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A Unique Temperate Rocky Coastal Hydrothermal Vent System (Whakaari–White Island, Bay of Plenty, New Zealand): Constraints for Ocean Acidification Studies

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A Unique Temperate Rocky Coastal Hydrothermal Vent System (Whakaari–White Island, Bay of Plenty, New Zealand): Constraints for Ocean Acidification Studies RESEARCH FRONT CSIRO PUBLISHING Marine and Freshwater Research, 2020, 71, 321–344 https://doi.org/10.1071/MF19167 A unique temperate rocky coastal hydrothermal vent system (Whakaari–White Island, Bay of Plenty, New Zealand): constraints for ocean acidification studies R. ZitounA,H,M, S. D. ConnellB, C. E. Cornwall C,D, K. I. CurrieH, K. FabriciusE, L. J. HoffmannF, M. D. LamareG, J. MurdochA,H, S. NoonanE, S. G. SanderA,H,I, M. A. SewellJ, N. T. ShearsK, C. M. G. van den BergL and A. M. SmithG ADepartment of Chemistry, University of Otago, PO Box 56, Dunedin, 9054, New Zealand. BSouthern Seas Ecology Laboratories, School of Biological Sciences, University of Adelaide, Adelaide, SA 5005, Australia. CSchool of Biological Sciences, Victoria University of Wellington, PO Box 600, Wellington, 6140, New Zealand. DSchool of Earth Sciences and Oceans Institute, ARC Centre of Excellence for Coral Reef Studies, University of Western Australia, Crawley, WA 6009, Australia. EAustralian Institute for Marine Science, PMB 3, Townsville MC, Qld 4810, Australia. FDepartment of Botany, University of Otago, PO Box 54, Dunedin, 9054, New Zealand. GDepartment of Marine Science, University of Otago, PO Box 56, Dunedin, 9054, New Zealand. HNational Institute for Water and Atmospheric (NIWA)/University of Otago Research Centre for Oceanography, PO Box 56, Dunedin, 9054, New Zealand. IInternational Atomic Energy Agency (IAEA) Environment Laboratories, Department of Nuclear Sciences and Applications, B.P. 800, 98000 Monaco, Principality of Monaco. JSchool of Biological Sciences, University of Auckland, Private Bag 92019, Auckland, 1010, New Zealand. KLeigh Marine Laboratory, Institute of Marine Science, University of Auckland, 160 Goat Island Road, Auckland, 0985, New Zealand LSchool of Environmental Sciences, University of Liverpool, 74 Bedford Street, Liverpool, L69 7ZT, UK. MCorresponding author. Email: [email protected] Abstract. In situ effects of ocean acidification are increasingly studied at submarine CO2 vents. Here we present a preliminary investigation into the water chemistry and biology of cool temperate CO2 vents near Whakaari–White Island, New Zealand. Water samples were collected inside three vent shafts, within vents at a distance of 2 m from the shaft and at control sites. Vent samples contained both seawater pH on the total scale (pHT) and carbonate saturation states that were severely reduced, creating conditions as predicted for beyond the year 2100. Vent samples showed lower salinities, higher temperatures and greater nutrient concentrations. Sulfide levels were elevated and mercury levels were at concentrations considered toxic at all vent and control sites, but stable organic and inorganic ligands were present, as deduced from Cu speciation data, potentially mediating harmful effects on local organisms. The biological investigations focused on phytoplankton, zooplankton and macroalgae. Interestingly, we found lower abundances but higher diversity of phytoplankton and zooplankton at sites in the direct vicinity of Whakaari. Follow-up studies will need a combination of methods and approaches to attribute observations to specific drivers. The Whakaari vents represent a unique ecosystem with considerable biogeochemical complexity, which, like many other vent systems globally, require care in their use as a model of ‘future oceans’. Additional keywords: carbon dioxide, trace metal speciation, volcanic submarine vent. Received 13 May 2019, accepted 2 September 2019, published online 18 November 2019 Journal compilation Ó CSIRO 2020 Open Access CC BY-NC-ND www.publish.csiro.au/journals/mfr 322 Marine and Freshwater Research R. Zitoun et al. Introduction conditions (e.g. Boatta et al. 2013; Fabricius et al. 2014; Three methods have generally been used to estimate the effects Dahms et al. 2018; Gonza´lez-Delgado and Herna´ndez 2018; of changing seawater chemistry: mathematical modelling Pichler et al. 2019) anchored to observational data, controlled experimentation in the limited area affected by vent emissions and resulting area the laboratory or field-based mesocosm studies, and the study of with low pH and potentially higher temperatures (Boatta et al. natural systems representing analogues of past, present or future 2013; Pichler et al. 2019) climate change scenarios (e.g. Boyd et al. 2018). Each of these the continuous supply of larvae and propagules from outside approaches has its strengths and weaknesses, but together they the vent system (e.g. Levin et al. 2016; Boyd et al. 2018; have proved useful in developing preliminary projections, elu- Hawkins et al. 2018), which hampers the ability to use these cidating connections and understanding synergies (Le Treut sites to determine whether dispersive populations could adapt et al. 2007) regarding ocean warming and ocean acidification to environmental stressors over multiple generations (OA; Wisshak et al. 2013; Riebesell and Gattuso 2015; Gattuso the eventuality that some organisms that live at CO2 vents et al. 2015). could have higher tolerance thresholds for environmental Most of our current understanding of how marine biota will stressors owing to the possibility of evolving and genetically respond to climate change originates from controlled, adapting over long timescales to extreme physicochemical laboratory-based, short-term experiments conducted in tanks conditions (e.g. Hall-Spencer et al. 2008) and mesocosms as well as modelling approaches based on these the chemical composition of hydrothermal fluids at many experimental data (Wernberg et al. 2012). Controlled, vent sites (i.e. the potential presence at toxic concentrations of laboratory-based manipulations (e.g. mesocosms) are useful in elements and gases), which may have confounding effects establishing a mechanistic understanding of how physical cli- on vent biota (e.g. Cunha et al. 2008; Chen et al. 2018; mate change is likely to drive ecological changes, but they tend Dahms et al. 2018; Gonza´lez-Delgado and Herna´ndez 2018; to exaggerate their measured effects and obscure key processes Hawkins et al. 2018; Pichler et al. 2019). (Goldenberg et al. 2018) because they are based on simplified Most CO vent studies to date have focused on the ecological artificial model systems ruled by first-order abiotic and biotic 2 consequences of lower pH, lower carbonate saturation state or effects and thus suffer from a lack of realism (Wernberg et al. higher CO (e.g. Hall-Spencer et al. 2008; Fabricius et al. 2011, 2012; Gonza´lez-Delgado and Herna´ndez 2018). To increase 2 2014; Brinkman and Smith 2015; Nagelkerken et al. 2016), realism and collective inference, as well as to strengthen the whereas elevated levels of heavy metals in vent fluids compared generality and accuracy of our understanding of climate change with non-hydrothermal environments and their potential effects as a driver of chemical and biological change in marine on the local environment (Chen et al. 2018; Hawkins et al. 2018) ecosystems, researchers have started using existing natural have either largely been overlooked, dismissed as insignificant gradients in climate variables to examine how increased pCO 2 or were studied using methods unable to detect bioactive trace (i.e. a change in ocean chemistry) will translate into ecological metals with necessary sensitivity. Emanating fluids of many changes (e.g. Hall-Spencer et al. 2008; Wernberg et al. 2012; volcanic submarine CO vents are typically characterised by Teixido´ et al. 2018). One example of an environment with 2 high concentrations of toxic metals such as Pb, Cd, Zn, Hg, Cu, natural abiotic gradients is the shallow submarine CO vent, 2 Co, Mo and Sr (Cunha et al. 2008; Chen et al. 2018; Hawkins and these vents are found around the globe (Tarasov et al. et al. 2018; Burger and Lichtscheidl 2019). These metal-rich 2005; Gonza´lez-Delgado and Herna´ndez 2018). Over the past fluids contaminate the surrounding water column, and poten- 10 years, shallow CO vents have emerged as analogues to 2 tially adversely affect the physiology of vent biota (Cunha et al. investigate the effects of OA on natural ecosystems (e.g. Hall- 2008; Chen et al. 2018; Hawkins et al. 2018). Thus, it is Spencer et al. 2008; Fabricius et al. 2011; Lombardi et al. 2011; surprising that so far most shallow vent studies of biological Calosi et al. 2013; Lamare et al. 2016; Dahms et al. 2018). They nature limited their element measurements to gases (e.g. CO , have enabled research into the effects of long-term in situ 2 H S, CH ,N,O; Pichler et al. 2019) and sediments (e.g. exposure of multiple biota to elevated pCO under natural 2 4 2 2 2 Vizzini et al. 2013), despite elements in solution being poten- environmental variability, food, light and hydrodynamic condi- tially key factors for the assessment of the suitability of vent tions, as well as natural levels of interactions between species and systems for the study of climate change effects on marine biota their environment (e.g. Hall-Spencer et al. 2008; Fabricius et al. (Vizzini et al. 2013). Consequently, an integrated picture of the 2011, 2014; Brinkman and Smith 2015; Nagelkerken et al. carbonate chemistry, biology and, in particular, the geochemis- 2016). Thus, submarine CO vents have gained increasing 2 try (i.e. element composition, metal speciation and popularity in the past decade as natural laboratories to obtain a bioavailability) of shallow submarine vents is required to simu- better understanding of CO effects on community, population, 2 late and investigate OA at CO vents. ecosystem structure and functionality changes, as well as 2 The most well-studied shallow submarine CO vents in the species-specific adaptation mechanisms in a natural environment 2 context of climate change are in the warm temperate Mediterra- (e.g. Lombardi et al. 2011; Calosi et al. 2013; Lamare et al. 2016; nean Sea (e.g. Hall-Spencer et al. 2008; Kroeker et al. 2011; Dahms et al. 2018; Gonza´lez-Delgado and Herna´ndez 2018). Lidbury et al. 2012; Vizzini et al. 2013; Baggini et al. 2014; The main limitations in using shallow marine hydrothermal Ziveri et al.
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