Trophic ecology surrounding kelp and wood falls in deep Norwegian fjords
Introduction
In the sublittoral zone of northern Europe, kelp forests provide important habitat and primary production to a large variety of pelagic and benthic fauna, including important commercial stocks of shrimp, crabs and fish (Steen et al., 2016). In Norway, the kelp Laminaria hyperborea grows densely attached to rock, covering an area of approximately 5000 km2. There has been unprecedented loss of kelp forests in this region, with an estimated reduction of 9500 km2 since 1970. This loss has been attributed to eutrophication, catastrophic urchin grazing events, and the complex stressors associated with climate change (Christie et al., 2019; Sivertsen, 1997; Steen et al., 2016; Steneck et al., 2002). A resurgence in kelp harvesting has further reduced kelp forest coverage in the country, with mechanised operations removing an estimated 130,000 to 180,000 tonnes per year (Steen et al., 2016; Vea and Ask, 2011). Macroalgal detritus produced in kelp forests can be transported for 10s–100s of kilometres into adjacent habitats, where it increases localised stocks of organic carbon, significantly increasing secondary production (Krumhansl and Scheibling, 2012). Reduction of kelp forests in these coastal systems is likely to greatly decrease the transference of this important subsidy to deep-sea communities in Norwegian fjords (Filbee-Dexter et al., 2018; Krause-Jensen and Duarte, 2016; Krumhansl and Scheibling, 2012). Deep-sea kelp falls support a rich community of fauna, particularly sulphur-tolerant enrichment specialists such as dorvilleid polychaetes and cumaceans, as well as fish, shrimp and amphipods (Bernardino et al., 2010; Jeffreys et al., 2010; Ramirez-Llodra et al., 2016; Renaud et al., 2015; Wolff, 1979). Increased microbial respiration in the surrounding sediment and in the kelp detritus itself can also create sulphidic conditions that attract chemosynthetic bacteria and archaea that fix inorganic carbon using sulphide as an electron donor (Bernardino et al., 2010; Erk et al., 2020).
The loss of Norwegian kelp forests is contrasted by progress in terrestrial land management and reforestation, which has tripled the area of boreal forests in Norway in the past 100 years (Amundsen, 2014). With such an expansion of the forested areas that fringe deep Norwegian fjords, an increase in the transport of wood material and forest detritus to these deep-sea habitats has been shown (Lalande et al., 2020). Wood from felled coniferous trees, like those commonly found at fjord margins, enters the sea and typically takes between 10 and 17 months to become waterlogged and sink (Häggblom, 1982). When wood reaches the sea floor, it is initially thought to be inaccessible to most detritivores due to its refractory structural compounds (mostly lignin and cellulose). Nonetheless, a variety of wood-consuming fauna have been reported to consume this debris, such as wood-boring bivalves (Voight, 2015), echinoids (Becker et al., 2009), munidopsid lobsters and galatheid crabs (Hoyoux et al., 2009; Macpherson et al., 2014), as well as copepods and isopods (Amon et al., 2017). Furthermore, suspension feeders such as poriferans, hydrozoans and serpulid polychaetes use the wood as a hard substrate on which to settle (Amon et al., 2015). The organically enriched sediments created in the immediate area surrounding wood falls also support a variety of chemosynthetic fauna that are dependent on the anoxic conditions that can be produced (Bernardino et al., 2010; Bienhold et al., 2013).
Food availability in fjords is unusual among deep-sea environments due to the increased availability of nutritional sources that are comparatively rare in the open sea, such as influxes of macrophytodetritus and terrestrial organic matter (McLeod and Wing, 2009; Renaud et al., 2015; Zaborska et al., 2018). In open waters, these deep-sea ‘organic falls’ have been shown to increase beta diversity, in comparison to surrounding, unenriched sediments (Bernardino et al., 2010; Gage, 2003; McClain et al., 2016; Wolff, 1979) and are thought to act as ‘stepping stones’ that enable species dispersal between reducing habitats (Cunha et al., 2013). While there have been successful studies of megafaunal trophic ecology at organic falls using traditional techniques such as in situ observation, mouthpart morphology and gut content analysis (e.g., Hoyoux et al., 2012; Ramirez-Llodra et al., 2016; Salindeho and Johnston, 2003), the trophic response of macrofauna is much more difficult to study using these methods due to their small size. Stable-isotope analysis allows the tracing of isotopic ratios (e.g., δ13C and δ15N) within the tissue of an organism to infer diet, trophic level and primary carbon source using trophic enrichment factors (TEF) and modelling. This type of analysis has been used effectively to reconstruct the trophic ecology of mega- and macro-fauna communities surrounding organic falls in the deep-sea (Alfaro-Lucas et al., 2018; Bernardino et al., 2012; Nishimoto et al., 2009; Nygard et al., 2012; Sweetman and Witte, 2008).
In this study, four benthic landers, especially designed and fabricated at University of Hawaii at Manoa and Friday Harbor Laboratories (University of Washington), were deployed for 10 months at 530 m depth between May 2017 and March 2018 in Osterfjorden from the RV “Solvik”. Each lander contained experimental substrates (wood blocks, kelp parcels), arranged in separate bins designed to collect settling mega- and macrofauna. Stable isotope analysis (13C, 15N) was used to investigate and compare trophic relationships between wood and kelp substrates and the macrofauna that colonised them (Fig. 1).
The following hypotheses were tested
- 1.
Fauna collected from wood and kelp samples exhibit δ13C and δ15N signatures that indicate that they are assimilating wood and/or kelp.
- 2.
Fauna collected from wood and kelp samples exhibit δ13C and δ15N that reflect ontogenetic trophic changes relating to dietary preference and/or trophic level.
Few studies have investigated macrofaunal trophic structure surrounding these novel substrates in deep-sea systems (e.g., Bernardino et al., 2010; Nishimoto et al., 2009) and there are no known studies that have investigated trophic structure on wood and kelp falls in deep Norwegian fjords. With an unprecedented loss of kelp from coastal systems (Christie et al., 2019; Sivertsen, 1997; Steen et al., 2016; Steneck et al., 2002) and increased forest coverage along the Norwegian coastline (Amundsen, 2014), this work is of vital importance in assessing the future of these inadequately understood deep-sea ecosystems.
Section snippets
Study area
Osterfjorden is a fjord located 15 km north of Bergen, Norway. The fjord is 27 km in length and 1–3 km wide. It has a typical fjord geomorphology with steep rocky sides dropping off to a relatively flat muddy seabed, reaching 639 m at its deepest point. The lander deployment sites were located at a depth of ~530 m (see Harbour et al., 2021 for lander locations). The temperature at this depth was 8 °C, measured during lander retrieval in March 2018, and is expected to remain relatively constant
Food sources
Each of the three potential food sources showed distinct δ13C and δ15N signatures (Table 1 and Fig. 1). Wood was considerably more depleted in both 13C and 15N than other food sources. Kelp was the most enriched in 13C of all the food sources and was enriched in 15N relative to wood, but lower than SPOM collected from the nearby Lurefjorden (Lalande et al., 2020). Sulphur oxidising bacteria (SOB) samples were analysed and were found to be the most depleted in 13C but relatively enriched in 15N.
Faunal signatures
Discussion
The results of this study provide evidence for the assimilation of both kelp and wood material by benthic macrofauna and megafauna in a deep-sea fjord, supporting the first hypothesis. Kelp detritus appeared to be particularly important – a large percentage was found in the diets of all macro- and megafauna found on the kelp samples, as well as for some mobile fauna that were found on wood samples (Fig. 4 and Table 2). These results are similar to those of other deep-sea organic fall
Conclusion
The results of this 10-month colonisation experiment provide evidence that kelp detritus plays an important role in the trophic ecology of communities living at the Norwegian deep-sea floor, highlighting the potential importance of kelp falls in this environment. Much less evidence was found for the trophic assimilation of wood material in the fauna analysed, with the exception of xylophagid molluscs, but the precise mechanism for their hypothesised role as ecosystem engineers was not clear
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
Thank you to Caterina Coral for her help in the construction and deployment of the landers. Thank you to Emily Young and Marta Cecchetto for their help in the recovery of the landers and initial sample processing. Landers were designed and fabricated by Craig R. Smith and Mario Williamson at the University of Hawaii and Friday Harbor Laboratories, with support from US NSF grant number 1155703 (OCE Biological Oceanography Program) to CRS. We thank Iris Altamira, Pavica Srsen, Adrian Glover, and
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