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Statolith Microchemistry Traces the Environmental History of the Boreoatlantic Armhook Squid Gonatus Fabricii

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Statolith Microchemistry Traces the Environmental History of the Boreoatlantic Armhook Squid Gonatus Fabricii MARINE ECOLOGY PROGRESS SERIES Vol. 333: 195–204, 2007 Published March 12 Mar Ecol Prog Ser Statolith microchemistry traces the environmental history of the boreoatlantic armhook squid Gonatus fabricii Karsten Zumholz1,*, Andreas Klügel2, Thor Hansteen1, Uwe Piatkowski1 1IFM-GEOMAR, Leibniz-Institut für Meereswissenschaften, Düsternbrooker Weg 20, 24105 Kiel, Germany 2Universität Bremen, Fachbereich Geowissenschaften, Postfach 330440, 28334 Bremen, Germany ABSTRACT: Statoliths of the gonatid squid Gonatus fabricii from Disko Bay, West Greenland, were analysed by laser ablation inductively coupled plasma mass-spectrometry (LA-ICP-MS) to determine the concentrations and spatial distributions of 9 minor and trace elements (Sr, Ba, Mg, U, Zn, Mn, Y, Zr, Na). Element composition was assigned in situ to distinct statolith regions, corresponding to onto- genetic stages of an individual squid’s life. Significant variations in concentrations of all measured elements except Na were found between different regions of the statolith. Variations in Ba/Ca ratios suggest that juveniles inhabit surface waters, while larger specimens move to deeper waters. U/Ca and Sr/Ca ratios increased towards the outer statolith region, suggesting migration of adult squid into colder waters. Mg/Ca ratios decreased progressively from the core to the edge, most likely related to changes in protein concentrations in their microstructure during ontogenesis. This study is one of the first to apply LA-ICP-MS to cephalopod statoliths. Our results emphasise the strong potential of spa- tially resolved statolith analyses to gather information on life history, migrations and habitat use of cephalopods. KEY WORDS: Statolith · Trace elements · Laser ablation ICP-MS · Cephalopods · Squid · Gonatus fabricii · Greenland Resale or republication not permitted without written consent of the publisher INTRODUCTION posed to take place at great depths (Arkhipkin & Bjørke 1999). Its early life stages are found in large The boreoatlantic armhook squid Gonatus fabricii numbers in west Greenland epipelagic waters (Lichtenstein, 1818) is the most abundant squid of the (Piatkowski & Wieland 1993), while larger squids occur arctic and subarctic waters of the North Atlantic and is mainly in mesopelagic and bathypelagic layers (Kris- considered to have some commercial potential (Nesis tensen 1984). 1965, Kristensen 1984, Zumholz & Frandsen 2006). Trace element analysis of biomineralised tissues has This species is frequently found in the stomachs of become a frequently used method for determining marine mammals and fishes (Lick & Piatkowski 1998, environmental histories of many aquatic organisms. Bjørke 2001) and is likely to play an important role in Although more commonly applied to fish otoliths the ecosystem off West Greenland. G. fabricii is caught (Campana 1999, 2005) and corals (e.g. Smith et al. frequently as by-catch in the fishery of deep-water 1979), many other marine organisms have calcified prawn Pandalus borealis, and locally it is kept and structures that may be similarly useful as natural tags used as bait. The life cycle of the squid is characterised (Zacherl et al. 2003a, Becker et al. 2005). Cephalopod by well-defined ontogenetic vertical migrations as de- statoliths share many structural similarities with fish scribed by Arkhipkin & Bjørke (1999). Hatching is pro- otoliths (Clarke 1978). They are composed primarily of *Email: [email protected] © Inter-Research 2007 · www.int-res.com 196 Mar Ecol Prog Ser 333: 195–204, 2007 aragonite crystals associated with an organic matrix The analysis of elemental signatures of whole dis- (Radtke 1983). Alternating layers of organic-rich and solved statoliths (‘elemental fingerprints’) makes it organic-poor material are deposited periodically. The possible to distinguish between populations and co- ‘one increment per day’ hypothesis has been validated horts. This has been demonstrated convincingly for for several species (Jackson 1994, Bettencourt & Loligo gahi (Arkhipkin et al. 2004). Furthermore, the Guerra 2001), though not for G. fabricii. A comprehen- same authors highlighted the potential of spatially sive review of recent developments in statolith studies resolved elemental analyses to determine stage-spe- is given by Arkhipkin (2005). cific migrations and habitat use. Several studies have shown that statoliths contain a Based on optical increment analysis, Kristensen number of elements at minor and trace levels (e.g. (1980) and Arkhipkin & Bjørke (2000) defined 4 distinct Hurley et al. 1985, Durholtz et al. 1997, Lipinski et al. growth zones (Z1, Z2, Z3, Z4) in the statoliths of Gona- 1997, Yatsu et al. 1998, Ikeda et al. 2002a,b, Arkhip- tus fabricii corresponding to different ontogenetic kin et al. 2004). Fundamental results on the biominer- stages and thereby different habitat use, separated alisation process have been presented by Bettencourt from each other by distinct checks. Z1 represents the & Guerra (2000), but the exact principles of elemental embryo phase before hatching; Z2 and Z3 develop uptake into statoliths are still unknown. Strontium has during the juvenile phase (up to 60 mm pen length). Z4 been shown to be essential for normal statolith devel- is formed during the subadult and adult periods. opment (Hanlon et al. 1989), while magnesium may No published information on the chemical composi- also be a key factor in the calcification process within tion of Gonatus fabricii statoliths has been available the statocyst (Morris 1991, Bettencourt & Guerra until now. In this study, transects on ground G. fabricii 2000). Inspired by an inverse relationship between statoliths from the core to the edge were analysed, Sr/Ca and temperature in scleractinian corals (Beck et thereby determining the chemical composition of the al. 1992), several studies have attempted to use Sr/Ca different growth zones. The aim of this study was (1) to ratios in statoliths as a temperature proxy (e.g. Rod- quantify the elemental composition and spatial distrib- house et al. 1994, Ikeda et al. 2003). Arkhipkin et al. ution of elements within G. fabricii statoliths and (2) to (2004) showed a good relationship between Sr/Ca and find possible relations between statolith elemental ambient temperature in statoliths of the Patagonian composition and the habitat use and life history of indi- longfin squid Loligo gahi collected in the field. How- vidual squids. ever, no experimental studies have shown evidence that Sr/Ca ratios in squid statoliths are temperature dependent. MATERIALS AND METHODS Sample collection. Specimens were sampled on board the RV ‘Paamiut’ as by-catch during a bottom trawl survey targeting deep-water prawn Pandalus borealis from July to August 2003 in Disko Bay, West Greenland (Fig. 1). Cephalopods were frozen on board immediately after capture and defrosted for further analyses at IFM-GEOMAR, Kiel. Sex was determined, and maturity stages (I–II, immature; III–IV, maturing; V, mature) were estimated according to the appear- ance and relative size of the reproductive organs (Lip- inski 1979). Pen length (PL) was measured to the near- est 1 mm; total body wet mass (BM) was measured to the nearest g. The sample used for this study consisted of 16 males (all specimens were assigned to maturity stage III) and 10 females (all specimens were assigned to maturity stage II). All specimens were caught within 3 hauls on the same day in the same area (stations: 68° 57.51’ N, 52° 07.35’ W; 69° 09.46’ N, 53° 20.15’ W; 69° 09.46’ N, 53° 02.85’ W). The statoliths were dis- sected from the cephalic cartilage, washed in distilled Fig. 1. Location of Disko Bay, West Greenland (box), where specimens of Gonatus fabricii were sampled from bottom water, stored in Eppendorf caps and kept dry. trawl hauls in 2003. Map plotted with Ocean DataView Statolith processing and reading. In total, 26 sta- (Schlitzer 2007) toliths were prepared and analysed. One statolith from Zumholz et al.: Statolith microchemistry of Gonatus fabricii 197 recorded during 90 s with 5 samples at each peak’s flat top and a total dwell time of 50 ms per isotope. Owing to the lack of matrix-matched standards, the glass ref- erence materials NIST610 (for 23Na, 43Ca, 88Sr) and NIST612 (for 23Na, 25Mg, 43Ca, 55Mn, 64Zn, 89Y, 90Zr, 93Nb, 138Ba, 238U) were used for external calibration taking the accepted concentrations of Pearce et al. (1997). Both standards were analysed and a new cali- bration line established after every 5 to 11 data points (standard bracketing) to compensate for any instru- mental drift. GeoPro software was used to define a blank of 8–20 s duration and a stable signal period of Fig. 2. Gonatus fabricii. Ground statolith showing the location 15–50 s duration following a pre-ablation period of of analytical points as laser ablation craters. Points are numbered from the core to the edge 5–13 s for each measured point. For quantification, the blank was subtracted and Ca was used as internal standard element with an assumed stoichiometric con- each pair was attached concave side up onto a micro- centration of 40 wt%. Single-point calibration was pre- scopic glass slide with thermoplastic resin (Buehler) ferred over 2-point calibration, because the 2 differ- and was ground on one side with wet waterproof lap- ently coloured NIST standards show distinct ablation ping film (3M®; 30 µm, 15 µm, 3 µm) until the ground behaviour and element fractionation at a laser wave- surface extended to the edge (i.e. the most extended length of 266 nm (Guillong et al. 2003). point) of the dorsal dome, and the core (corresponding The external analytical precision was determined to the embryonic phase) could be seen just beneath the through replicate analyses of the homogeneous stan- ground surface. Ground statoliths were finally pol- dard reference materials NIST612 and GOR128G ished with Buehler micropolish II (0.3 µm and 0.05 µm) (basaltic glass with low concentrations of some trace and observed under a Leitz Laborlux K microscope elements; Jochum et al. 2000). The data indicate a (250× magnification) to locate the growth zones as precision of better than 3% for concentrations above defined by Kristensen (1980).
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