Codium fragile subsp. fragile - Sputnik weed

‘Dead man’s fingers’ Codium fragile originates from the West Pacific Ocean, off the coast of Japan ^[2]. It is a typical green alga found in harbours, bays, tidal pools and other sheltered areas ^[3].

First observation in Belgium

This exotic species was observed for the first time in 1939, in the Sluice Dock of Ostend ^[4].

Spreading in Belgium

In the 1980s and 1990s, C. fragile often washed ashore on the beach of Koksijde. Probably, these were individuals from French populations, which in periods of favourable winds drifted to our regions and were washed ashore ^[5].

Between 1998 and 2000, C. fragile still formed dense populations in the Sluice Dock of Ostend, but – just like the Japanese wireweed – experienced a decline and has not been observed there since 2002. The most likely cause for the decrease in both species are fluctuations in the water level ^[6]. Since 2006, the number of algae spotted in the sluice-dock has increased, and they are mainly found near the edges ^[7].

Spreading in neighbouring countries

The discovery of some fragments of C. fragile washed ashore at Huisduinen in the Netherlands (1900) ^[8] was considered for a long time the first sighting of the species in Europe. However, DNA research on herbarium specimens proved that this species had already been collected near County Donegal in Northern Ireland in 1845. The same research showed that C. fragile occurred in 1891 near the Scottish Ronaldsay ^[9].

Not long after the first sighting in the Netherlands, this seaweed was found – both in wrack (marine vegetation cast ashore) and as attachments – along the coasts of Texel, Den Helder and Zeeland ^[8]. Today, C. fragile is present in the Netherlands in Lake Grevelingen and the estuaries of the Eastern and Western Scheldt ^{[10, 11]}. After it arrived in the Netherlands, C. fragile reached Denmark (1919), Sweden (1933) and Norway (1946). Since 1950, it can also be found in the Mediterranean. In 1998, its European range extended from North Africa to northern Norway, including the British Isles and the Mediterranean ^[3].

More than likely, the species arrived in Europe by attachment to ship hulls or attachment to transported shellfish, e.g. through the transport of the Japanese oyster Crassostrea gigas ^[3]. The latter seems unlikely for the observations in our area, as the first specimens of this green algae were discovered even before these oyster transports took place. However, it is possible that the species was introduced several times ^[12] and that some of the later introductions were made possible because of the transport of oysters ^[11].

C. fragile is an opportunistic species with few grazing enemies in harbours [13]. In addition, this non-indigenous species can reproduce sexually, asexually (by parthenogenesis, the development of unfertilised gametes into adult specimens) and by small pieces breaking off (i.e. vegetative reproduction), which facilitates rapid dispersal. Furthermore, the species does not have strict requirements regarding salinity and water temperature [3].

This green alga thrives in harbours and is often carried on the hulls of ships. Sea currents contribute to its secondary (local) dispersal ^[13].

‘Dead man’s fingers’ is a permanent species of the biofouling community of ship hulls, harbour infrastructures and shellfish cultures. This exotic weed can form large, thick and impenetrable mats over oyster and mussel beds, making it difficult for these molluscs to gather food and hindering their growth. Because of this, C. fragile can cause economic damage to shellfish cultures ^[3]. In addition, strong waves can knock the weed mats away, taking with them the shellfish on which they had attached themselves  ^{[14, 15]}. This phenomenon gave them the nickname ‘oyster thief‘ ^[15].

C. fragile may compete with indigenous weed species such as the velvet horn Codium tomentosum ^[13]. The latter often turns out to be the better competitor and wins from the invader (island of Guernsey (France), Spanish coasts, west coast of Ireland) ^{[16, 17]}. In new habitats, the species may impact the detritus cycle ^[18] and affect the species composition of the fauna and epiphytic algae, even though this does not usually have a negative impact on the species diversity and richness ^[19-23].

Some Canadian researchers showed that invasion of C. fragile can have a positive impact on the environment. More fauna lives associated with C. fragile, than with the native seagrass species. The reason for this observation is that C. fragile provides better shelter or because the weed reduces the strength of the water current, causing more sedimentation, which is attractive to certain animals. In itself, ‘dead man’s fingers’ does not have a major negative impact on native seagrass species. Nonetheless, researchers do call for vigilance against other invasive species that use the advantages created by C. fragile to spread ^[20].

Mechanical control is a temporary solution and does not help as residues regrow in the following year ^[24]. In Scotland, certain species of nudibranch effectively graze the seaweed and thereby inhibit its further spread ^[25]. In some cases, they even eliminate the invasive seaweed population.

C. fragile is a large, branched weed species that can grow up to 1 metre long and weigh up to 3.5 kg. The individual branches have a diameter of 3-10mm. The main branches are connected by a foot with which the weed attaches itself to the substrate. Due to the numerous floating gas vesicles, filled mainly with (94%) nitrogen gas, the branches stand upright in the water column or float on the surface ^[3].

There are probably two subspecies of C. fragile that can only be distinguished microscopically or genetically: C. fragile subsp. fragile and C. fragile subsp. atlanticum ^[26]. The latter is generally considered endemic to Europe but has not yet been observed in Belgium ^[6]. The most invasive subspecies is C. fragile subsp. fragile, which is now the most common subspecies in Europe ^[3].

[1]          World Register of Marine Species (WoRMS) (2020). Codium fragile subsp. fragile (Suringar) Hariot, 1889. [http://www.marinespecies.org/aphia.php?p=taxdetails&id=370562] (2020-11-17).

[2]          Silva, P.C. (1955). The dichotomous species of Codium in Britain. J. Mar. Biol. Ass. U.K. 34: 565-577. [http://www.vliz.be/en/imis?module=ref&refid=120949]

[3]          Trowbridge, C.D. (1998). Ecology of the green macroalga Codium fragile (Suringar) Hariot 1889: invasive and non-invasive subspecies. Oceanogr. Mar. Biol. Ann. Rev. 36: 1-64. [http://www.vliz.be/en/imis?module=ref&refid=1301]

[4]          Leloup, E.; Miller, O. (1940). La flore et la faune du Bassin de Chasse d'Ostende (1937-1938). Mémoires du Musée Royal d'Histoire Naturelle de Belgique = Verhandelingen van het Koninklijk Natuurhistorisch Museum van België, 94. Koninklijk Natuurhistorisch Museum van België: Brussel. 122 pp. [http://www.vliz.be/en/imis?module=ref&refid=5288]

[5]          Vanhaelen, M.-T. (1997). Viltwier, Codium spec. meer dan andere jaren aangespoeld in juli 1997 te Koksijde. De Strandvlo 17(3): 88. [http://www.vliz.be/en/imis?module=ref&refid=35986]

[6]          ICES Advisory Committee on the Marine Environment (2006). Report of the Working Group on Introductions and Transfers of Marine Organisms (WGITMO) 16-17 March 2006 Oostende, Belgium. CM Documents - ICES. CM 2006(ACME:05). ICES: Copenhagen. 330 pp. [http://www.vliz.be/en/imis?module=ref&refid=111237]

[7]          Heytens, M.; De Clerck, O.; Coppejans, E. (2007). Studie van macrowiergemeenschappen van de Spuikom van Oostende in functie van de Kaderrichtlijn water. Universiteit Gent - Vakgroep Biologie - Afdeling Algologie: Gent. 65 pp. [http://www.vliz.be/en/imis?module=ref&refid=118621]

[8]          Van Goor, A.C.J. (1923). Die holländischen Meeresalgen (Rhodophyceae, Phaeophyceae und Chlorophyceae) insbesondere der Umgebung von Helder, des Wattenmeeres und der Zuidersee. Verhandelingen der Koninklijke Akademie van Wetenschappen te Amsterdam, 2de reeks, XXIII(2). Koninklijke Akademie van Wetenschappen: Amsterdam, The Netherlands. 232, VI tables pp. [http://www.vliz.be/en/imis?module=ref&refid=119927]

[9]          Provan, J.; Booth, D.; Todd, N.P.; Beatty, G.E.; Maggs, C.A. (2008). Tracking biological invasions in space and time: elucidating the invasive history of the green alga Codium fragile using old DNA. Diversity Distrib. 14(2): 343-354. [http://www.vliz.be/en/imis?module=ref&refid=206668]

[10]        Severijns, N. (2009). Verslag van de meerdaagse SWG-excursie naar de Oosterschelde (Zeeland, Nederland) op 8 en 9 maart 2008. De Strandvlo 29(1): 5-14. [http://www.vliz.be/en/imis?module=ref&refid=134078]

[11]        Wolff, W.J. (2005). Non-indigenous marine and estuarine species in the Netherlands. Zool. Meded. 79(1): 3-116. [http://www.vliz.be/en/imis?module=ref&refid=101200]

[12]        Kerckhof, F.; Haelters, J.; Gollasch, S. (2007). Alien species in the marine and brackish ecosystem: the situation in Belgian waters. Aquat. Invasions 2(3): 243-257. [http://www.vliz.be/en/imis?module=ref&refid=114365]

[13]        Eno, N.C.; Clark, R.A.; Sanderson, W.G. (Ed.) (1997). Non-native marine species in British waters: a review and directory. Joint Nature Conservation Committee: Peterborough. ISBN 1-86107-442-5. 152 pp. [http://www.vliz.be/nl/imis?module=ref&refid=24400]

[14]        Dromgoole, F.I. (1975). Occurrence of Codium fragile subspecies tomentosoides in New Zealand waters. N.Z. J. Mar. Freshwat. Res. 9(3): 257-264. [http://www.vliz.be/en/imis?module=ref&refid=140391]

[15]        Naylor, R.L.; Williams, S.L.; Strong, D.R. (2001). Aquaculture: a gateway for exotic species. Science (Wash.) 294(5547): 1655-1656. [http://www.vliz.be/en/imis?module=ref&refid=20926]

[16]        Farnham, W.F. (1980). Studies on aliens in the marine flora of southern England, in: Price, J.H. et al. The shore environment: 2. Ecosystems. Systematics Association Special Volume, 17(b). Academic Press: London: pp. 875-914. [http://www.vliz.be/en/imis?module=ref&refid=121198]

[17]        Trowbridge, C.D.; Farnham, W.F. (2004). Spatial variation in littoral Codium assemblages on Jersey, Channel Islands (southern English Channel). Bot. Mar. 47(6): 501-503. [http://www.vliz.be/en/imis?module=ref&refid=120951]

[18]        Krumhansl, K.A.; Scheibling, R.E. (2012). Detrital subsidy from subtidal kelp beds is altered by the invasive green alga Codium fragile ssp. fragile. Mar.  Ecol. Prog. Ser. 456: 73-85. [http://www.vliz.be/en/imis?module=ref&refid=312308]

[19]        Armitage, C.; Sjøtun, K. (2016). Codium fragile in Norway: Subspecies identity and morphology. Bot. Mar. 59(6): 439-450. [http://www.vliz.be/nl/catalogus?module=ref&refid=312303]

[20]        Drouin, A.; McKindsey, C.W.; Johnson, L.E. (2011). Higher abundance and diversity in faunal assemblages with the invasion of Codium fragile ssp. fragile in eelgrass meadows. Mar. Ecol. Prog. Ser. 424: 105-117. [http://www.vliz.be/nl/catalogus?module=ref&refid=301616]

[21]        Schmidt, A.; Scheibling, R. (2006). A comparison of epifauna and epiphytes on native kelps (Laminaria species) and an invasive alga (Codium fragile ssp. tomentosoides ) in Nova Scotia, Canada. Bot. Mar. 49(4): 315-330. [http://www.vliz.be/nl/catalogus?module=ref&refid=312304]

[22]        Jones, E.; Thornber, C. (2010). Effects of habitat-modifying invasive macroalgae on epiphytic algal communities. Mar.  Ecol. Prog. Ser. 400: 87-100. [http://www.vliz.be/en/imis?module=ref&refid=312306]

[23]        Schmidt, A.L.; Scheibling, R.E. (2007). Effects of native and invasive macroalgal canopies on composition and abundance of mobile benthic macrofauna and turf-forming algae. J. Exp. Mar. Biol. Ecol. 341(1): 110-130. [http://www.vliz.be/en/imis?module=ref&refid=312309]

[24]        Galil, B.S. (2009). Codium fragile tomentosoides (v. Goor) Silva, green sea fingers (Codiaceae, Chlorophyta), in: DAISIE (Delivering Alien Invasive Species Inventories for Europe). Handbook of alien species in Europe. Invading Nature - Springer Series in Invasion Ecology, 3 Invading Nature - Springer Series in Invasion Ecology, 3. Springer: Dordrecht: pp. 277. [http://www.vliz.be/en/imis?module=ref&refid=134993]

[25]        Trowbridge, C.D. (2002). Local elimination of Codium fragile ssp. tomentosoides: indirect evidence of sacoglossan herbivory. J. Mar. Biol. Ass. U.K. 82(6): 1029-1030. [http://www.vliz.be/en/imis?module=ref&refid=31240]

[26]        Verbruggen, H.; Brookes, M.J.L.; Costa, J.F. (2017). DNA barcodes and morphometric data indicate that Codium fragile (Bryopsidales, Chlorophyta) may consist of two species. Phycologia 56(1): 54-62. [http://www.vliz.be/nl/catalogus?module=ref&refid=312301]

VLIZ Alien Species Consortium (2020). Codium fragile subsp. fragile – Dead man’s fingers. Non-native species of the Belgian part of the North Sea and bordering estuaries anno 2020. Flemish Institute for the Sea (VLIZ). 6 pp.