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The establishment of the invasive non-native macroalga Sargassum muticum in the north of Scotland

Published online by Cambridge University Press:  13 September 2023

Andrew Want Open the ORCID record for Andrew Want [Opens in a new window] ,
Iveta Matejusova  and
Jenni E. Kakkonen
Andrew Want*
Affiliation:
Heriot-Watt University – Orkney Campus, Stromness, UK Energy and Environment Institute, University of Hull, Hull, UK
Iveta Matejusova
Affiliation:
Marine Scotland Science, Aberdeen, UK
Jenni E. Kakkonen
Affiliation:
Orkney Islands Council – Marine Services, Kirkwall, UK
*
Corresponding author: Andrew Want; Email: a.want@hull.ac.uk
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Abstract

The spread of the brown seaweed Sargassum muticum is one of the best documented invasions of a non-native marine species. Observation of a potentially established population of S. muticum in the Orkney Islands archipelago, located off the northern coast of Scotland, was reported by recreational snorkellers in 2019 and 2020. The present study summarises a focussed investigation to confirm its presence and current local distribution, using data from 46 survey sites monitored as a part of the Orkney Islands Council Harbour Authority monitoring programme. Findings in this study represent the most northerly record of an established population of S. muticum in the United Kingdom, extending the latitudinal range in this country by 1.44° (159 km) northwards, and indicate only localised presence of this species. Analysis of a partial cytochrome oxidase I gene sequence confirmed the visual species identification. Possible vectors of introduction, gaps in the geographic range, local ecological and economic impacts, and the potential ameliorating factor of deep rockpools on wave exposed shores for S. muticum are discussed.

Keywords

British waterscytochrome oxidase Iinvasive speciesmacroalgaerock poolsSargassum muticum

Information

Type
Marine Record
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 103 , 2023 , e69
Creative Commons
Creative Common License - CCCreative Common License - BY
This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution and reproduction, provided the original article is properly cited.
Copyright
Copyright © The Author(s), 2023. Published by Cambridge University Press on behalf of Marine Biological Association of the United Kingdom

Introduction

Sargassum muticum (Yendo) Fensholt, commonly known as Wireweed, is a monoecious brown macroalga belonging to the order Fucales (Norton, Reference Norton1976). One of its distinguishing characteristics is the presence of numerous small air bladders that provide buoyancy to the fronds (Rueness, Reference Rueness1989). In its native Japanese waters, S. muticum fronds typically grow to 1–1.5 m (Rueness, Reference Rueness1989), from littoral to shallow sublittoral depths (Norton, Reference Norton1977; Knoepffler-Peguy et al., Reference Knoepffler-Peguy, Belsher, Boudouresque and Lauret1985; Stæhr et al., Reference Stæhr, Pedersen, Thomsen, Wernberg and Krause-Jensen2000). Outside of its native range, S. muticum has low substrate specificity, being commonly found on hard natural and artificial surfaces, as well as attached to shell fragments or coarse sediments, and embedded in mud (Critchley et al., Reference Critchley, Farnham and Morrell1983; Knoepffler-Peguy et al., Reference Knoepffler-Peguy, Belsher, Boudouresque and Lauret1985; Tweedley, Reference Tweedley, Jackson and Attrill2008). This seaweed is tolerant to wide ranges of temperature (−1 to 25°C) and salinity (Norton, Reference Norton1977; Steen, Reference Steen2004), although some studies indicate reproductive failure following prolonged exposure to salinities below 15‰ (Kjeldsen and Pinney Reference Kjeldsen, Pinney and Nisizawa1972; Steen Reference Steen2004). Sargassum muticum can be found on sheltered to moderately exposed shores (Deysher and Norton, Reference Deysher and Norton1982; Sanchez et al., Reference Sanchez, Fernandez and Arrontes2005), but requires protection from extreme wave action (Critchley et al., Reference Critchley, Farnham and Morrell1983). At small scales, abundance of S. muticum correlates with differences in depth and substrate (Stæhr et al., Reference Stæhr, Pedersen, Thomsen, Wernberg and Krause-Jensen2000).

Pathways/vectors of spread and establishment

Two main means of natural dispersal are utilised by S. muticum: release of planktonic propagules into the water column, and breaking free of floating vegetative fronds, assisted by the air-bladders (Rueness, Reference Rueness1989). The former means may result in dispersal over relatively limited range, typically on a scale of metres, with germlings detected up to 1.3 km from reproductively active adults (Deysher and Norton, Reference Deysher and Norton1982); the latter means may result in dispersal over extensive distances on a scale of tens or even hundreds of kilometres (Deysher and Norton, Reference Deysher and Norton1982). In both strategies, the direction and speed of wind and currents drive the dispersal range (Deysher and Norton, Reference Deysher and Norton1982; Stæhr et al., Reference Stæhr, Pedersen, Thomsen, Wernberg and Krause-Jensen2000).

In addition to rafting or floating of entire plants or detached fragments (Kraan, Reference Kraan2008), long distance dispersal of S. muticum can be facilitated through anthropogenic vectors (Davison, Reference Davison2009). Evidence suggests that the transportation of shellfish for aquaculture, e.g. oysters, may be one of the primary means of introduction of S. muticum (Deysher and Norton, Reference Deysher and Norton1982; Critchley, 1983). Other potential vectors may include entanglement of fragments in anchor chains and steering gear (Harries et al., Reference Harries, Harrow, Wilson, Mair and Donnan2007), attachment to ship hulls or transportation in ballast water (Kraan, Reference Kraan2008). Hulls and ballast tanks, however, may not be suitable for the transport of germlings of S. muticum (Deysher and Norton, Reference Deysher and Norton1982; Engelen et al., Reference Engelen, Serebryakova, Ang, Britton-Simmons, Mineur, Pedersen, Arenas, Fernandez, Steen, Svenson and Pavia2015).

Impacts on local biodiversity and potential economic impacts

In its native waters, S. muticum is an unremarkable member of the littoral community (Rueness, Reference Rueness1989). However, in introduced regions, Sargassum tends to form dense beds that may replace native vegetation (Druel, 1973; Farnham et al., Reference Farnham, Fletcher and Irvine1973; Rueness, Reference Rueness1989), resulting in reduced local biodiversity. The growth rate of this alga has been shown to far exceed that of other fucoids in comparative studies (Norton, Reference Norton1977; Nicholson et al., Reference Nicholson, Hosmer, Bird, Hart, Sandlin, Shoemaker and Sloan1981) and individuals have been recorded up to 16 m in length (Vaz-Pinto et al., Reference Vaz-Pinto, Rodil, Mineur, Olabarria, Arenas, Pereira and Neto2014). The expansive canopy-forming capacity of rapidly growing S. muticum may help outcompete other key macroalgae for space and light, producing systemic impacts on the local community and habitats (Ambrose and Nelson, Reference Ambrose and Nelson1982; Cosson, Reference Cosson1999; Stæhr et al., Reference Stæhr, Pedersen, Thomsen, Wernberg and Krause-Jensen2000; Sanchez et al., Reference Sanchez, Fernandez and Arrontes2005; Engelen et al., Reference Engelen, Serebryakova, Ang, Britton-Simmons, Mineur, Pedersen, Arenas, Fernandez, Steen, Svenson and Pavia2015). Dense stands may also reduce water motion (Deysher and Norton, Reference Deysher and Norton1982).

The rapid growth and success of S. muticum in introduced waters may be an example of the enemy release hypothesis (Elton, Reference Elton1958), wherein S. muticum as an introduced non-native species (NNS) is released from certain pressures that impact native seaweeds. Indeed, studies of macroalgal grazers in Portugal indicated preference for feeding on native seaweed compared with S. muticum (Engelen et al., Reference Engelen, Henriques, Monteiro and Santos2011). Furthermore, recent studies of the microbiome associated with S. muticum reveal this species may benefit by being a generalist host (Aires et al., Reference Aires, Kläui and Engelen2022). Ready replacement of its microbiome in new geographic regions may be another means by which S. muticum is able to spread so effectively.

The establishment of S. muticum in a new habitat appears to reduce the abundance of the existing dominant seaweed, especially ‘leathery’ macroalgae (Viejo et al., Reference Viejo, Arrontes and Andrew1995; Stæhr et al., Reference Stæhr, Pedersen, Thomsen, Wernberg and Krause-Jensen2000; Engelen et al., Reference Engelen, Serebryakova, Ang, Britton-Simmons, Mineur, Pedersen, Arenas, Fernandez, Steen, Svenson and Pavia2015). This replacement of dominance may extend to other photosynthesising species, such as seagrass (den Hartog et al., Reference den Hartog1997; Tweedley, Reference Tweedley, Jackson and Attrill2008). Impacts to local biodiversity may result in fewer species and reduced ecosystem complexity (Stæhr et al., Reference Stæhr, Pedersen, Thomsen, Wernberg and Krause-Jensen2000; Engelen et al., Reference Engelen, Serebryakova, Ang, Britton-Simmons, Mineur, Pedersen, Arenas, Fernandez, Steen, Svenson and Pavia2015). Conversely, studies in Spanish waters report increased biodiversity of opportunistic epiphytic species and primary productivity following establishment of S. muticum (Sanchez et al., Reference Sanchez, Fernandez and Arrontes2005); the potential changes to ecosystem services, as a consequence of these changes, could not be ascertained.

From an economic perspective, biofouling of netting and other gear is a concern to fishers (Critchley et al., Reference Critchley, Farnham and Morrell1986). Drift material from S. muticum can foul propellers and clog water intakes on ships and aquaculture and other industrial facilities (Critchley et al., Reference Critchley, Farnham and Morrell1986). Floating masses of seaweed may cause a loss in amenities and associated recreational activity, i.e. swimming, surfing, sailing, etc. (Eno et al., Reference Eno, Robin and Sanderson1997).

The spread of S. muticum in Europe and the UK

Sargassum muticum is native to Japanese waters (Norton, Reference Norton1977), from the Sea of Okhotsk to Shanghai, China (National Biodiversity Network, 2023a). After appearing on the west coast of North America in the 1940s (Norton, Reference Norton1977; Ribera and Boudouresque, Reference Ribera and Boudouresque1995), the first record of attached S. muticum in European waters was reported from Bembridge, Isle of Wight in 1973 (Farnham et al., Reference Farnham, Fletcher and Irvine1973). However, drift material had been observed the previous year in the Pas de Calais, France (Coppejans et al., Reference Coppejans, Rappe, Podoor and Asperges1980). Circumstantial evidence suggests that the original transport vector for this species may have been in association with aquaculture of the Pacific oyster (Magallana gigas) from Japanese or British Columbian waters (Druel, 1973; Engelen et al., Reference Engelen, Serebryakova, Ang, Britton-Simmons, Mineur, Pedersen, Arenas, Fernandez, Steen, Svenson and Pavia2015). Over the past half a century or so, reports of S. muticum in European waters form arguably the most complete record of the geographic spread of an invasive non-native aquatic species (Deysher and Norton, Reference Deysher and Norton1982; Critchley et al., Reference Critchley, Farnham and Morrell1983; Knoepffler-Peguy et al., Reference Knoepffler-Peguy, Belsher, Boudouresque and Lauret1985; Rueness, Reference Rueness1989; Harries et al., Reference Harries, Harrow, Wilson, Mair and Donnan2007; Kraan, Reference Kraan2008; Engelen et al., Reference Engelen, Serebryakova, Ang, Britton-Simmons, Mineur, Pedersen, Arenas, Fernandez, Steen, Svenson and Pavia2015). Since the 1980s, this species has been recorded in the Atlantic from Morocco to Norway (Rueness, Reference Rueness1989; Aires et al., Reference Aires, Kläui and Engelen2022), including the Mediterranean Sea (Engelen et al., Reference Engelen, Serebryakova, Ang, Britton-Simmons, Mineur, Pedersen, Arenas, Fernandez, Steen, Svenson and Pavia2015).

In UK waters, after a few years of apparent containment within the Solent strait, populations of attached S. muticum were recorded along the northern and southern coasts of the English Channel (Critchley et al., Reference Critchley, Farnham and Morrell1983). Since then, the distribution of S. muticum has steadily expanded westwards and northwards (Davison, Reference Davison2009), presumably aided by prevailing wind and current direction driving a clockwise dispersal of propagules and drift fragments (Harries et al., Reference Harries, Harrow, Wilson, Mair and Donnan2007). The discovery of attached populations is often preceded by observations of drift or beach-cast specimens (Deysher and Norton, Reference Deysher and Norton1982; Critchley et al., Reference Critchley, Farnham and Morrell1983; Rueness, Reference Rueness1989). By 2004, S. muticum was recorded in Scotland (Reynolds, Reference Reynolds2004). In 2020, the most northerly UK record of this species attached in situ was documented at Tulm Bay on the Isle of Skye (57.69419 N; 6.35647 W) (National Biodiversity Network, 2023b) (Figure 1).

Figure 1.

Map of the north of Scotland showing the previous and new records of the most northerly established UK populations of Sargassum muticum from Tulm Bay, Skye and Birsay Bay, Orkney.

Sargassum muticum in Orkney

In August 2015 at Warbeth, West Mainland (Figure 2), a beach-cast, i.e. not attached to a substrate, individual of S. muticum became the first accepted observation of this species recorded in Orkney waters (Derek Mayes, pers. comm., 2015; Kakkonen et al., Reference Kakkonen, Worsfold, Ashelby, Taylor and Beaton2019; National Biodiversity Network, 2023c). The first observations of potentially established populations were reported to the Orkney Islands Council Harbour Authority (OICHA) by recreational snorkellers in August 2019 from rock pools in Birsay Bay and in May 2020 at the Choin, Marwick (Alison Moore, pers. comm. 18 May 2020), both locations on West Mainland, Orkney.

Figure 2.

Survey sites monitored by the Orkney Islands Council Harbour Authority. Red dots indicate records of Sargassum muticum in Orkney. From the north: Birsay Bay (established population, 2019), the Choin (established population, 2020), and Warbeth Beach (first recorded beach cast specimen, 2015).

Genetic variation of S. muticum populations

To understand mechanisms behind NNS spread and to effectively manage them, invasion genetics have frequently been utilised to identify cryptic species and populations and track their origins (Geller et al., Reference Geller, Darling and Carlton2010). For marine NNS, a review of publications carried out in European seas, concluded that three quarters of studies reported similar level of genetic diversity in native and in some or all introduced populations but also highlighted marine species with limited genetic diversity in introduced populations (Rius et al., Reference Rius, Turon, Bernardi, Volckaert and Viard2015). For S. muticum, the traditional ribosomal (ITS2 spacer) or mitochondrial DNA (TrnW_I spacer) markers showed overall low diversity in both native and introduced populations (Cheang et al., Reference Cheang, Fujita, Yoshida, Hiraoka, Critchley, Choi, Duan, Serisawa and Ang2010). Alternatively, the cox3 mitochondrial gene inferred a high genetic diversity in the native range while introduced S. muticum populations all belonged to a single haplotype (Bae et al., Reference Bae, Ang and Boo2013). More recently, with advancements in technology, microsatellite and genome-wide single-nucleotide polymorphisms confirmed significantly lower diversity in the introduced S. muticum populations compared to the native ones (Le Cam et al., Reference Le Cam, Daguin-Thiébaut, Bouchemousse, Engelen, Mieszkowska and Viard2019). While analysis of 14 microsatellite loci showed no genetic diversity across both S. muticum introduced ranges, including 1269 individuals from nine distinct NE Pacific populations and 37 NE Atlantic populations, the genome-wide RAD-seq locus genotyping revealed three different genetic lineages. The observed genetic variation represents some potential to track origins of S. muticum introductions. The study by Le Cam et al. (Reference Le Cam, Daguin-Thiébaut, Bouchemousse, Engelen, Mieszkowska and Viard2019) unearthed some hidden diversity within the NE Pacific populations and suggested that the NE Atlantic population of S. muticum shares more genetic background with the Southern NE Pacific populations rather than the Northern NE Pacific population as previously thought (Engelen et al., Reference Engelen, Serebryakova, Ang, Britton-Simmons, Mineur, Pedersen, Arenas, Fernandez, Steen, Svenson and Pavia2015).

While S. muticum is not listed as one of the high-risk invasive species highlighted in the approved OICHA Ballast Water Management Policy for Scapa Flow (OICHA, Reference OICHA2017), identification of the potential arrival of this species has formed part of a monitoring programme continuing in these waters since 1974 (Jones, Reference Jones1980; Kakkonen, Reference Kakkonen2019; Kakkonen et al., Reference Kakkonen, Worsfold, Ashelby, Taylor and Beaton2019). The present study summarises the outcomes of a focussed investigation to confirm its presence at the Choin and Birsay Bay areas and a possible further spread throughout the Orkney Islands. The secondary aim of this study was to confirm the species identification by use of the cytochrome oxidase subunit I (COI) gene of mitochondrial DNA barcoding. Considering the limited number of samples available for analysis and high costs of genome-wide RAD-seq locus genotyping, invasion genetics-related analyses were outside of the study scope and not included here.

Materials and methods

The OICHA has been monitoring the shores and waters of Scapa Flow and the wider Orkney archipelago since 1974 (Jones, Reference Jones1980; Kakkonen, Reference Kakkonen2019). Surveys target 22 rocky and 13 sandy shores, 11 sites for radiological monitoring, and, since 2013, sites are also surveyed for presence of NNS (Atkins et al., Reference Atkins, Jones and Simpson1985; Kakkonen, Reference Kakkonen2019; J. Kakkonen unpublished data). OICHA survey sites are located throughout the Orkney Islands archipelago representing a range of environmental conditions along gradients of exposure, salinity, and pollution, as well as including different substrates (Table 1; Figure 2). Since 2014, rocky shore monitoring by the OICHA has adopted the MarClim survey protocol described by Mieszkowska et al. (Reference Mieszkowska, Leaper, Moore, Kendall, Burrows, Lear, Poloczanska, Hiscock, Moschella, Thompson and Herbert2005) and utilised as part of long-term monitoring on Scottish shores (Burrows et al., Reference Burrows, Twigg, Mieszkowska and Harvey2017). MarClim-style surveys are conducted by a team of two, with one person assigned to take photos and replicate counts of barnacles and limpets while the second person with the aid of survey form identifies and allocates species to a SACFOR abundance scale (Hiscock, Reference Hiscock1981). Any noteworthy species, including NNS, are included in the survey forms; species of interest which are not on the checklist are recorded and a SACFOR scale allocated.

Table 1.

Survey sites monitored by the Orkney Islands Council Harbour Authority

Non-native species monitoring (NNS); MarClim style rocky shore survey (MRS); sandy shore survey (SS); radiological monitoring (RM).

A dedicated snorkel survey of the Choin, Marwick (59.09864 N; 3.34949 W) was conducted in summer 2021 with the aim to locate and confirm the identity of purportedly established populations of S. muticum. The Choin (Figure 2) is a tidal rocky shore area connected to the open sea by a narrow channel and consists of two large pools extending southwards and northwards. A recreational survey team of two snorkellers (J. Kakkonen and A. Moore) surveyed both main pools. Images were collected and samples taken to the Marine Environmental Unit, Orkney Harbour Authority Building for examination and preservation in 90% ethanol for species barcoding. Additionally, a shore-based survey was conducted, a few kilometres north, along the rocky shores of Birsay Bay (59.13656 N; 3.32593 W) in summer 2022 with the aim to confirm the reported presence of S. muticum.

Ethanol-preserved tissue, from two samples of putative S. muticum, was homogenised for 2 min at 25 Hz on TissueLyser (Qiagen) using 125 g of glass beads, 450μl of 1% CTAB and 50 μl of Proteinase K and incubated at 56°C for an hour. Genomic DNA was extracted using DNeasy Plant extraction kit (Qiagen), according to the manufacturer's instruction and DNA was eluted in 200 μl AE buffer. A partial fragment of cytochrome oxidase I gene (COI) was amplified using the primers published in Lane et al. (Reference Lane, Lindstrom and Saunders2007). Approximately 30 ng of purified PCR product (illustra ExoProStar, VWR) was sequenced using the same primers as in the amplification reaction. Consensus sequences were generated and compared to other sequences deposited in GenBank using BLASTn searches (National Institutes of Health, 2023), with only Sargassum spp. sequences published in peer-reviewed literature considered for comparison.

Results

The OICHA's marine NNS monitoring programme has not recorded S. muticum during surveys conducted in the last 10 years; more general shore surveys completed since 1974 have not recorded S. muticum in the Orkney archipelago (Kakkonen et al., Reference Kakkonen, Worsfold, Ashelby, Taylor and Beaton2019; J. Kakkonen unpublished data).

During the 2021 snorkel survey, S. muticum was found to be abundant in the northern pool of the Choin. The algae were sub-tidal amongst native algae, attached to small rocks and had large fronds creating an extensive canopy which was easy to observe (Figure 3). Shore-based surveys identified attached populations with extended canopies in intertidal rock pools in Birsay Bay (Figure 4). Taxonomic guides (Hiscock, Reference Hiscock1979; Bunker et al., Reference Bunker, Brodie, Maggs and Bunker2017) were used to identify this organism as S. muticum; verification was provided by the National Biodiversity Network (2023d).

Figure 3.

In situ population of Sargassum muticum from rock pool at the Choin, West Mainland, Orkney (Image: Alison Moore).

Figure 4.

Detail of Sargassum muticum sampled from Birsay Bay, West Mainland, Orkney (Image: Andrew Want).

A PCR product of approximately 700 bp long was amplified from the two algae samples collected. All generated COI gene sequences were identical. Blastn searches of the GenBank database revealed that the generated consensus sequence (588 bp) (GenBank accession number OR051681) for both samples belonged to S. muticum. The COI sequences obtained from the Orkney S. muticum population were 100% identical to publicly available sequences generated from populations in Norway (MN184280, 84 and MN184364), British Columbia (FJ409213-15) and China (KJ938301).

Discussion

The confirmed establishment of S. muticum in Orkney represents a 1.44° (159 km) northwards extension of the latitudinal range of this species in UK waters. The timing of establishment in Orkney in 2019 is consistent with expected spread based on wind, currents, and the earlier discovery of drifted material in 2015 (Rueness, Reference Rueness1989; Stæhr et al., Reference Stæhr, Pedersen, Thomsen, Wernberg and Krause-Jensen2000; Engelen et al., Reference Engelen, Serebryakova, Ang, Britton-Simmons, Mineur, Pedersen, Arenas, Fernandez, Steen, Svenson and Pavia2015). Beyond the limited observations presented in this study, S. muticum has not been recorded at 46 OICHA survey sites, monitored annually since 1974, with attention to NNS since 2013 (Kakkonen et al., Reference Kakkonen, Worsfold, Ashelby, Taylor and Beaton2019), providing confidence that the S. muticum distribution in Orkney is currently restricted to the west coast of Mainland, Orkney.

The substantial distance between known established populations in Orkney and Skye may be due to several plausible explanations: (i) the remoteness of the northwest Scottish coastline and the low density of observers may mean that ‘stepping-stone’ populations exist but remain unknown; (ii) there may be a lack of suitable anthropogenic vectors between locations; and (iii) there may be no suitable habitat in between to allow establishment. The latter view is supported by Harries et al. (Reference Harries, Harrow, Wilson, Mair and Donnan2007) based on the unsuitably high level of wave exposure on these coasts. However, if the known Orkney sites, which are extremely wave-exposed, are indicative of the habitat of this species in the north of Scotland, its presence along the northwestern and northern coasts might indeed be expected. MarClim studies along these shores in 2014 found no evidence of S. muticum (Burrows et al., Reference Burrows, Twigg, Mieszkowska and Harvey2017). Interestingly, there are several records of drift specimens from the southern Outer Hebrides, but no records of attached individuals in the archipelago and no records from Harris and Lewis (Christine Johnson, Outer Hebrides Biological Recording, pers. comm. 2022). In general, the presence of deeper rock pools and other topographic features which reduce wave energy appears to sufficiently mitigate against extreme exposure (Johnson et al., Reference Johnson, Frost, Mosley, Roberts and Hawkins2003; Want et al., Reference Want, Waldman, Burrows, Side, Venugopal and Bell2023). Owing to the presence of aquaculture facilities and transport links between Orkney and Skye, it seems unlikely that the west coast of Mainland, Orkney – where there are no industrial facilities or substantial vessel infrastructure - would be at greater risk of introduction of S. muticum via anthropogenic vectors. Furthermore, in local Orkney areas of far greater industrial activity, e.g. Scapa Flow, as well as aquaculture facilities and marinas north of Skye, S. muticum has not been reported. There are two active Pacific oyster (M. gigas) farms in Orkney at Skaill Bay, Isle of Westray, and North Bay, Isle of Hoy. Both farms receive their oyster seeds from hatcheries, reducing the possibility of introducing NNS. As part of shellfish production planning process, the Orkney Islands Council requires every site to have a marine NNS biosecurity plan.

The establishment of S. muticum in Orkney is of concern to the region from ecological and economic perspectives. On northern and western Scottish coasts featuring suitable habitats, the tendency of S. muticum to displace native macroalgae, in particular ‘leathery’ species of the genera Fucus, Laminaria, Bifurcaria, Codium, and Halidrys (Viejo, Reference Viejo1997; Stæhr et al., Reference Stæhr, Pedersen, Thomsen, Wernberg and Krause-Jensen2000; Sanchez and Fernandez, Reference Sánchez and Fernández2018), may place key species at risk. The fucoid Halidrys siliquosa is typically found in deeper, rock pools on West Mainland, Orkney (Want, Reference Want2017) and it has been speculated that region-wide replacement of this species by S. muticum is possible (Stæhr et al., Reference Stæhr, Pedersen, Thomsen, Wernberg and Krause-Jensen2000; Arenas et al., Reference Arenas, Sanchez, Fernandez and Hawkins2003; Engelen et al., Reference Engelen, Santos and Alves2003). Regional Scottish waters are also home to protected beds of seagrass (James, Reference James2004; Thomson et al., Reference Thomson, Jackson and Kakkonen2014; Kent et al., Reference Kent, Lilley, Unsworth, Cunningham, Begg, Boulcott, Jeorrett, Horsburgh and Michelotti2021) vulnerable to replacement by S. muticum (den Hartog, Reference den Hartog1997; Kraan, Reference Kraan2008). Zostera marina may aid colonisation by S. muticum by trapping drift fragments, providing a suitable substrate for attachment (Tweedley, Reference Tweedley, Jackson and Attrill2008). Natural transport of floating S. muticum also poses a continuing risk of introducing NNS attached to drifting fragments (Lützen, Reference Lützen1998). Recently discovered invasive species in Orkney, such as Styela clava, could have arrived in this manner (Want and Kakkonen, Reference Want and Kakkonen2021).

From an economic perspective, areas with thriving fishing and aquaculture industries (e.g. salmon and shellfish farming), such as the west and north of Scotland, the fouling from S. muticum may have substantial economic impacts (Harries et al., Reference Harries, Harrow, Wilson, Mair and Donnan2007). Offshore renewable energy devices and infrastructure deployed in these waters provide artificial hard substrate for epibenthic organisms, including macroalgae, which may negatively affect performance and survivability of these technologies (Want et al., Reference Want, Crawford, Kakkonen, Kiddie, Miller, Harris and Porter2017). Unsightly masses of floating seaweed may pose a nuisance impactful to local economies, especially in areas dependent on tourism and recreational marine activities (Eno et al., Reference Eno, Robin and Sanderson1997).

In the northeast Atlantic, estimates of spread rate for S. muticum range from 15–17 km yr−1 (Stæhr et al., Reference Stæhr, Pedersen, Thomsen, Wernberg and Krause-Jensen2000) to 69 km yr−1 (Mineur et al., Reference Mineur, Davies, Maggs, Verlaque and Johnson2010). In the studies reported here, confirmed established records in Skye and Orkney are separated by a minimum sea distance of roughly 250 km and 9 years between observations. This represents a spread rate of approximate 28 km yr−1, consistent with existing estimates. The current results and estimate of spread rate may be of value to monitoring programmes in adjacent marine regions, i.e. Shetland and Caithness (Collin et al., Reference Collin, MacIver and Shucksmith2015; Vawdrey, Reference Vawdrey2021).

Somewhat unexpected is that the first known establishments in Orkney are recorded from the West Mainland, an area typically characterised by extreme wave exposure (Want et al., Reference Want, Crawford, Kakkonen, Kiddie, Miller, Harris and Porter2017) and considered unsuitable for this species (Viejo et al., Reference Viejo, Arrontes and Andrew1995; Harries et al., Reference Harries, Harrow, Wilson, Mair and Donnan2007). However, the presence of rock pools on gently sloped shores in areas forming (relative) embayments may mitigate against the most destabilising wave forces (Burrows et al., Reference Burrows, Harvey and Robb2008; Want, Reference Want2017) and thus may provide suitable substrate for S. muticum. Rock pools on West Mainland, Orkney are indeed colonised by relatively lower exposure macroalgae (e.g. Fucus serratus, H. siliquosa) in close proximity (within 100s of metres) to extreme exposure adapted species (e.g. Fucus distichus anceps, Fucus spiralis nanus) (Want, Reference Want2017). High wave exposure may prevent the survival of S. muticum in the shallow sublittoral zones adjacent to the rock pool populations on West Mainland, Orkney.

The traditional COI barcode was generated in this study to accompany the morphological identification of S. muticum found in Orkney. The generated COI sequence was identical to sequences of S. muticum collected from East Asia (Liu and Pang, Reference Liu and Pang2016) and both NE Pacific (McDevit and Saunders, Reference McDevit and Saunders2009) and NE Atlantic populations (Bringloe et al., Reference Bringloe, Sjøtun and Saunders2019), respectively. Such genetic homogeneity in the introduced populations of S. muticum is common and reflects outcomes from other barcoding genes (Cheang et al., Reference Cheang, Fujita, Yoshida, Hiraoka, Critchley, Choi, Duan, Serisawa and Ang2010; Bae et al., Reference Bae, Ang and Boo2013). However, more extensive sampling and RAD-seq genome-wide genotyping is necessary to fully characterise the genetic composition of the Orkney S. muticum population.

Conclusion

Establishment of S. muticum in Orkney, preceded by the discovery of drift specimens, closely follows predicted patterns of range expansion. Questions remain regarding the observed ability of S. muticum to survive adjacent to extremely exposed rocky shores and the lack of records between Skye and Orkney. A focussed survey programme to examine suitable shores in this hard-to-access region would be valuable in helping understand the local habitats and distribution patterns of S. muticum. Continued monitoring by the OICHA is an invaluable tool within Orkney waters. Similar programmes in Shetland (Collins et al., Reference Collin, MacIver and Shucksmith2015) and other parts of the UK may be interested in these results. Rising sea temperatures, associated with global climatic change, suggest that this species will continue to spread northwards (Stachowicz et al., Reference Stachowicz, Terwin, Whitlatch and Osman2002; Engelen et al., Reference Engelen, Serebryakova, Ang, Britton-Simmons, Mineur, Pedersen, Arenas, Fernandez, Steen, Svenson and Pavia2015) and into cooler waters along the North Sea coast.

Reactive surveys, described in this study as part of ongoing long-term monitoring, are a vital component of biosecurity surveys tasked with early detection of invasive NNS. The spread of invasive NNS is a serious concern to local ecosystems and economies. Eradication programmes are costly and are most effective following a rapid management action plan (Sambrook et al., Reference Sambrook, Holt, Sharp, Griffith, Roche, Newstead, Wyn and Jenkins2014). As S. muticum is not one of the high-risk invasive NNS highlighted in the OICHA Ballast Water Management Policy, there are no current plans to eradicate this species locally. Early detection may be enhanced through application of DNA-based monitoring approaches such as detection of environmental DNA, shed by living organisms into aquatic environment. In last five years, eDNA-based monitoring, either with use of the targeted species-specific real-time PCR assays (for example: Wood et al., Reference Wood, Pochon, Ming, von Ammon, Woods, Carter, Smith, Inglis and Zaiko2019; LeBlanc et al., Reference LeBlanc, Belliveau, Watson, Coomber, Simard, DiBacco, Bernier and Gagné2020) or metabarcoding approaches and generic COI gene primers (for example: Couton et al., Reference Couton, Comtet, Le Cam, Corre and Viard2019, Reference Couton, Lévêque, Daguin-Thiébaut, Comtet and Viard2022; Holman et al., Reference Holman, de Bruyn, Creer, Carvalho, Robidart and Rius2019), has been applied more frequently to monitor a wide range of marine NNS. The availability of the COI barcode for S. muticum can facilitate the development of eDNA-based surveillance for S. muticum in Orkney and elsewhere in a similar way as demonstrated for another marine invasive species, Didemnum vexillum (Matejusova et al., Reference Matejusova, Graham, Bland, Lacaze, Herman, Brown, Dalgarno, Bishop, Kakkonen, Smith and Douglas2021).

Acknowledgements

The authors would like to thank the following ‘citizen scientists’, professionals, and organisations: Alison Moore, for first notifying the OIC of attached individuals of this seaweed; Derek Mayes, for the first report of a beach-cast specimen in Orkney and Prof. Martin Wilkinson for confirmation of that specimen; David and Rona Craig for additional observations of attached populations in rock pools in Birsay; Neil Roberts and the Highland Biological Recording Group; Christine Johnson at Outer Hebrides Biological Recording; and, the team at the National Biodiversity Network. The authors also wish to express their gratitude to Jennifer Graham for genetic laboratory support. The authors thank the anonymous reviewers for their valuable comments which have improved this manuscript.

Authors’ contributions

AW performed the literature review and provided most of the text for this manuscript. IM carried out the sequence analysis and provided text relevant to invasion genetics. JK organised and led survey work and made a major contribution to the methods and results sections of the manuscript. All authors read, revised, and approved the final manuscript.

Financial support

All shore surveys were funded by OICHA.

Competing interest

None.

Ethicalstandards

Not applicable.

Consent for publication

Not applicable.

Availability of data and materials

Collected samples are deposited at Marine Scotland Science, Aberdeen and are available upon request.

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Figure 0

Figure 1. Map of the north of Scotland showing the previous and new records of the most northerly established UK populations of Sargassum muticum from Tulm Bay, Skye and Birsay Bay, Orkney.

Figure 1

Figure 2. Survey sites monitored by the Orkney Islands Council Harbour Authority. Red dots indicate records of Sargassum muticum in Orkney. From the north: Birsay Bay (established population, 2019), the Choin (established population, 2020), and Warbeth Beach (first recorded beach cast specimen, 2015).

Figure 2

Table 1. Survey sites monitored by the Orkney Islands Council Harbour Authority

Figure 3

Figure 3. In situ population of Sargassum muticum from rock pool at the Choin, West Mainland, Orkney (Image: Alison Moore).

Figure 4

Figure 4. Detail of Sargassum muticum sampled from Birsay Bay, West Mainland, Orkney (Image: Andrew Want).