Collin, R.

Cragg, Simon

Farrell, Paul

English

Portsmouth University Research Portal (Pure)

 Aquatic Invasions (2009) Volume 4, Issue 2: 377-380 
DOI  10.3391/ai.2009.4.2.13 
© 2009 The Author(s) 
Journal compilation © 2009 REABIC (http://www.reabic.net) 
This is an Open Access article 
 
 
 377
Short communication 
Confirmation of the identification and establishment of the South American 
slipper limpet Crepipatella dilatata (Lamark 1822) (Caenogastropoda: 
Calyptraeidae) in Northern Spain 
Rachel Collin1*, Paul Farrell2 and Simon Cragg2 
1Smithsonian Tropical Research Institute, Apartado Postal 0843-03092, Balboa, Ancon, Republic of Panama 
E-mail: collinr@si.edu  
2School of Biological Sciences, Institute of Marine Sciences, Ferry Road, Portsmouth P04 9LY, UK 
E-mails:  Paul.Farrell@port.ac.uk, Simon.Cragg@port.ac.uk 
*Corresponding author 
Received 22 February 2009; accepted in revised form 16 March 2009; published online 3 April 2009 
Abstract 
Calyptraeid gastropods have been introduced frequently in bays and ports around the world, and have become rampantly invasive 
in several cases. Here we confirm the identification and establishment of a recently-detected population of Crepipatella in 
northern Spain. Because their shells do not have many diagnostic features, introductions of calyptraeids are often accompanied 
by confusion about the identity and therefore origin of the species in question. We use DNA sequence data and developmental 
observations to verify the species identity of this population as the South American species Crepipatella dilatata. The apparently 
rapid spread of this species, which lacks a larval stage, may be due to human action. 
 
Key words:  Galicia, Crepidula, barcode, COI, direct development, exotic species 
 
Several species of calyptraeid gastropods 
(slipper limpets, cup-and-saucer limpets, and hat 
limpets) have been introduced and established 
populations outside their native ranges. Although 
many of these are restricted to small, local 
populations, two are now particularly widespread 
and abundant. Crepidula fornicata (Linnaeus, 
1758), native to eastern North America, has 
invaded much of the northern coast of Europe 
and the English Channel, since its introduction to 
England at the turn of the century (Blanchard 
1997; Minchin et al. 1995). In many areas of 
introduction, C. fornicata is a serious pest of 
commercial shellfisheries (Blanchard 1997), and 
is the dominant benthic species in many areas of 
the Solent UK, reaching densities of 1229 m-2 
(Farrell, unpublished). This species has also been 
reported in the Mediterranean (Gofas and 
Zenetos 2003). Crepidula onyx Sowerby, 1824, 
is a species similar to C. fornicata native to 
southern California. Crepidula onyx was first 
reported in Japan in 1968 (Woodruff et al. 1986), 
and is now widespread in Korea, Japan, and 
Hong Kong (Choe and Park 1992; Ekawa 1985; 
Morton 1987). 
The initial documentation of many introduced 
calyptraeids has been fraught with taxonomic 
confusion and misidentifications. For example, 
Asian populations of Crepidula onyx, a well-
known species from Southern California were 
originally identified as Crepidula fornicata. This 
mis-identification was corrected 20 years ago 
(Huang et al. 1983; Woodruff et al. 1986) but is 
still present in online databases of introduced 
species (e.g., DAISIE and BIOTIC [Rayment 
2008]). Similarly, a population of Crepidula 
convexa Say 1822 in Humbolt Bay on the West 
coast of the United States was initially identified 
as C. fornicata (Carlton 1992). The identification 
was corrected using evidence from DNA 
sequence data 16 years later (McGlashan et al. 
2008).  In this case, the shells of the two species 
can be distinguished and the mode of 
development also differs.  However, in many 
 
R .  Co l l i n  e t  a l .  
378 
cases closely related calyptraeids cannot be 
distinguished without developmental or genetic 
data (Collin 2001, 2005; Collin et al. 2007; Veliz 
et al. 2003).  Such propagation of taxonomic 
errors and the long time necessary to discover 
and correct them make it doubly important to 
carefully verify difficult species identifications 
when exotic species are first discovered. 
Northern Europe has a single native 
calyptraeid, Calyptraea chinensis (Linnaeus, 
1758), making detection of exotic calyptraeids 
relatively straightforward.  However the correct 
species-level identification of exotics is not 
always so easy.  The recent reported introduction 
of Crepipatella dilatata in Baia de Aldan (Rolán 
and Horro 2005) is noted by the authors to be a 
potentially ambiguous identification due to the 
existence of a morphologically cryptic sister 
species.  The original report was based primarily 
on the description of shell characters and body 
color (Rolan and Horro 2005). An additional site 
was subsequently also reported incidentally for 
2005 in a review of introduced gastropods in 
Galicia (O Grove Bay; Bañon et al. 2008).  
There are six species of Crepipatella (Collin 
et al. 2007) and the three species that co-occur in 
Chile (C. dilatata, C. fecunda (Gallardo 1979) 
and a currently un-described species) cannot be 
distinguished on the basis of shell characters or 
soft anatomy alone (Veliz et al. 2003; Collin et 
al. 2007). Some details of development can be 
used to distinguish between the three: Crepi-
patella fecunda has planktotrophic development, 
Crepipatella dilatata has non-planktotrophic 
development with nurse eggs that never cleave, 
and the undescribed species has non-plankto-
trophic development with nurse eggs that cleave 
and appear to gastrulate (Veliz et al. 2003; 
Collin et al. 2007).  These species can also be 
distinguished on the basis of DNA sequences of 
the DNA barcoding gene cytochrome oxidase I 
(COI) (Collin et al. 2007). Therefore the 
provisional identification of Rolan and Horro 
requires verification with additional data. 
In 2008 one of us (PF) discovered a previously 
unreported subtidal population of Crepipatella, at 
Playa de Beluso, in Bueu, on the Ria de Pontevedra 
(42°19'45.98"N, 8°47'44.83"W; Figure 1, site 4) 
next to a mussel-processing wharf.  The snails were 
found almost exclusively attached to mussels 
(Mytilus galloprovincialis (Lamarck, 1819)) (Figure 
2) and some empty shells of abalones (Haliotis 
tuberculata Linnaeus, 1758).  Approximately 50 
individuals from 5 – 36 mm in length were collected 
between 10-13 September 2008 and some were 
preserved in 95% ethanol for subsequent DNA 
sequencing. Nearby sites (Figure 1, sites 3, 5 and 6) 
with similar habitats, e.g. mussel-covered rocks in 
the subtidal area were also searched, and only one 
other specimen was found, at site 5. This animal was 
on an empty abalone shell being transported as cover 
by an urchin (Paracentrotus lividus (Lamarck, 
1816)). 
 
Figure 1. Survey sites for Crepipatella dilatata in Northern 
Spain. Site 1 (O Grove Bay), Site 2 (Baia de Aldan), and Site 4 
(Playa de Beluso) are reported locations of Crepipatella 
populations. Site 3 (42°20'09.11"N, 8°47'55.40"W), Site 5 
(42°19'39.33"N, 8°47'32.15"W) and Site 6 (42°19'57.02"N, 
8°46'20.48"W) were searched but no Crepipatella were found 
Fifteen females (30 % of total animals 
collected) were brooding and the embryos were 
examined and photographed with a dissecting 
microscope (Figure 3).  Egg capsules contained 
uncleaved nurse eggs and embryos with well-
developed coiled shells and velar lobes. 
Hatchlings crawled away from the capsules at 
shell lengths of about 1 mm. These features 
match those described for C. dilatata (Veliz et 
al. 2003; Collin et al. 2007).  
To confirm this identification genetically and 
to determine the source population, DNA was 
extracted from 5 specimens and 600 base pairs of 
cytochrome oxidase c subunit I (COI), and 506 
base pairs of 16S were sequenced for two 
animals, following the methods of Collin (2001). 
Comparisons with sequences previously reported 
by Collin et al. (2007) showed  that  the animals 
from Spain were indeed Crepipatella dilatata. 
Two of the COI haplotypes were identical to 
haplotype Dil5 (Genbank DQ811124), two where 
identical to Dil3 (Genbank DQ811118) and one 
was identical to haplotype Dil4 (Genbank 
AF546052).  Both 16S sequences were identical to 
the single sequence from C. dilatata in Genbank. 
 
Crep ipa t e l l a  i n  Spa in  
 
379 
 
Figure 2. (A) Living specimen and (B) dorsal and ventral views 
of a shells of Crepipatella dilatata collected from the shells of 
Mytilus galloprovincalis in September 2008.  Scale bar = 1 cm 
Collin et al. (2007) sequenced 22 individuals 
of C. dilatata from Chile and Argentina.  The 
haplotypes from Spain fall into both major 
haplotype clades reported in that paper.  These 
haplotypes have been found along most of the 
central coast of Chile (Coquimbo, San Carlos, 
near Puerto Montt, and Chiloe).  No Argentine 
haplotypes were detected in the Spanish sample.  
However the numbers of animals sequenced are 
not adequate to definitively exclude Argentina as 
the origin of the introduction.  These haplotypes 
demonstrate that at least 3 original females 
founded this Spanish population. 
Crepipatella dilatata fits the definition of an 
established exotic species put forward by Gofas and 
Zenetos (2003).  They consider any species that is 
documented by three reliable records or for which 
there is information on perennial populations as 
being established. The previous reports of 
Crepipatella in Baia de Aldan and O Grove Bay 
(Rolan and Horro 2005; Bañon et al. 2008) in 2005 
and the current  report  provide three records of 
populations of C. dilatata in a 15-km area, over 
three years. The 2008 samples from Playa de Beluso 
and the 2005 samples from Baia de Aldan both 
contained brooding females as well as animals as 
large as 25 mm (Rolan and Horro 2005) and 36 mm 
(reported here). Crepipatella dilatata is thus 
reproducing in Europe and should be considered 
established in Galicia. 
 
Figure 3. Developmental stages of C. dilatata. (A) A cluster of 
egg capsules early in development. Scale bar = 4 mm.  (B) Early 
intracapsular embryos showing the early development of the ridge 
that will become the velum surrounded by uncleaved nurse eggs. 
Scale bar = 600 μm.  (C) Fully developed embryos that have 
already lost the velum and are almost ready to hatch. Scale bar = 
1 mm. (D) A recent hatchling. Scale bar = 400 μm 
What is the possibility of an aggressive 
expansion or invasion of this species in northern 
Spain?  Rolan and Horro (2005) report that no 
Crepipatella were detected in the region during 
extensive dredging surveys in 1997 and that the 
mode of introduction is not clear.  If the original 
introduction was in this area the expansion has 
been fairly rapid for a species without a free-
living larval stage. It should be noted that the 
 
R .  Co l l i n  e t  a l .  
380 
two known invasive calyptraeids both have 
planktotrophic larval development.  In general, 
introduced calyptraeids with direct development 
have not expanded outside the protected bays 
from which they were first reported (e.g., 
Crepidula convexa and C. plana Say 1822 on the 
West Coast of North America). The fact that 
none were found after thorough searches at 
locations either side of the site at Bueu, and that 
this site is adjacent to a mussel processor, 
suggests that they are being or could be 
inadvertently spread via mussel culture. Rolan 
and Horro (2005) also suggested that this species 
might have been transported by dredging and re-
distribution of substrate in the area.  Such human 
activities could increase the spread of an animal 
with little ability to naturally spread rapidly. 
If C. dilatata populations expand in Spain, 
this species certainly has the potential to become 
a pest. Its preference for other marine mollusks 
as a substrate, makes this species a possible pest 
on mussel beds and aquaculture facilities.  At 
Bueu, many mussels were colonised by 
C. dilatata (Figure 2), which could compete with 
them for food and be a nuisance for bivalve 
production, as has been the case with 
C. fornicata. Crepipatella dilatata is a species 
that can also reach extraordinary high densities 
in its native range (Collin, unpublished), 
occurring on almost every mussel in some 
Chilean and Argentine mussel beds. 
Acknowledgements 
We are grateful to Maria Fernanda Vinasco, Axel 
Calderon and Eyda Gomez for work in the 
laboratory and Mark Torchin and Jim Carlton for 
commenting on a previous version of the 
manuscript. 
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Clarifying marine invasions with molecular markers: an illustration based on mtDNA from mistaken calyptraeid gastropod identifications.

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Recent marine introductions into Hong Kong.

Confirmation of the identification and establishment of the South American slipper limpet Crepipatella dilatata (Lamark 1822) (Caenogastropoda: Calyptraeidae) in Northern Spain

Name not available

Confirmation of the identification and establishment of the South American slipper limpet Crepipatella dilatata (Lamark 1822) (Caenogastropoda: Calyptraeidae) in Northern Spain

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