Occurrence of winter mortalities in the slipper limpet Crepidula fornicata (Linnaeus,

1758) in the Fal Estuary, Cornwall.

Amber G. Thornton*, Craig Baldwin, Claire Eatock

* Falmouth Marine School; email: amberthornton@hotmail.co.uk

Abstract

The natural climatic and geographic boundaries that have facilitated evolution in the past are

being bypassed by globalised anthropogenic activities, which have enabled the uncontrolled

spread of organisms. A relatively small number of these can become established, and even

fewer are a potential cause for ecological or economic concern, such as Crepidula fornicata.

This gastropod threatens biodiversity and commercial shellfish operations including the

Ostrea edulis fishery within the Fal Estuary. Winter mortality events have been observed to

affect C. fornicata, restricting its range and population size. This research aimed to find the

degree to which C. fornicata is affected by winter mortalities in the Fal Estuary during the

winter of 2010-11. Winter mortalities of -469.6% and -21.5% were observed at the two sites

studied, indicating that C. fornicata is not significantly affected. The former shows a clear

population increase, which may be due to continued recruitment of 2010 juveniles through

the winter, after the initial surveys. The lack of winter mortalities may be due to a winter that

did not feature many cold days, or did not exhibit particularly anomalous temperatures.

Considering the predicted northern shift of species caused by climate change continued

monitoring of the C. fornicata population in the Fal Estuary is recommended to facilitate the

development of suitable management strategies.

Key words

Crepidula fornicata; temperature; oyster beds

Introduction

Natural boundaries, whether geographic or climatic, have separated communities for millions

of years resulting in the evolution of species adapted to specific environments and integrated

within communities (Monroe and Wicander 2009). In recent years globalised anthropogenic

activities have enabled the uncontrolled spread of organisms (Hulme 2009). Whilst many

organisms are unable to survive in alien conditions, one tenth are considered to become

established (Williamson and Fitter 1996), and a small number of these are a cause for

potential ecological or economic concern (Thieltges et al. 2004).

One such potentially concerning organism is the American slipper limpet, Crepidula

fornicata (Linnaeus, 1758), a gastropod originating from the east coast of North America

(Walne 1956) which is now found across 24o

latitude (Blanchard 1997). Outside of its native

territory C. fornicata may change its environment by smothering it with pseudofaeces and by

sheer numbers (Barnes et al. 1973; Chauvaud et al. 2000). Once the limpet has reached the

adult morph a dearth of predators (Blanchard 2009) and parasites (Thieltges et al. 2004)

means that there is little natural control over their populations, which have reached

superabundance in some areas (Blanchard 2009). There is some evidence of consumption by

filter feeders whilst C. fornicata is in the larval stage (Pechenik et al. 2004).

C. fornicata population size and increase are thought to be limited by winter mortalities in

some regions (Thieltges et al. 2004). This is corroborated by Beukema (1979) who found that

the majority of species that suffered heavily from winter mortalities are found in the lower

intertidal and subtidal as is the case for C. fornicata. This is as a result of exposure to low air

temperatures, which exhibit greater fluctuations than water temperatures due to the buffering

capacity of water (Marshall and Plumb 2008). In addition to this, increased salinity may be

caused by the freezing out of sea water, oxygen content may be reduced and ice scouring may

occur through wind and tide movement, all of which can cause death to intertidal organisms

(Beukema 1979). C. fornicata is reported to become weakened and filled with mud when

exposed to temperatures colder than it is able to endure (Crisp, 1964).

The breeding season in the United Kingdom occurs from March to early September

(Chipperfield 1951; Orton 1912) and is considered to be triggered by sea temperature upon

reaching 6-7oC (Werner 1948; Thieltges et al. 2004) or 10

oC (Chipperfield 1951; Richard et

al. 2006), dependant on source. Females lay on average twice a year in England (Chipperfield

1951) and eggs take about a month to hatch (Richard et al. 2006). A free-swimming, pelagic

larval stage lasting about 35 days is followed by a motile benthic period until reaching 3-

5mm whereupon individuals are attracted to chains where they settle permanently

(Chipperfield 1951). First year growth in Southern England has been placed at a mean of

18mm by Chipperfield (1951), and 6-22mm by Orton (1950) and Walne (1956).

The first recorded presence of C. fornicata was in 1944 (Cole 1952 cited in Blanchard 1997),

previously recorded as unknown in the Fal estuary in 1939 (Orton 1940). Unlike the majority

of infestations which resulted from the commercial importation of a host species, Crassotrea

virginica (Gmelin, 1791), in the Fal it is considered to have been introduced from the hulls of

ships (Cole 1952 cited in Blanchard 1997). A native oyster Ostrea edulis (Linnaeus, 1758)

fishery is located within the Fal which is the only fishery of its kind worldwide that continues

to be fished under sail with only traditional methods of dredging permitted, due to a local

byelaw (Challinor et al. 2009). This culturally and economically important fishery is

currently considered in relatively good health, however periods of intense infection from the

oyster parasite Bonamia and the presence of slipper limpets, which exhibited a 12-15%

increase in biomass between 2006 and 2007 (Walker 2007), remain a threat. Outside of its

natural distribution C. fornicata is considered to have a detrimental effect on oysters and

oyster fisheries (Orton 1912; Blanchard 1997; Walker 2004, 2007; Fitzgerald 2007; Clark

2008).

Method

Survey area

The surveys were conducted in the Fal estuary, a designated Special Area of Conservation

located in southwest England. It is a macrotidal estuary with a flood current range extending

18.1km upriver and a highest spring tidal range of 5.3m. Throughout 2009 and 2010 water

temperatures ranged from 6.45oC to 17.48

oC (Falmouth Harbour Data 2011). Sample

locations were chosen on oyster beds within the Fal due to the propensity of C. fornicata to

occupy the same habitat as oysters (Walker 2004, 2007; Blanchard 2009) and also the related

economic interests. The two sites used were Turnaware Bar and Coombe Beach (see figures

2A and B for location), both chosen for their practical access to the oyster beds on a spring

low tide.

Methodology

Surveys were performed at two sites in August 2010, and again in February and March 2011.

Estimates of slipper limpet populations were determined in the field using shore-based

quadrat surveys, frequently used to survey intertidal and subtidal habitats (Thieltges et al.

2004; Firth et al. 2011; Wethey et al. 2011). The survey needed to occur on a low spring tide,

as C. fornicata populations are concentrated in the low intertidal (Thieltges et al. 2003) down

to about 20m (Blanchard 1997). Teams of 2-3 people were used who were familiar with

identification of C. fornicata and other relevant species (Wethey et al. 2011) At each site five

quadrats were sampled along each of four transects set 1m apart, using a 0.25m2 quadrat

(Wethey et al. 2011), resulting in a total of 20 quadrat samples per survey. The transects ran

parallel to the low tide line. Within the quadrats the GPS location, number of chains, number

of individuals and the length of each individual was recorded in situ. The organism was

measured along the anterior-posterior length at the longest straight (McNeill et al. 2010)

using callipers to the nearest millimetre. The GPS position was taken using a Garmin

GPSMAP 62 model. The data gained was compared between the timeframes, before and after

winter. This accounts for the population size in the preceding summer (Beukema 1979).

Analyses

An unpaired t-test was used to test the null hypothesis that there is no difference in population

size of C. fornicata before and after winter. Microsoft Office Excel was used to perform this

analysis following methodology from Dytham (2011).

Climatic and tidal data

Air temperature data was gained from the Met Office (2011a), recorded at the nearby

Culdrose station. Tidal information was obtained from Mylor Yacht Harbour Tide Table

2011, curtesy of Her Majesty’s Stationary Office and the UK Hydrographic Office.

Results

Over the four surveys 80 quadrats were sampled comprising a total of 298 slipper limpets.

This gives an average density of 15 individuals per 1m2 in total, with an average of 14 ind.

per 1m2 at Coombe Beach and 15 ind. per 1m

2 at Turnaware Bar. After winter, an increase of

22 ind. per 1m2 was recorded at Coombe, whilst Turnaware saw an increase of only 3 ind. per

1m2. This resulted in negative mortalities of -469.6% at Coombe and -21.5% at Turnaware.

After analysis using an unpaired t-test no statistical difference was found between

populations before and after winter at Turnaware Bar. At Coombe Beach, however, there was

a statistical difference found in populations before and after winter. This population can be

seen to have increased after winter. Overall the C. fornicata population is slightly larger at

Turnaware Bar (154), however the largest population surveyed was at Coombe (131) after

winter. The smallest surveyed was also at Coombe (23), before winter.

Figures 3A and B show an increase in individuals of less than 20mm in length in the surveys

performed after winter. An increase from 3 to 30 was seen at Coombe Beach, and a lesser

increase from 7 to 17 at Turnaware Bar.

Very cold conditions were observed through November and December, a period that did not

coincide with any extreme low spring tides. January was warmer, and February was mild.

Mean temperatures in the United Kingdom were 5.1oC below average in December, 0.3

oC

below average in January and 1.9oC above average in February (Met Office 2011b).

Discussion

The low or absent impact of winter mortalities in the Fal Estuary is demonstrated in this

study. It is probable that temperatures low enough to cause widespread mortalities of C.

fornicata do not occur with enough regularity, if at all, in this area of England. In the study

conducted by Thieltges et al. (2004) in the northern Wadden Sea, Germany, mean air

temperatures fell below 0oC for 24 and 37 days during the two winters (December – March)

investigated. This resulted in mortality levels of 33-97% and 26-93% respectively. This can

be compared to a total of 7 days in which the mean air temperature fell below 0oC in the area

of the Fal Estuary (Met Office 2011a) which resulted in negative mortality levels of -469.6%

and -21.5%. These temperatures may in fact be an overestimation, as the location of the

weather station is inland from the Fal Estuary and therefore may experience slightly lower

temperatures (Crisp 1964). In addition even during the severe winter of 1962-63 the Fal was

virtually unaffected by O. edulis mortalities, which has exhibited greater sensitivity to cold

temperatures than C. fornicata as seen in the same winter on the Essex and Kent coast; whilst

O. edulis mortality was 75%, C. fornicata mortality was only 25% (Crisp 1964). No

noteworthy ice cover was observed during the 2010-11 winter, so the scouring effect from ice

would have been absent as well as the effects of H2O build up and oxygen depreciation that

occur in the event of ice cover (Beukema 1979).

Wethey et al. (2011) consider the influence of extreme weather events upon the success of

invasive intertidal species. This is corroborated by the prohibitive effect extremely cold

winters in the north Wadden Sea were found to have on C. fornicata populations by Thieltges

et al. (2004). Further to this, Crisp (1964) describe the impact of temperature anomaly, rather

than the temperature itself, upon organisms. The 2010-11 winter minimum air temperature

average anomaly was -1.5oC in southwest England (Met Office 2011b), compared to a -5.4

oC

winter minimum air temperature average anomaly in Plymouth (southwest England) in the

severe winter of 1962-63 (Crisp 1964). This suggests that the temperature anomaly occurring

during the 2010-11 winter was not enough to cause significant winter mortalities in the Fal

Estuary.

At Coombe Beach there was a significant difference in C. fornicata populations before and

after winter, however it had increased after winter rather than decreased as expected. This

observed population increase after winter does not necessarily exclude the possibility of

winter mortalities. There are several possible explanations for this. Firstly, further recruitment

of 2010 juveniles could have increased population size. The initial survey was conducted in

late August and breeding may continue into September (Orton 1912; Chipperfield 1951). A

minimum of two months before settlement (Chipperfield 1951) therefore suggests that further

recruitment may occur through winter. The observed increase in individuals under 20mm at

both sites after winter corroborates this theory. On the other hand, Chipperfield (1951) found

that the percentage of females bearing spawn declined sharply after June, and successful

recruitment occurs only above 15oC (Clark 2008). This indicates that late season recruitment

would not contribute a large number. The increase could be considered due to the recruitment

of 2011 juveniles, however Orton (1912) and Chipperfield (1951) report that breeding begins

in March in southern England, which would exclude this possibility. If spawning does begin

at 6-7oC as supposed by Werner (1948) and Thieltges et al. (2004) breeding could

theoretically continue year round in a location such as the Fal Estuary in which temperature

did not drop below 6.45oC in 2009-10 (Falmouth Harbour Buoy 2011). A further possibility

is that the slight geographic disparity seen at Coombe in figure 2A may have given a different

result. This occurred because ground conditions forced the survey slightly along the coast;

however C. fornicata populations are affected by substrate type (Thieltges et al. 2004) and

may therefore exhibit difference in size over even a small distance.

Climate change has facilitated a northern shift in the biogeographic ranges of both native and

invasive species around the United Kingdom (Mieskowska et al. 2006). This change is

expected to continue, and at a faster rate in marine systems than terrestrial systems

(Mieskowska et al. 2006). The region to the south of the Fal Estuary area is Brittany, which

hosts superabundant numbers of the organism in many places (Blanchard 2009). Whilst there

are many other variables to consider, this certainly advocates further monitoring to determine

the effect that climate change will have upon the population of C. fornicata in the Fal

Estuary.

As C. fornicata is frequently considered an undesirable inhabitant of commercial oyster beds,

the occurrence of winter mortalities could therefore be considered advantageous in the efforts

to reduce their numbers. This study indicates however that winter mortalities cannot be

expected to significantly limit population size or range in the Fal estuary. Further to this, it is

likely that were temperatures anomalously cold enough to kill large numbers of C. fornicata

to occur, they would result in O. edulis mortalities in even greater numbers (Crisp et al.

1964), causing considerable economic impact to the fishery. Control of the invasive organism

would likely require anthropogenic intervention using such methods as described by

Fitzgerald (2007), which would be facilitated by continued monitoring alongside forecasting

models that would enable suitable management strategies to be implemented.

Acknowledgements

Falmouth Harbour Commissioners and Harriet Knowles for funding and support; Craig

Baldwin and Dr. Claire Eatock (Falmouth Marine School) for advice and support; Rich May,

Katie Sambrook, Emma Dobinson and Russell Thornton for assistance in the field; Paul

Ferris (The Port of Truro) for the invaluable local knowledge he shared of the oyster beds, the

oyster fishing industry and the Fal Estuary; and many others for information, advice and time.

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Figure 1. A chain of Crepidula fornicata specimens from the Fal Estuary (photo credit: AT).

Figure 2A. Map depicting distribution frequency of C. fornicata before and after winter at

Coombe Beach

Figure 2B. Map depicting distribution frequency of C. fornicata before and after winter at

Turnaware Bar.

Figure 3A. Graph depicting size frequency distribution of C. fornicata before and after

winter at Coombe Beach

0

5

10

15

20

25

0-4

.99r

5-9

.99r

10-1

4.9

9r

15-1

9.9

9r

20-2

4.9

9r

25-2

9.9

9r

30-3

4.9

9r

35-3

9.9

9r

40-4

4.9

9r

45-4

9.9

9r

50-5

4.9

9r

Fre

qu

ency

Size of Individuals

Graph showing Crepidula fornicata size frequency

distribution before and after winter at Coombe Beach

Coombe

(Aug '10)

Coombe

(Mar '11)

Figure 3B. Graph depicting size frequency distribution of C. fornicata before and after

winter at Turnaware Bar.

Annexes

Annex 1. Geo-referencing data for distribution frequency of C. fornicata at Coombe Beach

and Turnaware Bar in the Fal Estuary before winter (autumn).

BNG Ref

Number of

slipper limpets

SW 84377 40456 1

SW 84382 40456 5

SW 84369 40461 4

SW 84378 40462 4

SW 84380 40458 2

SW 84371 40459 1

SW 84368 40449 2

SW 83548 38355 7

SW 83554 38356 10

SW 83560 38366 3

SW 83582 38360 11

SW 83587 38360 3

SW 83590 38356 5

SW 83591 38350 3

SW 83594 38343 4

Annex 1. Geo-referencing data for distribution frequency of C. fornicata at Coombe Beach

and Turnaware Bar in the Fal Estuary after winter (spring).

BNG Ref Number of slipper

0

2

4

6

8

10

12

14

16

Fre

qu

ency

Size of individuals

Graph showing Crepidula fornicata size frequency

distribution before and after winter at Turnaware Bar

Turnaware

(Aug '10)

Turnaware

(Feb '11)

limpets

SW 84436 40460 8

SW 84442 40459 8

SW 84444 40458 9

SW 84450 40461 4

SW 84454 40461 7

SW 84440 40459 3

SW 84446 40459 5

SW 84451 40460 14

SW 84457 40461 6

SW 84438 40457 4

SW 84442 40457 3

SW 84446 40461 7

SW 84451 40463 7

SW 84456 40464 11

SW 84436 40461 2

SW 84443 40457 1

SW 84445 40466 15

SW 84450 40464 5

SW 84454 40464 9

SW 83561 38373 13

SW 83556 38365 1

SW 83557 38362 1

SW 83553 38357 7

SW 83558 38372 13

SW 83551 38365 1

SW 83545 38357 2

SW 83545 38355 3

SW 83550 38355 4

SW 83555 38376 19

SW 83552 38369 4

SW 83548 38355 3

SW 83546 38355 2