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Protective refuges for seeded juvenile scallops (Placopecten magellanicus) from sea star (Asterias spp.) and crab (Cancer irroratus and Carcinus maenas) predation Melisa C. Wong, Myriam A. Barbeau, Allan W. Hennigar, and Shawn M.C. Robinson
Abstract: We examined two methods to provide refuge for seeded juvenile sea scallops (Placopecten magellanicus) from sea star (Asterias spp.) and crab (Cancer irroratus and Carcinus maenas) predation by considering (i) initial density of seeded scallops and (ii) presence of an alternative prey species (blue mussel (Mytilus edulis)). In the seeding density experiment, underwater plots were seeded with different densities of scallops (1, 6, and 69·m–2). In the alternative prey experiment, plots were seeded with one density of scallops (5·m–2) and different densities of mussels (0, 5, and 30·m–2). Animal densities were monitored over time, and predation rate was estimated using tethered scallops. In the seeding density experiment, scallop density in plots initially seeded with 6 scallops·m–2 decreased at the slowest rate. Estimated predation rate of scallops in all plots tended to increase with prey density. In the alternative prey experiment, mussel density decreased immediately after seeding, while scallop density decreased after approximately 1 week. Estimated predation rate of scallops decreased with increasing mussel density. Also, sea stars aggregated in plots containing scallops and mussels. In both experiments, 17%–58% of seeded scallops were lost to dispersal, and final scallop density was approximately 1·m–2, independent of treatment. Résumé : Nous avons évalué deux méthodes pour procurer un refuge à de jeunes pétoncles (Placopecten magellanicus) ensemencés contre la prédation par les étoiles de mer (Asterias spp.) et les crabes (Cancer irroratus et Carcinus maenas) en tenant compte de (i) la densité initiale des pétoncles ensemencés et (ii) la présence d’une espèce de proie de rechange (la moule bleue, Mytilus edulis). Dans l’expérience sur la densité de l’ensemencement, nous avons ensemencé des parcelles sous-marines avec des densités différentes de pétoncles (1, 6 et 69·m–2). Dans l’expérience sur les proies de rechange, nous avons ensemencé les parcelles avec une seule densité de pétoncles (5·m–2) et différentes densités de moules (0, 5, 30·m–2). Nous avons suivi la densité des animaux au cours du temps et estimé le taux de prédation à l’aide de pétoncles attachés. Dans l’expérience de densité des ensemencements, les densités de pétoncles ont décliné le plus lentement dans les parcelles ensemencées au départ avec 6 pétoncles·m–2. Le taux estimé de prédation dans toutes les parcelles a tendance à augmenter en fonction de la densité des proies. Dans l’expérience sur les proies de rechange, la densité des moules diminue juste après l’ensemencement, alors que la densité de pétoncles diminue après environ 1 semaine. Le taux estimé de prédation des pétoncles décline en fonction inverse de la densité des moules. De plus, les étoiles de mer se rassemblent dans les parcelles contenant des pétoncles et des moules. Dans les deux expériences, 17– 58 % des pétoncles sont perdus à cause de la dispersion et la densité finale des pétoncles est d’environ 1·m–2, quel que soit le protocole expérimental suivi. [Traduit par la Rédaction]
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Introduction Refuges from predation are any type of strategy prey use to reduce their risk of predation (Sih 1987a). These strategies lower the probability of encounter between predators and prey or decrease the probability a prey is attacked, cap-
tured, or consumed after an encounter occurs (Sih 1987b). Prey may lower the probability of encounter by being cryptic, by limiting activity to when predators are absent, or by hiding in crevices in the surrounding habitat (Sih 1987b; Arsenault and Himmelman 1996). If prey are encountered by predators, a variety of antipredator strategies may be
Received 11 August 2004. Accepted 23 March 2005. Published on the NRC Research Press Web site at http://cjfas.nrc.ca on 26 August 2005. J18256 M.C. Wong1 and M.A. Barbeau. Department of Biology, University of New Brunswick, Fredericton, NB E3B 1E6, Canada. A.W. Hennigar. Division of Orthopaedic Surgery, QE II Health Sciences Centre, Halifax, NS B3H 3A7, Canada. S.M.C. Robinson. Fisheries and Oceans Canada, St. Andrews Biological Station, 531 Brandy Cove Road, St. Andrews, NB E5B 2L9, Canada. 1
Corresponding author (e-mail:
[email protected]).
Can. J. Fish. Aquat. Sci. 62: 1766–1781 (2005)
doi: 10.1139/F05-092
© 2005 NRC Canada
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used. For example, reductions in the probability of attack may occur if chemical defenses render prey unpalatable or toxic to predators (Avila et al. 2000), in the probability of capture if prey use flight responses (such as swimming) (Barbeau and Scheibling 1994a), and in the probability of consumption if prey have morphologies (such as thick shells and large body size) that make handling by predators difficult (Elner and Hughes 1978). In addition to these types of antipredator strategies, manipulation of certain characteristics of prey populations may create protective refuges for prey. In particular, the density of prey and the presence of multiple prey species may play an important role. In general, there are two categories of behavioural responses that predators display to changes in prey density (Taylor 1984): an aggregative response where predators aggregate in areas of high prey density, and a functional response where individual predators change their consumption rate. Aggregative responses of predators can lead to an increased probability of dying for prey owing to the increase in predators present. However, interference interactions between predators at high density may reduce the probability of attack, capture, and consumption of prey so that a portion of prey may be protected from predation (Sih et al. 1998). The functional response of predators can also play an important role in creating prey refuges. It has three common forms (Taylor 1984): a type I response, where predation rate increases linearly with prey density; a type II response, where predation rate increases at a decelerating rate as prey density increases to 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. When predation rate is transformed to proportional mortality of prey (which is equivalent to the probability of prey dying), the role of the functional response in providing prey refuges becomes more apparent. Proportional mortality is density independent for the type I functional response, negatively density dependent for the type II response, and initially positively density dependent and then negatively density dependent for the type III response. If predators have a type I functional response, there is no refuge from predation, since the probability of prey dying is independent of prey density. If predators have a type II functional response, prey may have a refuge from predation at high density, where their proportional mortality is lowest. If predators have a type III functional response, prey may have a refuge from predation at both low and high density of prey but not at intermediate densities. The presence of multiple prey species may also protect prey from predators by influencing the probability of encounter and the outcomes of encounters. When multiple prey species are available for consumption, predators may select a certain prey type over others (Chesson 1978). Prey selection, when one prey type is consumed disproportionately more than others (Chesson 1978), may exist for several reasons: the selected prey may be encountered most often, be easiest to handle, or be highest in net energy and profitability (Wong and Barbeau 2005). If predators select prey A over prey B, prey B may be encountered less than other prey types and obtain a refuge from predation. If the probability of encounter is not influenced, prey B may still be protected from predation if the probability of being attacked, captured,
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or consumed is lower than with prey A. For example, predators may not attack prey B if it is lowest in profitability, capture prey B if it has the best evasion behaviours, or consume prey B if morphological features make handling difficult. In coastal Atlantic Canada, sea stars (Asterias spp.) and rock crabs (Cancer irroratus) are important predators of juvenile sea scallops (Placopecten magellanicus) (Cliche et al. 1994; Barbeau et al. 1996). The green crab (Carcinus maenas), which invaded the area approximately 60 years ago, is also likely an important predator (Chapman et al. 2002). During the last two decades, there has been considerable interest in the bottom culture of scallops, where juveniles are released (seeded) onto the sea bottom for growth to commercial size (Ventilla 1982; Couturier et al. 1995; Gardner Pinfold IEC, Inc. 2001). To date, the success of bottom culture has been limited, since seeded scallop populations are often decimated by predators (Volkov et al. 1983; Cliche et al. 1994; Barbeau et al. 1996). Predator-related mortality is particularly important immediately after seeding, causing a rapid decline in scallop survival in the first 1–8 weeks (Barbeau et al. 1996; Hatcher et al. 1996; Barbeau and Caswell 1999). Scallop survival generally stabilizes thereafter. Thus, seeded scallops may need a protective refuge from predation during the beginning phase of bottom culture. In this paper, we examine two methods of creating protective refuges for seeded scallops by considering (i) the density of seeded scallops and (ii) the availability of an alternative prey species. Recent seeding trials have shown that sea stars and rock crabs do not have aggregative responses to increases in scallop density (Barbeau et al. 1996) but do have density-dependent predation on seeded scallops (Barbeau et al. 1994, 1998). Despite the potential importance of seeding density in creating protective refuges, most bottom culture operations simply seed the number of scallops available. Seeding density has ranged from 1 to 1000 scallops·m–2 (Volkov et al. 1983; Hatcher et al. 1996; Goldberg et al. 2000). Additionally, few studies consider whether the presence of other prey species can provide a protective refuge for seeded scallops. Field experiments were conducted in Passamaquoddy Bay, New Brunswick, Canada, to investigate these two strategies. In the seeding density experiment, three different densities of juvenile scallops were released into underwater plots. In the alternative prey experiment, a constant density of juvenile scallops was seeded into underwater plots, concurrently with one of three densities of alternative prey. We used the blue mussel (Mytilus edulis) as our alternative prey, since it is relatively immobile and less commercially valuable than scallops. To determine the effectiveness of the two methods in creating protective refuges, we quantified predator and seeded animal densities throughout the experiments using video surveys. Tethered scallops were used to quantify predation potential and identify predators.
Materials and methods Study site The seeding experiments were conducted in the summer of 2001 and 2002 near Tongue Shoal in Passamaquoddy Bay, New Brunswick, Canada (Table 1; Fig. 1). This site was selected based on preliminary video and manual transect © 2005 NRC Canada
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Table 1. Summary of surveys during seeding experiments at Tongue Shoal, Passamaquoddy Bay, New Brunswick, Canada. Experiment Seeding density experiment
Alternative prey experiment
Survey dates 9 August 2001 11 August 2001 12 August 2001 13 August 2001 15 August 2001 20 August 2001 4 September 2001 19 August 2002 20 August 2002 21 August 2002 22 August 2002 24 August 2002 26 August 2002 7 September 2002 29 September 2002
Day from seeding
Fig. 1. (a) Location of our field site at Tongue Shoal in Passamaquoddy Bay, New Brunswick, Canada. (b) Experimental setup at the field site (not to scale).
–2 0 1* 2 4* 9* 24* –1 0 1† 2† 4† 6† 18† 40†
*Dates when tether lines were retrieved in the seeding density experiment. † Dates when all tethered scallops (Placopecten magellanicus) were monitored in the alternative prey experiment.
surveys conducted in July 2000, which indicated the presence of predator and prey species of interest (crabs, sea stars, and juvenile and adult scallops). For the experiments, two 112-m-long baselines (lead-weighted lines) were placed 18 m apart on a 320° magnetic bearing. There was a slight depth gradient between the baselines, with the eastern-most baseline being slightly deeper (
