: A comparison of the physics of the northern and southern shelves of the eastern Bering Sea and some implications for the ecosystem. Deep-Sea Res. Pt. II, 65-70, 14-30, https://doi.org/10.1016/j.dsr2.2012.02.019.

Stabeno, P. J., S. W. Bell, N. A. Bond, D. G. Kimmel, C. W. Mordy, and M. E. Sullivan, 2019: Distributed biological observatory region 1: Physics, chemistry and plankton in the northern Bering Sea. Deep Sea Res. Pt. II, 162, 8-21, https://doi.org/10.1016/j.dsr2.2018.11.006.

Stevenson, D. E., and R. R. Lauth, 2019: Bottom trawl surveys in the northern Bering Sea indicate recent shifts in the distribution of marine species. Polar Biol., 42, 407-421, https://doi.org/10.1007/s00300-018-2431-1.

Thorson, J. T., 2019: Guidance for decisions using the Vector Autoregressive Spatio-Temporal (VAST) package in stock, ecosystem, habitat and climate assessments. Fish. Res., 210, 143-161, https://doi.org/10.1016/j.fishres.2018.10.013.

November 19, 2019

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