Author's personal copy Journal of Experimental Marine Biology and Ecology 371 (2009) 10–19 Contents lists available at ScienceDirect Journal of Experimental Marine Biology and Ecology journal homepage: www.elsevier.com/locate/jembe Predator–prey interactions from in situ time-lapse observations of a sublittoral mussel bed in the Gulf of Trieste (Northern Adriatic) Jennifer A. Sawyer a, Martin Zuschin a,⁎, Bettina Riedel b, Michael Stachowitsch b a Department of Paleontology, University of Vienna, Althanstrasse 14, 1090 Vienna, Austria b Department of Marine Biology, University of Vienna, Althanstrasse 14, 1090 Vienna, Austria article info abstract Article history: Hexaplex trunculus (Linnaeus, 1758) is one of the most abundant and widespread muricid gastropods in the Received 29 May 2008 Northern Adriatic Sea, but relatively little is known about the feeding ecology of this predator. We examined the Received in revised form 25 November 2008 activity of H. trunculus on a sublittoral mussel bed at 24 m depth through in situ time-lapse observations and bulk Accepted 21 December 2008 samples. The camera photographed a 0.25 m2 section of the mussel bed at 6-min intervals for ~23 h. Photos were examined frame-by-frame for gastropod movement and activities, especially interactions between H. trunculus Keywords: and Mytilus galloprovincialis (Lamarck, 1819). Our survey indicates high activity-levels of H. trunculus on the sea Benthos fl fi Hexaplex oor: all gastropods made minor movements, most made major movements, and most left the eld of view during Mediterranean the study-interval. On average, individuals remained stationary for only 7.3 h. Two predation attempts on Mytilus Mytilus involving conspecific competition were documented, and one Hexaplex was consuming a mussel at the onset of Predation the deployment. Additionally, 487 M. galloprovincialis from four diver-taken 0.25 m2 quadrates were measured and examined for traces of marginal chipping and drilling predation. Mytilus from surface samples ranged from 11.1 mm to 95.5 mm in length, and one of the four samples had a significantly different average shell length from the others. 114 H. trunculus were collected and measured. Hexaplex ranged from 22.1 mm to 86.1 mm and the mean shell length did not differ among samples, though they were overwhelmingly medium and large. Predation frequency (the ratio of successfully preyed upon bivalves to the total number of bivalves sampled) is high at the studied site (N55%), and large gastropods preferred a chipping mode of predation to drilling, supporting earlier laboratory studies showing a preference for M. galloprovincialis and this predation strategy. Prey effectiveness (the ratio of failed predatory attacks to total predatory attacks) is also high (63.8%), and no evidence of a size refuge was found. Feeding in H. trunculus is highly facultative, calling for caution when using drill holes to estimate predation intensities; whenever possible, traces of multiple predation modes should be considered. © 2008 Elsevier B.V. All rights reserved. 1. Introduction Harper and Peck, 2003), marginal chipping (Peharda and Morton, 2006) and wedging (Vermeij and Kool,1994). Moreover, at least one laboratory Predator–prey interactions are frequently investigated in laboratory study has documented muricids killing mussels without producing any experiments (e.g., Freeman and Byers, 2006; Peharda and Morton, 2006; visible damage to the prey shell (Kowalewski, 2004). Drill holes are Chattopadhyay and Baumiller, 2007). While this approach allows a high preserved in the shell and can be easily quantified in bulk samples. level of control, it often does not accurately reflect the same interactions Marginal chipping leaves characteristic damage on the shell's exterior in the natural environment: natural settings are complex, and most (Carriker, 1951; Warren, 1916) that can easily be quantified in complete laboratory experiments are designed to eliminate such complexities. shells with limited marginal damage from other sources. Moreover, most field data tend to be from more accessible intertidal Predation is a key process in structuring benthic communities habitats (e.g., Sanford et al., 2003; Meyer and Byers, 2005; Edgell and (MacArthur, 1972; Holt, 1977; Palmer, 1979; Bohannan and Lenski, Rochette, 2008) than from the methodologically more demanding 2000), and recent literature proposes low predation pressure as a general subtidal settings (e.g., Breen et al., 1982; Wahle and Steneck, 1992). We background condition in the Northern Adriatic (e.g., McKinney and build upon recent laboratory studies on the predatory behavior of Hex- Hageman, 2006; McKinney, 2007). McKinney (2007) lists asteroids, aplex trunculus (Peharda and Morton, 2006; Morton et al., 2007)to bottom-feeding fish, cephalopods, crustaceans, gastropods and poly- better understand its ecology in its natural setting. chaetes as carnivores in the Adriatic basin, but few studies have examined Three modes of predatory attack are documented in muricid the effects of these predators. Muricid gastropods play an important role gastropods: drilling (Peharda and Morton, 2006; Harding et al., 2007; in regulating the population dynamics of mussel, barnacle, tubeworm and limpet prey (Menge, 1974; Morton, 2004). H. trunculus is one of the ⁎ Corresponding author. most abundant and widespread muricid gastropods in the Northern E-mail address: [email protected] (M. Zuschin). Adriatic, where it is fished for human consumption and used as fish bait. 0022-0981/$ – see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.jembe.2008.12.010 Author's personal copy J.A. Sawyer et al. / Journal of Experimental Marine Biology and Ecology 371 (2009) 10–19 11 Also, Hexaplex's heavy consumption of cultured bivalve prey has rendered it a pest species (Benović,1997). Densities of up to 120 individuals/m2 have been reported at black mussel (Mytilus galloprovincialis)and European flat oyster (Ostrea edulis, Linnaeus, 1758) aquaculture fisheries (Zavodnik and Šimunović,1997). Wurzian (1982) studied the function of carnivores from epifaunal communities in the Northern Adriatic and determined that H. trunculus has a homogeneous distribution there (average density 0.2±0.1 individuals/m2). In a baiting experiment using a dead fish, 39 individuals were attracted, equivalent to every H. trunculus within 200 m2. The gastropod's diet consisted of Arca noae (Linnaeus, 1758), Chlamys varia (Linnaeus, 1758), Corbula gibba (Olivi, 1792), Venus sp. (Linnaeus, 1758), and Ophiothrix quinquemaculata (DelleChiaje, 1828); it also grazed on sponges. Despite its abundance and relative importance as a consumer of cultured bivalves, little is known about the ecology of H. trunculus.Most studies deal with the occurrence of imposex (Axiak et al., 1995; Terlizzi et al., 1998; Chiavarini et al., 2003) and its purple dye (Andreotti et al., 2004). Peharda and Morton (2006) and Morton et al. (2007) studied a variety of aspects of H. trunculus feeding behavior in laboratory settings, including predator size, mode of attack, prey choice, handling time and feeding rates using three species of bivalves common in the Northern Fig. 1. Study area: mussel bed located about 2 km off coast of Piran, Slovenia (Northern Adriatic: A. noae, M. galloprovincialis and Modiolus barbatus (Linnaeus, Adriatic Sea; 45° 32.69_N 13°34.94_E). 1758). According to their results, H. trunculus is capable of two modes of attack: drilling a hole through the shell and chipping, in which the gastropod uses a labral spine to chip or wedge the posterior portion of the to 11:01 on 25 September 2007. These photographs were examined bivalve shell. M. galloprovincialis was the preferred prey, and medium- frame-by-frame to document H. trunculus activity, including mobility, and large-sized predators (~55 mm and ~70 mm shell length, prey consumption, and potential predatory attempts. Every individual respectively) chose chipping over drilling when attacking these mussels gastropod was also examined for minor movements (less than one (Peharda and Morton, 2006). The authors calculated that an medium- body-length), major movements (greater than one body-length), sized H. trunculus consumes approximately 18 large M. galloprovinicalis conspecific interactions, predatory behavior, and time spent consuming (~65 mm long) per year. prey. Peharda and Morton's (2006) illustration of a Hexaplex drilling a According to Morton et al.'s (2007) results, H. trunculus tended to Mytilus shows the gastropod positioned atop the posterior portion of chip thin-shelled prey, but drilled bivalves with thicker shells. H. the mussel's shell. Those individuals that made movements ending in trunculus attacked M. galloprovincialis by drilling (either marginally or such prey grappling and manipulation were interpreted to be actively laterally) or chipping, based on the predator and prey size (Peharda searching for prey. These activities were noted, as were potential and Morton, 2006; Morton et al., 2007). Small gastropods tended to attempts to chip or drill the prey shell, and prey consumption. A short drill at the valve margin, medium gastropods tended to chip or drill (at time-lapse film was created from the full series of photographs (see the valve margin) in about equal proportions, and in contrast to online supplementary material). Peharda and Morton (2006), large gastropods tended to laterally drill medium and large-sized Mytilus. 2.2. Quantitative samples 2. Materials and Methods To evaluate predation frequency,