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Examining the production, export, and immediate fate of kelp detritus on open-coast subtidal reefs in the Northeast Atlantic
Author Contribution Statement: D.S. conceived the study, led manuscript development, and conducted fieldwork. A.P. and N.K. analyzed samples and data. P.M. co-conceived the study, led fieldwork, and designed the sampling program. All authors contributed to the development of the manuscript and provided significant intellectual input.
Associate editor: Catherine Ellen Lovelock
Kelp forests are highly productive coastal habitats and are emerging as important sources of organic matter for other ecosystems. Although their high rates of productivity and detritus release are expected to lead to substantial export of carbon, few studies have actually quantified rates of export or the persistence of detritus. We addressed this in eight subtidal kelp forests (Laminaria hyperborea) spanning the length (9° of latitude) of the United Kingdom. Specifically, we quantified detritus production, retention/export from source and adjacent habitats, and in situ decomposition rates. Detritus released via both dislodgment of whole plants and “May cast” shedding of old growth was highly variable between sites with greatest values recorded in our colder, northern sites. This was attributable to greater plant size biomass in northern regions, rather than plant density or dislodgement rates. On average, the annual production of kelp detritus was 4706 ± 700 g FW m−2 yr−1 or 301 g C m−2 yr−1. Low retention of detritus within the kelp forest and adjacent sedimentary habitats indicated very high rates of export (> 98% across the study). A litterbag experiment showed detritus may take > 4 months to decompose, suggesting great potential for long distance transport. Overall, our findings suggest that L. hyperborea forests export large amounts of detritus subsidies across their range, which can potentially shape the structure of distant benthic communities and constitute a relevant and largely overlooked flux in the coastal carbon cycle, which may represent an important component of natural carbon sequestration.
Highly productive coastal vegetated habitats such as kelp forests, seagrass meadows, and mangrove forests play pivotal roles in the ecology of marine ecosystems (Kathiresan and Bingham 2001; Steneck et al. 2002; Fourqurean et al. 2012). As well as providing biogenic structure and altering environmental conditions for associated communities (Attrill et al. 2000; Teagle et al. 2017), coastal vegetated habitats often exhibit high rates of primary production and biomass accumulation (Mann 1973; Duarte 2017; Smale et al. 2020). While some of the primary production is directly consumed and processed, in general most productivity enters detrital pathways (Krumhansl and Scheibling 2012), which may be exported to other ecosystems (Vanderklift and Wernberg 2008; Filbee-Dexter and Scheibling 2016). As such, detritus represents an important energy source within many coastal food webs (Mann 1988; Thresher et al. 1992; Renaud et al. 2015), provides a trophic link between spatially disconnected habitats (Vetter and Dayton 1998; Heck et al. 2008), and contributes to inshore carbon cycles (Fourqurean et al. 2012; Krause-Jensen and Duarte 2016).
Recently, macrophyte detritus has been highlighted as an important source of carbon that may be exported and transferred to sink habitats, and in doing so may play a significant role in natural carbon sequestration (Duarte et al. 2013; Krause-Jensen and Duarte 2016). As ecosystems with extensive detrital production may act as carbon “donors” to sink habitats that can bury and store carbon (Hill et al. 2015; Queirós et al. 2019), there is added incentive to effectively manage and conserve coastal vegetated habitats within the context of climate change mitigation (Nellemann et al. 2009). Despite its considerable importance, the patterns and underlying mechanisms governing detritus production and transport are poorly understood, and there is a pressing need to examine detrital pathways over broad temporal and spatial scales. Crucially, the current lack of fundamental information hinders the development of representative models of inshore carbon cycling, and predictions of how detrital subsidies will be affected by environmental change (Krumhansl and Scheibling 2012; Krumhansl et al. 2014).
Kelps, large brown seaweeds of the order Laminariales, form forest-like habitats that constitute some of the most widespread and extensive coastal ecosystems globally (Steneck et al. 2002; Teagle et al. 2017). Kelp forests are distributed from subtropical through to polar regions, extending across a quarter of the world's coastline (Wernberg et al. 2019; Jayathilake and Costello 2020). Their three-dimensional structure provides habitat and protection for many associated floral and faunal species (Teagle et al. 2017), while their high rates of primary productivity are important in fuelling coastal food webs (Krumhansl and Scheibling 2012; Pessarrodona et al. 2018). Although herbivores can remove substantial portions of kelp primary productivity (Hagen 1983; Watanabe and Harrold 1991; Ling et al. 2015), in many regions only a small fraction of kelp production is directly consumed and, instead, the majority (~ 80%) flows through detrital pathways (Krumhansl and Scheibling 2012). The vast majority of detritus is thought to be exported (Krumhansl and Scheibling 2012), although very few studies have actually quantified the amount or fraction of detritus that leaves the forest. Casual observations of kelp accumulations suggest that kelp can be transported to both adjacent (e.g., fjords, seagrass meadows) as well as distant (e.g., deep sea) habitats (Thrush 1986; Tzetlin et al. 1997), playing a vital role in linking spatially disconnected habitats via trophic subsidies (Harrold and Lisin 1989; Kirkman and Kendrick 1997; Vanderklift and Wernberg 2008). As such, kelp-derived organic matter may elevate secondary productivity and influence species distributions, abundances, and overall community structure far from its source (Duggins and Estes 1989; Bustamante and Branch 1996; Vetter and Dayton 1998; Renaud et al. 2015). Yet, the persistence of kelp detritus both in the forests and in recipient habitats remains poorly resolved.
In the Northeast (NE) Atlantic, Laminaria hyperborea (Gunnerus) Foslie 1884 is widespread and serves as the dominant habitat-former on wave-exposed rocky coastlines (Smale et al. 2013; Assis et al. 2016). Its geographical range stretches from Northern Norway and Svalbard southwards to the Iberian Peninsula (Assis et al. 2016), and it is predicted to inhabit an area > 18,000 km2 (Pessarrodona et al. 2018). L. hyperborea is a perennial stipitate kelp that can exceed 3 m in length, forming structurally complex forests that provide food and habitat to a wide range of fauna and flora (Christie et al. 2003; Teagle et al. 2018). A very small fraction of L. hyperborea primary production is thought to be consumed within the kelp forest (Norderhaug and Christie 2011), with the majority likely being exported to other habitats (Krumhansl and Scheibling 2012). As with other kelp species, the amount of detritus released and exported by L. hyperborea populations is likely to vary considerably between locations, due variation in physical factors such as wave exposure, tidal currents, and bathymetry (Vetter and Dayton 1999; Britton-Simmons et al. 2012; Filbee-Dexter and Scheibling 2012), and biological processes such as productivity (in turn linked to temperature, nutrients, and light), attachment strength, fouling by epibionts and consumption by grazers and detritivores (Saunders and Metaxas 2008; Smale and Vance 2015; Pessarrodona et al. 2018; Filbee-Dexter et al. 2020). Understanding the influence of these factors on rates of detritus release and export is relevant for predicting the effects of environmental change, such as ocean warming, increased storminess, and decreased water quality. As such, studies conducted across large spatial scales and environmental gradients can yield novel insights into carbon pathways in coastal marine ecosystems.
Despite the considerable ecological and socioeconomic importance of L. hyperborea populations along the Northwest European coastline (Vea and Ask 2011; Smale et al. 2013), information on energy flows, detritus production and export, and the contribution to inshore carbon cycling remains limited. That said, recent studies in both the United Kingdom (Pessarrodona et al. 2018) and Norway (Pedersen et al. 2020) have shown that L. hyperborea forests release considerable amounts of particulate organic carbon as detritus, while work in France has demonstrated that kelp-derived detritus can persist within coastal habitats for prolonged periods of time (de Bettignies et al. 2020; Frontier et al. 2021). Here, we expand on this recent research by examining rates and mechanisms of detritus production by L. hyperborea populations on eight open-coast subtidal reefs distributed across 9° of latitude in the United Kingdom. We quantified detritus retention within source populations and adjacent habitats, and examined the longevity of kelp-derived detritus at our study sites. The overall objective of the study was to assess how much detritus is generated by L. hyperborea populations, and what fraction of detritus is likely to be exported from open-coast subtidal reefs in the NE Atlantic.
We quantified rates of kelp detritus production, export, and breakdown within eight subtidal rocky reef habitats situated within four regions along a gradient of 9° of latitude. The four regions (north Scotland, west Scotland, south Wales, and south England) are broadly comparable with regards to wave fetch, turbidity, and nutrients, but differ in their climatology (see Smale et al. 2016, 2020 for a description of the sites and selection criteria). The two northernmost regions are, on average, 2–3°C colder than the two southernmost regions (Smale and Moore 2017). Within each region we selected two subtidal sites (randomly from a larger pool of potential sites) that were similar in terms of depth, geomorphology, and topography (Fig. 1). Paired sites differed somewhat in wave exposure, with Site “A” fully exposed to wave action and Site “B” slightly more protected, but still open-coast sites with high wave fetch values (details on wave fetch and other variables presented in Bué et al. 2020). All sites were known to support extensive kelp forest habitat dominated by L. hyperborea (Smale and Moore 2017; Pessarrodona et al. 2018). Relevant environmental data for each site are presented in Table 1 (for methodological details, see Pessarrodona et al. 2018; Smale et al. 2020).
|Site||Depth (m BCD)||Mean SST (°C)||Log wave fetch (km)||Log Chl a (mg m−3)||Echinus density (inds. m−2)||Detritivore density (inds. m−2)|
|N Scotland A||3||9.7||3.8||0.21||0.0||3.4|
|N Scotland B||4||9.8||3.5||0.26||0.5||9.0|
|W Scotland A||5||10.8||3.3||0.59||0.1||3.6|
|W Scotland B||4||10.7||3.1||0.65||0.1||11.8|
|S Wales A||5||11.7||3.7||0.43||0.2||1.1|
|S Wales B||4||11.8||3.5||0.43||0.3||5.3|
|S England A||3||12.4||4.1||0.28||0.1||3.0|
|S England B||4||12.4||3.5||0.28||0.0||1.7|
Density and biomass
To characterize the structure of L. hyperborea populations, SCUBA divers carried out surveys at each site in spring (April/May) 2015 and 2016 and summer (August/September) 2014, 2015, and 2016. During each sampling event, the density of L. hyperborea was quantified by haphazardly placing eight replicate 1-m2 quadrats on hard bedrock and recording the number of holdfasts of mature canopy-forming plants (plants defined sensu Bolton 2016). The density of urchins (exclusively Echinus esculentus) was also recorded. In addition, during three sampling events (spring 2015, summer 2014 and 2016), 15 mature canopy-forming L. hyperborea plants were randomly sampled by cutting them beneath the holdfast and returning them to the laboratory to measure fresh weight (FW). Sampled plants were spatially dispersed across the site and collected from within the kelp forest (i.e., >3 m from the reef's edge).
Detritus production in L. hyperborea results from three processes: (i) dislodgment of entire plants, (ii) loss of the lamina produced during the previous season of growth, which is usually cast between March and May and results in an acute pulse of detrital material known as the “May cast,” and (iii) chronic erosion of the lamina occurring throughout the year (Lüning 1969; Kain 1979; Pessarrodona et al. 2018). To determine how much detritus was produced via loss of entire kelp plants, we quantified dislodgement rates of canopy-forming plants. At each study site, three circular plots (~ 2 m diameter) were established and within each plot 15 adult kelps with distinct holdfasts (no fused holdfasts) were tagged by fastening a cable tie sheathed in fluorescent latex surgical tubing around the base of the stipe, as per de Bettignies et al. (2013). Plots were marked with a labeled clump weight to aid relocation and to identify specific replicate plots and tagged plants. Plots were established and revisited ~ 6 months later to record the number of remaining tagged plants. To quantify “summer” dislodgement rates, plots were established in March/April, plots for “winter” rates were established in September. This approach allowed for a quantification of loss rates of whole plants over both winter and summer, as well as an annual average. Loss rates were then applied to mean density and plant biomass values for each site to estimate the amount of FW lost through dislodgement.
To quantify the detrital input resulting from the “May cast,” 12–22 collars of old growth still attached to canopy-forming L. hyperborea plants were randomly selected, carefully removed, and subsequently weighed. Sampling of old growth collars was conducted in April/May 2015, just prior to shedding of tissue by most plants. Quantifying detritus release via the shedding of old growth collars was important for this species, as this mechanism underpins the majority of detritus production in some populations (Pedersen et al. 2020). The mean biomass of growth collars was then multiplied by the mean density of canopy forming plants at each site to estimate detritus production via this process. Finally, detritus is also produced by chronic erosion of lamina tissue, occurring mostly at the distal tips. This was not directly measured here but from previous work on L. hyperborea populations it is conservatively estimated at 20% of total annual detritus production (Pessarrodona et al. 2018; Pedersen et al. 2020).
Examining the immediate fate of kelp detritus
To investigate the retention and export rates of kelp detritus, SCUBA divers surveyed the reef habitat and adjacent soft-bottom habitat for detrital accumulation. In May and September, eight replicate 1-m2 quadrats were randomly placed on the reef within the kelp forest and all detached detritus was collected in calico bags and returned to the laboratory. Bags were placed over the detritus and all material (including detritivores) was carefully collected. Quadrats were placed at least 4 m part from one another, were representative of the reef structure, and included both reef flats and topographically complex features (e.g., crevices, gullies) where present. In the few cases where detrital fragments were only partially within quadrats, they were retained and sampled if more than ~ 50% of the fragment area was observed within the quadrat boundary. In the laboratory, the vast majority of detritus was identifiable as L. hyperborea (which included a mix of entire plants, stipe/holdfasts, old growth collars, and smaller blade fragments), with a relatively small amount of red algal detritus, most likely from epiphytic assemblages on kelp stipes (King et al. 2021), and some unidentifiable brown fragments. As such, detritus was coarsely sorted before weighing L. hyperborea detritus to obtain biomass values. Before sorting, material was passed through a 0.5-mm sieve and all associated macrofauna were retained and enumerated. The abundances of urchins and detritivores (which were numerically dominated by amphipods and gastropods) are provided as contextual information to characterize conditions at the sites and are presented in Table 1.
In addition, at each site triplicate 25 × 1-m belt transects were conducted from the edge of the reef into adjacent soft-bottom habitats. Divers randomly selected a starting point from the reef's edge and an approximate compass direction (away from the reef) and collected all detritus present within the sampling area. Soft-bottom habitats adjacent to kelp forests varied in substrate type from fine sand to shingle, and depth ranged from ~ 3 to 12 m (below chart datum). Again, detritus was immediately returned to the laboratory, sorted, and weighed. Given that only the initial 25 × 1 m from the reef was sampled, the full areal extent and complexity of adjacent habitats was not examined and, as such, retention rates were considered a coarse estimate. In both sampling approaches, divers hand-collected detritus fragments visible on the surface of the substratum; boulders and stones were not turned and fragments too small to see or collect by hand were not sampled. While, intuitively, this approach potentially under sampled smaller fragments, the vast majority of detrital biomass was sampled.
Finally, to examine the persistence of L. hyperborea detritus in these habitats, we conducted a decomposition experiment using litter bags. At each site, we deployed three litter bags (heavy-duty nylon bags, mesh size ~ 2 mm) packed with 500 g (FW) of freshly collected L. hyperborea material (laminae were first cut into strips of comparable size, approximately 20 × 10 cm) collected locally from each site. This mesh size allowed most macrodetritivores access to the kelp detritus while minimizing loss of lamina fragments. The three litter bags were secured to heavy weights and deployed within the kelp forest. The bags were deployed in spring (May 2016) and retrieved in autumn (September 2016), after a period of 15–16 weeks (all bags except a single replicate at the fully exposed site in S Wales were recovered). Any remaining material was carefully removed and reweighed to calculate decomposition rates.
Conversion to dry weight and carbon
All FW biomass values derived from the methods described above were converted to dry weight (DW) and subsequently to carbon (C) biomass using conversion factors. FW was converted to DW using a factor of 0.20, which was reported previously by Smale et al. (2020) and Pessarrodona et al. (2018) based on over 400 measurements of this relationship from different sections of kelp plants collected from these study sites. DW was then converted to g C using a factor of 0.31 based on measurements reported in Pessarrodona et al. (2018) and comparable to results from other studies presented in Smale et al. (2016).
Variability in kelp population structure (density, biomass), dislodgement rates (summer/winter dislodgement), detritus production (via dislodgement and shedding of May cast), and quantities of kelp detritus in within and in adjacent kelp forest habitats was determined using univariate permutational ANOVA (PERMANOVA) implemented using the “adonis” command in the r package “vegan.” Models consisted of Region (four levels; N Scotland, W Scotland, S Wales, S England) and Region(Site) (two levels; Site A and Site B nested within Region).
Kelp population structure
The density of canopy-forming L. hyperborea plants did not differ between regions but exhibited significant site-level variability (Table 2). Greatest within-region variability was observed in S England where the density of canopy-forming plants ranged from 8.1 ± 2.7 inds. m−2 (S England B) to 10 ± 3.2 inds. m−2 (S England A). These sites also represented the highest and lowest estimates of density across all of our study sites (Fig. 2A).
|Density (m2)||Biomass (g FW ind−1)||Summer dislodgement (%)||Winter dislodgement (%)||Dislodgement (g FW m−2 yr−1)||May cast (g FW m−2 yr−1)|
|Within spring (g FW m−2)||Within autumn (g FW m−2)||Adjacent spring (g FW m−2)||Adjacent autumn (g FW m−2)||Remaining (%)|
The FW biomass of plants differed between regions (Table 2). FW biomass of N Scotland (1777 ± 428 g FW) and W Scotland (1640 ± 508 g FW) was significantly greater than the southern regions of S Wales (478 ± 229 g FW) and S England (719 ± 217 g FW). Northern regions were similar to one another while S England was significantly greater than S Wales. FW biomass also exhibited significant site-level variability. Here, the greatest within-region variability was observed in W Scotland where FW biomass ranged from 1274 ± 348 g FW (W Scotland B) to 2006 ± 356 g FW (W Scotland A) (Fig. 2B).
Dislodgement of whole plants did not differ between regions or sites in summer or winter (Table 2). In summer, dislodgement of whole plants ranged from 0% to 33.3% per plot, with average rates per site ranging from 6.6% ± 6.6% (W Scotland A) to 17.8% ± 3.8% (S England B) (Fig. 2C). In winter, dislodgement rates ranged from 0% to 40% per plot, with site averages ranging from 17.7 ± 3.8 (N Scotland B) to 22.2 ± 10.2 (S England A) (Fig. 2D).
When rates were applied to average plant density and biomass values, marked differences between regions and sites were observed (Table 2). Here, detritus production in the northern regions of N Scotland (2531 ± 831 g FW m−2 yr−1) and W Scotland (2031 ± 719 g FW m−2 yr−1) was significantly greater than the southern regions of S Wales (775 ± 257 g FW m−2 yr−1) and S England (1154 ± 504 g FW m−2 yr−1). Northern regions were similar to one another while S England was significantly greater than S Wales. Detrital production also exhibited significant site-level variability. The greatest within-region variability was observed in W Scotland where estimates ranged from 2487 ± 640 g FW m−2 yr−1 (W Scotland A) to 1574 ± 459 g FW m−2 yr−1 (W Scotland B) (Fig. 2E).
For detritus generated by the “May cast” shedding of the old growth collar, estimates varied between regions and exhibited site-level variability. All regions were significantly different from one another with greatest “May cast” detritus production observed in N Scotland (3998 ± 1300 g FW m−2 yr−1) and the least in S Wales (901 ± 335 g FW m−2 yr−1). The greatest within-region variability was observed in W Scotland where estimates ranged from 1241 ± 359 g FW m−2 yr−1 (W Scotland B) to 2805 ± 722 g FW m−2 yr−1 (W Scotland B) (Fig. 2F).
We combined our values for detritus production from dislodgement of whole plants, May cast shedding and chronic erosion yields estimates of total annual detritus production for each site (Table 3). These estimates ranged from 1637 ± 402 g FW m−2 yr−1 (S Wales B) to 8878 ± 2195 g FW m−2 yr−1 (N Scotland A), with a study-wide average of 4706 ± 700 g FW m−2 yr−1 (or 301 g C m−2 yr−1).
|Site||Total annual detritus||Detritus retained||Detritus exported||Percent exported|
|N Scotland (A)||8.87 (568)||0.02 (1.5)||8.86 (567)||99.7|
|N Scotland (B)||7.45 (476)||0.06 (3.9)||7.39 (472)||99.2|
|W Scotland (A)||6.62 (423)||0.09 (5.5)||6.53 (418)||98.7|
|W Scotland (B)||3.52 (225)||0.10 (6.1)||3.43 (219)||97.3|
|S Wales (A)||2.55 (163)||0.01 (0.6)||2.55 (163)||99.7|
|S Wales (B)||1.63 (104)||0.10 (6.1)||1.54 (98)||94.1|
|S England (A)||3.52 (225)||0.02 (1.5)||3.50 (223)||99.3|
|S England (B)||3.47 (222)||0.05 (3.2)||3.42 (219)||98.6|
The fate of kelp detritus
The amount of detritus recorded within kelp habitats did not differ between regions or sites (Table 2). Instead, we observed high levels of variability between replicate quadrats in both spring and autumn. In spring, site-level averages ranged from 0 ± 0 g FW (S Wales A) to 110 ± 126 g FW (W Scotland B) (Fig. 3A), while in autumn averages ranged from 5 ± 14 g FW (S England B) to 72 ± 135 g FW (N Scotland B) (Fig. 3B). Across both sampling events, the occurrence of detritus within quadrats ranged from 25% (N Scotland A) to 50% (W Scotland B).
The amount of detritus recorded in adjacent soft-bottom habitats differed between regions, and there was considerable site-level variability in both spring and autumn. In spring, S Wales (2773 ± 3622 g FW m−2) was significantly greater than N Scotland (20 ± 33 g FW m−2) and S England (256 ± 236 g FW m−2) (Table 2). However, S Wales was also characterized by the greatest amount of within region variability which ranged from 53 ± 61 g FW m−2 (S Wales A) to 5493 ± 3256 g FW m−2 (S Wales B) (Fig. 3C). In autumn, values at W Scotland (2180 ± 2341 g FW m−2) were significantly greater than N Scotland (106 ± 43 g FW m−2). However, the greatest site-level variability was observed in W Scotland, which ranged from 4233 ± 1021 (W Scotland A) to 126 ± 117 (W Scotland B) (Fig. 3D). In general, the amount of detritus observed within or adjacent to kelp habitats was greater in spring than autumn, although overall values were low in both sampling periods. Across both sampling events, the occurrence of detritus within transects ranged from 67% (recorded at three sites) to 100% (recorded at five sites).
By combining our estimates of total detritus production with values for detritus retention in both the kelp forest and the adjacent habitat (averaged across sampling periods), we cautiously estimated the amount of detritus that is exported from these populations (Table 3). At all sites, > 94.0% of detritus was exported or rapidly turned over, with a study-wide average of 98.3%.
Our simple litter bag experiment showed that kelp detritus can persist at these dynamic open-coast sites for several months. After 15–16 weeks the amount of kelp detritus remaining in the mesh bags ranged from 0% to 79%, with site-level averages ranging from all detritus being lost 0% ± 0% (S Wales A) to 50% ± 33% (S England B). There was a regional effect with remaining detritus at S England (49% ± 23%) significantly larger than all other regions (Fig. 4).
While our understanding of mechanisms and rates of detritus production in kelp forests is improving (Krumhansl and Scheibling 2011; de Bettignies et al. 2013; Pessarrodona et al. 2018; Pedersen et al. 2020), rates of export and persistence of that detritus remain poorly known. Our study has shown that detritus production by L. hyperborea is substantial and that very little detritus (< 2% on average) is retained within either kelp forests or adjacent habitats. However, this estimate does not take into account local consumption by detritivores which, if significant, would reduce the biomass of exported detritus. We recorded low abundances of consumers within detritus accumulations, and larger macro-detritivores (particularly sea urchins) are generally found at low very low abundances across these sites (Pessarrodona et al. 2018; Smale 2020). Given that recent work conducted in this system showed that consumption of kelp detritus by amphipod and gastropod consumers is ~ 0.01 and ~ 0.2 g per day (DW), respectively (Gilson et al. 2021b), and observed densities of detritivores were low, we suggest that local in situ consumption rates are relatively low (but require formal testing). Therefore, while a small fraction of this detritus may be consumed locally, it is highly likely that the vast majority is exported to other habitats and ecosystems.
Across our study, the average annual production of particulate matter as kelp detritus was 4706 ± 700 g FW m−2 yr−1 or 301 g C m−2 yr−1. This estimate is likely to be broadly representative of L. hyperborea populations across its range in the NE Atlantic, as our northern populations are similar in structure to those in Norway and our southernmost populations akin to those in France and Spain (Jupp and Drew 1974; Pedersen et al. 2012; Pessarrodona et al. 2018). These findings support the emerging role of L. hyperborea forests as key donors of organic matter to a range of recipient habitats in the NE Atlantic (Smale et al. 2018; Ramirez-Llodra et al. 2021; Gilson et al. 2021a), and advance our understanding of rates of detrital release, export, and persistence along dynamic wave-exposed coastlines dominated by extensive kelp forests.
We recorded high rates of detritus export on our open-coast, shallow subtidal sites, as evidenced by very low detritus retention rates on the reef or within adjacent habitats. Given that most of these reefs are exposed to the highly dynamic NE Atlantic Ocean, which is characterized by periods of intense wave action throughout much of the year (Woolf et al. 2002), it is not unexpected that the vast majority of kelp detritus was exported from source populations. Some of these sites also experience moderate tidal flows at times (Smale et al. 2016), which again could resuspend and translocate detritus particles. Intuitively, hydrodynamic processes at these sites play an important role in exporting detritus, as has been shown in other systems (Vetter and Dayton 1999).
Detrital retention rates were minimal and highly variable, both within and between sites. On the reef within the kelp forest, highest values of detrital accumulation were observed within heterogeneous rugose features, such as gullies and overhangs, with very limited retention on reef platforms. Similarly, patches and sites with greater heterogeneity and rugosity in adjacent habitats, due to boulders or sand bars, for example, tended to accumulate more detritus (D. A. Smale and P. J. Moore pers. observ.), although some detritus was present in the majority of transects. In deeper areas, detritus accumulation is also dependent on small-scale topographical features, occurring mostly on substrate depressions and flat bottoms (Filbee-Dexter and Scheibling 2016), while at larger spatial scales fjords and canyons act as detritus aggregation and transport channels (Vetter and Dayton 1998). Given that macroalgae generally grow attached to hard substrates, kelp forests have no capacity for partial burial of detritus as a retention mechanism, in contrast to seagrass beds or saltmarshes, for example (Sousa et al. 2010; Tanaya et al. 2018). It is likely that a combination of hydrodynamics, topographical features, detritus characteristics, and the morphology and habitat preference of L. hyperborea led to extremely low rates of detrital retention and high rates of export.
The ultimate fate of exported kelp detritus is largely unknown (Fig. 5) and, while some may be consumed by local detritivores (Krumhansl and Scheibling 2012), it is likely that a substantial amount is transported to other coastal habitats including sandy beaches (Orr et al. 2014) and seagrass meadows (Wernberg et al. 2006), while some may be transported to offshore sedimentary habitats (Britton-Simmons et al. 2012; Queirós et al. 2019) or deep-water canyons or fjords (Vetter and Dayton 1998; Filbee-Dexter et al. 2018). The distance and direction of transport will be largely dependent on coastal hydrodynamic and larger-scale oceanographic processes, but in some cases macroalgal detritus has been recorded hundreds or even thousands of km from source populations (Nikula et al. 2010; Fraser et al. 2018; Kokubu et al. 2019; Macaya et al. 2020). The potential for long-distance transport will also depend on characteristics of the detritus itself, particularly particle size and density, buoyancy, and longevity (Hyndes et al. 2014; Wernberg and Filbee-Dexter 2018; Tala et al. 2019). Particles of L. hyperborea, detritus are often fairly large, dense, and negatively buoyant (e.g., whole stipes, May cast growth collar) which may limit their potential for dispersal compared with kelp species that may generate buoyant detritus (e.g., Macrocystis pyrifera, Nereocystis leutkeana). Our results show that detrital fragments can persist in highly dynamic coastal environments for several months, with some material remaining in the litter bags after ~ 4 months in situ at five of our eight sites. Interestingly, we did not record any consistent patterns related to wave exposure or temperature, even though high water flow enhances mechanical breakdown of detritus (dos Santos Fonseca et al. 2013) and higher water temperatures are known to increase kelp degradation rates (Vandendriessche et al. 2007; Rothäusler et al. 2009). Rather, the lowest rates of decomposition were observed in our warmest region (i.e., S England), suggesting that local factors such as small-scale hydrodynamics, sediment type and mobility, food availability, and the composition of detritivore and microbial assemblages are influential in determining rates of detrital breakdown.
Recent work on L. hyperborea detritus held under different conditions has also demonstrated that fragments can persist for many months and that biomass may even increase, given favorable conditions (de Bettignies et al. 2020; Frontier et al. 2021). Although particle tracking models for kelp detritus have yet to be developed for this species in this region, models that exist for other types of dispersive particles suggest that the potential for transport over this timescale is significant (Whomersley et al. 2018; Coscia et al. 2020). Moreover, work in Norway has documented kelp detritus accumulations at depths of > 400 m (Filbee-Dexter et al. 2018), detected kelp-derived carbon in deep sediments (Abdullah et al. 2017; Frigstad et al. 2021) and developed particle tracking models for detritus that predict cross-shelf transport distances of up to 200 km (Filbee-Dexter et al. 2020). Clearly, there is great potential for long-distance transport and long-term storage of particulate organic carbon released as kelp detritus, but empirical evidence is lacking and warrants focused research (Krause-Jensen et al. 2018; Smale et al. 2018).
For the populations studied here, the three mechanisms of detritus production (i.e., dislodgment of whole plants, the May cast of old growth collar and chronic erosion of blade tissue) were all important contributors to total production (with the latter assumed as a proportion of total detritus). With regards to dislodgement of entire plants, average rates of loss across the entire study were 13.0% ± 3.4% and 19.7% ± 1.7% through summer and winter, respectively. Although dislodgement rates of this magnitude would likely result in some thinning of canopies, they would not cause wide-scale canopy loss or deforestation, despite inshore significant wave heights > 8 m occasionally recorded near our study sites (Smale and Vance 2015). Clearly, L. hyperborea is highly resistant to wave action and can tolerate extremely wave-exposed conditions (Burrows 2012), more so than most other kelp species in the region (Smale and Vance 2015). Even so, we did record higher dislodgement rates in winter, which coincides with periods of greater wave heights and periods, and a higher probability of extreme wave action (Dodet et al. 2010). Work from elsewhere has shown that intense physical disturbance during winter storms can play a key role in generating and transporting macrophyte detritus to other habitats (Ebeling et al. 1985; Filbee-Dexter and Scheibling 2012). For example, a large decline in canopy cover and a rapid increase in detrital deposits below the kelp zone was recorded after Hurricane Earl struck Nova Scotia (Filbee-Dexter and Scheibling 2012). The highly dynamic wave-impacted nature of the western UK coastline is likely to promote both the production and transport of kelp detritus.
Despite relatively low loss rates, the biomass of detritus generated by dislodgment was comparatively high, due to the high mass of entire plants that include holdfasts and stipes as well as blades. The greatest production of detritus via dislodgement was recorded in N Scotland, which supports large-sized kelp plants and exhibited relatively high rates of plant loss. Previous work has shown that canopy-forming plants at our colder northern sites attain a much greater size and biomass, and that kelp populations are considerably more productive, compared with our warmer southern sites (Smale et al. 2016; Pessarrodona et al. 2018; King et al. 2020). This is likely a combination of lower temperatures and increased light availability at some northern sites (Smale et al. 2020). As such, with comparable dislodgement rates and plant densities between regions, detritus production via dislodgement was consequently greater for our northernmost populations. Like other studies on stipitate kelp species (e.g., de Bettignies et al. 2013), we did not observe greater detritus production from dislodgment at our more wave-exposed sites, which suggests that other mechanisms are more important drivers of dislodgment. For example, kelps exhibit high morphological plasticity and may exhibit a degree of local acclimatization to wave exposure by displaying drag-reducing (e.g., narrow blade) and strength increasing (e.g., large holdfast) traits, as observed in other kelp populations (Wernberg and Thomsen 2005; Bekkby et al. 2014).
Across the study, the “May cast” of old lamina tissue resulted in an average detrital input of 2.14 ± 0.13 kg FW m−2 or 133 ± 81 g C m−2. The total biomass of detrital material released at the northernmost regions was more than twice than the produced at the two southern regions. This variation was primarily related to the higher biomass of individual plants, rather than differences in plant density, as kelp in the northernmost regions were generally larger and formed more sizable collars of old growth. Detritus production associated with the “May cast” was typically greatest at the most wave-exposed site within each region (the only exception being S England), which was a consequence of generally higher canopy density and biomass under more exposed conditions. These findings align with previous studies reporting greater canopy biomass at wave-exposed sites and within higher latitude, colder regions (Rinde and Sjøtun 2005; Pessarrodona et al. 2018).
Contemporary environmental change poses a threat to L. hyperborea forests and the ecosystem services they provide (Smale et al. 2013). For example, recent ocean warming trends have, and will continue to, caused reductions in the spatial extent and abundance of L. hyperborea populations at its warm equatorward range edge on the Iberian Peninsula (Tuya et al. 2012; Voerman et al. 2013; Assis et al. 2016). Although range expansions into Arctic regions as ice-free coastal areas become favorable for growth may, to some extent, compensate for losses at lower latitudes (Krause-Jensen and Duarte 2014; Assis et al. 2016), it is evident that the magnitude of carbon flows through these habitats and the wider importance of kelp populations to inshore carbon cycling will be impacted by oceanic climate change (Pessarrodona et al. 2018; Pessarrodona et al. 2019; Smale 2020).
Kelp detritus is of considerable ecological importance to coastal temperate ecosystems, both as a direct resource and as a spatial subsidy (Duggins and Estes 1989; Bustamante and Branch 1996; Kaehler et al. 2006), yet processes underpinning the production and fate of kelp detritus remain poorly resolved (Krumhansl and Scheibling 2012). Our study has highlighted the importance of carbon flow through kelp forests in the NE Atlantic, which is characterized by high rates of detritus production and export and a persistence that indicates potential for long-distance transport (Fig. 5). Although the majority of kelp-derived particulate carbon is likely to be remineralized relatively quickly, if even a small fraction is transported to and stored within sink habitats (e.g., seagrass meadows, salt marshes, and deep-water bodies or sediments) it will likely represent a significant and thus far mostly overlooked contribution to inshore carbon cycling (Krause-Jensen and Duarte 2016; Smale et al. 2018; Queirós et al. 2019). By acting as a Blue Carbon “donor” (Hill et al. 2015), kelps may play an important role in natural carbon sequestration and, as such, climate change mitigation. However, most Blue Carbon practices, such as accounting, management, and protection, currently do not include macroalgal-derived carbon as it is not stored locally within source habitats, which may underestimate the perceived sequestration capacity of marine ecosystems and hinder effective management (Santos et al. 2021).
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D.S. is supported by a UKRI Future Leaders Fellowship (MR/S032827/1). P.M. is supported by a NERC-Newton Fund grant NE/S011692/2. We thank all participants of “Team Kelp (UK)” field expeditions (2014–2020), and Sula Divers, In Deep, NFSD and Tritonia dive teams for technical support.
Conflict of interest