Peeling out predation intensity in the fossil record: A test of repair scar frequency as a suitable proxy for predation pressure along a modern predation gradient

Palaeogeography, Palaeoclimatology, Palaeoecology 412 (2014) 141–147

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Peeling out predation intensity in the fossil record: A test of repair scar frequency as a suitable proxy for predation pressure along a modern predation gradient Darrin J. Molinaro a,⁎, Emily S. Stafford a, Ben M.J. Collins a, Kristina M. Barclay a, Carrie L. Tyler b, Lindsey R. Leighton a a b

Department of Earth and Atmospheric Sciences, University of Alberta, Edmonton, Alberta T6G 2E9, Canada Florida Museum of Natural History, University of Florida, Department of Natural History, Museum Road, PO Box 117800, Gainesville, FL 32611-7800, United States

a r t i c l e

i n f o

Article history: Received 23 May 2014 Received in revised form 16 July 2014 Accepted 28 July 2014 Available online 12 August 2014 Keywords: Predation Repair frequency Chlorostoma Cancer Crushing Durophagy

a b s t r a c t Predation represents a major cause of death within marine ecosystems, acting as a major agent of natural selection and evolution. Crushing predation in particular is important, as increasing intensity of durophagy through the Phanerozoic has been argued to influence evolution. Repair frequency (RF) is a common palaeoecological metric used to infer crushing predation pressure within the fossil record, yet whether repair frequency variation accurately represents attack frequency or predator success remains uncertain. To determine if repair frequency variation tracks attack frequency or predator success, repair scar frequency for eight, modern intertidal populations of the gastropod Chlorostoma funebrale was calculated along an environmental energy gradient in Barkley Sound, Canada. Attack frequency within intertidal settings is thought to decrease with environmental energy, as crab size, abundance, and intertidal foraging time are greater in sheltered settings than in exposed settings. Spearman's rank correlation of C. funebrale repair frequencies along the energy gradient produced a strong inverse correlation (p ≪ 0.0001) regardless of metric used. These results suggest that repair frequency within crab–gastropod systems serves as a proxy for predator attack frequency. Therefore, the inferences of predation pressure between morphologically similar fossil gastropod populations drawn from repair frequency data are likely accurate. © 2014 Published by Elsevier B.V.

1. Introduction Predation represents an influential process within many ecosystems (Paine, 1966; Kelley et al., 2003). Crushing predation is particularly important as it represents a major cause of mortality in marine ecosystems, and is therefore a major agent of natural selection and evolution (Cadée et al., 1997). Unfortunately, as the prey's skeletal remains are typically destroyed and removed from the fossil record following a successful crushing attack (Stafford and Leighton, 2011), and the predators themselves often have poor preservation potential, identifying and examining predation within the fossil record can be difficult. Thus, repair scars, the healed damage from a failed attack preserved on the prey shell, are often the only remaining evidence of crushing predation, and are measured as repair frequency, i.e., percentage of repairs or repaired individuals within a population (Schoener, 1979; Vermeij et al., 1980, 1981; Schindel et al., 1982; Vermeij, 1982; Geller, 1983; ⁎ Corresponding author. Tel.: +1 780 235 6277. E-mail addresses: [email protected] (D.J. Molinaro), [email protected] (E.S. Stafford), [email protected] (B.M.J. Collins), [email protected] (K.M. Barclay), ctyler@flmnh.ufl.edu (C.L. Tyler), [email protected] (L.R. Leighton).

http://dx.doi.org/10.1016/j.palaeo.2014.07.033 0031-0182/© 2014 Published by Elsevier B.V.

Vermeij, 1993; Dietl and Alexander, 1998; Alexander and Dietl, 2001; Kowalewski, 2002; Leighton, 2002; Alexander and Dietl, 2003; Dietl and Alexander, 2005, 2009; Dietl et al., 2010; Stafford and Leighton, 2011; Dietl and Kosloski, 2013; Leighton et al., 2013; Nagel-Myers et al., 2013). Variation in repair scar frequency between fossil populations is commonly used to identify differences in predation between populations (Leighton, 2002; Alexander and Dietl, 2003). Studies examining variation in repair frequency between populations of modern gastropods, however, suggest that the interpretation and meaning of trends in repair frequency through space or time may be ambiguous (Geller, 1983; Schmidt, 1989; Schindler et al., 1994; Cadée et al., 1997). This is problematic, as it suggests that repair frequency data cannot be used in the fossil record to accurately infer differences in predation between populations. The present study, therefore, aims to determine if repair frequency accurately tracks crushing attack frequency on intertidal gastropods along a common and well-known modern marine environmental and predation gradient near Bamfield, British Columbia, Canada. If differences in repair frequency between prey populations do accurately reflect differences in predation intensity, then meaningful conclusions may be drawn from repair scar data, both in the modern and the paleontological records.

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Although repair scars record actual attacks, there remain several concerns regarding how repair frequency should be measured, and how to interpret differences in repair frequency between localities, or through time (Dietl and Kosloski, 2013). Studies of modern gastropod populations suggest that repair frequency is quite spatially variable, and so may not be an appropriate measure of attack frequency across space or through time. For example, differences in repair frequency between gastropod populations in rocky intertidal versus sandy modern marine habitats demonstrate that repair frequency can vary, even on small geographic scales (Schmidt, 1989). Furthermore, variation in repair frequency of geographically separated gastropod populations can be so great that it would obscure repair frequency trends through time (Cadée et al., 1997). In addition to the difficulty of interpreting patterns in repair frequency, it is not clear that repair scars themselves represent an accurate measure of attack frequency (Leighton, 2002). Given that repair scars document unsuccessful (failed) attacks, an increase in repair frequency can arise from two possible end-member scenarios (Vermeij, 1987). The first is when the number of attacks on a population (attack frequency) increases, and the predator's ability to crush and kill prey (predator success rate) remains the same. This results in the number of both successful and unsuccessful attacks rising, increasing both the number of kills and of repair scars. The second scenario occurs when the predator's success rate decreases while the number of attacks remains constant. In this scenario repair frequency increases as a factor of the increased proportion of failed attacks. Although both scenarios result in repair frequency increasing, they involve opposite trends in successful attacks (kills). Therefore, repair frequency variation between population could represent either variation in the number of attacks (attack frequency), or predator success rate. The problem is further exacerbated by the possibility that larger, older, prey specimens have had more opportunities to be attacked (and survive); thus, differences in repair frequency can also be an artefact of differences in prey size among populations (Vermeij, 1987). Without an understanding of what drives repair frequency, interpreting repair scar data remains difficult. Modern systems, particularly crab–gastropod interactions, are in many ways ideal for determining which factors drive repair frequency in crushing predation scenarios. Many species of crabs are voracious predators capable of great crushing strengths (N50 N of force for larger individuals) that prey upon a wide variety of mollusks (Boulding, 1984). Gastropods grow their shells by accretion, and their visible growth lines make identifying and collecting repair scar data from them relatively straightforward. Both crabs and gastropods are abundant in many marine settings, making the study of their interactions over large scales possible in both the modern and fossil records. Attack frequency within intertidal settings is thought to vary with wave energy, as crab size, abundance, and intertidal foraging time differ between sheltered and exposed settings (Menge and Lubchenco, 1981; Robles, 1987; Boulding et al., 1999; Robles et al., 2001). Large adult cancrid crabs are most abundant in quieter (lower energy), more sheltered settings, moving in and out of the intertidal area with the tides to feed (Robles et al., 1989). Smaller, younger crabs are found within both exposed and sheltered settings, however they are less restricted and proportionally more abundant in exposed higher energy settings due to a lack of competition and predation from their larger conspecifics. Furthermore, sheltered, quieter water settings provide longer foraging times as their narrower swash zones and reduced currents do not cover large portions of the intertidal area during a change in tide. As crabs have difficulty navigating turbulent conditions, like those of the swash zone, more exposed, high energy settings typically have fewer crabs as the large swash zones limit crab foraging (Menge and Lubchenco, 1981; Robles, 1987). Generally, quieter, sheltered settings tend to have larger crabs on average and more dense crab populations than do more exposed settings (Robles, 1987; Robles, et al., 1989).

Given the difference in average crab size and population density between quieter and more exposed intertidal settings, crushing predation pressure experienced by prey (gastropods) within these settings will also vary. Greater crab densities, larger crab size, and longer foraging times generate higher attack frequencies (larger crabs eat more, longer foraging time) and attack success rate (larger crabs are stronger). Likewise, less dense crab populations, smaller crabs, and less foraging time reduces predation pressure, lowering attack frequency (smaller crabs eat less, shorter foraging time) and attack success rate (smaller crabs are weaker). These factors ultimately generate an environmentally controlled predation gradient, where crab population size and density differences between quieter and higher energy settings result in different predation pressures (Robles, 1987; Robles et al., 1989; Boulding et al., 1999). To determine whether attack frequency or predator success rate drive repair frequency, we examined repair frequency across an increasing energy gradient. If repair frequency is driven by attack frequency, then repair frequency should increase with decreasing wave-energy, as a result of environmentally driven changes in foraging time, crab size, and population density. Essentially, larger, more abundant crabs with more time to forage will produce more attacks. In contrast, if repair frequency is driven by predator success and failure, then repair frequency should decrease with decreasing wave-energy, as the larger, stronger crabs that live in quieter settings will be more successful, more likely to destroy the prey shell, and thus will leave fewer opportunities for repair. If repair frequency does not vary predictably with this known predation gradient, then repair frequency may not be a valid measure of predation intensity. 2. Materials and methods 2.1. Study location The southern coast of Barkley Sound and northern portion of Bamfield inlet, located along the western shores of Vancouver Island, British Columbia (Fig. 1), provides an environmentally controlled predation gradient in which to test whether attack frequency or predator success rate drives repair frequency. Eight sites varying in wave energy and predation pressure were chosen based on their proximity to the Sounds' opening to the Pacific Ocean (Fig. 1). The sites closest to the Pacific Ocean were characterised by higher environmental energy and larger waves. Sites located further northeast and inland towards the northern portion of Bamfield inlet were characterised by lower environmental energy and smaller waves. Localities were ranked in order based on their proximity to the open ocean (Table 1 with Whittlestone Point, the closest locality to the open ocean, ranked the highest (8) and Grappler Island, the farthest locality from the open ocean, ranked the lowest (1)). Although the ranking of sites in accordance to their proximity to the open ocean is relative, this ranking is consistent with previous studies documenting relative differences in environmental energy at these sites. Wave energy along the southern coast of Barkley Sound decreases from the mouth of the sound inland (Rawlings, 1994; Gosselin and Rehak, 2007). Mean maximum wave velocities decrease dramatically from Nudibranch Point (0.97 ± 0.5 m/s− 1) to Scott's Bay (0.52 ± 0.33 m/s− 1) (Robles et al., 1989.). The northern portion of Bamfield inlet possesses wave energies much less than those outside the inlet, and mean wave energy at Grappler Inlet (a point between our sites at Strawberry Point and Grappler Island) is 0.05 m/s−1 (Marchinko and Palmer, 2003; Neufeld and Palmer, 2008). The ranking of sites along the southern coast of Barkley Sound and northern Bamfield inlet used in this study, therefore, is a reasonable approximation of the observed differences in environmental energy experienced by each site. More exposed sites (Whittlestone Point, Nudibranch Point, and Prasiola Point) have steeper intertidal areas, with sparse, large rocks and kelp beds towards the subtidal–intertidal boundary. Exposed sites

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Fig. 1. Map of the study area, off of the west coast of Vancouver Island, British Columbia, Canada, with the location of all eight sampling sites indicated. A, Location of Vancouver Island, British Columbia; B, location of Barkley Sound; C, location of eight sampling sites along southern coast of Barkley Sound and northern portion of Bamfield Inlet.

also typically exhibited hard substrate, composed primarily of basaltic basement rock, encrusted by large swaths of mussels, barnacles, and Fucus. More sheltered and quieter water sites (Grappler Island and Strawberry Point) have shallow-sloped intertidal areas, supporting sandy substrates with rocky cover scattered throughout. Quieter sites also typically supported mussels, barnacles, and Fucus, but in much reduced densities and sizes than the more exposed sites. Intermediately ranked sites (Brady's Beach, Mather, and Scott's Bay) have moderately sloped basaltic basement rock supporting large to mid-sized boulder and cobble fields throughout. Sandy substrate was intermittently present within boulder and cobble fields at some intermediate sites. All intertidal site characteristics, including slope, substrate, and taxa, corroborated the existence of an environmental energy gradient across the study area.

2.2. Predator prey system Both the red rock crab Cancer productus (Fig. 2) and the black turban snail Chlorostoma funebrale (Fig. 3) are common within the near shore environment of much of the northeastern Pacific coast, and are abundant within the intertidal coastal zones of Barkley Sound, British Columbia. Both cancrid crabs and trochoid gastropods are well-represented in the Cenozoic fossil record, so results from the present study have potentially broad applications to paleontological studies. C. productus is the most common large durophagous crab found throughout the study area. C. productus possesses monomorphic chela, which display sharp tips and blunt broad molars typical of crushing crabs (Yamada and Boulding, 1998). Mature individuals of the species range in carapace width from around 10 to 20 cm, with mature males

Table 1 Environmental energy ranking of all eight examined sites based on their proximity to the open Pacific Ocean along with each of their locations using GPS coordinates, sample size (number of individuals), average shell height (cm), and repair frequency (RF1 and RF2). Sites were ranked with 1 being the farthest from the mouth of Barkley Sound and 8 being the closest to the mouth of the Sound (closest to the open Pacific Ocean). Rank

Locality

GPS location

Sample size

Avg. shell height (cm)

RF1

RF2

1 2 3 4 5 6 7 8

Grappler Island Strawberry Point Scott's Bay Mather Brady's Beach Prasiola Point Nudibranch Point Whittlestone Point

48°49′56.0″ N, 125°06′54.5″ W 48°49′57.1″ N, 125°07′45.8″ W 48°50′03.4″ N, 125°08′40.6″ W 48°49′56.6″ N, 125°08′55.8″ W 48°49′38.6″ N, 125°09′08.2″ W 48°49′00.3″ N, 125°10′06.5″ W 48°48′49.2″ N, 125°10′44.0″ W 48°48′29.1″ N, 125°11′03.0″ W

100 205 230 200 100 217 233 200

17.17 16.08 15.51 16.44 20.07 18.37 22.51 17.18

0.78 0.898 0.635 0.615 0.57 0.318 0.394 0.21

1.24 1.907 1.026 0.845 0.72 0.359 0.369 0.22

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Fig. 2. Cancer productus, a common durophagous predator present throughout all eight of our sampled sites.

being larger than mature females on average (Robles et al., 1989). C. productus can be found in both subtidal and intertidal marine settings, typically foraging at night to avoid predation by visual predators (Knudsen, 1964). Larger individuals have, however, been observed foraging during daylight, as they may be buffered against predation by their size and formidable strength (Robles et al., 1989). C. funebrale (Family Tegulidae) is a common prey item of the genus Cancer (Abbott and Haderlie, 1980; Geller, 1982) and occurs in great abundance throughout the Pacific Northwest. C. funebrale is the only relatively large gastropod (shell height ≥ 1.25 cm) that is common in both high and low energy environments of the study area, and their

shells are morphologically conservative across our study range, unlike other gastropods such as Nucella lamellosa or Nucella ostrina (Kitching, 1976; Palmer, 1985). As we observed that variation in shell morphology, ornament, and thickness across sites is minimal; differences in predator success between sites are unlikely to be caused by differences in shell shape and thickness. Repair scars are easily identifiable, represented by broken or intersecting growth lines across the exterior surface of the shell (Fig. 3). The majority of repair scars observed on C. funebrale are likely the result of apertural lip peeling by crabs (see Vermeij, 1978, 1982, 1987, 1993; Stafford and Leighton, 2011; Stafford and Leighton, in review); in the fossil record, these scars are identified as the trace fossil Caedichnus (Stafford and Leighton, in review; Stafford et al., accepted for publication). Repair scars are generated as the crab inserts its dactyl (moving finger of the chela) into the aperture of the gastropod shell and pries against the outer apertural lip, breaking the shell backwards into the body whorl and leaving a wedge shaped scar (Stafford and Leighton, 2011). If the crab is unable to reach the gastropod through this opening and kill the gastropod, the prey may survive long enough to regrow its shell, eventually producing the wedge shaped scar identifiable as a characteristic distortion in the shell's growth lines. Compared to other sources of apertural lip damage (e.g., rock chips, wave generated breakages, shell dissolution), predatory peel scars are distinct given their consistent shape and location on the gastropod shell (Stafford and Leighton, 2011; Stafford and Leighton, in review; Stafford et al., accepted for publication). Furthermore, the shape and size of peel scars are large enough that they remain identifiable on multiple whorls of the shells, even those above the body whorl in which growth lines are partially covered by newer shell growth. Despite the distinct shape and appearance of predatory repair scars, it is conceivable that some repair scars could be a response to breakage from transport or contact with debris. Intertidal settings are extremely harsh, as high energy and constant condition cycling make it difficult for organisms to persist within the intertidal compared to other, more stable, marine settings. As a result, gastropod shell breakage is not just limited to predatory interaction within the intertidal. For instance, apertural lip damage can also be caused in a number of ways, including shells being damaged by wave-borne debris, the gastropods themselves being swept off the substrate and thrown against rocks, or even shell dissolution from fresh water influx. Like predatory damage, these sources of damage can also generate repair scars, if the gastropods survive and are capable of continuing their shell growth. However, as non-predatory shell damage between intertidal localities is dependent on how harsh the conditions at each locality are, those with higher energy should display greater repair frequency based solely on their wave energy and tidal currents damaging gastropod shells more readily. Therefore, if repair frequency is driven by non-predatory shell damage, it should correlate positively with wave energy and our examined environmental energy gradient. 2.3. Repair scar survey

Fig. 3. Examples of C. funebrale with and without repair scars from Barkley Sound. A, Large C. funebrale exhibiting no repair scars; B, C. funebrale exhibiting two repair scars; C, smaller C. funebrale exhibiting one large repair scar. Images on left are photographs of actual specimens, images on the right are line drawings of the specimens to better depict the growth lines and repair scars. Arrows in all images point to the repair scars themselves.

Live individuals of C. funebrale were collected and examined from each of the eight study sites during low tide intervals between July and August of 2012 and 2013. Sites sampled during 2012 were resampled during 2013 to make sure that repair scar frequencies did not vary between years. A minimum of 100 live gastropods were randomly collected from across their entire tidal range at each site. Large numbers of individuals were surveyed at sites where C. funebrale populations were dense and laterally extensive to ensure that samples were representative of the site's entire population. Specimens were randomly collected from along a single linear transect parallel to the shore line. Small specimens (less than two whorls of growth) were not collected as their low spire height and small shell height made identifying repair scars problematic and unreliable. Given the great abundance of C. funebrale at all the sites, there was never an

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issue with collecting a minimum of 100 specimens. Once specimens were collected, they were examined for repair scars using either a hand lens or dissecting microscope. The number of repair scars, if present, was recorded, and the maximum height (linear measurement from the apex to base of apertural opening) of each specimen was measured using digital callipers (±0.02 mm). All specimens were then returned to their original location at each site. 2.4. Repair frequency calculations and statistics Repair frequency is commonly calculated using two somewhat similar, but distinct, methods (Leighton, 2002; Alexander and Dietl, 2003; Dietl and Kosloski, 2013). The first method (RF1), is thought to be more conservative (Leighton, 2002; Dietl and Kosloski, 2013), and is calculated by dividing the number of individuals exhibiting at least one repair scar by the total number of individuals within a sample. The second method (RF2) is calculated as the total number of repair scars divided by the total number of individuals within a sample (Alexander and Dietl, 2003; Dietl and Kosloski, 2013). It is important to note that while in the first method (RF1), it is impossible to achieve a repair frequency greater than 1, such values can be achieved using the second method (RF2). This occurs when a large portion of the sampled individuals contain multiple repair scars, such that the number of repair scars within the sample is greater than the number of individuals themselves. Given the use of both these forms of repair frequency (RF1 and RF2) within palaeoecological studies, both methods were calculated for each of the examined sites to determine if the results were consistent. After calculating repair frequencies (RF1 and RF2) for each site, two separate Spearman's rank correlations were calculated (a) to test whether there is an association between mean shell height (proxy for body size) and repair frequency, thus testing for the possibility of a size-related artefact; and (b) to determine whether repair frequency correlates with site ranking (from low to high wave energy). A Spearman's rank correlation is a standard non-parametric statistic, used to assess the degree of association between variables when one of the variables is a monotonic (ordered) function (in this case, the ranking of the geographic gradient from Whittlestone Point to Grappler Island that represents a decrease in energy, and a consequent increase in attack frequency, is a categorical, ordered variable). 3. Results C. productus was observed at all sites, either within the intertidal during high tides or within the subtidal, just below the intertidal, during low tides. The largest specimens of C. productus were routinely observed at Grappler Island, with smaller sizes becoming more common towards Whittlestone Point. Qualitative observations suggest that population size and density of C. productus were greatest at Grappler Island and Strawberry Point, with numerous crabs routinely observed, sometimes in the act of predation, just below water level during low tide, even during the day. Crab numbers and density also appeared to decrease approaching Whittlestone Point, where sightings became much rarer. Specimens of C. productus were commonly observed migrating in and out of the intertidal region with the tides to forage for food. In particular, the large crabs of Grappler Island and Strawberry Point were observed frequently, regardless of the time of day and light levels. Evidence of C. productus feeding on C. funebrale was also found at most sites, in the form of freshly peeled gastropod shells with tissue remains. In rare instances, C. productus was observed grappling specimens of C. funebrale. Captured crabs from various sites (being used in separate research studies at Bamfield Marine Station) would also readily crush and consume C. funebrale in laboratory settings. C. funebrale was extremely abundant at all eight sample sites, with most individuals located within and around tide pools, boulder/cobble fields, or a combination of both. Repair scars on C. funebrale were also

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present at all sites. The most commonly observed repair scars were wedge shaped breakage lines cutting backwards into the body whorl and across older growth lines of the shell (Fig. 3), which are typical of the predatory trace, Caedichnus scissora (Stafford et al., accepted for publication). Such scars were not just limited to the body whorl of shells, with many gastropods exhibiting similar scars on whorls above the lowest one. The lowest observed repair frequency (RF1 = 0.210 and RF2 = 0.220) of all sites was recorded from Whittlestone Point (Table 1). Strawberry Point recorded the highest repair frequency (RF1 = 0.898 and RF2 = 1.907). With the exception of one locality, there was a strong inverse correlation between energy and repair frequency; quieter settings, known to have greater predation pressure, had greater repair frequencies. The only locality whose repair frequency ranking did not match its geographic ranking along the environmental energy gradient was Grappler Island, whose repair frequency (RF1 = 0.780 and RF2 = 1.240) was less than that observed at Strawberry Point, although still the second highest among all localities. A Spearman's rank correlation of repair frequencies along the ranked energy gradient produced a significant and strong inverse correlation (r = − 0.976, p ≪ 0.0001 for RF1; r = − 0.952, p ≪ 0.0001 for RF2). A complete list of repair frequencies (RF1 and RF2), on a site by site basis, can be found in Table 1. Shell height varied from locality to locality, with Nudibranch Point and Scott's Bay displaying the largest and smallest shells, respectively, based on their averages (Fig. 4). Shell height was not correlative with the environmental energy gradient (r = 0.667, p = 0.079); however shell height was weakly, negatively associated with repair frequency (r = −0.714, p = 0.057 for RF1). 4. Discussion The observed negative correlation between repair frequency and the environmental gradient, and by extension attack frequency, strongly corroborates the hypothesis that repair frequency specifically tracks attack frequency. Lack of a positive correlation between repair frequency and the environmental gradient indicates that repair frequency is not driven by non-predator shell damage. Whittlestone Point, the highest energy intertidal site, displayed the lowest repair frequency. Furthermore, Grappler Island and Strawberry Point, where waves, hard substrates, and other typical high energy setting components are virtually nonexistent, display the greatest observed repair frequencies. Interestingly, the negative correlation (r = −0.714 for RF1) between shell size and repair frequency, although not quite statistically significant (p = 0.057), observed across our sites indicates that populations of smaller individuals have more repair scars than populations of larger individuals. This refutes the hypothesis that repair frequency in this

Fig. 4. Box and whisker plot of shell height by locality. Outliers, if present, are represented by individual points above and/or below the whiskers of each locality.

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system might be an artefact of body size, i.e., that larger specimens would have more repairs simply because larger specimens are more likely to be older and would have been exposed to more attacks. The fact that we observed the opposite result may possibly be due to the nature in which Caedichnus repair scars are generated, whereby crabs peeling a notch backwards into the body whorl of the gastropod shell relocate the aperture of the shell backwards along its growth axis. If peeling is significantly extensive, it reduces the shell's height by removing enough material that entire whorls are peeled away and lost. Each failed attack therefore reduces shell size, and the more failed attacks a gastropod shell incurs, the more material it loses along its growth axis. Similarly, gastropods that are never attacked may simply live long enough to grow large, whereas more heavily attacked populations may generally have shorter life-spans. Given the observed negative correlation between shell size (height) and repair frequency, gastropod populations experiencing greater attack frequencies and/or lower predator success rates conceivably might display smaller shell sizes. The extremely strong and inverse (negative) correlation between C. funebrale repair frequency and the environmental energy rankings corroborate the hypothesis that repair frequency across the observed environmental energy and predation gradient along the southern coast of Barkley Sound is primarily driven by attack frequency. Increased attack frequency in quieter low energy settings produces increased repair frequencies. If, in contrast, predator success, rather than attack frequency, drove repair frequency across the observed gradient, then the lower success rate of crabs within higher energy environments would have resulted in greater repair frequency in exposed, higher energy settings, and would have produced a strong positive correlation — exactly the opposite of what we observed. The results hold regardless of which method of calculating repair frequency (RF1 or RF2) is employed. These results are promising, as they not only suggest that inferences on predator prey interactions can be drawn from repair scar data, but also that repair scar frequency can provide insight into predation pressure. Although some researchers (Geller, 1983; Schmidt, 1989; Schindler et al., 1994; Cadée et al., 1997) have argued against the use of fossil repair frequency data because of the variation exhibited by this metric in modern environments, our findings suggest that repair frequency may still provide meaningful palaeoecological information. More importantly, our results suggest that differences in repair frequency among environments occur as a result of differences in attack frequency between populations. While it is unsurprising that predation pressure may vary between environments, this variation is accurately recorded by repair frequency. Cadée et al. (1997) record a similar trend in repair frequency variation as that observed in this study. If their localities are arranged in order of wave energy (sites 2, 1, then 3, the lowest wave energy to the highest of Cadée et al., 1997), repair frequency decreases with increasing energy, a very similar environmental-energy-controlled predation gradient to that of our study. This increase in repair frequency observed in Cadée et al. (1997) is thus also consistent with the hypothesis that differences in repair frequency are the result of differences in attack frequency. Schindler et al. (1994) also observed a similar pattern and proposed that repair frequency was greater in areas with large crab populations and therefore higher attack frequencies. Given that the relationship between gastropod repair scar frequency and attack frequency has been observed in Baja California (Cadée et al., 1997), Georgia (Schindler et al., 1994), and now Barkley Sound, the results of this study are not a localised phenomenon. Rather, intertidal gastropod repair frequencies in general are predictable across environmental gradients and thus are a useful proxy of crab attack frequency. Variation in attack frequency appears to arise from environmental variation, and as a result, environmental conditions may indirectly influence repair frequency in a predictable manner across environments. Research targeting additional habitats, and in different geographic regions (e.g., tropical environments), are needed to test this hypothesis further.

The fact that repair frequency is driven by attack frequency, and not predator success, in modern crab–gastropod predator prey systems is significant as it indicates that repair frequency differences between fossil gastropod assemblages likely reflects attack frequency differences between the assemblages. Comparison of repair frequency data between fossil and/or modern gastropod populations is therefore useful, especially in a palaeoecological context. However, if one is comparing repair frequencies at different temporal intervals, it is, however, still important that comparable environmental settings be examined, just as it is for any palaeoecological study through time. Trends through time should be a function of time, not an artefact of environmental variation. Similarly, caution should also be used when comparing repair frequency data between morphologically distinct groups. Morphological variation between gastropod populations or species may alter predator success rates, such that a predator may be more successful at killing one morphology compared to another, and unless morphology is accounted for, difference in predator success rate between prey morphologies will influence repair frequency differences between populations (Cadée et al., 1997). This is especially true if the morphological variation is significant between prey populations. Comparison of repair frequencies between morphologically distinct populations are thus not just reflecting differences in attack frequency, but also predator success rates. Ultimately, it is essential that differences between populations, other than repair frequency, be understood and accounted for, prior to making conclusions about attack frequency differences. 5. Conclusion Spearman's rank correlations of C. funebrale repair frequencies from along the southern coast of Barclay Sound, Canada, produce a strong inverse correlation (r = − 0.976, p ≪ 0.0001 for RF1; r = − 0.952, p ≪ 0.0001 for RF2) with environmental energy. These results suggest that repair frequencies within C. funebrale populations serve as a proxy for predator attack frequency, not predator success rate in our study area. The use of repair scars to identify and examine predation within the fossil record is not new. Debate surrounding the use of repair frequency data within palaeoecological studies has been ongoing since the work of Vermeij (1987). The results of this study confirm that repair frequency data may be useful towards understanding differences in predation pressure between prey populations. This is especially true for crab and gastropod predator prey systems where gastropod repair frequency is primarily driven by attack frequency and not predator success rate. Acknowledgements The authors would like to thank Chris Schneider, Amelinda Webb, Cory Redman, and Nicole Webster for assistance in site exploration and gastropod collection. Special thanks are also due to G. Vermeij and P. Kelly for their insightful reviews and helpful comments which bettered the manuscript. This research was completed in cooperation with the Bamfield Marine Science Centre, who generously provided housing, laboratory space, and marine transportation during field work. Funding for this research was provided by an NSERC Discovery Grant and a National Geographic Discovery Grant to Leighton. References Abbott, D.P.,Haderlie, E.C., 1980. Prosobranchia: marine snails. In: Morris, R.H., Abbott, D. P., Haderlie, E.C. (Eds.), Intertidal Invertebrates of California. Stanford University Press, California, pp. 230–307. Alexander, R.R.,Dietl, G.P., 2001. Shell repair frequencies in New Jersey bivalves: a recent baseline for tests of escalation with Tertiary, mid-Atlantic congeners. Palaios 16, 354–371. Alexander, R.R., Dietl, G.P., 2003. The fossil record of shell-breaking predation on marine bivalves and gastropods. In: Kelley, P.H., Kowalewski, M., Hansen, T.A. (Eds.),

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