Caprella mutica - Japanese skeleton shrimp

The Japanese skeleton shrimp – commonly referred to as ‘skeleton’ or ‘ghost’ shrimps – occurs naturally along the coasts of Northeast Asia, near Japan ^[2]. There it lives attached to floating algae or aquaculture structures. Outside its natural habitat, this species is often found in harbours: on pontoons, buoys and other hard substrates and mussels or weeds ^[3].

First observation in Belgium

In January 1998 ^[4] the Japanese skeleton shrimp was first spotted on a buoy marking the entrance of the port of Zeebrugge ^[5].

Spreading in Belgium

Since 1999, Caprella mutica has been fairly common on pontoons in the marina of Zeebrugge, although a serious decline in numbers has been observed since 2007 ^[6]. It thrives near harbour constructions as well as in more inland waterways (e.g. Baudouin Canal) characterized by a substrate consisting of stones and vegetation ^[7]. Furthermore, the species has been spotted in the port of Ostend and on pontoons and buoys, both in open water and near the coast, at the mouth of the Scheldt estuary, Knokke-Heist, Zeebrugge, Blankenberge, Ostend, Nieuwpoort and Koksijde ^[4].

Spreading in neighbouring countries

The first sighting in the Netherlands – and the first sighting in Europe – dates from the summer of 1993, in the Roompotsluis (literal translation: ‘sluice of Roompot’) in the Eastern Scheldt. Through 1994, the species remained numerous here ^[8]. One year later, the species was spotted in the inner harbour of ‘Neeltje Jans’ (Eastern Scheldt) ^[4]. In 1995, individuals were found in Burghsluis, a Dutch town on the Eastern Scheldt ^[9]. Initially, it was thought to be a previously undiscovered species and it was named Caprella macho. Later, it turned out that the Japanese skeleton shrimp had already been described in 1935 under the name Caprella mutica, which is its official scientific name ^[10]. Since then, this animal has been found all along the Dutch coastline on ships’ hulls, fishing nets, harbour structures, pontoons, buoys and attached to algae ^{[4, 11]}.

From the Netherlands, the Japanese skeleton shrimp spread to the west coast of Scotland, where it has been spotted in 2000 ^[12]. Here, the Japanese skeleton shrimp is exceptionally successful, forming colonies of more than 300,000 animals per m² in some locations ^[13].

In the same year, the species was observed in the harbours of Sylt and Helgoland, two islands north of Germany ^[4]. As of 2003, the exotic species was found in Ireland ^[14] and also observed in Norway ^[4] and Sweden ^[15]. A recent study from 2014 reports Northwest Spain (Ría de Arousa) as the current southernmost occurrence of this species in European Atlantic waters ^[16].

Both shipping and import of Japanese oysters Crassostrea gigas facilitated the introduction of the Japanese skeleton shrimp into European waters ^[12]. The Japanese skeleton shrimp can travel to other regions both in the ballast water of ships and on their hulls ^[17].

Vectors for secondary introductions include the hulls of pleasure boats and floating debris or seaweed ^{[8, 18]}. The animal has three pairs of small legs on its abdomen which it can use to hook itself onto a suitable surface. But, this shrimp can move around freely as well ^[19].

In Europe, Caprella mutica is mainly found in anthropogenic environments. Both in highly exposed and sheltered areas and in areas with high and low salinity ^[18]. This exotic species likes to attach itself to other species that have soft structures (such as tunicates, bryozoans and polyps) or fine filamentous algae associated with hard artificial substrates, such as ropes, buoys and pontoons ^{[3, 13, 17, 18, 20-24]}. In our regions, the species is often associated with another exotic species, namely the Japanese wireweed (Sargassum muticum), which occurs abundantly in the coastal areas of the North Sea. This relationship has been confirmed in the port of Zeebrugge ^[25].

The reason why artificial substrates such as ropes and buoys in port areas are so popular with this species is that these substrates often float above the bottom, therefore being less accessible to potential benthic predators ^[21]. It is also shown that the species can survive in disturbed (polluted) areas that are unfavourable for native species. On the other hand, the Japanese skeleton shrimp exhibits aggressive behaviour towards conspecifics ^[21].

In addition, Japanese skeleton shrimps can reproduce very rapidly. Females produce two broods on average, the first as early as the 53^rd day of life and the second just 20 days later ^[13]. On average, a brood has 11 to 25 individuals ^[13], although exceptionally this can be as much as 300 ^[21].

Finally, Japanese skeleton shrimps are known to be opportunists in terms of their diet and the way they gather their food. They can choose between several feeding strategies, depending on the type of food present. If algae are the main food source present, the Japanese skeleton shrimp scrapes the surface of the algae. Diatoms can be filtered out of the water column by the small hairs on their antennae ^[26]. Finally, it has been shown that the species can also feed on fairy shrimps (Anostraca) and pick up deposited dead organic material from the soil ^[21]

The Japanese skeleton shrimp can survive in temperatures between -1.8 and 25 °C and in water with salinity varying between 16 and 40 PSU (brackish to saline water). In comparison, the seawater in the North Sea has an average salinity of 35 PSU. In practical terms, this means that the temperature and salinity of the North Sea are very suitable for this species. Inland waters, estuaries and some other seas, such as the Baltic and the Mediterranean, are less suitable because of their lower salinity or - in the case of the Mediterranean – the high water temperature ^{[21, 22]}. As the Japanese skeleton shrimp does not have a free-swimming larval stage, transport via attachment to different substrates plays the biggest role in the distribution of this species. Long-distance transport is mainly facilitated by shipping or with oysters. Recreational boating and floating seaweeds are responsible for secondary (i.e. local) dispersal ^[3].

The above factors, such as fast growth, short developmental period, high reproductive rate, high tolerance to varying environmental conditions, omnivorous diet and efficient dispersal, facilitate the successful spread of the Japanese skeleton shrimp. The only limiting factor is whether or not this shrimp can find a suitable substrate for its transport ^[25].

It is regularly reported that the Japanese skeleton shrimp occurs in high densities, up to even more than 300,000 individuals per m² ^[13]. This can cause competition for space with individuals of other species, although this has not been proven in-situ. In the laboratory, it turned out that the Japanese skeleton shrimp can indeed outcompete other (European) skeleton shrimps such as the linear skeleton shrimp Caprella linearis ^[27].

The Japanese skeleton shrimp is also considered a plague for aquaculture ^[28]. After all, the species is very common on and around the hanging cultures of aquaculture farms, such as mussel farms. High concentrations of these shrimps may cause clogging of water pipes and possibly prevent the settlement of mussel larvae on the mussel culture ropes, although the latter has not yet been proven ^[21].

To date, no attempts have been made to combat the Japanese skeleton shrimp. On the contrary, it is currently examined whether the animal could be used as fish food in aquaculture ^[21].

The Japanese skeleton shrimp is one of the biggest skeleton shrimps. With their elongated bodies, males can grow more than 25 mm. Females are much smaller and do not exceed 20 mm ^[20]. They are very variable in colour: from almost transparent, through light to dark brown and from orange to reddish, with the female's brood pouch speckled with red spots ^{[12, 29]}.

The body is divided into segments (pereonites). The third to seventh pereonites have dorsal and lateral spines. Characteristic of this species is that the first two body segments of the males are very hairy. The ends (gnathopods) on the second segment are enlarged and contain claws that are hairy in males, but not in females. Furthermore, there are three pairs of small hind legs and on the head two pairs of antennae of which the first pair is strongly elongated in males ^{[9, 12]}.

When searching for food, the Japanese skeleton shrimp erects itself and spreads its antennae and claws, waiting for prey. The shrimp attaches itself to the substrate using its final three pairs of legs. By adopting this position, small particles and organisms are filtered through the hairs of their antennas. Contrary to expectations, the claws aren’t used for foraging. Instead, they use their gnathopods to defend themselves or compete with other males for females ^[30]

[1]         World Register of Marine Species (WoRMS) (2020). Caprella mutica Schurin, 1935. [http://www.marinespecies.org/aphia.php?p=taxdetails&id=146768] (2020-11-17).

[2]         Arimoto, I. (1976). Taxonomic studies of caprellids (Crustacea, Amphipoda, Caprellidae) found in the Japanese and adjacent waters. Special publications from the Seto Marine Biological Laboratory 3(3): 1-229. [http://www.vliz.be/en/imis?module=ref&refid=7233]

[3]         Ashton, G.V.; Willis, K.J.; Cook, E.J. (2007). Distribution of the introduced amphipod, Caprella mutica Schurin, 1935 (Amphipoda: Caprellida: Caprellidae) on the west coast of Scotland and a review of its global distribution. Hydrobiologia 590: 31-41. [http://www.vliz.be/en/imis?module=ref&refid=140453]

[4]         Cook, E.J.; Jahnke, M.; Kerckhof, F.; Minchin, D.; Faasse, M.; Boos, K.; Ashton, G. (2007). European expansion of the introduced amphipod Caprella mutica Schurin 1935. Aquat. Invasions 2(4): 411-421. [http://www.vliz.be/en/imis?module=ref&refid=120472]

[5]         Kerckhof, F. (2001). National report for Belgium, 2000, in: ICES Advisory Committee on the Marine Environment. Report of the working group on introductions and transfers of marine organisms, Barcelona, Spain, 21–23 March 2001. CM Documents - ICES. CM 2001(ACME: 08). ICES: Copenhagen: pp. 24-26. [http://www.vliz.be/en/imis?module=ref&refid=208978]

[6]         De Blauwe, H.; Dumoulin, E. (2009). De zeefauna en -flora uit de jachthaven van Zeebrugge, in het bijzonder de fouling-organismen van drijvende pontons. De Strandvlo 29(2): 41-63. [http://www.vliz.be/imis/imis.php?module=ref&refid=139489]

[7]         Hebbelinck, L. (2010). Monitoring van exotische macro-invertebraten in de Vlaamse havens. MSc Thesis. Universiteit Gent, Faculteit Bio-Ingenieurswetenschappen: Gent. 87 pp. [http://www.vliz.be/en/imis?module=ref&refid=197447]

[8]         Faasse, M. (1996). Caprella macho Platvoet e.a., 1995, een nieuwe spookkreeft. Het Zeepaard 56: 2-3. [www.vliz.be/en/imis?module=ref&refid=141643]

[9]         Platvoet, D.; de bruyne, R.H.; Gmelig Meyling, A.W. (1995). Description of a new Caprella species from The Netherlands: Caprella macho nov. spec. (Crustacea, Amphipodam Caprellidae). Bull. Zool. Mus. Amsterdam 15(1): 1-4. [http://www.vliz.be/en/imis?module=ref&refid=140443]

[10]       Faasse, M. (2005). Notes on diagnostic characters and morphological variability of Caprella mutica Schurin, 1935 in The Netherlands (Crustacea: Amphipoda: Caprellidea). Het Zeepaard 65(1): 22-28. [www.vliz.be/en/imis?module=ref&refid=70639]

[11]       Faasse, M. (1999). Nieuwe vindplaatsen van de spookkreeft Caprella macho Platvoet et al. Het Zeepaard 59(3): 86-87. [www.vliz.be/en/imis?module=ref&refid=141645]

[12]       Willis, K.J.; Cook, E.J.; Lozano-Fernandez, M.; Takeuchi, I. (2004). First record of the alien caprellid amphipod, Caprella mutica, for the UK. J. Mar. Biol. Ass. U.k. 84(5): 1027-1028. [http://www.vliz.be/en/imis?module=ref&refid=67862]

[13]       Cook, E.J.; Willis, K.J.; Lozano-Fernandez, M. (2007). Survivorship, growth and reproduction of the non-native Caprella mutica Schurin (Crustacea: Amphipoda). Hydrobiologia 590: 55-64. [http://www.vliz.be/en/imis?module=ref&refid=140452]

[14]       Tierney, T.D.; Kane, F.; Naughton, O.; Kennedy, S.; O'Donohoe, P.; Copley, L.; Jackson, D. (2004). On the occurrence of the caprellid amphipod, Caprella mutica Schurin 1935, in Ireland. Ir. Nat. J. 27: 437-439. [http://www.vliz.be/en/imis?module=ref&refid=140427]

[15]       Daneliya, M.E.; Laakkonen, H. (2012). The Japanese skeleton shrimp Caprella mutica (Amphipoda: Caprellidae) in Sweden (Eastern Skagerrak). Marine Biodiversity Records 5(36). [http://www.vliz.be/nl/catalogus?module=ref&refid=312307]

[16]       Almón, B.; Pérez, J.; Bañón, R.; Trigo, J. (2014). First record of Caprella mutica from the Iberian Peninsula: expansion southwards in European waters. Marine Biodiversity Records 7(e30): 1-4. [http://www.vliz.be/nl/catalogus?module=ref&refid=297209]

[17]       Buschbaum, C.; Gutow, L. (2005). Mass occurrence of an introduced crustacean (Caprella cf. mutica) in the south-eastern North Sea. Helgol. Mar. Res. 59(3): 252-253. [http://www.vliz.be/en/imis?module=ref&refid=121455]

[18]       Mineur, F.; Cook, E.J.; Minchin, D.; Bohn, K.; Macleod, A.; Maggs, C.A. (2012). Changing coasts: marine aliens and artificial structures. Oceangr. Mar. Biol. Ann. Rev. 50: 189-234. [http://www.vliz.be/nl/catalogus?module=ref&refid=232757]

[19]       Boos, K.; Ashton, G.; Cook, E.J. (2011). The Japanese skeleton shrimp Caprella mutica (Crustacea, Amphipoda): A global invader of coastal waters, in: Galil, B.S. et al. In the wrong place - alien marine crustaceans: Distribution, biology and impacts, 6. Invading Nature - Springer Series in Invasion Ecology: pp. 129-156. [www.vliz.be/en/imis?module=ref&refid=205516]

[20]       Ruppert, E.E.; Barnes, R.D. (1994). Invertebrate zoology. 6th edition. Saunders College Publishing: Orlando. ISBN 0-03-026668-8. 1056 pp. [http://www.vliz.be/nl/catalogus?module=ref&refid=9414]

[21]       Boets, P.; Lock, K.; Goethals, P.L.M. (2012). Assessing the importance of alien macro-Crustacea (Malacostraca) within macroinvertebrate assemblages in Belgian coastal harbours. Helgol. Mar. Res. 66(2): 175-187. [http://www.vliz.be/en/imis?module=ref&refid=206987]

[22]       Caine, E.A. (1977). Feeding mechanism and possible resource partitioning of the caprillidae (Crustacea: Amphipoda) from Puget Sound, USA. Mar. Biol. (Berl.) 42(4): 331-336. [http://www.vliz.be/en/imis?module=ref&refid=140513]

[23]       Ashton, G.; Willis, K.J.; Burrows, M.; Cook, E.J. (2007). Environmental tolerance of Caprella mutica: implications for its distribution as a non-native species. Mar. Environ. Res. 64(3): 305-312. [http://www.vliz.be/en/imis?module=ref&refid=140456]

[24]       Shucksmith, R.; Cook, E.J.; Hughes, D.J.; Burrows, M.T. (2009). Competition between the non-native amphipod Caprella mutica and two native species of caprellids Pseudoprotella phasma and Caprella linearis. J. Mar. Biol. Ass. U.K. 86(6): 1125-1132. [http://www.vliz.be/en/imis?module=ref&refid=141647]

[25]       ICES Advisory Committee on the Marine Environment (2004). Report of the Working Group on Introductions and Transfers of Marine Organisms (WGITMO), 25–26 March 2004, Cesenatico, Italy. CM Documents - ICES. CM 2004(ACME:05 Ref. E, G). ICES: Copenhagen. 147 pp. [http://www.vliz.be/en/imis?module=ref&refid=141648]

[26]       Faasse, M. (2019). Persoonlijke mededeling

[27]       Stichting ANEMOON (2018). Harige spookkreeft Caprella mutica Schurin, 1935. [http://www.anemoon.org/flora-en-fauna/soorteninformatie/soorten/id/326/harige-spookkreeft] (2018-08-06).

[28]       Cook, E.J.; Black, K.D.; Sayer, M.D.J.; Cromey, C.J.; Angel, D.L.; Spanier, E.; Tsemel, A.; Katz, T.; Eden, N.; Karakassis, I.; Tsapakis, M.; Apostolaki, E.T.; Malej, A. (2006). The influence of caged mariculture on the early development of sublittoral fouling communities: a pan-European study. ICES J. Mar. Sci./J. Cons. int. Explor. Mer 63(4): 637-649. [http://www.vliz.be/nl/catalogus?module=ref&refid=297210]

[29]       Ashton, G.V. (2007). Distribution and dispersal of the non-native caprellid amphipod, Caprella mutica Schurin 1935. PhD Thesis. University of Aberdeen: Scotland. vii, 180 pp. [http://www.vliz.be/nl/catalogus?module=ref&refid=300088]

[30]       Shucksmith, R. (2007). Biological invasions: the role of biodiversity in determining community susceptibility to invasion. PhD Thesis. University of Aberdeen: Scotland.  pp. [http://www.vliz.be/nl/catalogus?module=ref&refid=300089]

VLIZ Alien Species Consortium (2024). Caprella mutica – Japanese skeleton shrimp. Introduced alien species of the Belgian part of the North Sea and adjacent estuaries anno 2024. Flanders Marine Institute (VLIZ). 7 pp.