as a model system, they explored how (1) predator type, (2) predator diet and (3) injured conspecifics and heterospecifics influence Nucella behaviour. Taking laboratory flumes, they found that N. lapillus responded only to the invasive green crab, Carcinus maenas – the predator it most frequently encounters – and not to rock crabs (Cancer irroratus) or Jonah crabs (Cancer borealis), which are sympatric predators but do not frequently encounter N. lapillus because they are primarily subtidal. Predator diet did not affect whelk responses to risk, although starved predator response was not significantly different from controls. Since green crabs are generalist predators, diet cues do not reflect predation risk, and thus altering behaviour as a function of predator diet would not likely benefit N. lapillus. However, the whelk did react to injured conspecifics – a strategy that may allow it to recognise threats when predators are difficult to detect. N. lapillus did not react to injured heterospecifics including M. edulis and herbivorous snails, Littorina littorea, suggesting that they respond to chemical cues unique to their species, allowing them to minimise costs associated with predator avoidance. The ability of prey to detect and respond to predator signals varies with environmental conditions (Large et al. 2011 and references therein).
Sea stars are also important predators that influence the distribution and abundance of mussels on the lower shore and in the sublittoral zone. Sea stars predate on mussels and other bivalves either by using force or by secreting an anaesthetic from their stomach that numbs the mussel and causes it to gape. They then extrude their stomach through their mouth into the shell opening and digest the prey. Sea stars with short or inflexible arms (e.g. Astropecten or Luidia spp.) usually swallow their prey whole while digestion occurs in the stomach, before egesting shell pieces through the mouth. Semmens et al. (2013) have reported a novel neurophysin‐associated neuropeptide that triggers stomach eversion and retraction, which may provide a basis for development of nonpeptidic small molecule agonists or antagonists that mimic or block the effects of neuropeptides; this could be used for chemical control of starfish feeding.
There are numerous studies of the sea star–bivalve interaction on rocky shores, primarily because of the ease of observation and manipulation of this pairing. Such studies have led to a greater understanding of the causes of zonation, and have provided additional evidence on size and spatial refuges in bivalve populations (Dame 2012 and references therein). On the Pacific coast of the United States, the mussel M. californianus exists as a well‐defined band on rocky intertidal shores. The sea star, P. ochraceus, is a major predator of this mussel (Figure 3.10). In a series of classic studies, removal of sea stars over a 10‐year period produced marked changes in zonation patterns, with a notable downward shift in the lower limit of mussel distribution of about 2 m through redistribution of adults and normal settlement of mussel larvae (Paine 1974). Consequently, the starfish has been regarded as a ‘keystone’ predator, one which through its feeding activities exerts a disproportionate influence on community structure, in this case setting the lower limits of mussel distribution. In a keystone predator‐dominated system, other invertebrate predators have minor effects on community structure, but in the absence of the keystone predator, such species may adopt a major role in the altered system (Navarrete & Menge 1996; see also Menge 1992; Menge et al. 1994; Naverette et al. 2000; Gosnell & Gaines 2012).
Figure 3.10 The sea star Pisaster ochraceus predating on mussels, Mytilus californianus, on the US Pacific coast.
Source: David Cowles, http://rosario.wallawalla.edu/inverts. Reproduced with permission. (See colour plate section for colour representation of this figure).
Until recently, the accepted explanation for the distinct zonation patterns on wave‐exposed rocky shores was that dense populations of sedentary organisms, such as mussels, form in static prey refuges above the reach of natural predators. Robles et al. (2009) showed that prey refuges are not in fact static. On the West Coast of the United States, experimental alteration of starfish (P. ochraceus) densities caused the downward extension of the lower boundaries of the mussel M. californianus, while experimental increases in sea star densities caused the upward recession of the lower boundary well into the zone presumed to be a spatial refuge for mussels from predation. As small mussel prey are depleted by sea stars over time, larger mussels are attacked, including those that would otherwise represent the lower boundary of their distribution. Based partly on what is known of Pisaster’s feeding behaviour, moving into the higher reaches of the mussel bed at high tide, then retreating to the lower parts of the bed at low tide, one might predict that the predators are more susceptible to stress than their prey. This was tested in Oregon by transfering mid‐tidal‐level mussels in April to high and low edges of the mussel bed and caging half of them with Pisaster (Petes et al. 2008). Three caging combinations were employed: mussels with and without sea stars, and sea stars without mussels. At four four‐weekly intervals in the summer, both mussels and sea stars were assessed for growth and reproductive status, and tissues were sampled for levels of Hsp70 (see Chapter 9). Results showed that mussels in the high‐level cages spawned earlier and had significantly higher levels of Hsp70 than those in the low‐level cages. There was no significant difference in growth of mussels at the two levels. Sea stars suffered higher mortality at the upper edge of the mussel bed, while those at the lower edge lost body mass but saw less mortality. Sea stars at either level exhibited no significant changes in the level of Hsp70. The authors concluded that intertidal stress factors, such as desiccation and temperature, affect the motile predator more than its sedentary prey. In a subsequent study, Hayne & Palmer (2013) found that P. ochraceus on wave‐exposed shores had narrower arms and were lighter per unit arm length than those from sheltered sites. Narrower arms probably reduce both lift and drag in breaking waves, while on protected shores fatter arms may provide more thermal inertia to resist overheating, or more body volume for gametes.
In northern Europe, Asterias rubens is a serious predator of M. edulis. This sea star aggregates seasonally on mussel beds in large numbers – sometimes as high as 450 m−2 – often completely destroying local mussel populations (Dare 1982). In contrast to the results of laboratory‐based experiments, A. rubens shows no size selectivity when feeding in the field. The solid structure of interconnected mussels forming the bed, however, restricts predation to only those mussels situated at the bed surface, thus providing a refuge from predation for smaller mussels deeper down (Dolmer 1998). Not all mussels are equally susceptible to starfish predation. About 70% of M. edulis of North Sea origin were able to resist A. rubens, whereas all Baltic mussels (presumably M. trossulus) were opened within one hour (Norberg & Tedengren 1995; see also Lowen et al. 2013). M. edulis cultured in close vicinity to A. rubens were significantly smaller in shell length, height and width but had significantly larger posterior adductor muscles, thicker shells and more meat/shell volume. These morphological changes have an adaptive value in that predator‐exposed mussels have a significantly higher survival rate than unexposed mussels (Reimer & Tedengren 1996). Behavioural changes were also evident: predator‐exposed mussels in the laboratory formed larger aggregates, migrated less and sought structural refuges more often (Reimer & Tedengren 1997). Also, chemical aspects of epibionts, such as barnacles, algae, sponges and hydrozoans, on mussel (M. edulis) shells have the potential to modify the top‐down control by starfish (A. rubens) by changing or masking prey properties the sea stars cues upon, or by producing their own repellants (Laudien & Wahl 2004). This may explain why, in an earlier study, A. rubens was reported to prefer clean subtidal mussels over barnacle‐overgrown intertidal ones (Saier 2001). The most popular optimal foraging theory states that predators should maximise prey profitability (i.e. select that prey item that contains the highest energy content per handling
