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Timing of Shell Ring Formation and Patterns of Shell Growth in the Sea Scallop Placopecten Magellanicus Based on Stable Oxygen Isotopes Author(S): Antonie S

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Timing of Shell Ring Formation and Patterns of Shell Growth in the Sea Scallop Placopecten Magellanicus Based on Stable Oxygen Isotopes Author(S): Antonie S Timing of Shell Ring Formation and Patterns of Shell Growth in the Sea Scallop Placopecten Magellanicus Based on Stable Oxygen Isotopes Author(s): Antonie S. Chute, Sam C. Wainright and Deborah R. Hart Source: Journal of Shellfish Research, 31(3):649-662. 2012. Published By: National Shellfisheries Association DOI: http://dx.doi.org/10.2983/035.031.0308 URL: http://www.bioone.org/doi/full/10.2983/035.031.0308 BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. Journal of Shellfish Research, Vol. 31, No. 3, 649–662, 2012. TIMING OF SHELL RING FORMATION AND PATTERNS OF SHELL GROWTH IN THE SEA SCALLOP PLACOPECTEN MAGELLANICUS BASED ON STABLE OXYGEN ISOTOPES ANTONIE S. CHUTE,1* SAM C. WAINRIGHT2 AND DEBORAH R. HART1 1Northeast Fisheries Science Center, 166 Water Street, Woods Hole, MA 02543; 2Department of Science, U.S. Coast Guard Academy, 27 Mohegan Avenue, New London, CT 06320-8101 ABSTRACT The ratio of 18Oto16O in the shell material of bivalves depends on the ambient water temperature at the time the shell material was deposited. By analyzing samples of shell material taken sequentially from the umbo to the shell margin, we obtained the oxygen isotopic records from the shells of 14 sea scallops (Placopecten magellanicus) and compared the isotope data with the visible rings on the upper valve. Using generalized additive models, we show that ring formation is related significantly to water temperature, and that rings were typically laid down near the annual temperature maximum. Shell ring formation was generally annual, although 2 of the mid-Atlantic scallops appeared to have laid down 2 rings in 1 y. Some of the scallops appear to form new shell material and increase in shell height over the entire year for the first few years of life, and in later years reduce or halt accretion at the shell margin during the coldest temperatures. The isotopic records obtained from near the umbo of the shells suggest that all but one of the scallops were spawned in the fall. KEY WORDS: Placopecten magellanicus, oxygen isotopes, annual rings, growth, scallop INTRODUCTION scallops (Northeast Fisheries Science Center (NEFSC) 2010)). Growth increment data are less prone to error than age Visible bands of a different color or texture (rings) are often estimates from counting rings and are particularly useful for formed on the shells of bivalves when they undergo periods of sea scallops because the first 1 or 2 rings are sometimes obscure modified shell deposition (Stevenson & Dickie 1954, Merrill (Claereboudt & Himmelman 1996, Hart & Chute 2009b). et al. 1966, Haag & Commens-Carson 2008). Ring formation However, both methods require the assumption of annual ring may coincide with the reallocation of resources to the gonads formation. during spawning, or as the result of changes in metabolic pro- Another method that can be used to verify the annual cesses because of environmental extremes. These hypotheses are formation of rings is the seasonal variation in the ratio of not mutually exclusive because different mechanisms may be oxygen stable isotopes in the calcite of the shell itself. The ratio operating in different geographical areas, and possibly both of the heavy-to-light oxygen isotopes in the shell material is may operate simultaneously or at different times during the life determined predominantly by thermodynamic equilibrium of the organism. Water temperatures, which can be associated between the 18Oand16O isotopes (which differ in their with environmental stress, physiological processes, and rotational energies) in calcite and seawater at the time of shell spawning, may be particularly important in the formation deposition, as described in Urey (1948) and Zeebe and Wolf- and timing of rings (Naidu 1970, Jones & Quitmeyer 1996). Gladrow (2001). As a result, calcite that has been deposited at False annual rings, or checks, may be formed as a result of equilibrium with seawater has a higher 18O/16O ratio (or d18O physical trauma, such as having the shell or mantle damaged when expressed relative to a standard) than that of seawater. by contact with fishing gear (Merrill et al. 1966, Caddy 1989). Furthermore, the difference between d18O and d18O Results of previous studies support the hypothesis that rings calcite seawater increases as temperature decreases. This temperature depen- on the upper valve of most sea scallops Placopecten magellani- dency was first described in an empirical equation (for use as a cus (Gmelin 1791) are formed once a year. The methods used paleothermometer of minerals) by McCrae (1950). Modifica- to determine annual periodicity include visual examination tions of McCraeÕs equation for use as a temperature recorder of of shells collected monthly in the Bay of Fundy (Stevenson & biogenic minerals followed and are reviewed by Bemis et al. Dickie 1954), comparison of growth estimates from tagged (1998). scallops with those from shell rings (Posgay 1963, Merrill et al. Because the amount of 18O incorporated into the shell is 1966), and comparison of growth observed in size composition temperature dependent, d18O values from sequential calcite data from annual surveys to that inferred by shell rings (Hart & samples taken along the axis of growth of the shell produce Chute 2009b). The assumption that the rings are true annuli a record of relative water temperature over the life of the scallop allows for the estimation of growth curves based on the annual during the time it was depositing shell material. This informa- growth increment between rings or shell size at age analysis tion can be used to estimate the approximate time of year when (e.g., Verrill 1897, Posgay 1979, Serchuk et al. 1979, MacDonald the visible rings are formed as well as to infer the periods of time & Thompson 1985, Thouzeau et al. 1991, Hart & Chute 2009a). when the scallop is depositing shell material actively. Starting in Recently, growth increments between the rings on sea scallop the 1950s, stable oxygen isotope ratios from both fossil and shells, assumed to be a 1-y increase in shell height, were used to recent mollusc shells have been used to recreate temperature estimate annual population growth for size-structured stock time series (e.g., Urey et al. 1951, Epstein et al. 1953). Samples of assessment models and to predict potential productivity of sea shell material from long-lived animals, such as the ocean *Corresponding author. E-mail: [email protected] quahog Arctica islandica that regularly lives for more than DOI: 10.2983/035.031.0308 200 y, can provide historical ocean water temperature data 649 650 CHUTE ET AL. (Weidman et al. 1994). Shell isotope records have been used to were in the Mid-Atlantic Bight (Hudson Canyon, Elephant verify annual growth increments in several bivalve (Jones et al. Trunk, and Delmarva rotational areas), 1 was on Nantucket 1983, Dare & Deith 1990, Brey & Mackensen 1997, Ivany et al. Shoals (Nantucket Lightship closed area) and 2 were on 2003, Lomovasky et al. 2007, Haag & Commens-Carson 2008), Georges Bank (closed areas I and II, Fig. 1) for a total of 8 and univalve (Gurney et al. 2005, Naylor et al. 2007) mollusc collection sites. Four scallops each were analyzed from 2 sites species. (Nantucket Lightship and Elephant Trunk) to evaluate The 2 previous studies of P. magellanicus growth using stable within-site variability and replicability, whereas a single scal- oxygen isotopes analyzed 2 shells apiece. Krantz et al. (1984) lop was analyzed at the other sites. The collection sites ranged analyzed shells collected off Virginia (37°15# N) and suggested in depth from 53–98 m, and had mostly sandy bottom with that 2 visible rings were formed annually. Tan et al. (1988) some gravel in the Georges Bank/Nantucket Shoals sites and analyzed scallops from Browns Bank off Nova Scotia (42°50# N) some silt in the deeper mid-Atlantic sites. The scallops and suggested the formation of a single ring per year during the analyzed ranged in shell height (SH; body size measured from temperature minimum. Other studies of sea scallops from Nova the umbo to the shell margin) from 101–137 mm, with a mean Scotia have also indicated 1 annual ring is formed during the of 123 mm (Table 1). temperature minimum (Stevenson & Dickie 1954, Roddick et al. Shells with the least infestation by boring organisms were 1999). In this article, we examine oxygen isotopic records from 14 selected for isotope analysis from among all shells collected at P. magellanicus shells collected from 8 locations off the eastern a site. The visual location of each ring on the shell was marked, U.S. coast to determine the timing of ring formation and to and the distance to each ring from the umbo was measured in investigate patterns of growth and spawning. millimeters using a caliper. The shell was then scrubbed in warm water and allowed to dry completely. A dentistÕs drill was used MATERIALS AND METHODS to sample the top layer of calcite to a depth of approximately 0.5 mm, removing powdered calcite from lines ;1.5 cm in The 14 sea scallops used for this study were collected live length perpendicular to the long axis of the shell and parallel to during the annual NEFSC summer scallop survey or, in 2 cases, the shell margin at the time of deposition (Fig.
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