Boccardia proboscidea -

B. proboscidea is native to the North Pacific Ocean and occurred along the coasts of North America ^[2].

First observation in Belgium

In 2011, the bristle worm B. proboscidea was first reported from the southern North Sea ^[3].

Spreading in Belgium

The species occurs in limited numbers in ephemeral (temporal) habitats along the Belgian coast (i.e. habitats with limited fauna and flora during winter and recolonization in spring). Most likely, the species has permanently established itself in our country since it has been observed multiple times since its discovery in 2011. In Belgium, the species has been observed in Koksijde, Ostend and Zeebrugge. B. proboscidea is found on groynes in the lower intertidal zone and higher up, between barnacles, green algae and small mussels. In these locations, it is often the only spionid (Family Spionidae) that occasionally appears in large numbers ^[3].

Spreading in neighbouring countries

The species was first identified in Europe along the Spanish coast of the Basque country in 1996 ^[3]. The species got also observed along the Iberian coast, in the Gulf of Biscay ^{[4, 5]}. Along the coast of Scotland, the species has been observed on the island of Skye ^[6].

In the Netherlands, B. proboscidea has been observed in Vlissingen, Borssele, Zierikzee, Goese Sas and Yerseke. There, it often occurs in artificially heated seawater (Borssele). Its distribution is not restricted by this ^[3].

Along the French coast, the species is present in the Gulf of Biscay and the English Channel ^[7].

Currently, the species has an almost cosmopolitan distribution in temperate seas ^[3].

B. proboscidea occurs close to shipping routes and aquaculture zones for crustaceans. Most likely, it got introduced to Belgium and the Netherlands with transported crustaceans for aquaculture purposes. However, transport on ship hulls (biofouling) or as larvae in the ballast water cannot be ruled out ^[3]. Indeed, the presence of large ports such as Antwerp and Rotterdam makes shipping in this region a major vector for biological invasions ^{[8, 9]}. After the primary introduction, the species can disperse independently, stimulated by increased anthropogenic solid structures. In this way, permanent populations settled in the southern North Sea ^[3].  

B. proboscidea produces capsules containing in addition to the larvae some non-viable eggs. These eggs serve as a food source for the developing larvae within that same capsule. This additional food source allows the larvae to grow fast and hatch as juvenile organisms in just 11 days. Because of this, locally abundant populations can develop in a short period of time. On the other hand, the species produces planktotrophic larvae that stay long in the water column and need 19-36 days to develop into juveniles ^[10-12]. This additional characteristic promotes the spread of the species over larger areas ^[3].

B. proboscidea is frequently found near locations characterized by an outflow of urban wastewater. Increased concentrations of organic matter in sediment and lower salinity prove beneficial for the population size ^[13]. However, the preference for low salinity in these studies is probably related to the specificity of the research, in which the effect of sewage on the bristle worm was investigated. The worms showed a preference for fresh sewage because it has a higher nutrient content. The species usually occurs in seawater and brackish water but can tolerate high salinity, as it also occurs in pools at high tide ^[14].

The development of different types of larvae is influenced by temperature. At lower temperatures (12-17°C), the planktotrophic larvae are better able to develop, while the crawling larvae do better at higher temperatures (24-28°C). Therefore, the species can survive and develop in a wide range of temperatures, which benefits its dispersal capacity ^[15].

The occurrence of bristle worms, belonging to the family Spionidae (mud worms), causes concern among oyster farmers. Some of these species can drill holes in calcareous substrates such as the shells of molluscs ^[16-19]. This causes blistering and leads to a significant reduction in growth and survival ^[20]. B. proboscidea is a secondary driller ^[2]. However, some spionids exhibit different behaviours in different regions (drilling versus non-drilling, building tubes versus no tubes) ^[21].

B. proboscidea can form large mats of aggregated tubes in contaminated and demolished habitats, eliminating other types of sessile invertebrates ^[22-25]. In Mar del Plata (Argentina), the establishment of B. proboscidea got facilitated by sewage water. The species dominated and outcompeted the native mussel species, Brachidontes rodriguezii. As a result, the rise of B. proboscidea caused a reduction of species density and diversity ^[26].

B. proboscidea has a slim and elongated body, divided into 125 to 150 segments. The species is on average between 30 and 35 millimetres long but may grow longer. The maximum width is approximately 1.5 millimetres near the 8^th to 16^th segment. This worm has a deep yellow to orange colour with red branchial filaments ^[27]. There is usually a remarkable black spot on its head.

The essentially non-drilling B. proboscidea (secondary driller ^[17]) can move quickly, allowing it to flee or build a new tube as soon as it is removed from its habitat ^[28].

B. proboscidea has a wide ecological amplitude. It makes tunnels in different sizes and forms, in muddy to sandy sediments or in existing tunnels in soft rocks and shells of molluscs. In addition, it can be found between the algae and mussels ^{[2, 4, 11, 18, 27, 29, 30]}. The species is an indicator for organic enrichment of sediments and often occurs in large numbers ^{[22, 24, 25]}.

[1]          World Register of Marine Species (WoRMS) (2020). Boccardia proboscidea Hartman, 1940. [http://www.marinespecies.org/aphia.php?p=taxdetails&id=327249] (2020-11-17).

[2]          Simon, C.A.; Worsfold, T.M.; Lange, L.; Sterley, J. (2010). The genus Boccardia (Polychaeta: Spionidae) associated with mollusk shells on the south coast of South Africa. J. Mar. Biol. Ass. U.K. 90(3): 585-598. [http://www.vliz.be/nl/catalogus?module=ref&refid=296720]

[3]          Kerckhof, F.; Faasse, M.A. (2014). Boccardia proboscidea and Boccardiella hamata (Polychaeta: Spionidae: Polydorinae), introduced mud worms new for the North Sea and Europe, respectively. Marine Biodiversity Records 7(76): 1-9. [http://www.vliz.be/en/imis?module=ref&refid=240728]

[4]          Martínez, J.; Adarraga, I.; López, E. (2006). Nuevos datos del género Boccardia Carazzi, 1893 (Polychaeta: Spionidae) para la península Ibérica y el océano Atlántico. Bol. Inst. Esp. Oceanogr. 22(1): 53-64. [http://www.vliz.be/nl/catalogus?module=ref&refid=296695]

[5]          López, E.; Richter, A. (2017). Non-indigenous species (NIS) of polychaetes (Annelida: Polychaeta) from the Atlantic and Mediterranean coasts of the Iberian Peninsula: an annotated checklist. Helgol. Mar. Res. 71(19): 1-17. [http://www.vliz.be/nl/catalogus?module=ref&refid=290097]

[6]          Hatton, J.; Pearce, B. (2013). The first documented record of the non-native spionid Boccardia proboscidea in UK waters. Marine Biodiversity Records 6(e101): 1-4. [http://www.vliz.be/nl/catalogus?module=ref&refid=285150]

[7]          Spilmont, N.; Hachet, A.; Faasse, M.A.; Jourde, J.; Luczak, C.; Seuront, L.; Rolet, C. (2016). First records of Ptilohyale littoralis (Amphipoda: Hyalidae) and Boccardia proboscidea (Polychaeta: Spionidae) from the coast of the English Channel: habitat use and coexistence with other species. Mar. Biodiv. 48(2): 1109-1119. [http://www.vliz.be/nl/catalogus?module=ref&refid=299234]

[8]          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]

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[11]        Gibson, G.; Paterson, I.G.; Taylor, H.; Woolridge, B. (1999). Molecular and morphological evidence of a single species, Boccardia proboscidea (Polychaeta: Spionidae), with multiple development modes. Mar. Biol. (Berl.) 134(4): 743-751. [http://www.vliz.be/nl/catalogus?module=ref&refid=296697]

[12]        Oyarzun, F.X.; Mahon, A.R.; Swalla, B.J.; Halanych, K.M. (2011). Phylogeography and reproductive variation of the poecilogonous polychaete Boccardia proboscidea (Annelida: Spionidae) along the West Coast of North America. Evolution & development 13(6): 489-503. [http://www.vliz.be/nl/catalogus?module=ref&refid=296741]

[13]        Garaffo, G.V.; Jaubet, M.L.; Sánchez, M.A.; Llanos, E.N.; Vallarino, E.A.; Elias, R. (2016). Modelling the influence of environmental and weather factors on the density of the invasive polychaete Boccardia proboscidea. Mar. Ecol. 37(6): 1256-12656. [http://www.vliz.be/nl/catalogus?module=ref&refid=296698]

[14]        Hartman, O. (1941). Some contributions to the biology and life story of Spionidae from California:  With keys to species and genera and descriptions of two new forms. NOAA tech. memo. 7(4): 289-323 (Pl. 45-48). [http://www.vliz.be/nl/catalogus?module=ref&refid=285171]

[15]        David, A.A.; Simon, C., A. (2014). The effect of temperature on larval development of two non-indigenous poecilogonous polychaetes (Annelida: Spionidae) with implications for life history theory, establishment and range expansion. J. Exp. Mar. Biol. Ecol. 461: 20-30. [http://www.vliz.be/nl/catalogus?module=ref&refid=296699]

[16]        Hoeksema, B.W. (1983). Excavation patterns and spiculae dimensions of the boring sponge Cliona celata from the SW Netherlands. Senckenb. Marit. 15(1-3): 55-85. [http://www.vliz.be/nl/catalogus?module=ref&refid=296700]

[17]        Bailey-Brock, J.H. (2000). A new record of the polychaete Boccardia proboscidea (Family Spionidae), imported to Hawai’i with oysters. Pac. Sci. 54(1): 27-30. [http://www.vliz.be/nl/catalogus?module=ref&refid=296701]

[18]        Ruellet, T. (2004). Infestation des coquilles d’huîtres Crassostrea gigas par les polydores en Basse-Normandie: recommendations et mise au point d’un traitement pour réduire cette nuisance = Infestation of the oyster shells Crassostrea gigas by polydorid species in Normandy (France): recommendations and treatment to reduce this harmful effect. PhD Thesis. Université de Caen/Basse-Normandie: Caen. 537 pp. [http://www.vliz.be/nl/catalogus?module=ref&refid=296703]

[19]        Simon, C.A.; Thornhill, D.J.; Oyarzun, F.; Halanych, K.M. (2009). Genetic similarity between Boccardia proboscidea from Western North America and cultured abalone, Haliotis midae, in South Africa. Aquaculture 294(1-2): 18-24. [http://www.vliz.be/nl/catalogus?module=ref&refid=296704]

[20]        Sato-Okoshi, W.; Okoshi, K. (1997). Survey of the genera Polydora, Boccardiella and Boccardia (Polychaeta, Spionidae) in Barkley Sound (Vancouver Island, Canada), with special reference to boring activity. Bull. Mar. Sci. 60(2): 482-493. [http://www.vliz.be/nl/catalogus?module=ref&refid=296705]

[21]        Radashevsky, V.I.; Pankova, V.V. (2013). Shell-boring versus tube-dwelling: is the mode of live fixed or flexible? Two cases in spionid polychaetes (Annelida, Spionidae). Mar. Biol. (Berl.) 160(7): 1619-1624. [http://www.vliz.be/nl/catalogus?module=ref&refid=296725]

[22]        Johnson, R.G. (1970). Variations in diversity within benthic marine communities. American Naturalist 104(937): 285-300. [http://www.vliz.be/nl/catalogus?module=ref&refid=296726]

[23]        Daro, M.H.; Polk, P. (1973). The autecology of Polydora ciliata along the Belgian coast. Neth. J. Sea Res. 6(1-2): 130-140. [http://www.vliz.be/nl/catalogus?module=ref&refid=3470]

[24]        Blake, J.A.; Kudenov, J.D. (1978). The Spionidae (Polychaeta) from south-eastern Australia and adjacent areas with a revision of the genera. Mem. Natl. Mus. Vic. 39: 171-280. [http://www.vliz.be/nl/catalogus?module=ref&refid=296728]

[25]        Jaubet, M.L.; de los Ángeles Sánchez, M.; Rivero, M.S.; Garaffo, G.V.; Vallarino, E.A.; Elías, R. (2011). Intertidal biogenic reefs built by the polychaete Boccardia proboscidea in sewage-impacted areas of Argentina, SW Atlantic. Mar. Ecol. (Berlin) 32(2): 188-197. [http://www.vliz.be/nl/catalogus?module=ref&refid=296730]

[26]        Elías, R. (2015). Effect of the invader Boccardia proboscidea (Polychaeta: Spionidae) on richness, diversity and structure of SW Atlantic epilithic intertidal community. Mar. Pollut. Bull. 91(2): 530-536. [http://www.vliz.be/nl/catalogus?module=ref&refid=296731]

[27]        Hartman, O. (1940). Boccardia proboscidea, a new species of spionid worm from California. J. Wash. Acad. Sci. 30: 382-387. [http://www.vliz.be/nl/catalogus?module=ref&refid=285170]

[28]        Sato-Okoshi, W. (2000). Polydorid species (Polychaeta: Spionidae) in Japan, with descriptions of morphology, ecology, and burrow structure. 2. Non-boring species. J. Mar. Biol. Ass. U.K. 80(3): 443-456. [http://www.vliz.be/nl/catalogus?module=ref&refid=296734]

[29]        Woodwick, K.H. (1963). Taxonomic revision of two polydorid species (Annelida, Polychaeta, Spionidae). Proc. Biol. Soc. Wash. 76: 209-216. [http://www.vliz.be/nl/catalogus?module=ref&refid=296739]

[30]        Read, G.B. (2018). Guide to New Zealand shell polychaetes. [http://www.annelida.net/nz/Polychaeta/ShellsPoly/NZShellsPolychaeta.htm] (2018-07-23).

VLIZ Alien Species Consortium (2020). Boccardia proboscidea. Non-indigenous species in the Belgian part of the North Sea and adjacent estuaries anno 2020. Flanders Marine Institute (VLIZ). 6 pp.