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 10oC (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 35mm 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 17.48oC (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 1m2 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, 0.3oC 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 -5.4oC 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. References Barnes RSK, Coughlan J, Holmes NJ (1973) A Preliminary survey of the macroscopic fauna of the Solent, with particular reference to Crepidula fornicata and Ostrea edulis. Proceedings of the Malacological Society, London 40: 253 Beukema JJ (1979) Biomass and species richness of the macrobenthic animals living on a tidal flat area in the Dutch Wadden Sea: effects of a severe winter. Netherlands Journal of Sea Research 13 (2): 203-223 Blanchard M (1997) Spread of the slipper limpet Crepidula fornicata (L. 1758) in Europe. Current state and consequences. Scientia Marina 61(Sup 2): 109-118 Blanchard M (2009) Recent Expansion of the Slipper Limpet Population (Crepidula fornicata) in the Bay of Mont-Saint-Michel (Western Channel, France). Aquatic Living Resources 22: 11-19 Clark S (2008) Distribution of Slipper Limpet (Crepidula fornicata) around the South Devon Coast. Devon Sea Fisheries Committee, Devon Sea Fisheries Committee Report April 2008, 1-32 pp Challinor S, Solly N, Baugh J, Adnitt C, Hillyer K, Covington L, Velterop R, Drabble J, Potts M, Thornton P, Birch T (2009) Port of Falmouth development initiative environmental statement. Falmouth Harbour Commissioners, Falmouth Docks & Engineering Company. Final report 9S4181, 249-262 pp Chauvaud L, Jean F, Ragueneau O, Thouzeau G (2000) Long-term variation of the Bay of Brest ecosystem: benthic-pelagic coupling revisited. Marine Ecology Progress Series 200: 35-48 Chipperfield PNG (1951) The breeding of Crepidula fornicata (L) in the river Blackwater, Essex. Journal of the Marine Biological Association UK 30(1): 49-71
Crisp DJ (1964) The effects of the severe winter of 1962-63 on marine life in Britain. Journal of Animal Ecology 33(1): 165-210 Dytham C (2011) Choosing and using statistics: a biologist’s guide, 3rd edn. WileyBlackwell, Chichester, UK, 110-111 pp Falmouth Harbour Data (2011) Falmouth Harbour Commissioners environmental monitoring buoy data. Falmouth Harbour Commissioners, Falmouth, UK Firth LB, Knights AM, Bell SS (2011) Air temperature and winter mortality: implications for the persistence of the invasive mussel, Perna viridis in the intertidal zone of the south-eastern United States. Journal of Experimental Marine Biology and Ecology, doi:10.1016/j.jembe.2011.02.007 Fitzgerald A (2007) Slipper limpet utilization and management, final report. Port of Truro Oyster Management Group. Hulme PE (2009) Trade, transport and trouble: managing invasive species pathways in an era of globalisation. Journal of Applied Ecology, doi: 10.1111/j.1365-2664.2008.01600 Marshall J, Plumb RA (2008) Atmospheric, ocean, and climate dynamics: an introductory text. Elsevier Academic Press, Burlington, USA, 261-264 pp McNeill G, Nunn J, Minchin D (2010) The slipper limpet Crepidula fornicata Linnaeus, 1758 becomes established in Ireland. Aquatic Invasions 5 (1): 21-25 Met Office (2011a) Past Weather Data for Students. Met Office, Exeter, Devon, UK Met Office (2011b) Regional values – winter. http://www.metoffice.gov.uk (Accessed 4th May 2011) Mieszkowska N, Leaper R, Moore P, Kendall MA, Burrows MT, Lear D, Poloczanska E, Hiscock K, Moschella PS, Thompson RC, Herbert RJ, Laffoley D, Baxter J, Southward AJ, Hawkins SJ (2006) Marine biodiversity and climate change: assessing and predicting the influence of climatic change using intertidal rocky shore biota. Scottish Natural Heritage, Scottish Natural Heritage Commissioned Report No. 202 (ROAME No. F01AA402), 1-52 pp Monroe JS, Wicander R (2009) The changing earth: exploring geology and evolution, 2nd edn. Brooks/Cole, Belmont, USA, 55-56 pp
Orton JH (1912) An account of the natural history of the slipper-limpet (Crepidula fornicata), with some remarks on its occurrence on the oyster grounds of the Essex coast. Journal of Marine Biology Association UK 9: 437-443 Orton JH (1940) Fluctuations in oyster production in the Fal Estuary. Journal of the Marine Biological Association of the United Kingdom 24: 331-335 Orton JH (1950) Recent breeding phenomena in the American slipper limpet, Crepidula fornicata. Nature 165: 433-434 Pechenik JA, Blanchard M, Rotjan R (2004) Susceptibility of larval Crepidula fornicata to predation by suspension feeding adults. Journal of Experimental Marine Biology and Ecology 306: 75-94 Richard J, Huet M, Thouzeau G, Paulet Y (2006) Reproduction of the invasive slipper limpet, Crepidula fornicata, in the Bay of Brest, France. Marine Biology, doi 10.1007/s00227-005-0157-4 Thieltges DW, Strasser M, Reise K (2003) The American slipper limpet Crepidula fornicata, L. in the northern Wadden Sea 70 years after its introduction. Helgoland Marine Research 57: 27-33 Thieltges DW, Strasser M, Beusekom JEE, Reise K (2004) Too cold to prosper – winter mortality prevents increase of the introduced American Slipper Limpet Crepidula fornicata in Northern Europe. Journal of Experimental Marine Biology and Ecology 311 (2): 375-391 Walker P (2004) Distribution of the slipper limpet Crepidula fornicata (L.) within the limits of the Truro Oyster Fishery Order 2-4 March 2004. The Centre for Environment, Fisheries and Aquaculture Science. CEFAS Contract Report C2157, 1-17 pp Walker P (2007) Oyster and slipper limpet surveys 7-9 March 2006 & 13-15 February 2007. The Centre for Environment, Fisheries and Aquaculture Science. Shellfish Team Report No.69, 1-35 pp Walne PR (1956) The biology and distribution of the slipper limpet Crepidula fornicata in Essex rivers. Fishery Investigations, serII 20 (6): 1-50 Wethey DS, Woodin SA, Hilbish TJ, Jones SJ, Lima FP, Brannock PM (2011) Response of intertidal populations to climate: effects of extreme events versus long term change. Journal of Experimental Marine Biology and Ecology 400: 132-144 Williamson M, Fitter A (1996) The varying success of invaders. Ecology 77: 1661-1665
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.
25
Graph showing Crepidula fornicata size frequency distribution before and after winter at Coombe Beach
Frequency
20 15
Coombe (Aug '10)
10
Coombe (Mar '11)
5 0 50-54.99r
45-49.99r
40-44.99r
35-39.99r
30-34.99r
25-29.99r
20-24.99r
15-19.99r
10-14.99r
5-9.99r
0-4.99r
Size of Individuals
Figure 3A. Graph depicting size frequency distribution of C. fornicata before and after winter at Coombe Beach
16
Graph showing Crepidula fornicata size frequency distribution before and after winter at Turnaware Bar
14
Frequency
12 10 Turnaware (Aug '10)
8 6
Turnaware (Feb '11)
4 2 0
Size of individuals
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
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