Large-Scale Salmon Farming in Norway Impacts the Epiphytic Community of Laminaria Hyperborea

Vol. 13: 81–100, 2021 AQUACULTURE ENVIRONMENT INTERACTIONS Published March 25 https://doi.org/10.3354/aei00392 Aquacult Environ Interact OPEN ACCESS Large-scale salmon farming in Norway impacts the epiphytic community of Laminaria hyperborea Barbro Taraldset Haugland1,2,*, Caroline S. Armitage1, Tina Kutti1, Vivian Husa1, Morten D. Skogen1, Trine Bekkby3, Marcos A. Carvajalino-Fernández1, Raymond J. Bannister1, Camille Anna White4, Kjell Magnus Norderhaug1,2, Stein Fredriksen1,2 1Institute of Marine Research, PO Box 1870, Nordnes, 5817 Bergen, Norway 2Department of Biosciences, Section for Aquatic Biology and Toxicology, PO Box 1066, Blindern, 0316 Oslo, Norway 3Section for Marine Biology, Norwegian Institute for Water Research, 0349 Oslo, Norway 4Institute for Marine & Antarctic Studies, University of Tasmania, Taroona 7053, Tasmania, Australia ABSTRACT: Large-scale finfish farms are increasingly located in dispersive hard-bottom environments where Laminaria hyperborea forests dominate; however, the interactions between farm effluents and kelp forests are poorly understood. Effects of 2 levels of salmonid fish-farming effluents (high and low) on L. hyperborea epiphytic communities were studied by sampling canopy plants from 12 sites in 2 high-energy dispersive environments. Specifically, we assessed if farm effluents stimulated fast-growing epiphytic algae and faunal species on L. hyperborea stipes — as this can impact the kelp forest community composition — and/or an increased lamina epiphytic growth, which could negatively impact the kelp itself. We found that bryozoan biomass on the stipes was significantly higher at high-effluent farm sites compared to low-effluent farm and ref- erence sites, resulting in a significantly different epiphytic community. Macroalgal biomass also increased with increasing effluent levels, including opportunistic Ectocarpus spp., resulting in a less heterogeneous macroalgae community at high-effluent farm sites. This habitat heterogeneity was further reduced by the high bryozoan biomass at the high-effluent sites. Such changes in the epiphyte community could have implications for the faunal community that relies on the epiphytes for food and refuge. On the kelp lamina, no clear response to farm effluents was found. KEY WORDS: Laminaria hyperborea · Kelp · Epiphytes · Epiphytic community · Salmo salar · Atlantic salmon · Norway · Bryozoa 1. INTRODUCTION pogenic nitrogen emissions (Selvik & Sample 2018). However, the interactions between nutrient effluents Increased loading of nutrients from anthropogenic from fish farming and kelp forests are poorly under- activities can be a driver of ecosystem change in stood. Kelp forests face several stressors, such as sea coastal hard-bottom systems (e.g. Filbee-Dexter & urchin overgrazing, climate change, and harvesting Wern berg 2018) and has in some cases contributed to (reviewed by Steneck et al. 2002, Araújo et al. 2016). slow-growing perennial macrophytes such as kelp With more than a third of kelp forests worldwide forests being replaced by fast-growing ephemeral having been in decline over the last 50 yr (Krumhansl algae mats (e.g. Kraufvelin et al. 2006, Worm & Lotze et al. 2016) and better management of kelp forests 2006, Filbee-Dexter & Wernberg 2018). Along the being called for (Teagle et al. 2017), it is imperative to Norwegian coast, salmonid fish farming is currently discern the potential re sponse of kelp forest ecosys- the largest anthropogenic source of nutrients in tems to localised in creased nutrient loadings such as coastal waters, contributing 55% of the total an thro - fish farming effluents. © The authors 2021. 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 82 Aquacult Environ Interact 13: 81–100, 2021 Kelps (Laminariales) are important seaweeds in the aquaculture industry, both in Norway and globally, temperate coastal seas, as they provide important eco - will include further relocations to exposed, dispersive system services, e.g. supporting a diverse community coastal environments due to the observed higher resil- of associated epiphytic macroalgae (e.g. Christie et ience of soft-bottom habitats at such locations (Kee ley al. 2003) and fauna (e.g. seabirds: Fredriksen 2003; et al. 2013, 2019, Valdemarsen et al. 2015), increas- macrofauna: Christie et al. 2003, Fredriksen 2003; ingly overlapping with kelp forest habitats, making it fish: Norderhaug et al. 2005), having exceptionally critical to quantify any potential effects aqua culture high primary production and carbon assimilation effluents may have on kelp forest conditions. (Charpy-Roubaud & Sournia 1990, Steneck et al. 2002, Fish farming releases large amounts of effluents in Christie et al. 2009) with resulting kelp detritus pro- the form of dissolved nutrients and particulate organic viding a significant food source for local secondary matter (POM), which have the potential to affect kelp production (Fredriksen 2003, Norderhaug et al. 2003), forests, both directly and indirectly. The amount of in addition to subsidizing other habitats in deeper these effluents released along the Nor wegian coast waters (Krumhansl & Scheibling 2012, Pedersen et in 2018 was estimated by Husa (2019) to be 52000 t of al. 2020). Changes in our kelp forests could therefore dissolved inorganic nitrogen (DIN) (mainly ammonia; have cascading effects on ecosystem function and e.g. Sanderson et al. 2008), 7000 t of dissolved inor- services, both locally and beyond the coastal zone. ganic phosphorus (DIP) (Husa 2019), and 540000– The rapid growth of the Norwegian aquaculture 670000 t of POM (Hansen 2019). Effluent amount industry, from ca. 490000 t in 2000 (Gullestad et al. and dispersal from individual farms will depend on 2011) to ca. 1340000 t in 2018 (Fiskeridirektoratet the farm characteristics (biomass and feed levels, 2019), has made Norway one of the leading coun- related to the stage of the production cycle) and loca- tries worldwide in marine aquaculture production tion (i.e. the depth, wave exposure, and current (FAO 2018). A continuous restructuring of the industry strength and direction at the site) (Jansen et al. 2016). has followed this expansion; from small farms in shel- DIN is most likely to become a limiting nutrient for tered fjords (3000–5000 t maximum total biomass seaweed growth in undisturbed temperate coastal [MTB]) to larger farms (ca. 6000–14000 t MTB) in more waters (and DIP in freshwater systems) (e.g. Kain exposed and shallow coastal locations — locations 1989, Howarth & Marino 2006), especially in the where Laminaria hyperborea (Gunnerus) Foslie kelp warm summer months following the spring bloom forests typically thrive down to a depth of ca. 30 m (Rey 2004), which is when effluent release from fish (Kain 1979, Lüning 1990, Bekkby et al. 2009). Indeed, farms tends to be highest (Wang et al. 2012). Ephem - the majority of the Norwegian aquaculture expansion eral macroalgae, many of which grow as epiphytes over the last 10 yr can be attributed to a developing on kelp, can re spond faster to increased nutrient industry in the Frøya-Smøla archipelago (63° N) in the availability than perennial slow-growing macroalgae county of Trøndelag, an area where L. hyperborea (Pedersen & Borum 1996). Ephemeral macro algae also dominate the shallow hard-bottom habitats (Steen grow during summer, with L. hyperborea stipe and 2017, 2018). This current relocation together with lamina epiphyte biomass peaking in August (Christie larger farm-size is thus increasing the likelihood of et al. 2003), whereas the main growth season for Lami - impacts on L. hyperborea forests. In this specific area nariales is during winter and early spring (Kain 1979). (and along the central and northern coast of Norway) Hence, although fish-farm derived DIN may have a the habitat type L. hyperborea forests is currently listed positive effect on kelp, fast-growing ephemeral algae as ‘near threatened’ (Gundersen et al. 2018), making are thought to benefit more, and an increase in epi- impact-studies on this habitat type particularly rele- phytic algae growth on perennial macrophytes with vant. Few studies have examined the effect of nutrient enrichment is well documented (e.g. Rönn - salmonid fish farm effluents in exposed coastal loca- berg et al. 1992, Worm & Sommer 2000, Oh et al. 2015). tions or on kelp forests, with most previous work Some degree of epiphytic fouling on kelp laminae focussing on soft-bottom habitats (Holmer 2010) and is common in natural communities and tends to de - fjords (Kutti et al. 2007a,b). Effluents being released crease with increasing wave exposure (Jorde 1966, from the fish farms that are located at more exposed Pedersen et al. 2012). However, increased lamina sites are likely to be more dispersed (hence the epiphytic load can reduce growth and survival of allowance of larger farms compared to in sheltered kelp (Levin et al. 2002) by affecting the kelp's photo - fjords), potentially resulting in environmental re - synthetic performance and nutrient uptake (Ander- sponses being more diffuse and difficult to detect sen et al. 2011) and can reduce the light available to compared to in-fjord systems. Future expansion of the kelp by 90% (Andersen et al. 2019). Epiphytic fil- Haugland et al.: Fish farming impacts on kelp epiphytes 83 ter feeders (e.g. bryozoans and

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