**1. Introduction**

Cold-water coral (CWC) reefs form complex habitats in the deep sea, supporting rich associated fauna [1–4]. They play a major role in the circulation of organic carbon in the deep sea [5,6]. The reefs are recognized as vulnerable marine ecosystems (VMEs) by the United Nations [7] and as threatened and declining habitats by the OSPAR commission [8]. Warming and acidifying waters (i.e., decreasing pH and aragonite saturation state, ΩAr) are predicted to pose imminent and serious threats to CWC reefs within the next decades [9,10]. Hence, there has been an intensified focus to assess the range of biogeochemical and physical conditions tolerated by CWCs in situ [11–16] and in laboratory conditions [17–21]. Finally, a focus is on determining the baseline for optimal conditions for coral growth and reef development [22]. However, there is very little data on the small-scale temporal and spatial variability of biogeochemical and physical conditions in CWC settings, which could be pivotal in understanding their resilience to climate change, as observed for tropical coral reefs [23].

In the North Atlantic, CWC reefs are most commonly build by *Lophelia pertusa* (syn. *Desmophyllum pertusum* [24]), with around a third of all known *L. pertusa* occurrences being from Norwegian waters [25]. *L. pertusa* reefs are generally found on and around elevated

**Citation:** Juva, K.; Kutti, T.; Chierici, M.; Dullo, W.-C.; Flögel, S. Cold-Water Coral Reefs in the Langenuen Fjord, Southwestern Norway—A Window into Future Environmental Change. *Oceans* **2021**, *2*, 583–610. https://doi.org/10.3390/ oceans2030033

Academic Editor: Luis Somoza

Received: 30 October 2020 Accepted: 10 August 2021 Published: 25 August 2021

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**Copyright:** © 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

bathymetric structures such as mounds, offshore banks, seamounts, and sills [26–30], where relatively strong bottom flow associated with those structures enhances the flux of food particles [22,31–33] and facilitates sediment removal from CWCs or the seafloor to provide suitable settlement substrates for coral larvae [25,34]. While local hydrodynamics are important in regulating the distribution of CWCs, water column characteristics such as temperature, nutrient availability, carbonate chemistry (mainly aragonite saturation, ΩAr), and oxygen levels [2,12,15,35] act as additional and strong drivers in regulating coral growth. The latter two are vital in maintaining calcification and aerobic metabolism in corals, while low-temperature regimes decelerate food decay (enhancing food availability) and reduce metabolic energy demands [36].

Rising global ocean temperatures have been observed throughout the water column since the 1960s [37]. In coastal Norway, rapid warming of the Norwegian coastal water (NCW) and the North Atlantic water (NAW, SA < 35 g kg<sup>−</sup>1) in mid-layer waters has been reported since the 1980s [38]. Ocean warming is expected to affect both the fitness and the geographical distribution of many marine species in the coming decades. CWCs are usually found in waters with temperatures <12 ◦C [13,29,39], but occasionally they thrive in warmer waters of ~15 ◦C [15,40]. Even though CWCs can tolerate substantial fluctuations in temperature [41,42], a rise of only 2 ◦C for a few hours will significantly increase its energy demands [36,41], which could deplete energy stores if they are not met by increased food availability and/or uptake rates [35]. Ocean warming can also indirectly affect CWCs by changing primary production patterns [43] and reducing oxygen availability [44]. In southwestern Norway, the reduction in oxygen concentration has been ~0.5 mL L−<sup>1</sup> per decade over the past 40 years in the fjord basin waters [45].

Long-term decreasing trends of pH and aragonite saturation have been observed in the open ocean around the globe [46,47] as well as in coastal waters off Norway. Currently, the aragonite saturation horizon (ASH, ΩAr < 1) of the Norwegian Sea is at ~2000 m depth. At these depths, an annual decrease of 0.003 in ΩAr and 0.008 in pH has been observed between 2007 and 2017 [48]. The observed decrease inside the fjords, where ΩAr is currently >1 across the water column, is larger. A two-fold annual decrease of 0.007 in ΩAr and of 0.02 in pH compared to offshore and 2000 m depth has been observed at bottom water depths of ~670 m in Korsfjorden south of Bergen between 2007 and 2017 [48]. Calcifying marine organisms such as CWCs will be directly impacted by the shoaling of the ASH. Below the ASH depth, mineral dissolution occurs, dissolving the exposed dead coral framework that constitutes a major component of the reef, and waters are less favorable for skeletal growth [29,49,50]. The skeleton of *L. pertusa* is based on aragonite, the most labile form of calcium carbonate. Hence, the reefs are considered particularly susceptible to a decreasing ΩAr. If current trends continue at unchanged rates, the ASH is estimated to reach the surface by the year 2070 ± 10 in southwestern Norwegian fjords [51], while deeper waters (>600 m) off Norway will become corrosive already within the next 20 years [48]. Most of the Norwegian CWCs are observed in between these depths, so they are likely to experience corrosive conditions in the next 20–50 years.

The seasonal changes in carbonate chemistry in high latitude surface waters are driven by temperature, salinity, air-sea CO2 exchange, formation and decay of organic matter, and advection and vertical mixing with deeper, carbon-rich coastal water [51]. In western Norwegian fjords, the spring phytoplankton bloom yields maximum pH and reduced dissolved inorganic carbon (CT) values. Seasonal ΩAr variations align with those of surface temperature, both peaking in late summer. This seasonal forcing also affects the carbonate chemistry at the depths of living CWCs (i.e., 80–250 m). Generally, the CT and carbon dioxide (CO2) concentrations increase with depth. This is caused by enhanced respiration and remineralization of organic matter, which also yield to decreased pH [48,52–55]. Apart from Findlay et al. (2014) [53], who provided a high-resolution nutrient and carbonate chemistry data over a tidal cycle showing the influence of local upwelling for Scottish and Irish CWC reefs, very little data exist on diurnal variability and not least the seasonal dynamics of carbonate chemistry for deep waters. At present, carbonate chemistry and

nutrient data are primarily available from global data sets [56,57]. These are useful for making large-scale habitat predictions [13,58], but they lack the fine-scale spatial and temporal coverage that is required to understand the baseline of physicochemical dynamics around CWC reefs that plays a key role in determining the resilience of CWC reefs to future climate change.

This study investigated the natural variability of biogeochemical and physical conditions at five CWC reefs located within a narrow fjord in western Norway. This was achieved by collating water column measurements of carbonate chemistry and inorganic nutrient parameters for multiple stations and timepoints over 1.5 years and combining those with high temporal resolution data from two benthic observatories deployed at one of the reefs. Comparisons of environmental data from reefs growing on vertical walls with those growing on the fjord floor were used to elucidate the relative importance of topography-flow interaction and biogeochemical conditions for CWC occurrences.
