by log damage. Studies on the Olympic Peninsula, Washington, United States also show that by consuming the early successional stages, predators such as whelks and birds and herbivores such as chitons and limpets actually accelerate succession (Suchanek 1981; Paine 1984).
The importance of large‐scale ocean currents in the global distribution of bivalves has already been dealt with in this chapter. Locally, areas with strong currents usually provide favourable feeding conditions for bivalves. However, very strong currents can have an inhibitory effect on feeding and consequently growth. Also, strong currents may prevent larval settlement and byssal attachment of spat, ultimately resulting in local variability in recruitment.
Fishing methods can affect bivalve abundance directly by causing significant mortality and indirectly by causing shell damage. In Spain, mussel seed from intertidal exposed rocky shores is the method most used by farmers to seed ropes in mussel culture areas (Peteiro et al. 2007). This practice, while legal, must have a detrimental effect on mussel beds and their community structure, although to date there is no documented evidence of damage.
Biological Factors
Just as humans greatly appreciate the delicate flavour of bivalves, so also do a whole range of other organisms from groups as diverse as fish, birds, mammals, crustaceans, echinoderms, flatworms and even other molluscs. Bivalves are usually preyed upon by several of these groups, which operate at specific times of the year, and which generally focus on the smaller size classes. Predators are probably the single most important source of natural mortality in bivalve molluscs and have the potential to influence population size structure, overall abundance and local distribution patterns.
In this section, the main predators of mussels will be dealt with, along with major pests, fouling organisms and competitors. Most of the following information comes from studies in intertidal and shallow water environments.
Predators, Biofouling and Competitors
Gastropods are significant predators of mussels worldwide. The dogwhelk, Nucella lapillus, is widely distributed on exposed shores in northern Europe and on the east coast of North America, where it feeds extensively on barnacles and small mussels. Predation is often seasonal, with whelks remaining aggregated in pools and crevices over the wintertime. However, numbers on mussel beds on the low and mid shore start to increase in the spring, and densities as high as 300 whelks m−2 have been recorded over the summer months in NE England (Seed 1969). Profitability (energy assimilated from a food item relative to handling time) for dogwhelks feeding on mussels increases with prey size (Hughes & Dunkin 1984). Yet whelks prefer mussels smaller than the largest available. Hughes (1986) suggests that dogwhelks choose mussels with the maximum average profitability in the face of competition from other dogwhelks, which are attracted to the predator by olfactory stimuli from the damaged prey. Marples et al. (2018) recently suggested that profitability is a function of the current state of both the predator and the prey individuals, and that it should be considered to be an attribute of a particular encounter, in contrast to its present usage as an attribute of a prey species. The whelk uses the radula, a modified toothed chitinous structure, to drill a small hole through the thinnest part of the shell around the umbone or adductor muscle insertion regions (Seed 1976), or through the shell area overlying the glycogen‐rich digestive gland (Hughes & Dunkin 1984). Prior to drilling, the whelk softens the area using a secretion from the foot. The proboscis is inserted through the hole and the flesh of the prey is rasped away by the radula, converted into a ‘soup’ and devoured. Alternatively, a more efficient mechanism that is used by experienced whelks involves insertion of the proboscis through the valve gape and induction of muscular paralysis by injection of toxins. Feeding only occurs when conditions are conducive to such an activity, and during these times the dogwhelk consumes large quantities of food, so that the gut is always kept as full as possible. This allows shelter until more food is required, when foraging resumes. If waves are large or there is an excessive risk of water loss, the dogwhelk will remain inactive in sheltered locations for long periods. Feeding rates (drilling plus ingestion times) peak during the summer, but as water temperatures fall through the autumn, the time needed for ingestion lengthens, more than tripling the total handling time (Miller 2013). Prey handling time per mussel is generally in the range of two to three days, which agrees well with results from laboratory experiments showing that an adult whelk can consume about two mussels (1–3 cm shell length) per week during the summer (Seed 1969). Although this level of consumption may appear small, the high density of foraging whelks makes a serious impact on mussel coverage on exposed shores. For example, on rocky intertidal sites in Alaska, United States, where Nucella lima occurs at densities of >100 m−2, Carrol & Highsmith (1996) estimated that the whelk can eliminate 60–90% of mussels (M. trossulus) at a given site in one season. Preference for mussels, as opposed to barnacles, appears to be fixed in early life: adult whelks transferred from sites with no mussel cover to those with a high coverage of mussels largely ignored the mussels, preferring to feast on barnacles (Wieters & Navarette 1998). Mussels ‘fight’ back by ensnaring and immobilising whelks in their byssus threads. An ensnared whelk can be overturned, thus arresting the drilling process (Figure 3.9). Whatever the fate of the mussel, the whelk, once ensnared, is trapped and exposed to predation (Petraitis 1987; Davenport et al. 1998; Farrell & Crowe 2007; Chiu et al. 2011). Sherker et al. (2017) were the first to use organisms raised in the field (Atlantic Canada), rather than in the lab, to demonstrate that predator‐induced morphological responses in bivalve prey hinder predation. During the spring and summer of 2016, they ran a field experiment that manipulated dogwhelk presence to test their nonconsumptive effects on mussel traits. Dogwhelk cues elicited thickening at the lip, centre and base of mussel shells while simultaneously limiting shell length growth. As shell mass was unaffected by dogwhelk presence, a trade‐off between shell thickening and elongation was revealed. Thickening was most pronounced at the thinnest parts of the shell. Using the field‐raised organisms, a lab experiment showed that dogwhelks took, on average, 55% longer to drill and consume mussels previously exposed to dogwhelk cues than mussels grown without such a cue exposure. Dogwhelks drilled at the thinnest parts of the shell, but nevertheless the consumed cue‐exposed mussels had thicker shells at the borehole than the consumed mussels not previously exposed to cues, which likely explains the observed difference in handling time. As handling time normally decreases predation success, this study indicates that the plastic structural modifications in mussels triggered by dogwhelk cues in the field hinder predation by these drilling predators.
Figure 3.9 Photograph of a whelk, Nucella lapillus, flipped on its back by a mussel, Mytilus edulis. Mussels attach a number of byssus threads to the body whorl of the predator gastropod, then retract them, flipping the predator over and immobilising it, and thus exposing it to crab predation.
Source: Photo courtesy of P. Petraitis, Department of Biology, University of Pennsylvania, Philadelphia, Pennsylvania, USA. (See colour plate section for colour representation of this figure).
On the West Coast of the United States, Nucella canaliculata and N. emarginata are major predators of mussels but seem to favour the thinner‐shelled species, M. galloprovincialis, to the thicker‐shelled and less nutritious M. californianus (Suchanek 1981). Other predatory gastropods such as Ocenebra poulsoni, Acanthina sopirata, Ceratostoma nuttalli and Jaton festivus also feed on Mytilus (Shaw et al. 1988), while various birds, crustaceans and fish feed on N. lapillus (details in Crothers 1985). Chemical cues are commonly used by prey to evaluate risk. Large et al. (2010) conducted a study to investigate the nature of cues used by prey hunted by generalist predators. Using Nucella
