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Reconstruction of Temperature Experienced by Pacific Bluefin Tuna Thunnus Orientalis Larvae Using SIMS and Microvolume CF-IRMS Otolith Oxygen Isotope Analyses

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Reconstruction of Temperature Experienced by Pacific Bluefin Tuna Thunnus Orientalis Larvae Using SIMS and Microvolume CF-IRMS Otolith Oxygen Isotope Analyses Vol. 649: 175–188, 2020 MARINE ECOLOGY PROGRESS SERIES Published September 10 https://doi.org/10.3354/meps13451 Mar Ecol Prog Ser OPEN ACCESS Reconstruction of temperature experienced by Pacific bluefin tuna Thunnus orientalis larvae using SIMS and microvolume CF-IRMS otolith oxygen isotope analyses Yulina Hane1,2,*, Shingo Kimura1,2, Yusuke Yokoyama2,3,4, Yosuke Miyairi2, Takayuki Ushikubo5, Toyoho Ishimura6,7, Nobuhiro Ogawa2, Tomoya Aono2,6, Kozue Nishida6,8 1Graduate School of Frontier Sciences, The University of Tokyo, Kashiwanoha, Kashiwa, Chiba 277-8564, Japan 2Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwanoha, Kashiwa, Chiba 277-8564, Japan 3Department of Earth and Planetary Science, Graduate School of Science, The University of Tokyo, Hongo, Tokyo 113-0033, Japan 4Organization for Programs on Environmental Sciences, Graduate School of Arts and Sciences, The University of Tokyo, Komaba, Tokyo 153-8902, Japan 5Kochi Institute for Core Sample Research, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), Nankoku, Kochi 783-8502, Japan 6National Institute of Technology, Ibaraki College, Hitachinaka, Ibaraki 312-8508, Japan 7Graduate School of Human and Environmental Studies, Kyoto University, Yoshida-nihonmatsu-cho, Sakyo-ku, Kyoto 606-8501, Japan 8Graduate School of Life and Environmental Sciences, University of Tsukuba, 1-1-1 Tennodai, Tsukuba 305-8572, Japan ABSTRACT: This study aimed to reconstruct temperatures experienced during the larval period by adult Pacific bluefin tuna Thunnus orientalis using high-resolution otolith stable oxygen iso- tope (δ18O) analysis. A novel otolith sample preparation protocol for secondary ion mass spectro - metry (SIMS) analysis developed in this study reduced the background noise of SIMS measure- ments, enabling analyses of >10 times higher resolution around the otolith core compared to previous studies using conventional isotope ratio mass spectrometry (IRMS). The values obtained δ18 from SIMS were compared to those obtained by microvolume Ootolith analysis using micromilling and conventional continuous-flow IRMS (CF-IRMS). There was a systematic offset (average 0.41‰ with SIMS resulting in lower values) most likely caused by matrix effects on SIMS δ18 Ootolith values that can be calibrated using a strong linear relationship between SIMS and CF- 2 δ18 IRMS measurements (r = 0.78, p < 0.001). The core-to-edge Ootolith of 5 Pacific bluefin tuna revealed fine-scale seasonal variations in water temperature agreeing with known migration pat- terns. In addition, the ambient water temperature experienced during larval stages (about 10− 20 d post hatch) estimated from otolith core δ18O ranged from 26.7 to 30.7°C, overlapping with temperatures associated with the occurrence of larval Pacific bluefin tuna. Combining SIMS and δ18 microvolume CF-IRMS O otolith analyses offers a microscale examination of fish ecology that is not possible with conventional IRMS techniques. This novel method is particularly useful for understanding the early life history of fish that may be affected by climate change and recon- structing a well-resolved migration history for fish species that have small otoliths and/or narrow growth increments. KEY WORDS: Temperature reconstruction · Otolith · Oxygen isotope analysis · Secondary ion mass spectrometry · SIMS · continuous-flow isotope ratio mass spectrometry · CF-IRMS · Pacific bluefin tuna · Sample preparation protocol © The authors 2020. Open Access under Creative Commons by *Corresponding author: [email protected] Attribution Licence. Use, distribution and reproduction are un - restricted. Authors and original publication must be credited. Publisher: Inter-Research · www.int-res.com 176 Mar Ecol Prog Ser 649: 175–188, 2020 1. INTRODUCTION analysis (usually more than a few tens of micrograms with a minimum weight requirement of 15 μg). Ocean warming has significant impacts on marine Ambient water temperatures have previously been species and ecosystems, including high mortality, reconstructed using IRMS for sockeye salmon Onco- distribution shifts, and loss of spawning and nursery rhynchus nerka (Zazzo et al. 2006), alewife Alosa habitats (Perry et al. 2005, Kimura et al. 2010, Muh- pseudoharengus (Dufour et al. 2008), Atlantic cod ling et al. 2011, 2015). Species that spawn seasonally Gadus morhua (Jones & Campana 2009, von Leesen in relatively limited areas are particularly vulnerable et al. 2020), turbot Scophthalmus maximus (Imsland to increasing water temperature, as their optimum et al. 2014), and chub mackerel Scomber japonicus range in spawning temperatures tends to be re stric - (Higuchi et al. 2019), most of which have a monthly ted. Pacific bluefin tuna Thunnus orientalis (PBT) is a to annual resolution depending on the otolith size. highly migratory species that spawns in waters near The limited temporal resolution due to the sample the Nansei Islands in the western North Pacific from mass requirement of the IRMS is inevitable and May to June and in the Sea of Japan from July to makes it particularly difficult when analyzing the August (Yonemori 1989, Ohshimo et al. 2017). Adult otolith core and edge. fish in the western North Pacific spawn at tempera- Recent developments in secondary ion mass tures between 26 and 29°C, whereas those in the Sea spectrometry (SIMS) δ18O analysis of otoliths have of Japan initiate spawning at temperatures greater enabled a high-resolution reconstruction of migra- than 20°C (Chen et al. 2006, Tanaka 2011, Suzuki et tion and life history characteristics of marine species al. 2014, Okochi et al. 2016). In the laboratory, the (Hanson et al. 2010, Matta et al. 2013, Shiao et al. growth rate and survival of PBT larvae significantly 2014, Helser et al. 2018a, Shirai et al. 2018, Willmes decrease when temperatures exceed 29°C (Kimura et al. 2019). Unlike conventional IRMS, SIMS is capa- et al. 2007). In fact, projected temperature in the cur- ble of determining isotopic composition within a spa- rent spawning sites is expected to increase by more tial resolution of 5 to 15 μm, which allows sub- than 3°C by 2100 under the most extreme Intergov- annual, seasonal, and even weekly or much shorter ernmental Panel on Climate Change (IPCC) climate- timescale analyses with high accuracy and precision warming scenario (IPCC 2007) and become unsuit- (Kita et al. 2009, Valley & Kita 2009). While a recent able for PBT to spawn (Kimura et al. 2010). As PBT study (Sakamoto et al. 2019) reconstructed migration larvae are particularly vulnerable to thermal stress, histories of an individual Japanese sardine Sardinops warming sea temperatures are likely to have signifi- melanostictus with 10 to 30 d resolution (20 to 30 d cant impacts on their early growth and survival. around the core regions and 10 to 15 d toward the However, the effects of ongoing climate change on edge) using microvolume isotope analysis measured the early life stages of PBT are poorly understood due by continuous-flow IRMS (CF-IRMS), SIMS provides to a lack of empirical evidence and methods to study even finer temporal resolution, particularly for the such effects. otolith core and edge. High-resolution reconstruction δ18 δ18 Oxygen isotope ratios ( O) in otoliths, biogenic of experienced temperatures using SIMS Ootolith is calcium carbonate (aragonite) found in the inner ear an effective method for investigating the early life of teleost fish (ray-finned bony fish), has been widely history of fish in response to increasing water tem- used as a natural tag to reconstruct water tempera- perature associated with climate change. tures and salinity conditions experienced by fish In this study, we developed a method to reconstruct (Thorrold et al. 1997, Campana 1999, Jones & Cam- ambient water temperatures experienced during pana 2009). Such reconstructions of past environ- the larval period of an individual fish using SIMS δ18 δ18 ment are possible because otoliths generally develop Ootolith analysis. Ootolith values of 5 adult PBT at or close to the isotope equilibrium with ambient otolith samples were measured from the otolith core δ18 water, and many studies have demonstrated the tem- to edge by SIMS, and the measured SIMS Ootolith perature dependency of otolith δ18O for various fish values were compared to those measured by CF- species under laboratory conditions (Kalish 1991, IRMS. Water temperatures were then estimated Thorrold et al. 1997, Høie et al. 2004, Kitagawa et al. using a temperature-dependent oxygen isotope frac- 2013). Existing methods of temperature reconstruc- tionation equation for PBT larvae that had already δ18 tion for fish mostly rely on Ootolith measurements been established in a previous study (Kitagawa et al. by conventional isotope ratio mass spectrometry 2013). The temperature reconstruction technique (IRMS), which often involves a milling process to presented here allows high-resolution investigation obtain a relatively large amount of otolith powder for of the early life history of fish and provides a more δ18 Hane et al.: Temperature reconstruction using SIMS Ootolith analysis 177 thorough understanding of the characteristics of sur- vivors and the thermal environment that may con- strain their early growth and survival. 2. MATERIALS AND METHODS 2.1. Sample collection and sample preparation protocol Sagittal otoliths, the largest of 3 pairs of otoliths, were collected from the heads of PBT caught in waters south of Japan in the Pacific by local longline fishing vessels and small ships
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