Daisy parsons

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D. E. M. Parsons / J. Exp. Mar. Biol. Ecol.

Baseline Investigation into Sargassum muticum (Yendo) Fensholt Distribution in the Fal and its commercial potential.

Daisy Elizabeth Minnie Parsons 11 Oak Ridge, Lifton, Devon, PL16 0LD Falmouth Marine School, Killigrew Street, Falmouth, Cornwall, TR11 3QS

__________________________________________________________________

ABSTRACT Sagassum muticum is an invasive brown macro algae which was believed to have been originally introduced to British waters in imported oyster spat from Japanese oysters during the 1970’s. Due to the species ability to survive for long periods as a floating mass with no holdfast and to reproduce by releasing fertile fronds S. muticum has become widespread throughout British waters. Surveys undertaken around the Fal Estuary in Cornwall have located areas where S. muticum is present, research gathered in the effects of S. muticum on localized biodiversity of seaweeds and an insight into the species commercial potential. The study found S. muticum to only be present in the entrance of the Fal, particularly at Castle Beach, with some rock pools displaying up to 96% coverage. The Fal is an important habitat for BAP species of maerl; Lithothamnion coralloides and Phymatolithon and Eel grass Zostera marina. Were the species to encroach further into the Fal these protected ecosystems could be threatened.

Keywords; Sargassum muticum, invasion, biodiversity, macro algal assemblages, Falmouth

__________________ E-mail address: daizyed@gmail.com (D. E. M. Parsons).

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1. Introduction 1.1. Sargassum muticum; British history; Sargassum muticum is an invasive brown macro algae, native to Japan, which has been recorded in UK waters since 1973, believed to have been accidentally introduced through importation of Crassostrea gigas (Japanese oyster) (Farnham et al, 1973). IUCN (2000), define an invasive species as “an alien species that becomes established in natural or semi-natural ecosystems or habitats, being an agent of change, and threatens native biodiversity”. Grosholz (2002) recognizes one of the main declines of native population biodiversity, ecosystem processes and community dynamics as being caused by biological invasions, and since the introduction of S. muticum in the early 1970’s the spread has been rapid across the Atlantic coast of Western Europe. (Critchley, Farnham, Morrel 1986) This halophyte is monoecious, but can also disperse by releasing fertile, mature fronds. These drifting fronds are capable of surviving in the water column indefinitely, helping to make it one of the most successful invasive species of brown algae (Baer, Stengal 2010). S. muticum has many asymmetrically positioned pneumatocysts which ensure floating, thus keeping the seaweed on the surface where it can continue to photosynthesise. Zhao, Liu et al. (2007) highlight the importance of S. muticum in the maintenance of the structure and function of littoral ecosystems along the North coast of China, with the long fronds integral to the formation of seaweed beds in the littoral and shallow sublittoral regions; providing nursery, feeding and spawning grounds for various marine organisms, including fish and shellfish. (Tsukidate, 1984) Since these relatively early days in the ‘Sargassum invasion’ extensive research has been done into the distribution, (Grosholz 2002) genetic variability, (Zhao et al. 2007) growth rates (Baer, Stengal, 2010) and commercial uses but there is little hard evidence that S. muticum causes quantifiable damage to marine ecosystems. Mike Mcguiry, renowned by local seaweed forager Rory MacPhee amongst others as being an expert in the area; goes so far as to suggest the potentially positive side; that the species ability to withstand variable salinity and temperature allows it to thrive in areas sparse of algal development, thus creating habitats for small crustaceans and fish. Conversely the anthropogenic issues created such as entanglement of steering gear of vessels, obscuration of oyster beds and general annoyance to swimmers (Cheang, Chu et al. 2009) suggest that commercial usage of the species, and thus increasingly financially viable removal, could be beneficial. Previous attempts at removal have proven to not be financially viable, or successful. These have included mechanical removal, manual removal and use of pesticides. (Critchley, Farnham, Morrel 1986) In the species native habitat S.muticum generally only grows to about 2m but plants have been recorded at 16m (Mcguiry, M. 2011) in some areas around the British coast, indicating that we could only be seeing the beginning of the problem. Sanchez and Fernandez concluded in their 2005 paper, of questionable ethicality, that they had found “no evidence that S. muticum altered the successional sequence of this macroalgal assemblage. Species richness, diversity and percentage cover of native macro algae did not show significant differences between control and removal treatments”. Considering the rigorous methodology; incorporating total clearance of living organisms using a blow torch in the control sites and over two years of bi-monthly sampling applied to the study, Sanchez and Ferdanez concluded that S. muticum is not a threat to biodiversity in the low intertidal zone. On the other hand, research conducted by Hartog (1997) showed that S. muticum had infested littoral pools normally dominated by Zostera marina, even though S. muticum is an epithitic species abundant on rocky substrates whereas Z. marina is a root bearing species of sea grass, inhabiting sandy and muddy substrates. (Lewey, L. A. 1976) Z. marina has been identified (Hartog 1997) as a species which is vulnerable to environmental changes, although the beds located on muddy and sandy substrate may not be affected by the spread of S.muticum, the littoral infestation in the areas of mixed substrate is yet another restriction on the ability of Z. marina to maintain permanent communities. (Critchley, Farnham, Morrel. 1986) 1.2. The Fal and Helford SAC. The entire area of the Fal and Helford estuaries and the bays at the entrance, from St Anthony’s Head to The Manacles has been designated as a Special Area of Conservation (SAC), with Zostera marina and maerl species; Phymatolithon calcareum and Lithothamnion corallioide present. These species are listed under Annex I of the EU Habitat Directive under “sandbanks partially covered by water at all times” (JNCC no date) as discovered by Critchley, Farnham and

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D. E. M. Parsons / J. Exp. Mar. Biol. Ecol.

Morrel; S. muticum can be a threat to Z. marina, and being as Maerl can grow from 40m depth up to the tide line (JNCC 1999) the spread of S. muticum could pose problems for both of these nationally recognised important and rare habitats.

2. Method.

2.1. Study sites; The study was carried out between March and April 2012 over eight beaches around the Fal estuary. 1. St Anthony’s Head, 2. St Mawes, 3. St Just in Roseland, 4. Restroguet Weir, 5. Mylor Bridge, 6. Castle Beach, 7. Little Dennis, 8.

Gyllingvase. (See fig.1. Map of the survey points). The littoral zones surveyed ranged in substrate from muddy silt at Restronguet Weir to jagged outcrops of rocks at St Anthony’s Head. The beaches also exhibited differences in levels of exposure which one would expect to have an effect on seaweed biodiversity. St Anthony’s Head has the highest level of exposure with ample fetch across the English Channel. Both Mylor Bridge and Restronguet Passage are examples of extremely sheltered shores. The survey points were chosen as they are representative of various different types of shore. The biodiversity of seaweeds would be expected to vary depending on the different levels of exposure, as discussed in W J Ballantine’s 1961 seminal paper.

The surveys were conducted at the low spring tides, with the greatest tidal height above astronomical low being 0.7m.

The method chosen is based upon a combination of research undertaken by Sanchez and Fernandez in Spain between 2002 and 2004 and the MCS’s (Marine Conservation Society) scientifically recognised survey techniques. Their study was designed to quantify the impact of S.muticum on the surrounding biodiversity. The research undertaken herein has been adapted due to time constraints and is as a result a baseline investigation incorporating random sampling techniques as recommended by the MCS. The main aim of this project is to map where S. muticum is present in the Fal. The effect on seaweed biodiversity will then be statistically analysed with a view to determining whether the presence of S.muticum is detrimental to the native macro algae assemblage. This will be discussed further in the discussion.

2.2. Method; Seaweed biodiversity will be recorded in 10 0.5m by 0.5m quadrats at each survey site at the low spring tide. The first quadrat will be randomly selected by standing at the lowest accessible point of the littoral zone and throwing the quadrat over my shoulder. The quadrats will be randomized by tying knots at random lengths of a piece of string (Hawkins, Jones, 1992) and moving the distance dictated by the knot along the beach. This method is specifically designed for sampling which needs to be taken along the same level on a beach. The seaweed biodiversity in each quadrat is then recorded and an average cover of each seaweed calculated ready for statistical analysis to determine whether the biodiversity of seaweeds increases in quadrats where S. muticum is present.

3. Theory/calculation Ho There will be no significant difference in seaweed biodiversity in quadrats where S. muticum is present.

H1 There will be a significant difference in seaweed biodiversity in quadrats where S. muticum is present.

The results of this experiment will be statistically tested using Spearman’s Rank Coefficient R1 =

6∑d2 1-

______

n (n 2-1)

(Biology Investigation, 2003)

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D. E. M. Parsons / J. Exp. Mar. Biol. Ecol.

Figure 1. Map of survey points. (Digimaps 2012)

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4. Results The statistical test showed that there is no significant difference between seaweed biodiversity on beaches where S. muticum is present compared to biodiversity on beaches where S. muticum is not present.

Table 1. Breakdown of average percentage of seaweeds found on the 8 survey sites; 1. St Anthony’s Head, 2. St Mawes, 3. St Just in Roseland, 4. Restroguet Weir, 5. Mylor Bridge, 6. Castle Beach, 7. Little Dennis, 8. Gyllingvase.

Divided by colour, green algae first, (Shaded light grey), brown (shaded darker grey) and finally red algae (darkest grey shading). The shaded columns indicate S. muticum is present at the site.

1

2

3

4

5

6

Blidingia minima

Phylum

X

Chlorophyta

0.6

X

Chlorophyta

10.8

X

Chlorophyta

X

Phaeophyceae

Pacific, N.A Cornwall 1907

Phaeophyceae

X

Phaeophyceae

X

Phaeophyceae

X

Phaeophyceae

X

Phaeophyceae

X

Phaeophyceae

13.6

X

Phaeophyceae

7.6

X

Phaeophyceae

X

Phaeophyceae

X

Phaeophyceae

X

Phaeophyceae

X

Phaeophyceae

8

0.4

Enteromorpha intestinalis

1.2

1.4

2

Ulva Luctuca

9.6

8.4

1.6

Ascophyllum nodosum

2.6 1

0.8

13.3

0.2

7.4

Colpomenia peregrina

1.2

Dictyota dichotoma

0.2

Fucus ceranoides

0.6

0.4

0.2

Fucus seratus

12.6

Fucus spiralis

1.6

75.6

84.8

81.8

14.6

36.5

9.9

64.9

Fucus vesiculosus

5.8

Himanthalia elongata

4.9

Laminaria digitata Laminaria saccharina Pelvitia canaliculata

Invasive? (country of origin, intr. to. date)

7

1.6

2

4

0.4

1.2

Petalonia fascia

4.6

0.4

Phytomatolithon purpureum

2.4

1.4

Sargassum muticum

32.8

13.3

45.5

Japan, Isle of Wight, 1973

Phaeophyceae

Asparagopsis armata

1.2

0.4

0.9

Aus. /NZ. Lundy 1949

Rhodophyta

Corallina officinalis

5.8

8.8

X

Rhodophyta

0.2

X

Rhodophyta

4.6

X

Rhodophyta

0.8

X

Rhodophyta

X

Rhodophyta

X

Rhodophyta

X

Rhodophyta

7.4

0.2

4.2

0.6

6

Dilsea carnosa Furcellaria lumbricalis

0.8

2

Gastroclonium ovatum Gelidium pusillum

18

Gigartina stellata

1.2

2

4

0.4

Gracilaria verrucosa

0.6

2.6

0.6

0.6

0.8

2.4

2.2

1.1

12.9

0.2

0.5

0.7

Heterosiphonia plumosa

0.6

X

Rhodophyta

Laurencia pinnatifida

0.8

X

Rhodophyta

6 Lomentaria articulata

D. E. M. Parsons / J. Exp. Mar. Biol. Ecol.

0.6

Membranoptera alata

1.8

0.6

0.8

2

0.6

2

0.8

Nemalion helminthoides

2.4

X

Rhodophyta

X

Rhodophyta

X

Rhodophyta

X

Rhodophyta

1

X

Rhodophyta

1.1

X

Rhodophyta

0.2

Palmaria palmata

0.8

Porphyra umbilicalis Rhodymenia pseudopalmata

0.2

0.6

1.6

There was found to be a significant difference in biodiversity between exposed areas of shoreline and less exposed areas of shoreline. Restronguet Weir exhibited almost [96% and 98%] total coverage of Fucus seratus in three of the quadrats.

5. Discussion The earlier surveys, undertaken in March found S. muticum to be in later stages of development than several other species present. Holdfasts of Himanthalia elongata were discovered in stages of early development in close proximity to examples of S. muticum of over 70 centimetres in length. In order to understand the full effects of S. muticum on the biodiversity of intertidal rock pools in the Fal further studies would need to be undertaken incorporating removal techniques and control sites as seen in the studies undertaken by Sanchez and Ferdanez in 2005. Were the rock pools which were found to be heavily populated with S muticum cleared and new growth removed regularly to allow other algae the chance to thrive a clearer picture could be painted on the repercussions of this seaweed.

Holly Latham’s 2012 unpublished research looking at changes in epifaunal activity between mooring areas and nonmooring areas was a partnership project with Falmouth Harbour Commission using Plymouth Universities ROV which found S. muticum to be present within the Helford where there are large areas or both Eelgrass and Maerl. The Fal is macrotidal, with a tidal range of about 4.6m; most of the beaches surveyed had a low shore profile, muddy substrate and few or no rocks to attach to. Hawkins and Jones 1992, state that S. muticum is most commonly found in sheltered harbours and estuaries, on boulders and stones; however the three beaches where S. muticum were present were the three most exposed of the shores. The reason for this is likely to be the very dense coverage of the fucoids or wracks. As there is very little wave action on the shores within the estuary the fucoids form very clear zonation patterns. (Ballantine 1961), Although the fucoids were present in the more exposed areas of coasts the plants were exhibited textbook growth, displaying reduced numbers of bladders with plants shorter and bushier (Hawkins, Jones 1992) than their cousins within the estuary and without the clearly defined zonation patterns typical of sheltered shores.

5.1. Commercial potential of Sargassum muticum; 5.1.1. Metal absorption of brown macro algae; Various studies have been undertaken into the biosorption of heavy metals using seaweeds. Davis et al recognize that heavy metals present at above natural levels in water supplies resultant from effluent from industries such as mining and metal processing are an important environmental priority due to the inability of numerous species to tolerate above lethal levels. (Bryan, Langston 1992, Bryan, Gibbs 1983) There are various environmental regulations such as the Mining Wastes Directive (MWD) 2009 (NetRegs 2012) and the requirement for companies to hold an Environmental Permit in order to carry out mining waste operations backed up with a Waste Management Plan (WMP) (NetRegs 2012) in place to ensure safe removal. Whilst these legislations should control any further increases in levels of heavy metal content in the water there is the existing legacy remaining in the Fal from the past heavy industries carried out largely at Carrick Roads. Brown algae have a gel form of an alginate in the cell walls which is responsible for metal sorption (Fourest and Volesky 1997). The cell walls of brown algae are characteristically thin, adding to their ability to be highly absorbent. The flat chip like shape of the phallus as opposed to the more standard

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spherical shape often exhibited in algae “facilitates rapid ion mass transfer and effective metal binding”. (Yang and Volesky, 1999) For centuries the Fal has been subject to run off from mining activities and species within the Fal have been found to have increased levels of heavy metals within their cells (Warwick 2001) 5.1.2. Nutritional viability of Sargassum muticum Aitkin and Senn discuss the abundance of important vitamins present in marine plants which makes them ideal candidates for plant fertilizer. The high levels of nitrogen, potassium and phosphates present in S.muticum can be easily absorbed through plant roots as the organic matter aids water and mineral retention in the top layers of the soil.

(Aitken and Senn 1965) 5.1.3. Health implications of Sargassum muticum Sargassum muticum amongst other sea weeds are rich in polysaccharides which could be harvested and used in health applications for both humans and animals. (Sullivan et al 2010) Polysaccharides have the potential to be exploited as prebiotic functional materials. These increase the activity of beneficial gut microbiota which increases the effectiveness of the gastrointestinal tract. Foods such as these are referred to as ‘functional foods’ as they fulfil criteria other than nutrition. (O Sullivan et al 2010) 6. Conclusion It is clear from the table of results that brown algae are the most abundant phylum, with coverage ranging from 37.2% to 86.8%. Where fucoids were abundant there was commonly low levels of biodiversity, for example in the 9th quadrat on Mylor Church Beach there was 100% cover of Fucus seratus.

There was one quadrat recorded at Gyllingvase which had 100% cover of Sargassum muticum with the algae in a mature stage of development. There was a relatively high level of biodiversity in the other quadrats measured on Gyllingvase [between 4 and 7 other seaweeds recorded] which clearly shows that Sargassum muticum can be responsible for out-competing native seaweeds; the bushy nature of the algae quickly blocks out sunlight, stopping other species from photosynthesising.

The statistical test showed that there was no significant difference in biodiversity between beaches with S. muticum and those without, but this does not mean that the alien species is not a potential threat to biodiversity as the beaches surveyed were very different in terms of exposure levels and abundance of fucoids. Fucus seratus is a hardy brown macro algae with limited seasonal change in substrate coverage (personal observations). This would make attachment of S. mutium nigh on impossible. In order to collect a more scientifically viable conclusion quadrat surveys would have to be undertaken on beaches with similar exposure levels to the beaches where S. muticum was found.

Acknowledgements Project kindly sponsored by Falmouth Harbour Commissions Falmouth Habitat Project.

Glossary

Alien Species a non-established introduced species (q.v.), which is incapable of establishing self-sustaining or self-propagating populations in the new area without human interference (cf. 'introduced species'; 'non-native').

Biodiversity "The variability among living organisms from all sources including, inter alia, terrestrial, marine and other aquatic ecosystems and the ecological complexes of which they are part; this includes diversity within species, between species and of ecosystems." (UN Convention on Biological Diversity, 1992).

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Brackish Referring to mixtures of fresh and seawater. Usually regarded as between 0.5 ‰ and 30 ‰ salinity (q.v.) (based on McLusky, 1993).

Epiphytic Growing on the surface of a living plant (but not parasitic upon it) (Marlin, no date) Enclosed Coast a marine inlet or harbour fully enclosed from the open sea except at the entrance, not normally open to the sea at two ends. The connection with the open sea is normally less restricted than is the case with lagoons (based on Hiscock, 1990.)

Estuary 1) a semi-enclosed coastal body of water which has a free connection with the open sea, and within which sea water is measurably diluted by fresh water derived from land drainage (Pritchard 1967).

Extremely Exposed Of wave exposure - open coastlines which face into the prevailing wind and receive both wind-driven waves and oceanic swell without any offshore obstructions such as islands or shallows for several thousand kilometres and where deep water is close to the shore (50 m depth contour within about 300 m) (from Hiscock, 1990).

Extremely sheltered Of wave exposure - fully enclosed coasts with a fetch of no more than about 3 km (from Hiscock, 1990).

Factor Environmental - a component of the physical, chemical, ecological or human environment that may be influenced by natural events or anthropogenic activity (Tyler-Walters & Jackson, 1999).

Heavy Metal A generic term for a range of metals with a moderate to high atomic weight, for example cadmium, mercury, lead.

Although many are essential for life in trace quantities, in elevated concentrations most are toxic and will bioaccumulate, and so are important pollutants (MarLIN no date).

Halophyte Species of plants which are capable of living in waters with high salinity.

Monoecious Plants which can reproduce independently as they have both male and female reproductive organs on different parts of the same plant.

Ria A drowned river valley in an area of high relief; most have resulted from the post-glacial rise in relative sea-level (based on Allaby & Allaby, 1990). As defined for the EC Habitats Directive, 'rias and voes' are "drowned river valleys (not of glacial origin) with relatively deep narrow well-defined channels which are predominantly marine throughout".

ROV: Remotely Operated Vehicle.

Sheltered Of wave exposure - coasts with a restricted fetch and/or open water window. Coasts can face prevailing winds but with a short fetch (< 20 km) or extensive shallow area offshore, or may face away from prevailing winds (from Hiscock, 1990).

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Appendix I. Area graphs of results representing seaweed cover on the beaches surveyed.

St Anthony's Head Seaweed Biodiversity 120 Ulva Luctuca Sargassum muticum

100

Rhodymenia pseudopalmata

% cover of seaweed

Phytomatolithon purpureum 80

Pelvitia canaliculata Lomentaria articulata Gracilaria verrucosa

60

Gigartina stellata Gelidium pusillum

40

Furcellaria lumbricalis Fucus spiralis 20

Fucus seratus Enteromorpha intestinalis Corallina officinalis

0 1

2

3

4

5

6

7

8

9

10

Asparagopsis armata

Quadrat no.

Figure 2. Area graph showing the biodiversity of seaweeds found at St Anthonyâ&#x20AC;&#x2122;s Head

Castle Cove St Mawes Seaweed Biodiversity 120 Ulva lactuca % cover of seaweed

100

Rhodymenia pseudopalmata Membranoptera Alata

80

Lomentaria articulata

60

gracilaria verrucosa

40

Gigartina stellata Fucus spiralis

20

Enteromorpha intestinalis 0 1

2

3

4

5

6

7

Quadrat number

8

9

10

Corallina officinalis Ascophyllum nodosum

Figure 3. Area graph showing the biodiversity of seaweeds found at castle Cove

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D. E. M. Parsons / J. Exp. Mar. Biol. Ecol.

Between St Just in Roseland and St Mawes Seaweed Biodiversity 120

100 % cover of seaweed

Ulva Luctuca Membranoptera alata

80

Laminaria saccharina Lomentaria articulata

60

Gracilaria verrucosa 40

Gigartina stellata Fucus vesiculosus

20

Fucus seratus Enteromorpha intestinalis

0 1

2

3

4

5

6

7

8

9

10

Quadrat number

Figure 4. Area graph showing the biodiversity of seaweeds found at St Just in Roseland.

Restronguet Weir Seaweed Biodiversity 120

% cover of seaweed

100 Ulva Luctuca

80

Membronoptera alata Laminaria saccharina

60

Lomentaria articulata Gracilaria verrucosa

40

Gigartina stellata Fucus seratus

20

Corallina officinalis

0 1

2

3

4

5

6

7

8

9

10

Quadrat number

Figure 5. Area graph showing the biodiversity of seaweeds found at Restronguet Weir.

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D. E. M. Parsons / J. Exp. Mar. Biol. Ecol.

Mylor Church Seaweed Biodiversity % cover of Seaweed

120 100

Ulva Luctuca

80

Lomentaria articulata

60

Laminaria saccharina

40

Gigartina stellata

20

Gelidium pusillum

0 1

2

3

4

5

6

7

8

9

10

Fucus seratus

Quadrat number

Figure 6. Area graph showing the biodiversity of seaweeds found at Mylor Church Beach.

Castle Beach Seaweed Biodiversity 120 Ulva Luctuca Sargassum muticum 100

Rhodymenia pseudopalmata Porphyra umbilicalis Phytomatolithon purpureum Petalonia fascia

% Cover of Seaweed

80

Pelvitia canaliculata Nemalion Helminthoides Lomentaria articulata

60

Himanthalia elongata Gracilaria verrucosa Gigartina stellata

40

Gelidium pusillum Furcellaria lumbricalis Fucus seratus Enteromorpha intestinalis

20

Dictoyota dichotoma Corallina officinalis Colpomenia peregrina

0

Asparagopsis armata 1

2

3

4

5

6

7

8

9

10

Quadrat number

Figure 7. Area graph showing the biodiversity of seaweeds found at Castle Beach

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D. E. M. Parsons / J. Exp. Mar. Biol. Ecol.

Little Dennis Seaweed Biodiversity 120 Ulva Luctuca Phytomatolithon purpureum

100

Palmaria palmata

% Cover of Seaweed

Laurencia pinnatifida 80

Laminaria digitata Himanthalia elongata Heterosiphonia plumosa

60

Gigartina stellata Gelidium pusillum Gastroclonium ovatum

40

Furcellaria lumbricalis Fucus seratus 20

Fucus ceranoides Corallina officinalis Colpomenia peregrina

0 1

2

3

4

5

6

7

8

9

10

Blidingia minima

Quadrat number

Figure 8. Area graph showing the biodiversity of seaweeds found at Little Dennis.

Gyllingvase Seaweed Biodiversity 120 Ulva Luctuca

% Cover of Seaweed

100

Sargassum muticum Pelvitia canaliculata

80

Nemalion Helminthoides Gigartina stellata

60

Fucus seratus 40

Enteromorpha intestinalis Dilsea carnosa

20

Corallina officinalis Colpomenia peregrina

0 1

2

3

4

5

6

7

8

9

10

Asparagopsis armata

Quadrat number

Figure 9. Area graph showing the biodiversity of seaweeds found at Gyllingvase.

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