Predicting Potential Impacts of Ocean Acidification on Marine Calcifiers from the Southern Ocean

Predicting Potential Impacts of Ocean Acidification on Marine Calcifiers from the Southern Ocean

bioRxiv preprint doi: https://doi.org/10.1101/2020.11.15.384131; this version posted November 17, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. Predicting potential impacts of ocean acidification on marine calcifiers from the Southern Ocean 1 Blanca Figuerola1*, Alyce M. Hancock2, Narissa Bax2, Vonda Cummings3, Rachel Downey4, 2 Huw J. Griffiths5, Jodie Smith6, Jonathan S. Stark7 3 1Institute of Marine Sciences (ICM, CSIC), Pg. Marítim de la Barceloneta 37-49, 08003, Barcelona, 4 Spain 5 2Institute for Marine and Antarctic Studies, University of Tasmania, Hobart, Tasmania 7004 6 3National Institute of Water and Atmospheric Research (NIWA), Wellington, New Zealand 7 4Australia National University, Fenner School of Environment and Society, Canberra, Australia 8 5British Antarctic Survey, High Cross, Madingley Rd, Cambridge CB3 0ET, UK 9 6Geoscience Australia, GPO Box 378, Canberra, ACT 2601, Australia 10 7Australian Antarctic Division, Channel Highway, Kingston, Tasmania, Australia 11 12 13 Correspondence: 14 Dr. Blanca Figuerola 15 [email protected]; [email protected] 16 Keywords: carbonate mineralogy, magnesium, aragonite, climate change, vulnerability, 17 Antarctica, saturation horizon. 18 Abstract 19 Understanding the vulnerability of marine calcifiers to ocean acidification is a critical issue, 20 especially in the Southern Ocean (SO), which is likely to be the one of the first, and most severely 21 affected regions. Since the industrial revolution, ~30% of anthropogenic CO2 has been absorbed by 22 the oceans. Seawater pH levels have already decreased by 0.1 and are predicted to decline by ~ 0.3 23 by the year 2100. This process, known as ocean acidification (OA), is shallowing the saturation 24 horizon, which is the depth below which calcium carbonate (CaCO3) dissolves, likely increasing the 25 vulnerability of many marine calcifiers to dissolution. The negative impact of OA may be seen first 26 in species depositing more soluble CaCO3 mineral phases such as aragonite and high-Mg calcite 27 (HMC). These negative effects may become even exacerbated by increasing sea temperatures. Here 28 we combine a review and a quantitative meta-analysis to provide an overview of the current state of 29 knowledge about skeletal mineralogy of major taxonomic groups of SO marine calcifiers and to 30 make predictions about how OA might affect different taxa. We consider their geographic range, 31 skeletal mineralogy, biological traits and potential strategies to overcome OA. The meta-analysis of 32 studies investigating the effects of the OA on a range of biological responses such as shell state, 33 development and growth rate shows response variation depending on mineralogical composition. 34 Species-specific responses due to mineralogical composition suggest taxa with calcitic, aragonitic 35 and HMC skeletons may be more vulnerable to the expected carbonate chemistry alterations, and low 36 magnesium calcite (LMC) species may be mostly resilient. Environmental and biological control on 37 the calcification process and/or Mg content in calcite, biological traits and physiological processes 38 are also expected to influence species specific responses. 39 40 41 bioRxiv preprint doi: https://doi.org/10.1101/2020.11.15.384131; this version posted November 17, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 42 1 Introduction 43 Since the industrial revolution, the concentration of carbon dioxide (CO2) released to the atmosphere 44 has increased from 280 to above 400 µatm due to human activities such as burning of fossil fuels and 45 deforestation. Approximately 30% of this has been absorbed by the oceans (Feely et al., 2004). 46 Seawater pH levels have already decreased by 0.1 and are predicted to decline by ~ 0.3 (851-1370 47 µatm) by the year 2100 (IPCC, 2014, 2019). This process, known as ocean acidification (OA), also 2- 48 lowers both carbonate ion concentration ([CO3 ]) and saturation state (Ω) of seawater with respect to 2- 49 calcium carbonate (CaCO3) minerals. In particular, Ω is a function of [CO3 ] and calcium ion 50 concentrations ([Ca2+]) expressed as &' &+ 51 Ω = [$% ][$)* ]/-./ 52 where Ksp is the solubility product, which depends on the specific CaCO3 mineral phase, temperature, 53 salinity, and pressure (Zeebe, 2012). 54 Surface waters are naturally supersaturated with respect to carbonate (Ω > 1), where the highest 2- 2- 55 [CO3 ] is found as a result of surface photosynthesis. The [CO3 ] decreases, and the solubility of 56 CaCO3 minerals (such as aragonite) increases, with depth due to the higher pressure and lower 57 temperature. Thus, Ω is higher in shallow, warm waters than in cold waters and at depth (Feely et al., 58 2004). Current aragonite saturation in Southern Ocean (SO) surface waters ranges from Ωarag of 1.22 59 to 2.42, compared with values of 3.5 to 4 in the tropics (Jiang et al., 2015), and varies spatially, e.g. 60 across ocean basins, and seasonally. However, OA is both decreasing saturation levels and 61 shallowing the carbonate saturation horizon, which is the depth below which CaCO3 can dissolve (Ω 62 < 1). This is likely to increase the vulnerability of CaCO3 sediments and many marine calcifiers 63 (CaCO3 shell/skeleton-building organisms) to dissolution (Fig. 1) (Haese et al., 2014). As CaCO3 64 sediments have important roles in global biogeochemical cycling and provide suitable habitat for 65 many marine calcifying species, undersaturated seawater conditions will also lead to unprecedented 66 challenges and alterations to the function, structure and distribution of carbonate ecosystems exposed 67 to these conditions (Andersson et al., 2008). 68 A number of marine calcifiers, particularly benthic populations from the tropics and deep waters, are 69 already exposed to undersaturated conditions with respect to their species-specific mineralogies 70 (Lebrato et al., 2016). This suggests some organisms have evolved compensatory physiological 71 mechanisms to maintain the calcification process (Lebrato et al., 2016). This does not mean that these 72 taxa will cope with sudden decreases in the Ω, rather it illustrates the complexity of taxon-level 73 responses. For instance, SO marine calcifiers may be particularly sensitive to these changes since the 2- 74 SO is characterized by much lower natural variability in surface ocean [CO3 ] (Conrad and 75 Lovenduski, 2015). The processes responsible for making calcifying organisms vulnerable to OA 76 have been much discussed. Recent research suggests that the reduction in seawater pH mainly drives 77 changes in calcification rates (the production and deposition of CaCO3), rather than the reduction in 2- 78 [CO3 ] (Cyronak et al., 2016), with a predicted drop in calcification rates by 30 to 40% by mid- 79 century due to OA (Kleypas et al., 1999). The long-term persistence of calcifying taxa depends on 80 calcification exceeding the loss of CaCO3 that occurs through breakdown, export and dissolution 81 processes (Andersson and Gledhill, 2013). Therefore, even though species-specific responses to OA 82 are expected, a tendency toward reduction in overall CaCO3 production at the local or community 83 level is anticipated (Andersson and Gledhill, 2013) with potentially adverse implications across SO 84 ecosystems. 2 bioRxiv preprint doi: https://doi.org/10.1101/2020.11.15.384131; this version posted November 17, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 85 1.1 Southern Ocean acidification 86 The Southern Ocean, which covers about 34.8 million km2, is widely anticipated to be the one of the 87 first, and most severely affected region from OA due to naturally low levels of CaCO3, the increased 88 solubility of CO2 at low temperatures, and a lower buffering capacity (Orr et al., 2005). Thus, 89 understanding the vulnerability of Antarctic marine calcifiers to OA is a critical issue, particularly in 90 Antarctic Peninsula, which is also one of the fastest warming areas on Earth (Vaughan and Marshall, 91 2003). To establish the potential threat of OA to SO marine calcifiers, it is crucial to consider 92 different factors that may influence the vulnerability of their skeletons to OA. These include 93 interacting factors (e.g. warming), the local seasonal and spatial variability in the carbonate system, 94 the distribution of sedimentary CaCO3 (which provides suitable habitat for many benthic calcifiers), 95 and a range of different phyla and species with diverse geographic range, skeletal mineralogies, 96 biological traits, physiological processes and strategies to combat pH changes. 97 1.1.1 Local seasonal and spatial variability in carbonate system 98 The depth of the present-day SO Aragonite Saturation Horizon (ASH) exceeds 1,000 m across most 99 of the basin, while naturally shallower saturation horizons (~400 m) occur in the core of the Antarctic 100 Circumpolar Current due to upwelling of CO2-rich deep water (Negrete-García et al., 2019). The 101 Calcite Saturation Horizon (CSH) is much deeper (> 2000 m in some parts of the SO) than the ASH, 102 since aragonite is more soluble than calcite (Feely et al., 2004; Barnes and Peck, 2008). It is thus 103 predicted that the ASH will reach surface waters earlier than the CSH (McNeil and Matear, 2008). In 104 particular, it is anticipated that aragonite in some SO regions (south of 60°S) will be undersaturated 105 by 2050 (Orr et al., 2005; McNeil and Matear, 2008) and that 70% of the SO could be undersaturated 106 by 2100 (Hauri et al., 2016). OA will drive even the least soluble form of calcium carbonate, calcite, 107 to undersaturation by 2095 in some SO waters (McNeil and Matear, 2008). However, the depth and 108 year of emergence of a shallow ASH can vary spatially due to natural variation in the present-day 109 saturation horizon depth and in the physical circulation of the SO (Negrete-García et al., 2019).

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