Site and Age Discrimination Using Trace Element Fingerprints in The
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Journal of Experimental Marine Biology and Ecology 522 (2020) 151249 Contents lists available at ScienceDirect Journal of Experimental Marine Biology and Ecology journal homepage: www.elsevier.com/locate/jembe Site and age discrimination using trace element fingerprints in the blue mussel, Mytilus edulis T ⁎ Aaron Honiga, , Ron Ettera, Kyle Peppermanb, Scott Morelloa, Robyn Hanniganc a Biology Department, University of Massachusetts, Boston, 100 Morrissey Blvd, Boston, MA 02125, United States of America b Downeast Institute for Applied Marine Research and Education, 39 Wildflower Lane, Beals, ME 04611, United States of America c School for the Environment, University of Massachusetts, Boston, 100 Morrissey Blvd, Boston, MA 02125, United States of America ARTICLE INFO ABSTRACT Keywords: The ability to accurately estimate population connectivity and larval dispersal among mussel populations in the Trace element fingerprinting Gulf of Maine is important to better understand ongoing declines in blue mussel abundances. Such efforts are Bioincorporation crucial for crafting conservation strategies targeting important spawning and settlement sites necessary to Blue mussel support threatened local shellfisheries, and to mitigate the potential effects of rapid climate change on larval Population connectivity dispersal and survivorship. Trace element fingerprints can be used to infer larval dispersal and population connectivity, but require a reference map of geographic variation in elemental fingerprints to infer natal sites of settled mussels. Previous work has suggested rearing mussel larvae in situ to create a reference map because biomineralization differs between larval and post-metamorphic mussels, which might lead to differences in trace element fingerprints. To test whether elemental fingerprints differed between larval and juvenile (post-meta- morphic) mussels (Mytilus edulis), we reared them in situ and under controlled laboratory conditions. Trace element concentrations in larval and juvenile shell matrices were quantified using laser ablation inductively coupled plasma mass spectrometry (LA-ICPMS). The majority of trace element concentrations, normalized to calcium, differed between larval and juvenile mussels, resulting in elemental fingerprints that were consistently distinct between age classes. Larval and juvenile fingerprints differed consistently whether they were reared in the lab or field, probably reflecting age-specificdifferences in biomineralization. To use trace element finger- prints to estimate larval dispersal and population connectivity, our results suggest that a spatial map of ele- mental fingerprints should be created by rearing larval, not juvenile, mussels at potential source populations. Our results are consistent with what has been found for other mussels and thus may be true for all mussels, and likely true for any bivalves with age-specificdifferences in biomineralization. 1. Introduction et al., 2007; Cowen and Sponaugle, 2009; Lowe and Allendorf, 2010; Leis et al., 2011). Quantifying patterns of larval dispersal and population connectivity A widely used approach to empirically estimate dispersal and con- in marine ecosystems is important to further our understanding of nectivity in marine organisms relies on trace element fingerprints (TEF) ecology, evolution, conservation and management, and will be essential derived from the chemical signatures found in calcified structures for predicting how organisms might respond to anthropogenic stresses (Lopez-Duarte et al., 2012). TEFs take advantage of the chemical signal (Cowen et al., 2007; Gaines et al., 2007; Siegel et al., 2008; Carson incorporated into growing calcified structures such as shells (Becker et al., 2011; Puckett and Eggleston, 2016; Kroll et al., 2018). However, et al., 2007; Carson, 2010; Fodrie et al., 2011; Broadaway and tracking minute pelagic larvae that drift with the ocean currents and Hannigan, 2012), statoliths (Zacherl et al., 2003; Zacherl, 2005; Warner potentially travel tens of kilometers during several weeks of develop- et al., 2009) or otoliths (Thorrold et al., 2001; Dorval et al., 2007; Leis ment is extremely difficult (DiBacco and Levin, 2000; Thorrold et al., et al., 2011). For example, as bivalves grow they deposit layers of 2002; Knights et al., 2006; Levin, 2006; Cathey et al., 2012). Because of CaCO3 (calcite and aragonite) on a matrix of proteins to form a shell its importance to ecology, evolution and conservation, a number of (Marin and Luquet, 2004). The calcite-aragonite shell chemistry reflects methods have been developed to estimate dispersal and population the elemental and isotopic chemistry of the surrounding water mass connectivity in marine ecosystems (reviewed in Levin, 2006; Thorrold through geochemically passive and biologically active transport to the ⁎ Corresponding author. E-mail address: [email protected] (A. Honig). https://doi.org/10.1016/j.jembe.2019.151249 Received 11 April 2018; Received in revised form 26 April 2019; Accepted 12 October 2019 0022-0981/ © 2019 Elsevier B.V. All rights reserved. A. Honig, et al. Journal of Experimental Marine Biology and Ecology 522 (2020) 151249 site of shell deposition (Klein et al., 1996; Carson et al., 2013). Trace abundance allows us to identify potential sources for declines within elements in the shell can be quantified using laser ablation inductively the Gulf of Maine, provide important insights into the ecological forces coupled plasma mass spectrometry (LA-ICPMS; Liu et al., 2013). Re- shaping regional dynamics and contribute to more effective manage- sulting trace element fingerprints (e.g., Mg/Ca, Mn/Ca, Ba/Ca, La/Ca, ment and conservation strategies for this ecologically and economically Pb/Ca), vary spatially (< 50 km; Becker et al., 2007); and temporally important species (Botsford et al., 2001, 2009; Bode et al., 2008; (monthly and annual periodicity; Miller et al., 2013, Carson et al., Hayhurst and Rawson, 2009; Sorte et al., 2013; Bryson et al., 2014; 2013), characterize different water masses, and can be used to identify Morello and Etter, 2017). the location where shell material was deposited (Becker et al., 2005; The potential importance of using TEFs in quantifying population Levin, 2006; Broadaway and Hannigan, 2012; Carson et al., 2013). connectivity, and the likely impact of environmental chemistry on shell Because many adult bivalves retain their larval shell even after meta- TEFs has led to the suggestion that larvae should be outplanted and morphosis and settlement, TEFs of the larval shell can be used to assign reared in all potential source populations to generate an appropriate settlers to likely natal sites, through a reference map of site-specific reference map of fingerprints (Becker et al., 2007). Although TEFs ap- TEFs generated during natural spawning events (Becker et al., 2005). pear to differ between larval and adult shells for some bivalves (Becker Temporal changes in host water mass and shell geochemistry necessi- et al., 2007; Strasser et al., 2007, 2008), this has not been tested in tate TEF reference maps be generated through in-situ rearing when Mytilus edulis. Because outplanting larvae and rearing them at potential adults are spawning (Putten et al., 2000; Carré et al., 2006; Lazareth source populations requires considerable time and resources, it is im- et al., 2013, Kroll et al., 2018). High seasonal and annual variability of portant to test whether TEFs differ between larval and post-meta- element ratios (particularly Mn, Co relative to Ca) in outplanted Mytilus morphic (juvenile) shell material. Here we test whether TEFs differ sp. shells was observed by Carson et al. (2013), likely in part due to between age classes of Mytilus edulis and whether any age-specific dif- interannual variability in site-specific environmental factors that im- ferences exceed geographic variation in natural populations in the GOM pact biomineralization (geology, freshwater input, upwelling, anthro- that would preclude accurately inferring natal sites. pogenic impact, e.g., Miller et al., 2013). Estimating the variability among site-specific TEFs is therefore critical to evaluate the analytical 2. Material and methods utility of TEF reference maps, and at what spatial and temporal scale TEFs should be effectively used to estimate patterns of dispersal and 2.1. Laboratory experiment population connectivity (site vs region, week vs month; Becker et al., 2005, 2007). Both laboratory and in-situ field experiments were conducted to To estimate dispersal and population connectivity using TEFs, a determine if TEFs differed between larvae and juvenile mussels. Initial reference map of geographic differences in fingerprints is necessary to laboratory experiments were conducted at the Downeast Institute's infer natal sites (reviewed in: Levin, 2006; Becker et al., 2007; Carson shellfish hatchery on Beals Island, ME (DEI, Fig. 1). Adult mussels et al., 2013). A reference map is typically developed from TEFs of se- (≥5 cm), representing multigenerational brood stock originally locally dentary adults collected from potential source populations (DiBacco collected on Beal's Island, were conditioned during the spring of 2015 and Levin, 2000). However, larval and adult mussels precipitate dif- and spawned in June. Resulting larvae (70 μm diameter, n = 100,000) ferent calcium carbonate polymorphs during shell growth, which might were reared alongside juvenile mussels (2–4 mm shell length, n = 100) influence TEFs (Medaković, 2000; Weiss et al., 2002; Dalbeck et al., in large, shallow