|General Biology Additional Information||The ecology, physiology and genetics of Nucella lapillus has been extensively studied. Therefore, the following review is based on more detailed reviews by Fretter & Graham (1994) and Crothers (1985), to which the user should refer for further detail. The original references are given where appropriate.
Growth rates vary depending on wave exposure, prey type and starvation. Sheltered shore populations grow faster than wave exposed shore populations, resulting in larger more elongate shells (Osborne, 1977; Crothers, 1985; Etter, 1989). Feare (1970b) reported that juveniles reached 10mm with a year, ca 15 mm at 2 years old and entered maturity at ca 20 mm at Robins Hood Bay in Yorkshire. Moore (1938a) reported that dog whelks reach 10-15 mm at I year, 21-26 at 2 years and 29.5 mm at maturity. Maturity was calculated to be reached at 2.5 years at which point shell growth stops (Fretter & Graham, 1994). However, Etter (1996) suggested that adults continued to grow but extremely slowly. Osborne (1977) noted that juveniles <12 mm grew at the same speed above which sheltered individuals grew faster than wave exposed individuals. Etter (1996) reported that juveniles grew 6 mm/150 days on wave exposed shores but 9 mm/150 days in sheltered conditions. Mussels supported the highest growth rates (Hughes & Drewett, 1985). Etter (1996) transplanted juveniles between shores of different wave exposure, and concluded that growth was determined by environmental factors and depressed by wave exposure since it reducing foraging or feeding time.
Crothers (1985) suggested that, although crabs select the largest first year class dog whelks, rapid growth may allow dog whelks to grow beyond the predators preferred size range and decrease their susceptibility to predation.
Nucella lapillus is an important intertidal predator and preys mainly on barnacles and mussels but may also prey on cockles, other bivalves and gastropods.
Factors affecting feeding
- As in many neogastropods, the mouth and radula are born on an extensible proboscis, which in Nucella lapillus is approximately the same length as the shell in each individual (Barnes, 1980; Crothers, 1985).
- Nucella lapillus feeds by either
- pressing the proboscis between the valves of bivalves or plates of barnacles and removing flesh by the rasping radula, or
- by boring a hole in the shell of its prey and inserting the proboscis through the hole.
- The victims shell is bored by a combination of mechanical rasping by the radula in the proboscis and chemical attack by secretions of the accessory boring organ (ABO) situated in the sole of the foot.
- Once penetrated, the prey is narcotized by secretions of the accessory salivary glands, which also secrete a cement like substance that may help keep the proboscis attached to the prey (Andrews, 1991; Fretter & Graham, 1994). The hypobranchial gland also secretes a pharmacologically active choline ester that may be involved in narcotization (Carriker, 1981; Crothers, 1985), however its function is disputed by Fretter & Graham (1994).
- The dog whelk secretes digestive enzymes into the body of the prey and then ingests the resultant tissue 'soup' (Crothers, 1985).
- The 'gape' attack method is energetically more effective (Fretter & Graham, 1994) and is more likely to be used by dog whelks with experience of handling the prey than inexperienced dog whelks and results in a lower prey handling time than boring (Rovero et al., 1999). Large dog whelks can also force the proboscis between the opercular plates of barnacles to apply the narcotic (Carriker, 1981; Fretter & Graham, 1994). The 'gape' attack is presumed to rely on successful application of the narcotic (Rovero et al., 1999).
- Rovero et al. (1999) reported that the 'gape' attack method resulted in prey handling time (including inspection, narcotization and ingestion) of 49-51 hrs depending on experience, compared with a handling time of ca 100 hrs by boring. Morgan (1972) reported that boring could take 3 days to complete. Therefore, handling time can span several tidal cycles during which the dog whelk is vulnerable to desiccation, wave exposure and predation (Hughes & Drewett, 1985; Rovero et al., 1999).
- It has been shown that experience of a particular food type reduces handling time (Dunkin & Hughes, 1984; Hughes & Dunkin, 1984), which may partly explain dog whelks preference for a particular type of prey even in the presence of others.
- Once fed the dog whelk rests in a crevice or other shelter, up to 2-4 tides after feeding on barnacles and 7-9 tides after mussels (Hughes & Drewett, 1985). However, larger dog whelks have higher energy demands and rest for shorter periods (Bayne & Scullard, 1978).
- Crothers, (1985; Table 1) lists 24 potential recorded food species. Nucella lapillus usually favours Semibalanus balanoides > Balanus spp. > Mytilus edulis > Eliminius modestus > (Crothers, 1985).
- Larger dog whelks tend to handle larger prey than small dog whelks. Hughes & Burrows (1993 ) found that dog whelks avoided mussels <5 mm and preferred 10-20 mm mussels (Hunt & Scheibling, 1998). Hunt & Scheibling (1998) noted that although juveniles (<3 mm) rarely fed on mussels <2 mm and post recruits (<5 mm) only rarely consumed mussels <5 mm both were capable of feeding on the full size range of mussels presented. Mussels > 40 mm seem to be safe from dog whelk attack, and Crothers (1985) suggested that 20 mm long mussels were optimum for a 30 mm long dog whelk (Bayne & Scullard, 1978; Crothers, 1985).
- Feeding rates vary, depending on size (hence shell thickness) of prey, temperature and season.
- Crothers (1985) suggested a mean annual consumption of 15-40 mussels per dog whelk (Largen, 1967a; Bayne & Scullard, 1978) and reported rates of 0.5 or 0.59 mussels/day or 1.1 Semibalanus balanoides /day in summer (Connell, 1961; Fretter & Graham, 1962; Anala, 1974).
- Largen (1967b) noted that feeding rates decreased with temperature, from an average of 16 barnacles or 0.7 mussels per week at 20 °C to 10.2 barnacles and 0.4 mussels per week at 15 °C.
- Connell (1961) noted that the time spent feeding on open rock surfaces decreased from about 60% in July to September to only 13% in January to March.
- Although foraging patterns on a given shore are similar, they vary between locations depending on the type of shore, its wave exposure, and local weather. Dog whelks from sheltered shores forage less in sunny, warm weather, whereas animals from wave exposed shores favoured calm periods even when sunny (Burrows & Hughes, 1989; Fretter & Graham, 1994).
- Stickle et al. (1985) demonstrated that starvation could overcome the dog whelks tendency to avoid stressful conditions e.g. low salinity. Feeding rates were reduced at low salinity and temperature, e.g. only 25% of dog whelks examined fed at 25 psu and 5°C or 15 psu and 8.5°C. When exposed to air (emersion) ingestion rates were affected by the air and water temperatures, the difference between these temperatures, salinity, humidity, weather conditions and appetite (Stickle et al., 1985) (see sensitivity).
- Dog whelks avoid dense mussel beds, preferring the diffuse margins between the mussel bed and the surrounding barnacle dominated substratum, or solitary mussels (Petraitis, 1987; Fretter & Graham, 1994; Davenport et al., 1996). This was partly because mussels can immobilise gastropods (Nucella lapillus and Littorina littorea) crossing the mussel bed with their byssus threads. Davenport et al., (1996) found that although Littorina littorea broke free of at least 14 byssus threads within 45 mins, Nucella lapillus attached by 1-18 byssus threads took 4-12 hrs to escape. Some specimens, however, were found immobilised by at least 30 byssus threads. Dog whelks take a long time to feed, hence, increasing the chance of them being immobilised. Petraitis (1987) suggested that mussels co-operated to flip over predatory dog whelks. However, Davenport et al., (1996) found that byssus attachments occurred to areas of the shell closest to the substratum, their was no evidence of selective attachment to flip the shell over. Petraitis (1987) calculated that nearly 30% of dog whelks in a mussel bed perished due to being immobilised.
Shell shape, colour and sculpture variation
Nucella lapillus is highly variable in the appearance of its shell, depending on wave exposure and location (see Crothers, 1983; 1985 for review).
Shell shape variation
- Shell colour may be white, brown shading to black, mauve grading to pink, yellow shading to orange and rarely true orange, pink or black (Moore, 1936; Berry & Crothers, 1974; and Crothers, 1985, Plate 2). The white form predominates in the UK, but coloured shells predominate in the southern limits of its range (Portugal and Northern Spain) and in northern populations in Iceland (Crothers, 1985).
- Nucella lapillus also exhibits a variety of banded forms, with a mixture of un-banded, thin or thick banded (see Crothers, 1985 for discussion).
- Palmer (1984) demonstrated the inheritance of colour, banding and spiral shell sculpture using breeding experiments in Nucella emarginata. Similar breeding experiments have not been carried out in Nucella lapillus (Crothers, 1985), however it seems likely that colour and banding are under genetic control.
- In some populations, mainly sublittoral or from the intertidal in North Kent, the growth lines extend outwards to form flounces or ruffles, and this variety of dog whelk is called Nucella lapillus var. imbricata. The imbrication is genetically determined but may appear less marked due to abrasion (Largen, 1971; Crothers, 1985).
- The shell may also bear white dentiform tubercles on the inside edge of the shell lip, which develop once the shell has stopped growing (ca 2 years ). However, interruption of growth earlier in life, possibly due to starvation or parasitism may result in additional rows of teeth (Crothers, 1985).
Variation in shell shape and length has been extensively studied (see Crothers, 1985 for a review). Key points follow.
- Sheltered shore animals grow faster than wave exposed individuals (Osborne, 1977) and sheltered shore populations have longer shells than wave exposed populations. Populations of exceptional length (up to 60 mm) occur subtidally or at extreme low water at Porlock Weir in the Severn Estuary, between Swanage and Kimmeridge, Dorset and at some sites in western Scotland (Crothers, 1985).
- Nucella lapillus from wave exposed shores tend to have shorter, squatter shells than those from sheltered shores, which are more elongate. A progression from squat to elongate form is seen with decreasing wave exposure (Cooke, 1895; Kitching & Ebling, 1967; Crothers, 1985). The shape of the shell can be expressed in terms of the shell length relative to the aperture length (see Crothers, 1985 for review). The possible reasons for the relationship between wave exposure and shell shape are noted below.
- Short squat shells offer less resistance to water flow and wave action and exhibit a larger aperture and larger foot and hence increased pedal surface area, which increases their adhesion the substratum (Cooke, 1895; Kitching & Ebling, 1967; Crothers, 1985; Etter, 1988).
- Etter (1988) noted that the foot grows faster in wave exposed conditions rather than in sheltered conditions and that foot size increased in dog whelks transplanted to more wave exposed shores but change little in the reciprocal transplant (Etter, 1988; Fretter & Graham, 1994).
- Longer, elongated shells have a relatively smaller foot but can hold a significantly greater volume of water within its mantle cavity when emmersed and are more tolerant of desiccation (see sensitivity) (Osborne, 1977, Kirby, 1994a).
- Short squat shells are more prone to predation, their rounded shape makes them easier to swallow for birds such as gulls and eider duck. In addition, the animal is not able to withdraw completely into the shell making them susceptible to crabs and oystercatchers whereas the elongate shell form can withdrawn completely and the narrow aperture does not allow crabs to gain adequate purchase on the shell. (Osborne, 1977) (see sensitivity to wave exposure).
- Crothers (1985) reported that the squat shell shape was absent from wave exposed sites in south-east England, the north coast of Wales, the Solway Firth and the Severn Estuary. Crothers (1985, Figure 33) suggested that the UK population of Nucella lapillus was divided into two groups, a south western group bearing the genes for the squat shell shape and another north-eastern from, which lacks the genes for the squat form and can only develop as the elongate form.
In addition to the colour variation mentioned above, Nucella lapillus has been shown to demonstrate clines in allozyme (Day & Bayne, 1988; Day, 1990; Kirby, 1994a, b) and mitochondrial DNA polymorphisms (Kirby et al.,1997), Robertsonian translocation (Staiger, 1957; Bantock & Cockayne, 1975; Page 1988; Pascoe & Dixon, 1994; Pascoe et al., 1996), peri-and para-centric chromosomal inversions (Page 1988; Pascoe & Dixon, 1994; Pascoe et al., 1996; Pascoe, 2002). Variation in chromosome number was found to vary greatly between different populations, within some populations and even within some individuals (Pascoe, 2002).