Phenology of Sargassum muticum (Phaeophyta, Fucales) in Limfjorden
    T. Wernberg-Møller, M. S. Thomsen & P. A. Stæhr
    Roskilde University, Dept. of Life Sciences and Chemistry, Po. box 260, 4000 Roskilde, Denmark
    (This poster was presented at the 10. Marine Research Conference in Hirtshals (Denmark) january 21.-23. 1998) 

    Introduction

    For the past 25 years Sargassum muticum (Yendo) Fensholt has been known for its invasive colonisation of European waters1,2,3. In Denmark the first specimen of S. muticum (Japweed/Butblæret sargassotang) was found in 1984 in Nissum Bredning, Limfjorden4. Since then it has spread throughout the fjord, where it is now the dominating macroalgae5.

    S. muticum is a brown algae which originates from Asia6. It belongs to the order Fucales6,7 and its closest relative in Danish waters is Halidrys siliquosa (Skulpetang). However, it is also closely related to other conspicous macroalgae, namely Fucus spp. (e.g. Bladderwrack/Blæretang).

    S. muticum is a relatively new species. It was first described just after the turn of the century by Yendo6 as a forma of another Sargassum species (S. kjellmanianum = S. miyabei8). However, it took 50 years before it recieved specific rank, as the forma was revised by Fensholt9.

    S. muticum possesses characteristics of both r- and K-selected species such as high growth rate (r)10,11,12, large propagule production (r)10,13, high thallus differentiation (K)7,14 and long lifespan (K)15. This combination is thought to be one of the reasons for its succesfull invasion of American and European waters2,10.

    This study of the phenology of S. muticum is part of a larger investigation of the species' distribution and ecology in Limfjorden (see5,16). It provides context specific information on important biometric relationships, enabling conversions and comparisons of data with different origin.

    Similar but more extensive studies has previously been conducted in the vicinity of our study site17.

    Methods

    The studies were conducted at Bjørndrup in Dråby Vig, western Limfjorden during April-November 1997. Once a month 16-30 individuals were collected by SCUBA divers at a depth og c. 2.5m.Furthermore, divers estimated cover within a 0.27 m2 ring in 11-17 samples, whereafter biomass was sampled. Before processing individuaks were cleaned for epibionts.

    Morphology

    The thallus of S. muticum is highly differentiated and has several distinct morphological features6,7,14,18. Hold fast, main axis, basal leaves vesicles and receptacles (figure 1).

    From a small discoid holdfast, 1-3cm across, a 2-5cm stipelike main axis arises. From here several primary laterals radiates (see figure 1). Besides from being 1-3mm wide, the length and habitus of these primary laterals is very variable (see figure 2 and figure 3). When fully developed, laterals of higher orders (e.g. secundary) can be seen as branches on the primary laterals. Basal leaves are generally 1-5cm long, 0.5-1cm wide, lanceolate and serrated. Vesicles are a few mm in diametre. Receptacles are 0.5-2cm long, 1-3mm wide and dark brown when fertile.

    The thallus can be differentiated in a perennial and an annual part. These two parts are easily distinguished by colour and texture, the perennial part being dark brown (almost black) and tough whereas the annual parts are lighter and more crisp.

    Figure 1: Specimen of S. muticum from Dråby Vig, April 1997.

    Habitus

    A marked seasonal variation in thallus morphology is characteristic for S. muticum1.

    In spring individuals are dominated by the dark tough perennial part (see figure 1). The new generation of annual primary laterals are represented by short crisp branches with large serrated basal leaves. Some large vesicles are present.

    As the season progresses the number of vesicles increases and secundary laterals start to appear on the longest of the primary laterals. The colour becomes increasingly light.

    In the middle of the season basal leaves are gone or strongly reduced. Laterals of higher orders (tertiary) appear and the number of vesicles is large. This results in a slim erect stature. Receptacles start to form but none are fertile. The colour is now yellowish.

    In late summer fertile receptacles dominate, giving a dark brown appearance. There are almost no vesicles and the stature is somewhat collapsed. Laterals are desintegrating.

    At the end of the season new primary laterals are budding from older perennial parts (see figure 1, figure 3 and figure 4). They appear crisp with large basal leaves. Some outworn old primary laterals remain.

    Figure 2a-e: Development in habitus. Y-axis is relative importance in terms of appearance.

    Lenght (Height)

    It can be seen in figure 3 that there is a significant (p<0.05) seasonal development in thallus length. Values are distributed almost symmetrically around a high July (118.4cm) with low values at the ends in April (17.1cm) and November (14.1cm).

    Figure 3: Seasonal development in individual length (height).

    Number of primary laterals

    In figure 4 it can be seen that the number of primary laterals is negatively correlated with progression of the season (Spearman Rank Correlation; rs=-0.89; p=0.03), until a new generation of primary laterals start to develop in November.

    Figure 4: Seasonal development in the number of primary laterals.

    Various photos

    Unfortunately not all photos are yet available at the present time. They will be included later.

    Photo 1: Not available.

    Photo 2: Two individuals of Sargassum muticum standing at a depth of ca. 3 m. The visibility is usually very poor at this time of the year.
     
     
     
     
     
     
     
     
     
     
     
     
     
     
     
     
     
     

    JulyPhoto 3: These two individuals of S. muticum were collected at ca. 3 m depth at an eastward protected coast (left) and a westward exposed coast (right) in July. Note the sublethal effects on habitus, not necessarily affecting cover. Scale is 150 cm.
     
     
     
     
     
     
     
     
     
     
     
     
     
     
     
     
     
     
     

    AugustPhoto 4: Epibionts on decaying primary lateral of S. muticum in August. Abundant settlement of small tunicates (Clavellina lepadiformis) and a sea anemone (Sagartia sp. - upper right corner).
     
     
     
     
     
     
     
     
     

    Photo 5: Cast primary laterals on the beach.
     
     
     
     
     
     
     
     
     
     
     
     

    Biomass

    Figure 5 show that individuals of S. muticum has a significantly (p<0.05) higher biomass in July (27.1 gDWind-1) than at any other time. The peak in maximum biomass both rise and fall very abrupt. That this is caused by the increase in secundary laterals from June (227 sec. lat. ind.-1) to July (462 sec. lat. ind.-1) is evident since the weight of secundary laterals is not significantly (p<0.05) different from total biomass. The inserted graph shows the seasonal variation in relative importance of annual and perennial parts respectively.

    Figure 5: Seasonal development in individual biomass.

    Cover and biomass

    The cover of S. muticum varies over season10,16. However, much of the growth of S. muticum is directed upwards (cf. figure 3) and therefore does not influence the cover per se. This means that in terms of standing biomass, cover is a very poor estimate of abundance - especially when comparing time series. This is illustrated in figure 6 where it can be seen that the standing biomass per % cover, in August is more than 7 times that in September.

    In table 1 is given linear models of the relationship between percent cover of area (C) and biomass (B; gWWm-2). It can be seen that the linear models are quite good estimates of the relationship between cover and biomass, even though the relationships are not linear from a theoretical point of view. Obviously, the models are only valid from 0-100% cover.

    Figure 6: Seasonal development in the relationship between
    cover and biomass. Datapoints are the coefficients from table 1.
     
    Linear regression model N R p
    May B = 11.1 * C + 149.7 11 0.94 < 0.0001
    June B = 20.5 * C + 291.0 17 0.86 < 0.0001
    July B = 28.9 * C + 296.1 16 0.94 < 0.0001
    August B = 67.7 * C - 978.7 14 0.87 < 0.0001
    September B = 8.6 * C + 81.3 14 0.89 < 0.0001
    November B = 10.3 * C + 55.3 13 0.90 < 0.0001
    Table 1: Linear regression models for the relationship between
    cover (C) and biomass (B). Coefficients are plottet in figure 6. 

    Lenght and biomass

    Figure 7 show a classical relationship between individual length (height) and biomass (weight).

    Calculations are made in dry weight (DW). However, using table 2, data can be converted to wet weight (WW). From the table it can be seen that the DW of the perennial parts account for 20% of the WW whereas it accounts for only 13% in the annual parts. This reflects differences in amounts of structural tissue.

    Figure 7: Relationship between length (height)
    and biomass (weight).
     
    Thallus part DW:WW SD n
    Annual
    0.13
    0.038
    7
    Perennial
    0.20
    0.019
    7
    Total
    0.14
    0.023
    7
    Table 2: Relations between DW and WW.
    n refer to monthly averages of 16-30 individuals. 

    Conclusions

    The most obvious and important conclusion - which has been reached several times1,17 - is that the biometry of S. muticum varies considerably during a season. This is very important to have in mind whenever working with the species.

    Four phases of growth can be recognised:

    • Initial growth. Large basal leaves, increases the highly photosynthetic surface area during a period of poor light conditions - due to depth and season.
    • Elongation growth. Large amounts of vesicles keep the thallus erect and close to the source of light.
    • Reproductive growth. Allocation of energy is shiftet from the production of structural material (elongation) to the production of reproductive tissue (receptacles).
    • Degeneration. Primary laterals degenerate and float away, carrying fertile propagules.
    This alternating adjustment of morphology shows a highly specialized adaptation to life in a seasonal environment.

    Furthermore, it can be concluded that...

    • Individuals start out with many primary laterals. As the season progresses there is a gradual thinning, as the plant concentrate on more viable laterals.
    • In early summer growth rates (elongation) are very high (c. 1.5-2cmday-1).
    • The bulk of the standing biomass during a year is made up of laterals of higher orders.
    Related posters...

    Invasion and productivity of Sargassum muticum (Yendo) Fensholt in Limfjorden, Denmark
    Presented at the 32nd EMBS, Lysekil, Sweeden, 16. - 22. August 1997.

    Invasion of Sargassum muticum (Phaeophyta, Fucales) in Limfjorden, Denmark
    Presented at the 10th Marine Research Conference, Hirtshals, Denmark, 21.-23. January 1998.

    Spatial and temporal distribution of Sargassum muticum (Phaeophyta, Fucales) in Dråby Vig, Limfjorden
    Presented at the 10th Marine Research Conference, Hirtshals, Denmark, 21.-23. January 1998.

    Acknowledgements

    This poster is part of our Master Thesis in Environmental Biology at the Departement of Life Sciences and Chemistry at Roskilde University. The work was made possible through financial support from the staff-student committee (BIO-SN).
    Thanks to Morten Foldager Pedersen for superb supervision. 

    References

    1 Chritchley, A.T.; Farnham, W.F. & Morell, S.L. (1983): A chronology of new European sites of attachment for the invasive brown alga Sargassum muticum 1973-1981. J. mar. biol. Ass. U.K., vol. 63 pp. 799-811.
    2 Rueness, J. (1989): Sargassum muticum and other introduced Japanese macroalgae: Biological pollution of European coasts. Marine Pollution Bulletin, vol. 20 no. 4 pp. 173-176.
    3 Loo, L.-O. & Karlsson, J. (1995): Marin biodiversitet: Utbredning, kolonialiseringspotential och effekter av den introducerade brunalgen Sargassum muticum. Internet homepage: http://130.241.163.21/TMBL/PROJ/LOSargassum/sarg.html.
    4 Christensen, T. (1983): Sargassotang, en ny algeslægt i Danmark. Urt, no. 4 pp. 99-104.
    5 Stæhr, P.A.; Wernberg-Møller, T. & Thomsen, M.S. (1998): Invasion of Sargassum muticum (Phaeophyta, Fucales) in Limfjorden, Denmark. Poster presented at the 10th Marine Research Conference,Hirtshals, Denmark, January 21.-23.. http://users.cybercity.dk/~dko10792/poster2.htm.
    6 Yendo, K. (1907): The Fucaceæ of Japan. J. Coll. Sci. Imp. Univ. Tok. Jap., vol. 21 art. 12 pp. 1-174 + 18 plates.
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    12 Arena, F.; Fernadéz, C.; Rico, J.M.; Fernandéz, E. & Haya, D. (1995): Growth and reproductive strategies of Sargassum muticum (Yendo) Fensholt and Cystoseira nodicaulis (Whit.) Roberts. Sci. Mar., vol. 59 (supl. 1) pp. 1-8.
    13 Norton, T.A. & Deysher, L.E. (1989): The ecology of Sargassum muticum at different latitudes. In Ryland, J.S. & Tyler, P.A. (eds.): Reproduction, genetics and distributions of marine organisms. Proc. 23rd EMBS, pp. 147-152.
    14 Jensen, J.B. (1974): Morphological studies in Cystoseiraceae and Sargassaceae (Phaeophyceae) - with special reference to apical organization. Univ. Calif. Publ. Bot., vol. 68 pp. 1-61.
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    17 Knudsen, L. (1995): Årscyklus for butblæret sargassotang (Sargassum muticum) på en tæt bevokset lokalitet i Limfjorden. Notat fra Bio/consult udarbejdet til Limfjordssamarbejdet v/Ringkøbing Amtskommune.
    18 Tseng, C.K. & Chang, C.F. (1954): Studies on Chinese Sargassums, II. Sargassum kjellmanianum Yendo. Acta Botanica Sinica, vol. III no. 4 pp. 362-387. 

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