The invasive, non-native slipper limpet Crepidula fornicata is poorly adapted to sediment burial
Graphical abstract
Introduction
Non-native species (NNS) are not naturally found within a certain area and are also referred to as “non-indigenous”, “alien” and “exotic” species (Manchester and Bullock, 2000). An invasive NNS (INNS) is a species that passed all stages of the invasion process including its release into a new environment, establishment and subsequent spread (Richardson et al., 2000; Bohn et al., 2015). INNS can cause harm to the environment and are regarded as one of the biggest threats to global biodiversity by outcompeting and dominating native species and often entire ecosystems (Thouzeau et al., 2000; Bax et al., 2003). Globalisation and human activity have both accidentally and deliberately transported INNS across major geographic barriers for centuries (Decottignies et al., 2007; Mineur et al., 2012). It is estimated that at any one time, 10,000 species are in transit around the world in ballast water, making it almost impossible to control the spread of species to new habitats (Manchester and Bullock, 2000; Bax et al., 2003). >90 marine and brackish NNS have been identified in Britain and Ireland alone (Cook et al., 2015). Many NNS bring diseases, modify habitats and affect ecosystem functioning and can have indirect interactions with intermediate and top predators (Cook et al., 2015; Grason and Buhle, 2016). The extent to which a NNS impacts a community depends on its interactions with native species (Grason and Buhle, 2016).
The American slipper limpet, Crepidula fornicata is one of the most invasive non-native sessile invertebrates in Europe (Dupont et al., 2007). It is a suspension-feeding marine gastropod native to North America (Hancock, 1969; Clark, 2008). Its shell grows up to 50 mm in length, 25 mm in height, with a kidney shaped aperture and individuals attach to each other forming stacks (Clark, 2008) (Fig. 1). Human-mediated transport and its long-lived, free-swimming planktonic larvae have caused it to spread rapidly throughout Europe (Untersee and Pechenik, 2007; Rigal et al., 2010). In the UK, C. fornicata extends from Pembrokeshire to Yorkshire including the Bristol Channel (Clark, 2008). Hotspots include the Solent and Essex where C. fornicata forms a carpet over the seafloor, producing cohesive pseudofaeces as it filter feeds (Hancock, 1969; Thouzeau et al., 2000; Clark, 2008; Syvret and FitzGerald, 2008). In the UK C. fornicata was introduced to Essex attached to oysters, Crassostrea virginica, between 1887 and 1890 and is now well known as their most abundant competitor (Orton, 1912; Clark, 2008; Bohn et al., 2013). The limpet can be found in most oyster producing areas in England and Wales where it occurs in enormous numbers (Hancock, 1969; Thieltges, 2005; Clark, 2008). The limpet competes with oysters and other suspension feeders for space and food (Hancock, 1969; de Montaudoüin et al., 2001; Moulin et al., 2007). Populations of the blue mussel Mytilus edulis can decrease dramatically when overgrown by slipper limpets (Nehls et al., 2006). The influence of C. fornicata on commercially important shellfish species can have huge economic implications (Thieltges, 2005). C. fornicata modifies the nature and structure of habitat through biodeposition and the accumulation of its shells, often creating an unsuitable substratum for many native species (Thieltges, 2005; Valdizan et al., 2009).
Its success can be explained by its strong reproductive viability and opportunistic feeding strategies together with the fact that it has few natural predators (Dupont et al., 2007; Clark, 2008; Syvret and FitzGerald, 2008; Valdizan et al., 2009). It is also tolerant to a wide range of salinities (Syvret and FitzGerald, 2008; Rigal et al., 2010) and is found attached to a variety of substrates in the low intertidal and subtidal (Bohn et al., 2013; Cook et al., 2015). C. fornicata is a protandrous hermaphrodite that breeds from February to October and has a long-distance dispersal ability (Dupont et al., 2007). The availability of suitable substratum for settlement is crucial in determining its distribution (Barnes et al., 1973).
Numerous methods have been employed to eradicate C. fornicata. Earliest attempts focused on eradication by dumping dredged C. fornicata above the high water mark and removing them by hand (Hancock, 1969; Bolam et al., 2010; Cook et al., 2015). Since the 1950s, brine dipping has been trialed (Syvret and FitzGerald, 2008); brine immersion for over 5 min resulted in 100% mortality (Syvret and FitzGerald, 2008). This method is however not practical, especially for large amounts of material (Cook et al., 2015). Other attempts crushed C. fornicata stacks and fed their flesh to scavenging birds, or it was used as whelk bait (Hancock, 1969; Clark, 2008; Valdizan et al., 2009). Chain riddles were used to break up stacks in Kent and Essex (Cook et al., 2015). This disturbance had, however, the unintended consequence to act as a dispersal vector for C. fornicata, further exacerbating the problem (Clark, 2008; Cook et al., 2015). The slipper limpet was successfully eradicated from a commercial mussel lay in Wales, UK, by smothering with seed mussels of double the usual stocking density (Syvret and FitzGerald, 2008; Cook et al., 2015). In the United States, INNS including C. fornicata, have been smothered with heavy duty polythene sheeting and then relayed with oysters (Hancock, 1969), but this method was extremely costly and time consuming.
The disposal of dredged material during the construction and maintenance of coastal infrastructure represents a significant problem in coastal management (Marmin et al., 2014; Callaway, 2016). >40 million tons of sediment must be disposed of appropriately each year (Bolam, 2011). Following dredge spoil dumping, changes in benthic communities are commonly reported since many species are smothered with sediment (Hutchinson et al., 2016). The greatest ability to emerge from burial for a range of macroinvertebrates is 2 cm depth (Hendrick et al., 2016). Changes in the community structure are not restricted to the site of disposal and are often found kilometers away from the dumping area (Hendrick et al., 2016). The ability of species to escape burial through vertical migration is not well understood (Bolam, 2011). The tolerance and responses of species to burial are species specific and cannot be generalized; species tolerance to burial depends on its adaptation and behaviour (Hendrick et al., 2016). Following burial, benthic invertebrates may recover by vertical or lateral migration and/or the planktonic recruitment of larvae (Bolam, 2011). Emergence from sediment burial is central to the chance of survival since failure to re-surface is assumed to eventually lead to death (Bolam, 2011; Hendrick et al., 2016).
During the construction and maintenance of coastal infrastructure dredged spoil is disposed at designated sites. Dredged material may contain INNS, but legislation prohibits their release and spread (http://www.legislation.gov.uk/ukpga/1981/69/section/14). However, C. fornicata may not survive the dredging and disposal process. We hypothesized that smothering methods may kill any alive C. fornicata in dredge spoils. While some speculative assessment of the intolerance of C. fornicata to burial has been made there is a lack of evidence to support assumptions for informed management decisions (Johnson, 1972; Rayment, 2008; Cook et al., 2015; Syvret and FitzGerald, 2008). The aim of this study was therefore to assess the mortality of C. fornicata under sediment burial to determine whether smothering could be an effective way to prevent its spread. A multifactorial experiment was conducted to test burial intolerance using various burial depths and durations, and both stacks and individuals of C. fornicata were assessed.
This study had the following objectives
- i)
Identification of the preferred habitat of C. fornicata;
- ii)
Assessment of C. fornicata presence at a dredge spoil disposal site;
- iii)
Quantification of survival rates of C. fornicata under different sediment burial regimes.
Section snippets
Study site
Intertidal and subtidal C. fornicata surveys were carried out in Swansea Bay, South Wales, UK (Fig. 2). Swansea Bay is located along the northern coastline of the Bristol Channel and has the second largest tidal range in the world with mean spring tides of 8.5 m and neap tides of 4.1 m (Collins et al., 1979; Smith and Shackley, 2006). The bay stretches roughly 12 km from Mumbles Head to Port Talbot with the Eastern side facing directly towards the Atlantic Ocean (Collins and Banner, 1980;
Intertidal surveys
A total of 1416 C. fornicata individuals were recorded during the intertidal surveys. The slipper limpet was present at 30.2% of stations surveyed (n = 262) and 18.2% of quadrats (n = 770) from all 5 survey sites in densities up to 412 individuals per m2 (Fig. 5). No C. fornicata were recorded at sandy site Blackpill. C. fornicata density was highest at the Swansea East site, especially towards the breakwater, and it was generally more abundant towards the lower shore. According to the Phase I
Discussion
This study showed that the invasive, non-native slipper limpet Crepidula fornicata was present in intertidal habitats, but it was not found at a nearby subtidal dredge spoils disposal ground. Generally, benthic species can be severely impacted by dredge materials and traditional methods of discarding dredged spoils often result in burial depths that exceed the emergence ability of the resident fauna (Wilber et al., 2007). Disposal of sediment in thin layers <15 cm deep potentially allows
Acknowledgements
We are grateful to Swansea Bay Tidal Lagoon for co-funding the project, particularly to Gill Lock. Thanks to the skipper Keith Naylor for his assistance with boat work and setting up laboratory tanks. Chiara Bertelli, Dr. Christopher Lowe, Rebecca Stone and Duncan Dumbreck assisted with field work. Thanks to Ben Wray, Gabrielle Wyn and Maggie Hatton-Ellis from Natural Resources Wales as well as Prof. Stuart Jenkins for their advice. This work was a KESS project part-funded by the European
References (60)
- et al.
Marine invasive alien species: a threat to global biodiversity
Mar. Policy
(2003) - et al.
Larval microhabitat associations of the non-native gastropod Crepidula fornicata and effects on recruitment success in the intertidal zone
J. Exp. Mar. Biol. Ecol.
(2013) - et al.
A laboratory assessment of the survival and vertical movement of two gastropod species, Hydrobia ulvae (pennant) and Littorina littorea (Linnaeus), after burial in sediment
J. Exp. Mar. Biol. Ecol.
(1998) - et al.
Chapter 11 sediment transport by waves and tides: problems exemplified by a study of Swansea Bay, Bristol Channel
Elsevier Oceanog. Ser.
(1980) - et al.
The hydrodynamics and sedimentology of a high (tidal and wave) energy embayment (Swansea Bay, northern Bristol Channel)
Estuar. Coast. Mar. Sci.
(1979) - et al.
Maintaining turbidity and current flow in laboratory aquarium studies, a case study using Sabellaria spinulosa
J. Exp. Mar. Biol. Ecol.
(2009) - et al.
Trophic interactions between two introduced suspension feeders, Crepidula fornicata and Crassostrea gigas, are influenced by seasonal effects and qualitative selection capacity
J. Exp. Mar. Biol. Ecol.
(2007) - et al.
Comparing the influence of native and invasive intraguild predators on a rare native oyster
J. Exp. Mar. Biol. Ecol.
(2016) - et al.
Collaborative approach for the management of harbor-dredged sediment in the bay of seine (France)
Ocean Coast. Manag.
(2014) - et al.
Estimating the spatial distribution of dredged material disposed of at sea using particle-size distributions and metal concentrations
Mar. Pollut. Bull.
(2009)
Using KCL to determine size at competence for larvae of the marine gastropod Crepidula fornicata (L.)
J. Exp. Mar. Biol. Ecol.
Effects of the closure of a major sewage outfall on sublittoral, soft sediment benthic communities
Mar. Pollut. Bull.
Comparative studies on the influence of oxygen deficiency and hydrogen sulphide on marine bottom invertebrates
Neth. J. Sea Res.
Rôle des interactions biotiques sur le devenir du prè-recrutement et la croissance de Pecten maximus (L.) en rade de Brest
Life Sci.
Responses of benthic macroinvertebrates to thin-layer disposal of dredged material in Mississippi sound, USA
Mar. Pollut. Bull.
A preliminary survey of the macro-scopic bottom fauna of the Solent, with particular reference to Crepidula fornicata and Ostrea edulis
Proc. Malacol. Soc. Lond.
The effect of substrate disturbance and burial depth on the venerid clam, Katelysia scalarina
J. Shellfish Res.
Recent expansion of the slipper limpet population (Crepidula fornicata) in the bay of Mont-saint-Michael (Western Channel, France)
Aquat. Living Resour.
The Distribution and Potential Northwards Spread of the Non-native Gastropod Crepidula fornicata in Welsh Coastal Waters. PhD dissertation
The invasive gastropod Crepidula fornicata: Reprodution and recruitment in the intertidal at its northernmost range in Wales, UK, and implications for its secondary spread
Mar. Biol.
The distribution of the invasive non-native gastropod Crepidula fornicata in the Milford haven waterway, its northernmost population along the west coast of Britain
Helgol. Mar. Res.
Burial survival of benthic macrofauna following deposition of simulated dredged material
Environ. Monit. Assess.
Vertical migration of macrofauna following sediment placement on intertidal mudflats: an in situ experiment
Macrofaunal recolonisation following the intertidal placement of fine-grained dredged material
Environ. Monit. Assess.
Historical data reveal 30-year persistence of benthic fauna associations in heavily modified waterbody
Front. Mar. Sci.
Classification of bivalve mollusc production areas in England and Wales
Distribution of Slipper Limpet (Crepidula fornicata) Around the South Devon coast
Marine biosecurity: protecting indigenous marine species
Res. Rep. Biodi. Stud.
The influence of organic material and temperature on the burial tolerance of the blue mussel, Mytilus edulis: considerations for the management of marine aggregate dredging
PLoS One
Why does the introduced gastropod Crepidula fornicata fail to invade Arcachon Bay (France)?
J. Mar. Biol. Assoc. UK
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