Gracilaria vermiculophylla -
SCIENTIFIC NAME
Gracilaria vermiculophylla (Ohmi) Papenfuss, 1967
2011 - 2020
NW Pacific
Aquaculture - importing live animals
Gracilaria vermiculophylla originally occurred only in the Pacific Northwest along the coasts of China, Korea, Vietnam [2] and the east and west coasts of Japan [3, 4]. In Russia, it is found only in the Sea of Japan, an inland sea of the Pacific Ocean [4]. This seaweed prefers sheltered estuaries and shallow bays as a habitat. It can be found lying on sandy and muddy bottoms as well as fixed to hard substrates (e.g. pebbles, mussel beds, rocks, oysters, etc.) [5, 6].
First observation in Belgium
On the 3rd of November and the 29th of December 2011, Gracilaria vermiculophylla was found for the first time in Belgium, more specifically in the Flemish nature reserve ‘Bay of Heist’, located on the eastern breakwater of the Port of Zeebrugge. Today, this species is common there. However, no fertile specimens have been found yet, only vegetative ones [7]. At the same time, the non-native species Caulacanthus okamurae was also found in the Bay of Heist [7].
Spreading in Belgium
In the Bay of Heist, Gracilaria vermiculophylla was found between mussel beds in the low intertidal area (i.e. the area between the high and low tide lines). At low tide, the seaweeds are dry. For the time being, this is the only place where the species is present; nothing is known about its possible further spread in Belgium [7].
Spreading in neighbouring countries
The first observation of Gracilaria vermiculophylla in France, in the estuary of ‘Le Bélon’ on the coast of Brittany, dates back to 1996. Not much later, individuals were found in Roscoff (Brittany), in the vicinity of oyster farms [8, 9]. From there, this red seaweed probably spread both to the north and south along the Breton coast, where they form extensive mats
Gracilaria vermiculophylla was already found in the Netherlands in the 1980s, more specifically in ‘Oostvoornse Plas’, a brackish water lake [5]. In 1994, this red seaweed was observed near Yerseke, while the occurrence of the species in the Wadden Sea was officially reported for the first time in 2009 [5, 11]. Today, Gracilaria vermiculophylla is widely found in the Dutch Wadden Sea, from Texel to Lauwersoog [5]. In the neighbouring German Wadden Sea, the species was observed in 2002 [6]. Further north, the species is found in Denmark (since 2003), in Sweden (2003) and on the Baltic coast of Germany (2005, in Kiel) [6].
The saltwater knotweed also spread to the south of Europe. The species was detected in Portugal (2004) and on the Spanish Atlantic Coast (2003) [9]. Recently (2008), the species has appeared in the Mediterranean Sea, at the Po Delta in Italy [12]. Large populations of the seaweed are now found all along the coast of northern Europe, and in most places, it is the most abundant species [13].
Outside Europe, the species is also abundant as an exotic species. This is the case in estuaries on the Atlantic coast of North America, on the coast of Virginia [13] and North Carolina (USA) (1999) [14].
Oyster transport is the most likely transport vector, as the species is often found near oyster farms [9] and is rarely found in ship’s ballast water or attached to ships’ hulls [6]. However, the species is extremely well adapted to survive in conditions similar to ballast water [15]. Secondary transport over shorter distances can take place via shellfish transport. Furthermore, the weed can entangle in fishing gear, boat propellers, diving gear and migrating birds [15]. Loose weed fragments can travel a limited distance via the currents [6].
It is unknown how Gracilaria vermiculophylla ended up in Belgium. Presumably, the species came from the Netherlands or France by one of the short-range mechanisms mentioned above [7].
The success of Gracilaria vermiculophylla can be partly explained by the food preference of native grazers. After all, native grazers tend to prefer native algae to Gracilaria vermiculophylla [16, 17]. The exact reasons for this preference are unknown. Scientists refer, among other things, to the low nutritional value and nitrogen concentration of the species [18]. In addition, Gracilaria vermiculophylla produces metabolic substances that deter herbivores. Although native species also have a defence system, several studies have shown that exotic species with a defence system are stronger competitors than those without [19]. Furthermore, Gracilaria vermiculophylla tolerates desiccation, burial and a large interval of light [16] and nutrient levels [20, 21]. This seaweed can grow at a salinity of 10-35 PSU [3, 22] and temperatures between 2-35°C [3, 9, 23]. These euryhaline and eurythermal characteristics allow the species to tolerate a wide range of marine environments [24].
The species is therefore classified as one of the four most potentially invasive species in Europe (out of 114 species of macroalgae) [25].
The seaweed has an isomorphic life cycle and can reproduce both sexually and asexually (vegetative fragmentation) [21, 24]. Through fragmentation, small pieces of the seaweed break off, all of which can grow into adult individuals. Because broken-off fragments of only 1mm in size can survive and continue to grow, the species can rapidly reproduce [9, 21, 24]. These fragments maintain their growth capacity for a long time (up to 175 days) [26].
It usually grows on mud and fine sand but can also settle on hard substrates such as rocks or shells. Cleared substrates are quickly colonised by this seaweed [27]. Colonisation is further facilitated by indigenous invertebrates, for example, by providing substrates or by grazers, which break up the seaweed into pieces, increasing fragmentation and dispersal rates [6]. Usually, individuals from non-native colonies do not attach themselves to the substrate (a result of vegetative multiplication) [28].
The presence of Gracilaria vermiculophylla creates competition that hinders the growth of indigenous species [29]. This is because the exotic species forms mats that can grow over eelgrass (Zostera) [27]. Experimentally, it has already been shown that Gracilaria vermiculophylla reduces the survival rate of the narrow-leaved eelgrass Zostera marina [30]. The introduction of Gracilaria vermiculophylla creates new structural complexity, which may have a positive impact on some invertebrates [31]. The seaweed can provide additional shelter, a substrate for adhesion or be a new food source for other species [26, 32]. In a comparative study between Gracilaria vermiculophylla and Ulva rigida, higher species richness and diversity in the macrofauna was found in the presence of Gracilaria vermiculophylla [33]. The species may also be able to influence nitrogen concentration by uptake, storage and release of nutrients, which may have potential effects on the ecosystem [6, 34, 35].
In North Carolina (USA) the introduction of Gracilaria vermiculophylla is causing problems for fisheries and industry as the species attaches itself to fishing nets and clogs pipes of cooling water systems [14].
A potential method for controlling the species is the mechanical removal (harvesting) of Gracilaria vermiculophylla and use it for the production of agar, among other things [36]. As a second control, scientists suggested the common periwinkle Littorina littorea, which can control the Gracilaria vermiculophylla population. However, grazing causes the breakdown of the weed into smaller fragments that accelerate its spread on a small scale [6]. The effects of this invasion in Belgium remain uncertain.
Gracilaria vermiculophylla has a brown to wine red colour. The seaweed forms loosely branched bushes that are attached to the substrate with a holdfast, a structure that is usually difficult to see. The seaweed consists of cylindrical shafts of 15-100 centimetres in length [7]. The Agarophyton and Gracilaria genera contain about 300 species, which are distributed worldwide. However, the distinction between species is not always clear. With the increasing number of species discovered, more and more problems in taxonomy are emerging. These are now being resolved by comparative studies of the reproductive structures and by molecular research [9].
The endemic species Gracilaria gracilis, another red alga, was found in the Sluice dock at Ostend. However, this species shows few morphological differences from Gracilaria vermiculophylla. They can be distinguished microscopically by the depth of the male conceptacles, in which the reproductive structures are sheltered. In Gracilaria gracilis, the depth of the conceptacles is less than 50 μm.
Gracilaria vermiculophylla is an agarophyte, an agar-producing alga. Agar is a jelly-like substance formed from polysaccharides derived from the cell walls. It gets used as a culture medium in microbiological work as well as in the food, pharmaceutical and cosmetics industries. Considering the economic value of agarophytes, scientists recently suggested mechanically removing this alien species and using the harvest for the production of agar [37]. Little is known about how and in which countries this would be possible.
[1] World Register of Marine Species (WoRMS) (2020). Agarophyton vermiculophyllum (Ohmi) Gurgel, J.N.Norris & Fredericq, 2018. [http://www.marinespecies.org/aphia.php?p=taxdetails&id=1327786] (2020-11-17).
[2] Tseng, C.K.; Xia, B.-M. (1999). On the Gracilaria in the Western Pacific and the Southeastern Asia Region. Bot. Mar. 42(3): 209-217. [http://www.vliz.be/en/imis?module=ref&refid=218209]
[3] Yokoya, N.S.; Kakita, H.; Obika, H.; Kitamura, K. (1999). Effects of environmental factors and plant growth regulators on growth of the red alga Gracilaria vermiculophylla from Shikoku Island, Japan. Hydrobiologia 398-399: 339-347. [http://www.vliz.be/en/imis?module=ref&refid=218312]
[4] Skriptsova, A.V.; Choi, H.G. (2009). Taxonomic revision of Gracilaria "verrucosa" from the Russian Far East based on morphological and molecular data. Bot. Mar. 52(4): 331-340. [http://www.vliz.be/en/imis?module=ref&refid=218499]
[5] Gittenberger, A.; Rensing, M.; Stegena, H.; Hoeksema, B.W. (2009). Inventarisatie van de aan hard substraat gerelateerde macroflora en macrofauna in de Nederlandse Waddenzee. GiMaRIS Rapport. Marine Research, Inventory and Strategy Solutions: Leiden. 63 pp. [www.vliz.be/en/imis?module=ref&refid=218160]
[6] Thomsen, M.S.; Stæhr, P.A.; Nyberg, C.D.; Schwaerter, S.; Krause-Jensen, D.; Silliman, B.R. (2007). Gracilaria vermiculophylla (Ohmi) Papenfuss, 1967 (Rhodophyta, Gracilariaceae) in northern Europe, with emphasis on Danish conditions, and what to expect in the future. Aquat. Invasions 2(2): 83-94. [http://www.vliz.be/en/imis?module=ref&refid=218205]
[7] Kerckhof, F.; Verbeke, D.; Bauwens, F. (2012). Nieuws uit de Baai van Heist: de roodwieren Caulacanthus ustulatus (Mertens ex Turner) Kützing, 1843 en Gracilaria vermiculophylla (Ohmi) Papenfuss 1967 nieuw voor de Belgische kust en een merkwaardig habitat van intertidale mossels. De Strandvlo 32(1): 19-23. [http://www.vliz.be/en/imis?module=ref&refid=215164]
[8] Mollet, J.-C.; Rahaoui, A.; Lemoine, Y. (1998). Yield, chemical composition and gel strength of agarocolloids of Gracilaria gracilis, Gracilariopsis longissima and the newly reported Gracilaria cf. vermiculophylla from Roscoff (Brittany, France). J. Appl. Phycol. 10(1): 59-66. [http://www.vliz.be/en/imis?module=ref&refid=218171]
[9] Rueness, J. (2005). Life histories and molecular sequences of Gracilaria vermiculophylla (Gracilariales, Rhodophyta), a new introduction to European waters. Phycologia 44(1): 120-128. [http://www.vliz.be/en/imis?module=ref&refid=217988]
[10] 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]
[11] Stegenga, H.; Karremans, M.; Simons, J. (2007). Zeewieren van de voormalige oesterputten bij Yerseke. Gorteria 32(2006): 125-143. [http://www.vliz.be/en/imis?module=ref&refid=206430]
[12] Sfriso, A.; Maistro, S.; Andreoli, C.; Moro, I. (2010). First record of Gracilaria vermiculophylla (Gracilariales, Rhodophyta) in the Po delta lagoons, Mediterranean Sea (Italy). J. Phycol. 46(5): 1024-1027. [http://www.vliz.be/en/imis?module=ref&refid=218201]
[13] Thomsen, M.S.; Gurgel, C.F.D.; Fredericq, S.; McGlathery, K.J. (2005). Gracilaria vermiculophylla (Rhodophyta, Gracilariales) in Hog Island Bay, Virginia: a cryptic alien and invasive macroalga and taxonomic correction. J. Phycol. 42(1): 139-141. [http://www.vliz.be/en/imis?module=ref&refid=218440]
[14] Freshwater, D.W.; Greene, J.K.; Hamner, R.M.; Montgomery, F. (2006). Seasonality of the invasive seaweed Gracilaria vermiculophylla along the southeastern coast of North Carolina. J. North Carolina Acad. Sci. 122(2): 49-55. [http://www.vliz.be/en/imis?module=ref&refid=218158]
[15] Nyberg, C.D.; Wallentinus, I. (2009). Long-term survival of an introduced red alga in adverse conditions. Mar. Biol. Res. 5(3): 304-308. [http://www.vliz.be/nl/catalogus?module=ref&refid=218311]
[16] Jensen, A.T.; Uldahl, A.G.; Sjøgren, K.P.; Khan, M. (2007). The invasive macroalgae Gracilaria vermiculophylla — effects of salinity, nitrogen availability, irradiance and grazing on the growth rate. MSc Thesis. Roskilde University: Roskilde. pp. [http://www.vliz.be/nl/catalogus?module=ref&refid=301933]
[17] Teso, S.V.; Bigatti, G.; Casas, G.; Piriz, M.L.; Penchaszadeh, P.E. (2009). Do native grazers from Patagonia, Argentina, consume the invasive kelp Undaria pinnatifida? Revista del Museo Argentino de Ciencias Naturales (1999) 11(1): 7-14. [http://www.vliz.be/nl/catalogus?module=ref&refid=297339]
[18] Nejrup, L.B.; Pederson, M.F.; Vinzent, J. (2012). Grazer avoidance may explain the invasiveness of the red alga Gracilaria vermiculophylla in Scandinavian waters. Mar. Biol. (Berl.) 159(8): 1703-1712. [http://www.vliz.be/en/imis?module=ref&refid=255680]
[19] Nylund, G.M.; Weinberger, F.; Rempt, M.; Pohnert, G. (2011). Metabolomic assessment of induced and activated chemical defence in the invasive red alga Gracilaria vermiculophylla. PLoS One 6(12): 12. [http://www.vliz.be/en/imis?module=ref&refid=218498]
[20] Thomsen, M.S.; McGlathery, K.J. (2007). Stress tolerance of the invasive macroalgae Codium fragile and Gracilaria vermiculophylla in a soft-bottom turbid lagoon. Biological Invasions 9(5): 499-513. [http://www.vliz.be/en/imis?module=ref&refid=218204]
[21] Abreu, M.H.; Pereira, R.; Sousa-Pinto, I.; Yarish, C. (2011). Nitrogen uptake response of Gracilaria vermiculophylla (Ohmi) Papenfuss under combined and single addition of nitrate and ammonium. J. Exp. Mar. Biol. Ecol. 407(2): 190-199. [http://www.vliz.be/nl/catalogus?module=ref&refid=297341]
[22] Weinberger, F.; Buchholz, B.; Karez, R.; Wahl, M. (2008). The invasive red alga Gracilaria vermiculophylla in the Baltic Sea: adaptation to brackish water may compensate for light limitation. Aquat. Biol. 3: 251-264. [http://www.vliz.be/nl/catalogus?module=ref&refid=297343]
[23] Raikar, S.; Lima, M.; Fuijita, Y. (2001). Effect of temperature, salinity and light intensity on the growth of Gracilaria spp. (Gracilariales, Rhodophyta) from Japan, Malaysia and India. Indian J. Mar. Sci. 30: 98-104. [http://www.vliz.be/nl/catalogus?module=ref&refid=297345]
[24] Hu, Z.-M.; Juan, L.-B. (2014). Adaptation mechanisms and ecological consequences of seaweed invasions: a review case of agarophyte Gracilaria vermiculophylla. Biological Invasions 16(5). [http://www.vliz.be/nl/catalogus?module=ref&refid=297347]
[25] Nyberg, C.D. (2007). Introduced marine macroalgae and habitat modifiers: the ecological role and significant attributes. PhD Thesis. Department of Marine Ecology, Göteborg University: Göteborg. 61 pp. [http://www.vliz.be/nl/catalogus?module=ref&refid=301938]
[26] Nyberg, C.D.; Thomsen, M.S.; Wallentinus, I. (2009). Flora and fauna associated with the introduced red alga Gracilaria vermiculophylla. Eur. J. Phycol. 44(3): 395-403. [http://www.vliz.be/en/imis?module=ref&refid=218162]
[27] Wijsman, J.W.M.; De Mesel, I. (2009). Duurzame schelpdiertransporten. IMARES Wageningen Report. Imares: Wageningen. 111 pp. [http://www.vliz.be/nl/catalogus?module=ref&refid=207323]
[28] Krueger-Hadfield, S.A.; Kollars, N.M.; Byers, J.E.; Greig, T.W.; Hammann, M.; Murray, D.C.; Murren, C.J.; Strand, A.E.; Terada, R.; Weinberger, F.; Sotka, E.E. (2016). Invasion of novel habitats uncouples haplo-diplontic life cycles. Mol. Ecol. 25(16): 3801-3816. [http://www.vliz.be/nl/catalogus?module=ref&refid=312443]
[29] Thomsen, M.S.; Wernberg, T.; Tuya, F.; Silliman, B.R. (2009). Evidence for impacts of nonindigenous macroalgae: a meta-analysis of experimental field studies. J. Phycol. 45(4): 812-819. [http://www.vliz.be/nl/catalogus?module=ref&refid=297350]
[30] Martínez-Lüscher, J.; Holmer, M. (2010). Potential effects of the invasive species Gracilaria vermiculophylla on Zostera marina metabolism and survival. Mar. Environ. Res. 69(5): 345-349. [http://www.vliz.be/en/imis?module=ref&refid=218315]
[31] Thomsen, M.S. (2010). Experimental evidence for positive effects of invasive seaweed on native invertebrates via habitat-formation in a seagrass bed. Aquat. Invasions 5(4): 341-346. [http://www.vliz.be/en/imis?module=ref&refid=218178]
[32] Byers, J.E.; Gribben, P.E.; Yeager, C.; Sotka, E.E. (2012). Impacts of an abundant introduced ecosystem engineer within mudflats of the southeastern US coast. Biological Invasions 14(12): 2587-2600. [http://www.vliz.be/nl/catalogus?module=ref&refid=297352]
[33] Munari, C.; Bocchi, N.; Mistri, M. (2015). Epifauna associated to the introduced Gracilaria vermiculophylla (Rhodophyta; Florideophyceae: Gracilariales) and comparison with the native Ulva rigida (Chlorophyta; Ulvophyceae: Ulvales) in an Adriatic lagoon. Ital. J. Zoolog. 82(3): 436-445. [http://www.vliz.be/nl/catalogus?module=ref&refid=297353]
[34] Tyler, A.C.; McGlathery, K.J. (2006). Uptake and release of nitrogen by the macroalgae Gracilaria vermiculophylla (Rhodophyta). J. Phycol. 42(3): 515-525. [http://www.vliz.be/en/imis?module=ref&refid=218207]
[35] Tyler, A.C.; McGlathery, K.J.; Macko, S.A. (2005). Uptake of urea and amino acids by the macroalgae Ulva lactuca (Chlorophyta) and Gracilaria vermiculophylla (Rhodophyta). Mar. Ecol. Prog. Ser. 294: 161-172. [http://www.vliz.be/en/imis?module=ref&refid=218206]
[36] Invasive Species Specialist Group (ISSG) (2013). issg.org. [http://www.issg.org/] (2013-07-17).
[37] Villanueva, R.D.; Sousa, A.M.M.; Gonçalves, M.P.; Nilsson, M.; Hilliou, L. (2010). Production and properties of agar from the invasive marine alga, Gracilaria vermiculophylla (Gracilariales, Rhodophyta). J. Appl. Phycol. 22(2): 211-220. [http://www.vliz.be/en/imis?module=ref&refid=218208]
VLIZ Alien Species Consortium (2024). Gracilaria vermiculophylla. Introduced alien species of the Belgian part of the North Sea and adjacent estuaries anno 2024. Flanders Marine Institute (VLIZ). 7 pp.