Vol. 660: 53–67, 2021 MARINE ECOLOGY PROGRESS SERIES Published February 18 https://doi.org/10.3354/meps13613 Mar Ecol Prog Ser OPEN ACCESS Carbon sequestration potential increased by incomplete anaerobic decomposition of kelp detritus Morten Foldager Pedersen1,*, Karen Filbee-Dexter2,3, Nikolai Lond Frisk1, Zsuzsa Sárossy4, Thomas Wernberg1,2,3 1Department of Science and Environment (DSE), Roskilde University, Universitetsvej 1, PO Box 260, Roskilde 4000, Denmark 2Institute of Marine Research, His, Arendal 4817, Norway 3UWA Oceans Institute and School of Biological Sciences, University of Western Australia, Crawley, WA 6009, Australia 4Department of Chemical and Biochemical Engineering, Technical University of Denmark, Søltofts Plads, Kgs. Lyngby 2800, Denmark ABSTRACT: Kelps are highly productive macroalgae that form habitats along one-quarter of the worlds’ coastlines. Emerging evidence suggests that kelps have the potential to sequester carbon through the export of detritus to deep marine sinks, yet how much of this detrital carbon is rem- ineralized through grazing and microbial decomposition before it reaches these sinks remains a critical knowledge gap. We measured decay of Laminaria hyperborea detritus in shallow kelp forests (10 m) and adjacent deep fjords (300 m), and experimentally tested the effect of tempera- ture and oxygen conditions similar to those at these habitats in ex situ experiments. Initial decay rate (k) was high (−0.107 to −0.183 d−1) with 40−60% of the original carbon biomass being lost within few weeks, after which decay rates slowed down (k = −0.009 to −0.038 d−1). Temperature had little effect on the rate and extent of decomposition within the temperature range tested (4−10°C). Blade detritus decomposed almost completely in 300 d under aerobic conditions. Anaer- obic decay of both blade and stipe detritus ceased, in contrast, after 150−200 d, leaving 20−30% of the initial biomass to decompose extremely slowly or not at all. Decomposition was followed by changes in chemical composition; C:N ratios increased substantially, while mannitol and pheno- lics disappeared almost completely from the detritus matrix. Slow and incomplete anaerobic decomposition suggest that the potential for long-term burial and sequestration of kelp carbon will be enhanced if detritus is exported to nearby deep areas with permanent or periodic hypoxia near the bottom. KEY WORDS: Laminaria hyperborea · Blue carbon · Carbon sink · Burial · Refractory compounds · Macroalgae 1. INTRODUCTION increased attention (e.g. Mcleod et al. 2011, Duarte 2017, Filbee-Dexter & Wernberg 2020), and coastal Blue carbon is defined as carbon (C) captured by wetland habitats, such as seagrass meadows, marsh- marine living organisms (Nellemann et al. 2009), and lands and mangrove forests are already recognized sequestration of blue C through long-term burial is as effective long-term C sinks (Chmura et al. 2003, considered one of several criteria for identifying mar- Donato et al. 2011, Fourqurean et al. 2012). The role ine habitats as being blue C ecosystems (Lovelock & of macroalgal C in the global C budget is, in contrast, Duarte 2019). The importance of blue C has received a subject of current debate, and it remains unclear © 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 54 Mar Ecol Prog Ser 660: 53–67, 2021 whether or not macroalgal C (especially kelp) con- slowly or not at all over measurable time scales tributes substantially to C sequestration (e.g. Howard (Adair et al. 2008). Aging detritus, therefore, contains et al. 2017, Krause-Jensen et al. 2018, Smale et al. often increasing concentrations of relatively inert 2018). Any type of vegetation (terrestrial or aquatic) com pounds (Arndt et al. 2013). Decomposition rate must meet some basic criteria to contribute meaning- and the extent to which detritus decomposes are fully to C sequestration: (1) it must cover a substantial affected both by intrinsic and extrinsic (environmen- proportion of the Earth’s surface area, (2) it must tal) factors. Decomposition rate is positively corre- have a high net production per unit area and time, (3) lated with the content of nitrogen (N) and phospho- the consumption of live and dead biomass must rus (P) in the detritus, when compared across plant be small enough to minimize mineralization of C types ranging from microalgae to trees (Enríquez et through respiration at higher trophic levels, and al. 1993), but negatively correlated with the amount finally (4) part of the detritus must be in a form (or of structural cell wall compounds, such as lignin, cel- under environmental conditions) such that it decom- lulose, hemicellulose and phenolic compounds (e.g. poses slowly and/or incompletely, because that will Aber et al. 1990). Kelps and other macroalgae do not increase the probability of permanent burial in soils contain lignin, and contain less cellulose and hemi- or sediments. cellulose than vascular plants, but their cell walls Large, slow-growing perennial brown algae (kelps contain other structural compounds (e.g. alginates, and fucoids) constitute the major foundation species xylans, carrageans, agars and phenolics) which may along one-quarter of the coastlines globally (Wernberg decompose slower and/or less completely than low et al. 2019, Jayathilake & Costello 2020). Kelp systems molecular compounds (Trevathan-Tackett et al. are among the most productive habitats on Earth, with 2015). Decomposition is also affected by environ- primary production averaging 500−600 g C m−2 yr−1 mental conditions, and decay rate usually increases (Krumhansl & Scheibling 2012) and high rates exceed- with increasing temperature (Arnosti et al. 1998, ing 2000 g C m−2 yr−1 (e.g. Mann 1973, Abdullah & Pomeroy & Wiebe 2001, Price & Sowers 2004), al - Fredriksen 2004). Grazing on live kelp is typically low though the relationship between decomposition rate (0−20% of the production; Burkepile & Hay 2006), and temperature is not straightforward and may although it can be exceptionally high in disturbed depend on microbial physiology, reaction pathway(s), systems with outbreaks of herbivores (e.g. sea urchins: involved time-scales and the magnitude of tempera- Filbee-Dexter & Scheibling 2014, or range-extending ture changes (Arndt et al. 2013). Decomposition also fish: Bennett et al. 2015). Most kelp production is depends on the availability of electron acceptors thus channeled to the detrital pool within or outside (Kristensen et al. 1995, Hulthe et al. 1998). Oxygen the kelp forest (Krumhansl & Scheibling 2012), and (O2) is a powerful electron acceptor, and decomposi- these systems are therefore considered potentially tion is fast under aerobic conditions but slows down important C donors to blue carbon sediments in ad - when O2 is depleted and replaced by alternative jacent ecosystems (Hill et al. 2015, Krause-Jensen & electron acceptors (e.g. nitrate, sulfate, iron). Envi- Duarte 2016, Filbee-Dexter & Wernberg 2020). ronmental conditions that disfavor decomposition The amount of C fixed by, and stored in, live kelp (i.e. low temperature and/or anoxia) may thus delay forests can be substantial (e.g. Pedersen et al. 2012, or prevent decomposition and increase the probabil- 2020, Smale et al. 2016, Filbee-Dexter & Wernberg ity of C burial. 2020), but such storage is transient, because C-fixation Laminaria hyperborea is the dominant kelp species is balanced by equivalent losses of C through grazing in the NE Atlantic, where it is common from northern and formation of detritus, unless the range distribution Portugal in the south to the Russian Murmansk and/or total kelp biomass is increasing. The same ap- region in the north (Lüning 1990). Recent studies plies to detrital kelp C; inputs to the detrital pool will be from the UK and Norway show that L. hyperborea balanced by decomposition, unless some of the detritus produces between 280 and 500 g detrital C m−2 yr−1 becomes permanently buried under conditions that and that the majority of that detritus is delivered as disfavor mineralization through micro bial respiration. coarse particulate matter such as whole stipes, Detritus is made up by several fractions (i.e. groups blades or visible blade fragments (Pessarrodona et al. of chemical compounds) that decompose at different 2018, Pedersen et al. 2020). Some of that detritus gets rates and to a different extent. Low molecular weight trapped within the kelp forest, where it may be con- compounds, such as amino acids and simple sugars, sumed and/or shredded by detritivores (Filbee-Dex- are typically broken down quickly, whereas struc- ter et al. 2020) or decompose at relatively high tem- tural (e.g. cell wall) compounds decompose more perature and under aerobic conditions, while the Pedersen et al.: Incomplete decomposition of kelp detritus 55 remaining fractions may be exported and end up as articles/suppl/m660p053_supp.pdf) by bubbling the beach cast or, more commonly, enter adjacent, deeper water in each of these tanks with atmospheric air, −1 areas (Filbee- Dexter et al. 2018, 2020), where decom- while hypoxic conditions (0.6−0.7 mg O2 l ; Table S1) position may proceed at lower temperature and under were obtained in the remaining tanks by bubbling hypoxic conditions (Gage 2003). their water with N2. The aim of this study was to investigate decompo- Blade and stipe materials were cut into smaller sition of kelp L. hyperborea detritus within high lati- pieces using the mid 25−30 cm of the blades and the tude kelp forests and their adjacent deep fjords, top 25 cm of the stipes. A subsample of the fragments known to receive inputs of kelp detritus. We meas- (n = 8 of each) was frozen and freeze-dried for analy- ured decomposition in the laboratory under different sis of initial chemical composition. The remaining frag- temperature and O2 levels that mimicked environ- ments were weighed (initial fresh weight; initial FW), mental conditions encountered within kelp forests and placed in litterbags with a mesh size of 1 mm.