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Bivalves As Indicators of Environmental Variation and Potential Anthropogenic Impacts in the Southern Barents Sea Over Multiple Time Scales

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Bivalves As Indicators of Environmental Variation and Potential Anthropogenic Impacts in the Southern Barents Sea Over Multiple Time Scales Published as: Carroll, M.L., B. Johnson, G.A. Henkes, K.W. McMahon, A. Voronkov, W.G. Ambrose Jr., S.G. Denisenko. 2009. Bivalves as indicators of environmental variation and potential anthropogenic impacts in the southern Barents Sea over multiple time scales. Marine Pollution Bulletin 59:193-206. doi:10.1016/j.marpolbul.2009.02.022. Bivalves as indicators of environmental variation and potential anthropogenic impacts in the southern Barents Sea Michael L. Carroll1,*, Beverly J. Johnson2, Gregory A. Henkes2,3†,Kelton W. McMahon4, Andrey Voronkov5,6, William G. Ambrose, Jr.1,3, Stanislav G. Denisenko5 1) Akvaplan-niva, Polar Environmental Centre, N-9296 Tromsø, Norway 2) Bates College, Department of Geology, Lewiston, Maine 04240, USA 3) Bates College, Department of Biology, Lewiston, Maine 04240, USA 4) Woods Hole Oceanographic Institution, MIT-WHOI Joint Program in Biological Oceanography, Woods Hole, MA 02543-1541 USA 5) Zoological Institute, Russian Academy of Sciences, Universitetskaya nab. 1, St. Petersburg, 199034, Russia 6) Norwegian Polar Institute, Polar Environmental Centre, N-9296 Tromsø, Norway † Current Address: Smithsonian Institution, Museum Conservation Institute, 4210 Silver Hill Road, MRC 534, Suitland, MD 20746-2863, USA * Corresponding Author: M.L. Carroll Tel: +47 7775 0318 Fax: +47 7775 0301 Email: [email protected] Running Head: Arctic bivalves as indicators of environmental variation Key Words: Arctic, Barents Sea, benthic community, bivalve growth, climate oscillation, environmental forcing, North Atlantic Oscillation, White Sea, sclerochronology, Serripes groenlandicus, shell geochemistry, stable isotopes, trace element ratios Arctic bivalves as indicators of environmental variation 1 Abstract 2 3 Identifying patterns and drivers of natural variability in populations is necessary to 4 gauge potential effects of climatic change and the expected increases in commercial activities 5 in the Arctic on communities and ecosystems. We analyzed growth rates and shell 6 geochemistry of the circumpolar Greenland smooth cockle, Serripes groenlandicus, from the 7 southern Barents Sea over almost 70 years between 1882 and 1968. The datasets were 8 calibrated via annually-deposited growth lines, and growth, stable isotope (18O, 13C), and 9 trace elemental (Mg, Sr, Ba, Mn) patterns were linked to environmental variations on weekly 10 to decadal scales. Standardized growth indices revealed an oscillatory growth pattern with a 11 multi-year periodicity, which was inversely related to the North Atlantic Oscillation Index 12 (NAO), and positively related to local river discharge. Up to 60% of the annual variability in 13 the Ba/Ca could be explained by variations in river discharge at the site closest to the rivers, 14 but the relationship disappeared at a more distant location. Patterns of 18O, 13C, and Sr/Ca 15 together provide evidence that bivalve growth ceases at elevated temperatures during the fall 16 and recommences at the coldest temperatures in the early spring, with the implication that 17 food, rather than temperature, is the primary driver of bivalve growth. The multi-proxy 18 approach of combining the annually integrated information from the growth results and higher 19 resolution geochemical results yielded a robust interpretation of biophysical coupling in the 20 region over temporal and spatial scales. We thus demonstrate that sclerochronological proxies 21 can be useful retrospective analytical tools for establishing a baseline of ecosystem variability 22 in assessing potential combined impacts of climatic change and increasing commercial 23 activities on Arctic communities. M.L. Carroll et al. 2 Arctic bivalves as indicators of environmental variation 24 1. Introduction 25 26 The Arctic is warming and consequently becoming more accessible to industrial and 27 commercial activities such as petroleum and mineral extraction, shipping, and fisheries 28 (ACIA, 2005). As these activities increase, pre-industrial baselines of the natural system are 29 necessary in order to assess the effects of anthropogenic activities on the Arctic marine 30 ecosystem. This necessitates observations and data collections over time scales that capture 31 the seasonal to decadal scales of system processes. Unfortunately, due to the remote setting 32 and harsh nature of much of the Arctic marine ecosystem, relevant scales of observation are 33 rarely adequate with traditional marine biological sampling plans, which usually provide a 34 spatially- and temporally-limited view of the system. While continuously-recording 35 observatories are a promising development (e.g. Morison et al., 2002), they are still in their 36 infancy in the Arctic and currently provide data for limited locations. Biological proxies may 37 provide an immediate alternative approach for assessing the variability of marine ecosystems 38 over longer time frames, including the ability for retrospective reconstruction of 39 environmental variability over historical time frames. Marine bivalves (clams) show great 40 promise for investigating environmental variability in the Arctic. Arctic bivalves are long- 41 lived (decades to centuries), sessile, and often dominate the biomass of many Arctic benthic 42 communities (Zenkevich, 1963; McDonald et al., 1981; Dayton, 1990; Feder et al., 1994). 43 Since bivalve growth is strongly regulated by temperature and food availability (Beukema et 44 al., 1985; Jones et al., 1989; Lewis and Cerrato, 1997; Decker and Beukema, 1999), analyzing 45 variations in growth can provide insight into seasonal to decadal variations in these factors 46 over the animal’s life. 47 Reconstructing environmental conditions from animal soft tissues offers a limited 48 view of the past because of the rapid turnover rates of these highly metabolically-active 49 tissues. Aragonitic bivalve shells, however, are secreted sequentially with external growth M.L. Carroll et al. 3 Arctic bivalves as indicators of environmental variation 50 lines as the animal grows (Rhoads and Lutz, 1980), recording the growth histories, 51 metabolism and environmental conditions experienced during the deposition of that shell 52 material. The growth and chemistry of accretionary hard-parts precipitated by marine 53 organisms have proved valuable in developing histories of environmental change in marine 54 systems (Pannella, 1971; Andrews, 1972, 1973; Rhoads and Lutz, 1980; Jones, 1981; 55 Weidman et al., 1994; Witbaard et al., 1999; Ambrose et al., 2006; reviewed in Richardson, 56 2001). High-latitude bivalves have provided uninterrupted long-term records of hydrographic 57 conditions experienced during the lifetime of the organism (Thompson et al., 1980; Witbaard 58 et al., 1999; Dutton et al., 2002; Müller-Lupp and Bauch, 2005). 59 The shell material of bivalves preserves chemical proxies for ambient seawater 60 conditions when the organism is actively precipitating shell carbonate. Profiles of stable 61 oxygen and carbon isotopes (Jones and Quitmyer, 1996; Klein et al., 1996; Müller-Lupp and 62 Bauch, 2005; Simstich et al., 2005) and incorporated trace elements (Torres et al., 2001; 63 Vander Putten et al., 2000; Khim et al., 2003; Freitas et al., 2006; Gillikin et al., 2006a) from 64 sequential sampling along the shell height can provide high-resolution records of seawater 65 chemistry useful for interpreting spatial and temporal patterns in temperature, salinity, and 66 hydrography. External growth lines on bivalve shells often represent annual growth checks, 67 as has been demonstrated for Serripes groenlandicus (Khim, 2002; Khim et al., 2003; 68 Ambrose et al., 2006; Kilada et al., 2007). Provided the date of death is known, growth lines 69 can be used to determine growth rates and assign calendar years to geochemical proxies. The 70 combined use of growth rate and shell geochemistry allows us to compare proxy information 71 on specific environmental parameters and their biological manifestation, thereby allowing 72 broader inferences on mechanistic relationships of bio-physical coupling. 73 The Barents Sea, a continental shelf sea bounded by Norway and Russia to the south 74 and the Arctic Ocean basin to the north, is both bathymetrically and hydrographically M.L. Carroll et al. 4 Arctic bivalves as indicators of environmental variation 75 complex (Loeng, 1991; Vinje and Kvambekk, 1991). The northern and eastern regions are 76 dominated by Arctic water with origins in the Arctic Ocean and Russian shelf seas. The 77 southern region is strongly influenced by warm, saline Atlantic source water from temperate 78 latitudes. The coastal areas of the southern Barents Sea are under the influence of the eastern- 79 flowing Murman Coastal Current as well as freshwater discharges from the Mezen’, 80 Severnaya Dvina, and Pechora Rivers (Loeng 1989, 1991; Loeng et al., 1997). These 81 oceanographic regions and their hydrographic properties have strong influences on regional 82 and local primary production and ecosystem structure (Wassmann et al., 2006), including 83 benthic community structure (Carroll et al., 2008a) and functioning (Renaud et al., 2008). 84 The overriding influence of these oceanographic provinces on properties of marine 85 ecosystems is modified by regional climatic drivers which oscillate between different phases 86 and are accompanied by substantially different atmospheric and hydrograhic properties over 87 decadal scales. The North Atlantic Oscillation Index (NAO), usually defined as the 88 atmospheric pressure difference between Iceland and
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