The Effects of Environment on Arctica Islandica Shell Formation and Architecture

Biogeosciences, 14, 1577–1591, 2017 www.biogeosciences.net/14/1577/2017/ doi:10.5194/bg-14-1577-2017 © Author(s) 2017. CC Attribution 3.0 License. The effects of environment on Arctica islandica shell formation and architecture Stefania Milano1, Gernot Nehrke2, Alan D. Wanamaker Jr.3, Irene Ballesta-Artero4,5, Thomas Brey2, and Bernd R. Schöne1 1Institute of Geosciences, University of Mainz, Joh.-J.-Becherweg 21, 55128 Mainz, Germany 2Alfred Wegener Institute for Polar and Marine Research, Am Handelshafen 12, 27570 Bremerhaven, Germany 3Department of Geological and Atmospheric Sciences, Iowa State University, Ames, Iowa 50011-3212, USA 4Royal Netherlands Institute for Sea Research and Utrecht University, P.O. Box 59, 1790 AB Den Burg, Texel, the Netherlands 5Department of Animal Ecology, VU University Amsterdam, Amsterdam, the Netherlands Correspondence to: Stefania Milano ([email protected]) Received: 27 October 2016 – Discussion started: 7 December 2016 Revised: 1 March 2017 – Accepted: 4 March 2017 – Published: 27 March 2017 Abstract. Mollusks record valuable information in their hard tribution, and (2) scanning electron microscopy (SEM) was parts that reflect ambient environmental conditions. For this used to detect changes in microstructural organization. Our reason, shells can serve as excellent archives to reconstruct results indicate that A. islandica microstructure is not sen- past climate and environmental variability. However, animal sitive to changes in the food source and, likely, shell pig- physiology and biomineralization, which are often poorly un- ment are not altered by diet. However, seawater temperature derstood, can make the decoding of environmental signals had a statistically significant effect on the orientation of the a challenging task. Many of the routinely used shell-based biomineral. Although additional work is required, the results proxies are sensitive to multiple different environmental and presented here suggest that the crystallographic orientation physiological variables. Therefore, the identification and in- of biomineral units of A. islandica may serve as an alterna- terpretation of individual environmental signals (e.g., water tive and independent proxy for seawater temperature. temperature) often is particularly difficult. Additional proxies not influenced by multiple environmental variables or animal physiology would be a great asset in the field of paleoclimatology. The aim of this study is to investigate the poten- 1 Introduction tial use of structural properties of Arctica islandica shells as an environmental proxy. A total of 11 specimens were ana- Biomineralization is a process through which living organ- lyzed to study if changes of the microstructural organization isms produce a protective, mineralized hard tissue. The con- of this marine bivalve are related to environmental condi- siderable diversity of biomineralizing species contributes to tions. In order to limit the interference of multiple parame- high variability in terms of shape, organization and miner- ters, the samples were cultured under controlled conditions. alogy of the structures produced (Lowenstam and Weiner, Three specimens presented here were grown at two different 1989; Carter et al., 2012). Different architectures at the water temperatures (10 and 15 ◦C) for multiple weeks and micrometer and nanometer scale and different biochemical exposed only to ambient food conditions. An additional eight compositions determine material properties that serve spe- specimens were reared under three different dietary regimes. cific functions (Weiner and Addadi, 1997; Currey, 1999; Shell material was analyzed with two techniques; (1) confo- Merkel et al., 2007). Besides these differences, all miner- cal Raman microscopy (CRM) was used to quantify changes alized tissues are hybrid materials consisting in hierarchical of the orientation of microstructural units and pigment dis- arrangements of biomineral units surrounded by organic ma- trix, also known as “microstructures” (Bøggild, 1930; Carter Published by Copernicus Publications on behalf of the European Geosciences Union. 1578 S. Milano et al.: The effects of environment on Arctica islandica and Clark, 1985; Rodriguez-Navarro et al., 2006), “ultra- efforts to develop alternative techniques to reconstruct envi- structures” (Blackwell et al., 1977; Olson et al., 2012) or ronmental variables from mollusk shells (Schöne et al., 2010; overall “fabrics” (Schöne, 2013; Schöne et al., 2013). The Milano et al., 2017). carbonate and organic phases represent the fundamental level This study investigates the possibility using shell mi- of the organization of biomaterials (Aizenberg et al., 2005; crostructure properties to serve as a new environmental Meyers et al., 2006). The mechanisms of microstructure for- proxy. For this purpose, the effects of seawater tempera- mation and shaping, especially in mollusks, has attracted in- ture (grown at 10 and 15 ◦C) and dietary regime on the mi- creasing attention during recent decades. At present, it is crostructural units of Arctica islandica cultured under con- commonly accepted that the organic compounds play an trolled conditions were analyzed and quantified. A. islandica important role in the formation of the inorganic phases of was chosen as model species because of its great potential in biominerals (Weiner and Addadi, 1991; Berman et al., 1993; paleoclimatology and paleoceanography (see Schöne, 2013; Dauphin et al., 2003; Nudelman et al., 2006). However, the Wanamaker et al., 2016). Its extreme longevity of up to more identification of the exact mechanisms driving biomineral- than 500 years makes this species a highly suitable archive ization is still an open research question. Previous studies for long-term paleoclimate and environmental reconstruc- conducted on mollusks show that environmental parameters tions (Schöne et al., 2005; Wanamaker et al., 2008, 2012; can influence microstructure formation (Lutz, 1984; Tan Tiu Butler et al., 2013). and Prezant, 1987; Tan Tiu, 1988; Nishida et al., 2012). These results set the stage for research that focuses on the use of shell microstructures as proxies for reconstructing en- 2 Materials and methods vironmental conditions (Tan Tiu, 1988; Tan Tiu and Prezant, 1989; Olson et al., 2012; Milano et al., 2017). The analyses were conducted on 11 A. islandica shells. Three Mollusks are routinely used as climate and environmen- juvenile A. islandica shells, sampled for the seawater temper- tal proxy archives because they can record a large amount ature experiment, were collected alive on 21 November 2009 of environmental information in their shells (Richardson, aboard the F.V. Three of a Kind off Jonesport, Maine, USA 2001; Wanamaker et al., 2011a; Schöne and Gillikin, 2013). (44◦2609.82900 N, 67◦26018.04500 W), in 82 m water depth. Whereas structures at nanometric levels are still underex- From 2009 to 2011, all animals were kept in a flowing seawa- plored as potential environmental recorders, shell patterns at ter laboratory at the Darling Marine Center, Walpole, Maine, lower magnification, such as individual growth increments, USA (see Beirne et al., 2012, for additional details). In 2011, are commonly used for this purpose (Jones, 1983; Schöne clams were grown at two different temperature regimes for et al., 2005; Marali and Schöne, 2015; Mette et al., 2016). 16 weeks (Table 1). At the completion of the experiment, Mollusks deposit skeletal material on a periodic basis and shells were estimated to be between 4 to 5 years old. Eight at different rates (Thompson et al., 1980; Deith, 1985). Dur- 1-year old juveniles were collected in July 2014 from Kiel ing periods of fast growth, growth increments are formed, Bay, Baltic Sea (54◦320 N, 10◦420 E; Fig. 1) and kept alive whereas during periods of slower growth, growth lines are in tanks at 7 ◦C for 6 months at the Alfred Wegener Insti- formed (Schöne, 2008; Schöne and Gillikin, 2013). The pe- tute (AWI) for Polar and Marine Research, Bremerhaven, riodicity of such structures ranges from tidal to annual (Gor- Germany. During this time interval, the animals were fed don and Carriker, 1978; Schöne and Surge, 2012). By cross- with an algal mix of Nannochloropsis sp., Isochrysis gal- dating time series with similar growth patterns it is possible bana and Pavlova lutheri. Then, they were transferred to the to construct century- and millennia-long master chronologies Royal Netherlands Institute for Sea Research (NIOZ), Texel, (Marchitto et al., 2000; Black et al., 2008, 2016; Butler et al., the Netherlands, and cultured in tanks at three different di- 2013). This basic approach, in combination with geochem- etary conditions for 11 weeks (Table 1). ical methods, has great potential in reconstructing past cli- matic conditions (Wanamaker et al., 2011b). At present, the 2.1 Seawater temperature experiment most frequently used and well-accepted geochemical proxy 18 is oxygen isotopic composition of shell material (δ Oshell/ The seawater temperature experiment started on 27 March (Epstein, 1953; Grossman and Ku, 1986; Schöne et al., and ended on 21 July 2011. Prior to the start of the exper- 2004; Wanamaker et al., 2007), which may serve as a pa- iment the animals were marked with calcein. The staining leothermometer and/or paleosalinometer (Mook, 1971; An- leaves a clear fluorescent marker in the shells that can be 18 drus, 2011); however, δ Oshell value is influenced by both used to identify which shell material has formed prior to seawater temperature and the

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