Prey selection and the functional response of sea stars (Asterias vulgaris Verrill) and rock crabs (Cancer irroratus Say) preying on juvenile sea scallops (Placopecten magellanicus (Gmelin)) and blue mussels (Mytilus edulis Linnaeus)
Introduction
Predators in nature often include an array of prey types in their diet. Further, in the presence of multiple prey types, they often select certain prey types over others. Selection for a certain prey type is evident when the relative frequency of that prey type in a predator's diet differs from its relative frequency in the environment (Chesson, 1978). An observed selection may result from predators actively choosing a prey type (a process termed active selection) (Rapport and Turner, 1970, Liszka and Underwood, 1990, Sih and Moore, 1990). Alternatively, an observed selection may simply reflect the prey's vulnerability or catchability (a process termed passive selection) (Pastorok, 1981, Sih and Moore, 1990). The observed selection may also result from a combination of both active and passive selection (Barbeau and Scheibling, 1994). Active selection (or active predator choice) occurs when a predator consumes more of a prey type than expected when given a choice of prey types than when not given a choice (Underwood et al., 2004). The prey choice model of foraging theory can be a useful conceptual framework for studying active selection (Sih and Moore, 1990, Barbeau and Scheibling, 1994). The prey choice model predicts that, to maximize energy intake per unit foraging time, a predator consumes prey items of higher profitability (ratio of energy gain to handling time) and ignores items of lower profitability (Stephens and Krebs, 1986). As well, this model predicts that the decision of whether a prey type is attacked or not depends on its profitability and on the encounter rate with other prey types of higher profitability. If maximization of the rate of energy intake does occur in a predator–prey system, then active selection should be influenced by prey profitabilities. Passive selection depends on differential prey vulnerabilities, and is affected by prey morphology (such as body size and shell strength) and prey behaviours (such as escape responses).
To understand predation patterns and observed prey selection, it is useful to describe the predation process mechanistically using the predation cycle. This cycle describes a series of behaviours that characterize predation events, and includes searching for, attacking, capturing, and consuming prey (Holling, 1966, O'Brien, 1979). Based on this cycle, predation rate can be divided into a number of components such as encounter rate, the probability of attack upon encounter (Pr{attack∣encounter}), the probability of capture upon attack (Pr{capture∣attack}), and the probability of consumption upon capture (Pr{consumption∣capture}). These components can be associated with active or passive selection. For example, active selection can be associated with a predator's decision to attack an encountered prey (i.e., Pr{attack∣encounter}). Passive selection, which reflects prey vulnerability, can be associated with encounter rate between predators and prey and with Pr{capture∣attack}. Pr{consumption∣capture} can be influenced by both active and passive selection, since a predator may decide to reject a captured prey (e.g. Elner and Hughes, 1978) or it may simply not be able to handle the captured prey.
The density of available prey types may influence active selection, passive selection and the resulting dynamics between predators and prey. For example, a predator may avoid or reject a prey type that is at low density and is thus unfamiliar. The prey type at low density would have a reduced Pr{attack∣encounter} or Pr{consumption∣capture} compared to a prey type that is at a higher density. Whatever the mechanism, predators can respond to differences in prey density by disproportionately consuming the most abundant prey, a phenomenon termed switching (Murdoch, 1969). Evidence for switching may be apparent when observing prey selection of predators over a range of prey densities.
The presence of alternative prey species may affect the functional response of predators on the target prey species (Chesson, 1989). The functional response represents the relationship between predation rate of individual predators and density of a prey species (Hassell, 1978). Two types of functional responses are commonly observed: the type II response, where predation rate increases at a decelerating rate as prey density increases and reaches a plateau at high prey density; and a type III response, where predation rate increases at an accelerating rate at low prey density and then at a decelerating rate to a plateau at high prey density. In the presence of an alternative prey species, the plateau of the functional response on the target prey may be lower than in its absence. Also, predator behaviours may change in the presence of an alternative prey, influencing the type of functional response on the target prey.
Sea scallops (Placopecten magellanicus) are vulnerable to predation mainly when they are juveniles (< 50–60 mm shell height) (Elner and Jamieson, 1979, Barbeau and Scheibling, 1994). In coastal Atlantic Canada, sea stars (Asterias sp.) and rock crabs (Cancer irroratus) are major predators of juvenile sea scallops (Barbeau et al., 1996). Large portions of juvenile scallops released (seeded) onto the sea bottom for growth by aquaculturists are often lost to predation. Consequently, aquaculturists are concerned with providing seeded scallops with a refuge from predation. The presence of an alternative prey species may provide such a refuge, as predators may select the alternative prey and consume fewer scallops. Mussels (Mytilus edulis) are being considered as alternative prey, since they are less commercially important (Wong et al., in press). Density of both prey species may also play a role in protecting juvenile scallop populations by influencing a predator's functional response on scallops.
The objectives of our study were to examine (i) prey selection of sea stars (A. vulgaris) and rock crabs (C. irroratus) when offered two prey types, juvenile sea scallops (P. magellanicus) and blue mussels (M. edulis), and (ii) the effect of prey density on predation, prey selection, and component behaviours. Laboratory experiments were used to quantify predation rate when mussels (2 levels: absence, presence) and scallops (6–9 levels of density) were offered to predators concurrently. The components underlying predation rate, such as the proportion of time spent searching for prey, encounter rate, Pr{attack∣encounter}, Pr{capture∣attack} and Pr{consumption∣capture}, were quantified.
We predicted that sea stars and rock crabs would select a particular prey species, since scallops and mussels would differ in escape behaviours, shell strength and profitability. Specifically, we predicted that sea stars would select mussels over scallops, a result of passive selection. The Pr{capture∣attack} would be lower for scallops than for mussels, since scallops can effectively escape by swimming away from sea stars while mussels cannot. Thus, mussels would be the easiest prey for sea stars to capture. We predicted that rock crabs would select scallops over mussels, a result of passive and active selection. Since scallops do not tend to swim when attacked by a crab (Barbeau and Scheibling, 1994), passive selection would be associated with prey shell strength and not with differential escape capabilities of the prey. Scallops likely have a lower shell strength than mussels, because scallops require a lighter shell for effective swimming escape from predators (Vermeij, 1987). Crabs would be able to open scallops more easily and more often than mussels. Consequently, Pr{consumption∣capture} would be highest for scallops. Also, handling time would be lower for scallops than for mussels, resulting in scallops being highest in profitability. Active selection would result from crabs having a higher Pr{attack∣encounter} on scallops than on mussels. Furthermore, we predicted that changes in the density of the target prey would not change prey selection. Based on previous work that investigated sea star and crab predation on scallops in the absence of mussels (Wong, 2004), we predicted the simplest scenario. Specifically, we predicted that with increased density of the target prey, encounter rate between the target prey and a predator would increase, but the proportion of time a predator spends searching, Pr{attack∣encounter}, Pr{capture∣attack}, Pr{consumption∣capture} and handling time per prey would not change. This would result in a type II functional response on the target prey. We also predicted that the plateau of the functional response on the target prey would be lower in the presence of the alternative prey species than in its absence, since some alternative prey would be consumed.
Section snippets
Experimental materials
Four experiments were conducted at Huntsman Marine Science Centre, in St. Andrews, New Brunswick, Canada, to examine prey selection and functional response of sea star (Asterias vulgaris) and rock crab (C. irroratus) predators when offered juvenile sea scallops (P. magellanicus) and blue mussels (M. edulis) (Table 1). Juvenile scallops were obtained from Sea Perfect Cultivated Products, Arichat, Nova Scotia, Canada. Mussels were collected from the intertidal zone at Brandy Cove and Indian
Sea star prey selection and predation rate
Sea stars strongly selected mussels over scallops in both the one-factor and two-factor experiments (Fig. 1a,c). The selectivity index did not change over scallop density (Table 2, Table 3), even when scallop density was higher than mussel density (i.e., 67, 83, 111 scallops m− 2 in the one-factor experiment). Active selection was detected underlying observed selection (one-factor experiment: χ12 = 370.3, p < 0.001; two-factor experiment: χ12 = 113.1, p < 0.001).
In the presence of mussels, predation
Prey selection
Sea stars (A. vulgaris) and rock crabs (C. irroratus) selected particular prey species when offered juvenile sea scallops (P. magellanicus) and blue mussels (M. edulis) concurrently. Components of the predation cycle (encounter rate, encounter probabilities) and prey characteristics (handling time per prey, energy content, shell strength) were quantified to help identify mechanisms underlying the observed selection.
We predicted that sea stars would select mussels over scallops, and that passive
Acknowledgements
We thank M. Dowd, B.A. MacDonald, S.M. Robinson and two anonymous reviewers for valuable comments. C. Boone, S. Horsmen, J. Johnson and D. Morrell provided technical support. M.C.W. was supported by a Natural Sciences and Engineering Research Council of Canada (NSERC) Post-Graduate Scholarship, a Vaughan Graduate Fellowship in Marine Sciences, and a R.C. Frazee Scholarship in Marine Studies. The research was funded by a NSERC Discovery Grant to M.A.B. [AU]
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