Vita Malacologica 7: 15-20 16 December 2008 The variability of the operculum in Nucella lapillus (Gastropoda, Muricidae) from a colony in Audresselles, France

Marc KEPPENS Research Associate, Royal Belgian Institute of Natural Sciences, Department of Malacology, Vautierstraat 29, B-1000 Brussels, Belgium e-mail: [email protected]

Kelly DHONDT Onderstraat 28, 8-9890 Gavere, Belgium e-mail: [email protected]

Henk K. MlENlS Mollusc Collection, National Natural History Collections, Berrnan Building, Hebrew University of Jerusalem, IL-91904 Jerusalem, Israel and Mollusc Collection, National Collections of Natural History, Department Zoology, Tel Aviv University, IL-69978 Tel Aviv, Israel email: [email protected]

Key words: Molluscs, Muricidae, Nucella lapillus, operculum, predation, France

ABSTRACT diet of N. lapillus and the pigmentation of the shell. The inte- rior of the shell is usually white with brown or purple and the In April 2007 the first two authors investigated the rocky outer lip of it may cany teeth. outcrops on the beach of Audresselles, northwest France, for Sinistral specimens have been found occasionally in Great the presence of marine molluscs. Special attention was paid to Britain, France and The Netherlands (Mienis, 1972). Because Nucella lapillus (Linnaeus 1758), also known as the Atlantic of the variability in form, sculpture and colour many aberra- dog-whelk. A study of the collected material revealed that tions have been described in the past as different taxa and part of the specimens possessed a strongly reduced opercu- received separate Latin names, which from the taxonomical lum, some animals were even completely devoid of an oper- point of view should be considered synonyms. However, culum. The aim of this article is to provide some information some names could be used to indicate forms, if one wishes to concerning the variability of the operculum in this population use names for them. of N. lapillus. Due to the fact that the animals of N. lapillus, like several other species of the family Muricidae, were used in the past for the dyeing of cloth with purple in Brittany, France (Co- INTRODUCTION caign, 1997) and in Ireland and Wales (Joyce, 1906), this species received the common name "Purple snail" in several The morphology of the shells of Nucella lapillus (Lin- languages. Some other species of Muricidae from the Medi- naeus 1758), the Atlantic dog-whelk, belonging to the family terranean Sea were also used to obtain purple-dye. However, Muricidae, is for a large part dependent on the type of shore one needed an enormous amount of snails in order to obtain this species is living on. Specimens living on wave-protected one gram of purple. It is therefore understandable that purple- coasts have usually thicker shells, in this way they are better dye, used for dyeing among others the cloaks of senators and protected against predators sharing the same habitat. The emperors during Roman times, was once more expensive than shells of N. lapillus collected from exposed coasts, with heavy gold. surf and wave action, are usually thinner and they have a The natural distribution of N. lapillus ranges from Nor- wider aperture because of the low density of predators. way till NW-Africa. N. lapillus does not live in the Medite- Moreover, these animals are in the possession of a larger foot, ranean Sea, likewise it is absent from the Canary Islands and necessary for a better hold to the rocks. Also the colour of the Madeira. This species occurs also in the Western Atlantic shell is variable: the exterior can be white, brown, yellow, Ocean, along the east coast of North America from the south- grey and purple, with or without spiral bands (pl. 1 figs 1-9). em part of Labrador down to New York (Abbott, 1974). According to Moore (1936) there is a connection between the

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Figure 1. The location of Audresselles in north western France.

DESCRIPTION OF THE RESEARCH AREA from the Jurassic period. In the area south of Boulogne-sur- Mer these Jurassic rocks are again replaced by extensive dune The Opal Coast is a coastal area in the northwest of formations. France. It includes the whole area of department Pas-de- Audresselles, where we collected N. lapillus, is a small Calais, from Bray-Dunes near the Belgian border to Berck fishing-village on the Opal Coast with a beach area showing a near the estuary of the river Authie (fig. 1). The character of rich variety of habitats. During high tide the water is reaching the coast differs from place to place: the vicinity of Dunker- almost the houses, while during low tide large areas with que is more or less flat with a small row of dunes, while the rocky outcrops become exposed. These rocks are covered coastline at Cap Blanc Nez is characterized by chalk-rocks, with a large variety of algae and are interspersed by tide pools from the Cretaceous period, projecting high above the sea. and areas with fine sand (fig. 2). It is therefore quite under- More to the south at the Cap Gris Nez area, the cliff coast standable that this coastal area is attracting a large number of consists of alternating layers of limestone, clay, sandstone etc. students of marine biology the whole year round (Elen, 1982).

Figure 2. The beach of Audresselles at low tide.

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MATERIAL AND METHODS VARIATION OF THE OPERCULUM

As part of a long-term research dealing with the biodiver- A follow up study of the collected material revealed not sity of the malacofauna of the coast of Audresselles, France, only a rather high variability in form and colour of the shell, Marc Keppens and Kelly Dhondt carried out an intensive col- but also in that of the operculum. Several large adult speci- lecting survey of the rocky outcrops on the beach of that area mens were even devoid of an operculum, other specimens in April 2007. During the whole period of low tide, the littoral showed a strongly reduced operculum, while others, both area between the high- and low-water marks was surveyed for small and large specimens, were provided with a large and the presence of living marine molluscs. Special attention was heavy operculum (pl. 1, figs 10-18). This variation of the paid to the presence of N. lapillus. Both small and large rocks operculum, from complete absence to strongly developed, were inspected carefully for the presence of this species, and within a single colony, had already been observed by Cooke also the tidal pools were investigated. (1917). We collected a total of 260 live specimens of N. lapillus In Table 1 we have sorted the 260 specimens according to which were either sitting between or under the rocks or colour and subsequently according the development of the actively crawling around in the tidal pools. The population of operculum in three categories: 1) specimens with a good N. Iapillus in Audresselles consisted of numerous adult and developed operculum; 2) specimens with a poorly developed juvenile specimens. or malformed operculum; 3) specimens lacking an operculum. A preliminary report in Dutch has been published by Although we noticed a large variability in brown hues Keppens et al. (2007), here some more information is given among the collected shells, from pale (yellow)brown up to concerning the variability of the operculum and its possible rather dark (purple)brown, we did not differentiate between causes. the brown hues because this would be based on a subjective The collected material has been lodged permanently in the interpretation of the colours. private collection of the two first authors and the Mollusc The brownish colour morph is represented by the highest Collection of the Tel Aviv University, Israel (TAU MO number of specimens i.e. 77.7 %, the white morph by 22.3 %. 59204114). Among the material were 43 shells (16.5 %) with one or more colour bands per whorl. Of the total number of collected N. lapillus, a normally developed operculum was encountered in 77.3 %, a poorly RESULTS developed or malformed operculum was found in 10.8 %, while an operculum was missing in 11.9 %. Both the variability in form and colour of N. lapillus in In brown coloured shells without colour bands a well the colony at Audresselles was extremely high. We found developed operculum was present in 76.4 %, a poorly devel- adult specimens with a very small shell, specimens with a oped or malformed operculum in 12.4 % and no operculum in large, wide and heavy shell, with or without labral teeth, and 11.2 %. In brown coloured shells with colour bands the fol- regularly we collected also specimens showing a scaly sculp- lowing percentages were encountered: 79.2 % with a normal ture. Although brown coloured shells were most common, we operculum, 8.3 % with a degenerated operculum and 12.5 % found also regularly white ones. Some specimens showed without an operculum. even one or more coloured spiral bands. The colour of the In complete white shells 76.9 % showed a well devel- aperture was also rather variable: white, orange, brown or oped, 7.7 % a partially developed or malformed operculum, purple. while in 15.4 % the operculum was missing. In banded white shells we noted the following numbers: 84.2 % with a normal- ly developed operculum, 5.3 % with a less developed or mal- formed operculum, while 10.5 % were lacking an operculum.

brown white total without with without with bands bands bands bands operculum well developed 136 19 30 15 201

operculum poorly developed or malformed 22 2 3 1 28

operculum absent 20 3 6 2 3 1

total 178 24 39 19 260

Table 1. Variation in the operculum of Nucella lapillus according to colour of the shell

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DISCUSSION rus Linnaeus 1758 and the Swimming crab Portunus puber (Linnaeus 1758) (Ebling et al., 1964; Feare, 1970; Vermeij, Like in the case described by Cooke (1917), we noticed in 1976 & 1978; Lawton & Hughes, 1985) and birds like the our research that in specimens with a badly developed opercu- Oystercatcher Haematopus ostralegus Linnaeus 1758, the lurn the aperture could be closed only in part, while in some Purple sandpiper Calidris maritima (Brunnich 1764) and the N. lapillus the operculum was reduced to a rather thin, light- Turnstone Arenaria interpres (Linnaeus 1758) (Feare, 1967 & brown film or membrane in stead of the normal dark-brown 1971 ; Vermeij, 1978). From his study appears that the opercu- and firm operculum. In specimens where the operculum was lurn plays an important role in the defence mechanism against completely lacking, the foot showed a rough spot on the place predation. Specimens of N. lapillus without an operculum, or where the operculum should have normally adhered. with a strongly reduced operculum, are all living higher in the Obviously, this rough spot took temporarily the place of an littoral zone. Their presence over there can be explained by operculum, before the usual regeneration of a missing opercu- the fact that crabs tend to follow the movements of the tides lum. When an operculum is removed intentionally from the and therefore less time remains for these predators to attack body of a snail, both the interior of the operculum and the N. lapillus living at the high-water mark. Specimens of N. area where the operculum was adhered to the body is quite lapillus without or with a very small operculum have there- smooth (Mienis, unpublished). fore more opportunities to survive at the high-water mark. At Although N. lapillus is present in large numbers on the the other hand Dog-whelks living at high water mark are rocks in Audresselles, it is impossible to state that all these more exposed to predation by birds especially during low shortcomings in the development or presence of the opercu- tide. The latter tend to feed however on small juvenile speci- lurn are caused by overpopulation. Also bad nutrition can be mens. Specimens living at the low-water mark or in tide pools out ruled for the (partially) absence of an operculum. will develop a larger and heavier operculum as a form of pro- Although we registered the presence of only few specimens of tection against predation by crabs. the preferred prey Mytilus edulis Linnaeus, 1758, numerous specimens of Patella vulgata Linnaeus, 1758, various species of Littorina, Gibbula and barnacles, another preferred food CONCLUSION item, served most likely as an alternative source of food. Therefore we have to look for other possible explanations The survey carried out in the littoral rocky tidal zone on causing the variability of the operculum in N. lapillus. the beach of Audresselles, France, yielded interesting study Although at first glance a strong operculum seems to play an material. Of the 260 collected specimens of N. lapillus, 201 important role in avoiding desiccation, research has shown specimens were in the possession of a good developed oper- that that is not the case (Gibson, 1970). Especially the thick- culum, 28 specimens showed a strongly reduced or mal- ness of the shell, the size of its aperture and foot and behav- formed operculum, while 31 specimens were completely iour of its inhabitant seem to be of more importance. For devoid of an operculum. Research carried out in the past has example the position and size of the aperture in relation to the shown that the operculum in N. lapillus plays a more impor- substrate on which N. lapillus lives, plays a crucial role in tant role in the protection against predators, especially crabs, avoiding desiccation because they remain usually adhered to than against desiccation. the rocks with their foot and close only the aperture with the operculum when they loose their foothold (Cooke, 19 17). Dog-whelks living on exposed rocks with heavy surf show a REFERENCES much wider and larger aperture and ditto foot in order to have a much better foothold, than specimens living in a protected ABBOTT, R.T., 1974. American Seashells - The Marine area (Kitching et al, 1966). This explains also observations of Mollusca of the Atlantic and Pacific Coasts of North Ame- large, adult specimens without operculum in the surroundings rica. Second Edition. 663 pp. Van Nostrand Reinhold Com- of high water mark and therefore in the area with the highest pany, New York, Cincinnati, Toronto, London, Melbourne. risk of desiccation. At the other hand specimens collected at COCAIGN, J.Y., 1997. Le pourpre (Nucella lapillus) et son low water mark do possess always an operculum. utilisation comme teinture en Amorique. - Annales de Since the cause of the variation in size of the operculum Bretagne et des Pays de llOuest, 104: 7-22. can not be explained as a means of protection against desicca- COOKE, A.H., 1917. A colony of Nucella (olim Purpura) tion, Gibson (1 970) studied also the influence of a biotic fac- lapillus (Linn.) with operculum malformed or absent. - tor like that of predation on the grade of development of the Proceedings of the Malacological Society of London, 12: operculum. Well known predators of N. lapillus, which leave 23 1-232. the shells often intact, but remove the operculum and animal EBLING, F.J., J.A. KITCHING, L. MCTNTZ & C.M. TAY- by penetrating the shell through the aperture are small indi- LOR, 1964. The ecology of Lough Ine. XIII. Experimental viduals of crabs like the European shore crab Carcinus mae- observations of the destruction of Mytilus edulis and nus (Linnaeus 1758), the Edible or Brown crab Cancerpagu- Nucella lapillus by crabs. - Journal of Animal Ecology,

VITA MALACOLOGICA, 7: 18 Keppens et al.. - The operculum of Nucellu lapillus

PLATE I Figs 1-18. Nucella lapillus (Linnaeus, 1758) from Audresselles, France. Figs 1-9. Colour variations. Figs 10-18. Shells with the operculum, showing the variation in the operculum. The x in fig. 11 indicates that this animal was found without operculum.

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33: 73-83. KITCHING, J.A., L. MUNTZ & F.J. EBLING, 1966. The ELEN, H., 1982. Ambleteuse, studie van de zeekust. Tweede ecology of Lough Ine. XV. The ecological significance and druk. 234 pp. Vereniging van Afgestudeerden in body forms in Nucella. - Journal of Animal Ecology, 35: Plantkunde en Dierkunde van de Universiteit te Leuven. 113-126. Leuven. LAWTON, P. & R.N. HUGHES, 1985. Foraging behaviour FEARE, C.J., 1967. The effect of predation by shore-birds on of the crab Cancer pagurus feeding on the gastropods a population of Dog-whelks Thais lapillus. - Ibis, 109: Nucella lapillus and Littorina littorea: comparisons with 474. optimal foraging theory. - Marine Ecology Progress FEARE, C.J., 1970. A note on the methods employed by Series, 27: 143-154. crabs in reaching shells of dogwhelks (Nucella lapillus). - MIENS, H.K., 1972. Een voorlopige inventarisatie van links- Naturalist, 913: 67-68. gewonden purperslakken (Thais lapillus lapillus) (Lin- FEARE, C.J., 1971. Predation of Limpets and Dogwhelks by naeus, 1758) forma sinistrorsa. - Correspondentieblad van Oystercatchers. - Bird Study, 18 (3): 121-129. de Nederlandse Malacologische Vereniging, 148: 104- 106. GIBSON, J.S., 1970. The function of the operculum of Thais MOORE, H.B., 1936. The biology of Purpura lapillus. I. lapillus (L.) in resisting desiccation and predation. - Shell variation in relation to environment. -Journal of the Journal of Animal Ecology, 39: 159- 168. Marine Biological Association, 2 1: 61 -89. JOYCE, P.W., 1906. A smaller social history of ancient VERMEIJ, G.J., 1976. Interoceanic differences in vulnerabili- Ireland. 574 + 4 pp. London. ty of shelled prey to crab predation. - Nature, 260 (5547): KEPPENS, M., K. DHONDT & H.K. MIENIS, 2007. 135-136. Purperslakken en de variabiliteit van het operculum bij VERMEIJ, G.J., 1978. Biogeography and adaptation. Patterns Nucella lapillus in een kolonie te Audresselles, Frankrijk. of Marine Life. 332 pp. Harvard University Press, Cam- - Spirula, 357: 97-102. bridge & London.

Accepted: 23 July 2008

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