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Ontogenetic Shifts in the Predatory Habits of the Northern Moonsnail (Lunatiaheros) on the Northwestern Atlantic CoastAuthor(s): Jeff C. Clements and Timothy A. RawlingsSource: Journal of Shellfish Research, 33(3):755-768. 2014.Published By: National Shellfisheries AssociationDOI: http://dx.doi.org/10.2983/035.033.0310URL: http://www.bioone.org/doi/full/10.2983/035.033.0310

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ONTOGENETIC SHIFTS IN THE PREDATORY HABITS OF THE NORTHERN MOONSNAIL

(LUNATIA HEROS) ON THE NORTHWESTERN ATLANTIC COAST

JEFF C. CLEMENTS1,2* AND TIMOTHY A. RAWLINGS1

1Department of Biology, Cape Breton University, P.O. Box 5300, 1250 Grand Lake Road, Sydney, NovaScotia B1P 6L2, Canada; 2Department of Biology, University of New Brunswick, P.O. Box 5050, 100Tucker Park Road, Saint John, New Brunswick E2L 4L5, Canada

ABSTRACT Naticid gastropods provide a highly tractable system for exploring ontogenetic changes in diet because the

telltale boreholes they leave behind in their hard-shell molluscan prey can be linked reliably to naticid size. In this study,

ontogenetic changes in diet and size selectivity across 7 common prey species of Lunatia heros (Say, 1822) were explored using

a forensic approach based on beach-collected shells from the eastern coast of Nova Scotia, Canada. Laboratory experiments

were also undertaken to assess the relationship between predator size and outer borehole diameter (OBD) for 3 of these prey

species. The results confirmed a strong relationship between OBD and shell length for L. heros and demonstrated that this

relationship was consistent across prey species varying in shell thickness and composition. Analyses of drilled, beach-collected

shells revealed that L. heros clearly differentiates among prey with respect to size and species, with ontogenetic changes in prey

selection appearing to reflect shifting predator–prey size relationships. Among prey species, larger predators demonstrated the

capacity to select larger prey species and avoid smaller prey taxa. Similarly, within prey species, larger predators preyed on larger

individuals of a given species, but also exploited a wider selection of prey sizes than smaller moonsnails. The moonsnail L. heros

also exhibited borehole site specificity for both bivalve and gastropod prey, but did not discriminate between left versus right

valves when drilling bivalve taxa. The results of this study are important for understanding the changing role of L. heros across

its life span within soft-sediment communities. This research should now be broadened to encompass the full suite of prey species

targeted by this drilling predator.

KEY WORDS: gastropods, marine, ontogeny, predation, soft sediment, Lunatia heros, moonsnail, Naticidae

INTRODUCTION

Naticid gastropods have been significant predators of ben-thic marine molluscs since the Cretaceous (Sohl 1969), withtheir presence in nearshore habitats evident in telltale boreholes

left behind in the shells of their molluscan prey (e.g., Guerrero&Reyment 1988, Kabat 1990, Kelley & Hansen 2003, Dietl &Kelley 2006, Harper 2006). Along northwest Atlantic coastlines,

naticids consume a wide array of molluscan fauna, includingmany commercially valuable species (e.g., Dietl & Alexander1995, Clements et al. 2013), with corresponding effects on thespatial patterns and abundance of their prey (Wiltse 1980). On

the New Jersey coast, for example, naticid predation can accountfor as much as 21% of Atlantic surfclam [Spisula solidissima(Dillwyn, 1817)] mortality (Weissberger & Grassle 2003), and in

eastern Maine, the northern moonsnail [Lunatia heros (Say,1822) (generic assignment based on Torigoe & Inaba [2011])]alone is estimated to consume more than 70% of juvenile

softshell clams (Mya arenaria Linnaeus 1758) (Beal 2006).Furthermore, naticid predation can be significant enough acrossNew Jersey shorelines to reduce spatial differences in Atlantic

surfclam densities resulting from variable larval settlement(Quijon et al. 2007). Despite their past and current role asimportant predators of molluscs, however, many aspects ofnaticid predation are still poorly understood (Kelley & Hansen

2003, Harper 2006).Althoughmany naticids have broad diets (e.g., Edwards 1974,

Edwards & Huebner 1977, Ansell 1983, Clements et al. 2013),

many are also capable of selective predation with respect to preyspecies, prey size, prey shell thickness, and borehole location.

When size selectivity exists, larger predators tend to feed on largerprey items within a given prey species (‘‘intraspecific size

selectivity’’; e.g., Rodrigues et al. 1987, Kingsley-Smith et al.2003, Chiba & Sato 2012), with the correlation coefficient (R2) ofthe relationship between predator size and prey size representing

the strength of their selectivity (Dietl & Alexander 1997). Suchselective predation may be driven by size limitations in the abilityof smaller moonsnails to subdue and drill larger prey items (Berg

1975, Boggs et al. 1984, Kelley 1991, Dietl & Alexander 1995),possibly related to the size of the predator�s foot relative to itsprey (Russell-Hunter & Russell-Hunter 1968, Chiba & Sato

2012). ‘‘Interspecific prey selectivity’’ has also been observedin naticid species associated with selection of prey species that,for a certain size class of prey and predator, offer a better

energetic reward per unit handling time (e.g., Kitchell et al.1981, Kelley 1991, Dietl & Alexander 1995, Kelley & Hansen

1996).Numerous studies have documented selective predation in

naticid gastropods. Kelley andHansen (1996) reported evidence

of both intra- and interspecific selective naticid predationspanning Paleogene, Neogene, and Recent molluscan assem-blages. Likewise, Dietl and Alexander (1995, 1997) described

intra- and interspecific prey selectivity for two extant naticidspecies, Lunatia heros and Neverita duplicata (Say, 1822), alongthe Atlantic coast of North America. At least one naticid,

Polinices lewisii (Gould, 1847), is also known to prey selectivelyon individuals with a thinner shell of the bivalve Protothacastaminea (Conrad, 1837), although the mechanism by which this

predator discriminates between thick- and thin-shelled prey isunclear (Grey et al. 2005). Borehole site specificity (‘‘stereotypy’’)in both bivalve and gastropod prey is also extremely common

in many naticid species (e.g., Kelley 1991, Dietl & Alexander1997, Kingsley-Smith et al. 2003, Cintra-Buenrostro 2012). Such

*Corresponding author. E-mail: j.clements@unb.ca

DOI: 10.2983/035.033.0310

Journal of Shellfish Research, Vol. 33, No. 3, 755–768, 2014.

755

drill site fidelity may be associated with the predator�s handlingposition of its prey, prey shell morphology, or access to tissues

within the prey once drilled (Berg 1975, Dietl & Alexander1995).

Although there is strong evidence of selective predation bynaticid gastropods, it is less apparent how prey selectivity

translates to changes in diet across the life span of thesepredators. With increased predator size influencing prey sizeselection (intraspecific size selection), and the potential to

subdue and drill more profitable prey species (interspecific preyselection), one might expect to find strong evidence of ontoge-netic changes in prey selection in a given naticid species.

Surprisingly, however, few studies have documented suchchanges in diet with size and/or age. A few naticid species areknown to switch diets during early benthic development,consuming algae and drilling nonmolluscan prey such as

foraminifera and ostracods as early juveniles, and later switch-ing to a diet of bivalves and gastropods (Bernard 1967, Page &Pedersen 1998, Culver & Lipps 2003, Reyment & Elewa 2003),

whereas others are thought to commence predation immedi-ately upon metamorphosis (Berg 1976). Size has also beenassociated with diet changes in some naticid species, with

larger moonsnails feeding on different prey than smallermoonsnails (Kabat 1990). Although cost–benefit analyseshave attempted, with some success, to match predictions of

naticid foraging with empirical data for given size classes ofpredator and prey (e.g., Kitchell et al. 1981, Kelley & Hansen1996, Dietl & Alexander 1995), these analyses have notchronicled ontogenetic changes in prey selection across the

life of a moonsnail. Consequently, for many naticid species,a true understanding of their ecological impacts on benthicmolluscan communities awaits a more complete assessment of

prey selection across their life span.The moonsnail Lunatia heros is a common predator of hard-

shell molluscs in soft-sediment environments ranging from

southern Labrador to North Carolina and from intertidalhabitats to depths of 130 m (Rosenberg 2009). This large naticid(maximum shell length, 115 mm) is of considerable ecologicalinterest across its distribution because of its broad diet (Clements

et al. 2013) and significant impact on bivalve populations,particularly clams of commercial species, including softshell clamsand Atlantic surfclams (e.g., Commito 1982, Weissberger &

Grassle 2003, Beal 2006). In eastern Canada, L. heros has a dietbreadth spanning 20 species of benthic molluscs, for a total of 24reported prey species (16 bivalves and 8 gastropod species) across

its entire geographic distribution (Clements et al. 2013). Paleon-tological and Recent studies of L. heros and a co-occurringnaticid, Neverita duplicata, have demonstrated size selective pre-

dation as well as borehole site stereotypy at locations along theeastern seaboard of the United States (Kelley 1991, Dietl &Alexander 1997). Evidence of size matching of L. heros and theirsoftshell clam prey (Vencile 1997, Beal 2006) has also led to the

recognition that prey may reach size refuges from L. heros,particularly in areas where naticid predators are segregatedspatially according to size (e.g., tidal habitats, shallow versus

deeper waters) (Commito 1982, Kabat 1990, Alexander & Dietl2001, Martinell et al. 2010). Less is known about ontogeneticchanges in prey selection and the corresponding community-

wide effects of this species. Most studies to date haveexamined predation on one or two species of prey at a time,rather than the broader role of this predator in soft-sediment

environments (e.g., Commito 1982, Alexander & Dietl 2001,Weissberger & Grassle 2003, Beal 2006, Quijon et al. 2007).

As such, it is necessary to examine prey selectivity across thelife span of L. heros to understand the breadth of influence ofthis predator across the soft-sediment communities in which itresides.

To explore ontogenetic changes in diet and prey selectivityof Lunatia heros, a forensic approach was employed based onbeach-collected shells of benthic molluscs along the eastern

coast of Cape Breton Island, Nova Scotia. Although boreholesof this predatory naticid have been documented in 20 hard-shell molluscan prey species along this coastline (Clements

et al. 2013), the present study was limited to an examination of7 common prey species of L. heros: 3 gastropods (Ilyanassatrivittata [Say, 1822], Littorina littorea [Linnaeus, 1758], andL. heros) and 4 bivalves (Gemma gemma [Totten, 1834], Mya

arenaria, Spisula solidissima, and Tellina carpenteri Dall,1900). In addition, to link borehole diameters to known sizesof predators, field collections of drilled shells were supple-

mented with laboratory-based assessments of the relationshipbetween borehole size and predator shell length for 3 preyspecies.

MATERIALS AND METHODS

Prey Size Selectivity

This study was conducted along Port Morien beach(46�6#55$ N, 59�53#10$ W), located in Port Morien Bay on

the eastern coast of Cape Breton Island. The moonsnail Lunatiaheros is the only species of naticid present in this bay, where itcan be commonly observed foraging in intertidal and shallow

subtidal waters. Beach-deposited drilled molluscan shells werecollected along wave-sheltered and wave-exposed shorelines ofPort Morien beach by using ‘‘coarse’’ and ‘‘fine’’ sampling

methods for a collection period that spanned from May toDecember 2010 (see Clements et al. [2013] for more details).During coarse sampling, two ormore individuals scanned a 0.5–1 km stretch of wave-sheltered and wave-exposed beach during

low tide for shells with boreholes, collecting drilled shells largerthan 2 cm in shell length. During fine sampling, smaller andmore delicate shells potentially overlooked during coarse

sampling were collected by sieving small patches of sediment(0.35m30.35m; 2 mmmesh sieve) from areas rich in shell hash.After collection, shells were brought back to the laboratory,

washed, dried, and identified to the species level. For all shells,prey shell length was recorded and used as a proxy for prey size.For bivalve prey, prey shell length was defined as the distance

from the anterior margin to the posterior margin of the shell,whereas in gastropods shell length was defined as the distancefrom the apex to the outermost tip of the apertural lip. For thosetaxa collected by fine sampling, shell length was measured using

a dissecting microscope with a calibrated ocular micrometer tothe nearest 0.01 mm; for all other sampling techniques, shelllength was measured with digital calipers. Outer borehole

diameter (OBD) was also measured and used as a proxy forpredator size (Kitchell et al. 1981). Outer borehole diameter wasdefined as the distance between outer borehole edges across the

center of the borehole, with the shell apex or umbo positioneddorsally. Borehole diameter measurements were taken usinga dissecting microscope as described earlier.

CLEMENTS AND RAWLINGS756

Outer Borehole Diameter Calibration

A strong relationship between OBD and predator shell

length is typical of naticid gastropods (e.g., Kitchell et al.1981, Beal 2006, Chiba & Sato 2012). To assess this relationshipfor Lunatia heros, a laboratory-based study was undertaken todetermine the size of boreholes drilled by predatory moonsnails

of known shell lengths. This relationship was examined acrosstwo bivalve species (Mya arenaria andMytilus edulis Linnaeus,1758) and one gastropod species (Littorina littorea) to test the

widely held assumption that borehole diameter is consistentacross different prey species, even those differing in shellthickness and composition.

Our laboratory setup consisted of 6 10-gal aquarium tanksfilled with seawater and lined with approximately 25 cm (depth)of sieved sediment (0.5 mm mesh size, <0.5 mm fraction)

collected from Dominion Beach, Nova Scotia (46�13#17$ N,60�02#24$ W). Twomoonsnails of distinctly different sizes wereplaced in each tank with the 3 different prey taxa (Mya arenaria,Mytilus edulis, and Littorina littorea). The small gastropod

L. littorea (maximum shell length, 43mm [Rosenberg 2009]) hasa much thicker shell thanM. edulis, which is a moderately thin-shelled epifaunal bivalve with a bimineralic shell comprised of

approximately equivalent amounts of calcite and aragonite(e.g., Freer et al. 2013). In contrast, the thin-shelled infaunalbivalve M. arenaria is comprised almost entirely of aragonite

(Kennedy et al. 1969). Temperature and salinity were measuredand recorded every 2–3 days using a YSI 85 Oxygen Conduc-tivity Salinity & Temperature gauge, and remained relatively

constant at 20�C and 24–27&, respectively. Bivalve prey werefed 15 drops of Instant Algae Marine Microalgae ConcentratesShellfish Diet 1800 (Reed Mariculture Inc.) every 2–3 days.

Tanks were checked for prey consumption weekly, with OBD

and prey shell length measured for each prey item. Moonsnailswere removed from the experiment and measured when represen-tatives of at least 2 of the 3 prey species had been eaten.MeanOBD

measurements for each predator–prey combination were plottedagainst predator shell length. These relationships were then used toestimate predator size (shell length) from OBD measurements.

Ontogenetic Shifts in Dietary Composition

The ontogenetic changes in the diet of Lunatia heros wereexplored in two ways. First, to examine ontogenetic changes inprey selection within a prey species, the frequency of boreholes of

different size classes of predators was categorized (as representedby different OBD classes) across different size classes within eachprey species. Drilled shells, measured for shell length and OBD,

were divided into borehole size classes (0.5 mm size increments),and the size frequency of shells in each borehole size class wasrecorded for a given prey species. Second, to explore ontogeneticchanges in prey selection across prey species, the changing

distribution of prey taxa across different predator size classeswas examined by assessing size–frequency distributions of preywithin particular OBD classes.

Borehole Site Specificity

Borehole location was also recorded in prey shells to examine

borehole site stereotypy. To categorize borehole location, shellsof all 4 bivalve species (Gemma gemma, Mya arenaria, Spisulasolidissima, and Tellina carpenteri) were partitioned into 4

approximately equal-size partitions—a modification of previousapproaches (Kelley 1988, Kowalewski 1990, Anderson 1992,

Kingsley-Smith et al. 2003, Amano 2006) (Fig. 1A). Likewise,shells of 3 gastropod species (Ilyanassa trivittata, Littorinalittorea, and Lunatia heros) were divided into 8 partitions, eachcomprising 45-deg of a 360-deg apical view of the shell, according

to the methodology of Kelley (1991) (Fig. 1B). For each drilledshell, borehole location was scored according to its locationwithin assigned partitions, and the percent occurrence of bore-

holes in each shell region was totaled for all drilled specimens foreach prey species examined. The percent occurrence of boreholesin a particular valve was also determined for 3 of the 4 bivalve

species examined (M. arenaria, S. solidissima, and T. carpenteri).Right and left valves were denoted by observing the position ofthe pallial sinus with respect to the umbo (when the umbo isdorsal, a right-positioned pallial sinus indicates a right valve).

Statistical Analyses

All statistical analyses were run using R version 2.14.1, with

a significance threshold of a ¼ 0.05. Assumptions of normalityand homoscedasticity were tested using Q-Q plots andCochran�s tests, respectively. Unless otherwise noted, data did

not violate the assumptions of their respective statistical tests.Linear regression was used to assess the relationship betweenprey size and predator size (OBD) for each given species. Chi-

square goodness-of-fit tests were conducted to test for signifi-cant differences in borehole frequency across prey shell regionsand among the valves of each bivalve species, comparing theobserved borehole frequencies in each region/valve with the

expected frequency if no preferences were evident. Analysis ofcovariance was used to test the null hypothesis that boreholesize did not differ across prey species (n¼ 3) with different shell

thicknesses and compositions; some nonlinearity existed, and sodata were log-transformed prior to analyses.

RESULTS

Relationship of OBD to Predator Shell Length

Based on the strength of correlation coefficients (R2), the

relationship between OBD and predator shell length was bestapproximated in the form of a curvilinear rather than linearfunction (Fig. 2). For all 3 prey types, borehole diameter

increased with increasing predator shell length; however, nosignificant differences were evident in the slopes (F2,39 ¼ 0.006,P ¼ 0.994) or elevations of these relationships (Table 1, Fig. 2).

Consequently, borehole diameter was assumed to be consistentacross prey taxa of different shell thicknesses and compositions.As such, data were pooled across prey species to derive a pre-

Figure 1. (A, B) Division of prey shell regions for bivalves (A) and

gastropods (B) used to categorize borehole sites.

ONTOGENETIC CHANGES IN LUNATIA HEROS PREDATION 757

dictive model for estimating predator shell length from OBD

measurements. This was calculated using a power functionmodel from the untransformed data:

x ¼ y

0:3486

� �1:4263

where x is the predicted predator shell length and y is theobserved OBD. Although this model was derived from moons-

nails ranging in shell length from 15–40 mm (Fig. 2), it wasassumed that it was also applicable to moonsnails smaller(<15 mm) and larger (>40 mm) than the sampled data set.

Prey Size Selectivity

Across all beach-collected shells of gastropod and bivalve

prey species examined, predator boreholes ranged from 0.50–6.89 mm in diameter, corresponding to predicted predator shelllengths of 1.67–70.53mm. This range encompassed shell lengthsof Lunatia heros collected from Port Morien beach over several

years of sampling (Clements & Rawlings, pers. obs.). Linearregression between predator size (OBD) and prey size (shelllength) revealed significant positive slopes for all 7 common

prey species (Fig. 3), demonstrating prey size selectivity by these

predators; larger predators selected larger prey items withineach prey species. The strength of correlation coefficients (R2)

and steepness of slopes varied markedly across prey species.High R2 values are indicative of few predator–prey mismatchesin size, and thus strong size selectivity (Dietl &Alexander 1997).HighR2 values were evident forLittorina littorea,Mya arenaria,

and Spisula solidissima (0.57, 0.81, and 0.72, respectively), lowerR2 values were associated with Ilyanassa trivittata, L. heros, andTellina carpenteri (0.22, 0.28, and 0.25, respectively), and a very

low R2 value (0.13) was evident in the relationship betweenpredator shell length and prey shell length for Gemma gemma.Size–frequency histograms also reinforced this trend, illustrat-

ing the strong difference in prey size classes across predator sizeclasses for L. heros, L. littorea, M. arenaria, and S. solidissima(Fig. 4). Differences in slopes of predator size versus prey sizewere indicative of differences in the rate of increase of predator

size with prey size (Fig. 3). Slopes $1.0 were evident for allpredator–prey combinations except for M. arenaria, indicatinga faster scaling of predator size relative to prey size for the

majority of predator–prey combinations.In terms of size differences between predators and prey (Fig. 3),

in the majority of predator–prey encounters, predators were

larger in shell length than their corresponding prey shell length(majority of symbols above the dashed line in Fig. 3). The onlymajor exception to this was forMya arenaria; moonsnails were

slightly smaller in shell length than their prey (majority ofsymbols below the dashed line). The size advantage necessaryfor predation was most evident in instances of cannibalism—moonsnails feeding on other moonsnails. Based on regression

analysis, moonsnail predators were approximately 20 mmlarger than their moonsnail prey (Fig. 3), and in only 2 of 80cases were predators of equal size or smaller. The size differential

between predator and prey was often less than 20 mm. Tounderstand more fully how large moonsnail predators had to beto consume conspecific prey, prey shell lengthwas plotted against

the difference between predator shell length and prey shell length,where a gap in the distribution represents the minimum sizedifferential between predators and prey. A gap was evident from0–3 mm in shell length, indicating that, when consuming

conspecific prey, moonsnail predators are typically $3 mmlarger than their prey (Fig. 5). The importance of predator sizewas also revealed when examining the largest prey item con-

sumed across distinct size classes of moonsnails (Fig. 6). Across 4of the 7 prey species (M. arenaria, Spisula solidissima, Littorinalittorea, and Lunatia heros), larger moonsnails were clearly able

to exploit larger prey items than smaller moonsnails.

Ontogenetic Shifts in Dietary Composition

Borehole analyses revealed a change in moonsnail dietacross ontogeny (Fig. 7). Four of the 7 prey species—Gemmagemma, Tellina carpenteri,Mya arenaria, and Spisula solidissima—

were associated with boreholes in the smallest size range (0.5–0.99 mm). Of these, the prey speciesG. gemma and T. carpenteriwere associated exclusively with small boreholes, and thus

smaller size classes of predators compared with S. solidissimaand Lunatia heros, which dominated as prey of the largest sizeclasses of predators. The prey speciesM. arenaria, L. littorea, and

L. heros were prey items across 9 or more predator size classes,with S. solidissima associated with the greatest size range,spanning 13 predator size classes. The only two prey species

Figure 2. The relationship between outer borehole diameter and predator

shell length across 3 prey species (Littorina littorea, n$ 18;Mya arenaria,

n $ 16; Mytilus edulis, n $ 11) from laboratory feeding experiments

conducted at Cape Breton University from June to December 2010. Axes

are scaled logarithmically.

TABLE 1.

Analysis of covariance results for laboratory feeding experi-ment assessing OBD–predator size relationships and borehole

consistency across different prey taxa.

df SS MS F P value

Predator size 1 0.168 0.168 69.56 <0.001*

Prey species 2 0.004 0.002 0.82 0.446

Error 41 0.099 0.002

Outer borehole diameter was the dependent variable, with predator

size (shell length) and prey species (Littorina littorea, n ¼ 18; Mya

arenaria, n ¼ 16; andMytilus edulis, n ¼ 11) as independent variables.

* P < 0.001.

CLEMENTS AND RAWLINGS758

associatedwith the largest borehole size classes wereS. solidissima

and L. heros. There was a clear association between maximumshell length of prey (as reported by Rosenberg [2009], with theexception ofT. carpenteri, which was derived fromAbbott [1974])

and the size ranges of naticids that preyed on them. The preyspeciesG. gemma andT. carpenteri, withmaximum shell lengthsof 3.8 mm and 8.5 mm, respectively, were associated with

the smallest predators. Conversely, larger, thick-shelled taxa

such as L. littorea and L. heros (maximum shell lengths of43 mm and 115 mm, respectively) were prey of largernaticids. The surfclam, S. solidissima, which reached the

largest shell length of any of the 7 prey species examined(maximum shell length, 200 mm) also spanned the greatest sizerange of predators.

Figure 3. The relationship between predicted predator shell length and shell length of drilled prey collected from Port Morien beach betweenMay 2010

and December 2010 for Gemma gemma (n$ 50), Ilyanassa trivittata (n$ 48), Lunatia heros (n$ 80), Littorina littorea (n$ 192),Mya arenaria (n$

93), Spisula solidissima (n$ 78), and Tellina carpenteri (n$ 50). The dashed line displays the relationship if predators consumed equal-size prey (as

measured by shell length, in millimeters). Predator shell lengths were derived from the predictive model for estimating predator size from outer borehole

diameter (OBD) measurements.

ONTOGENETIC CHANGES IN LUNATIA HEROS PREDATION 759

Borehole Site Specificity

Predators were selective with respect to where they drilled theirprey for all gastropod and bivalve prey examined (Table 2).Boreholes were found most often in region 1 of bivalves, with

68%, 100%, and 74% of boreholes found near the umbo for Myaarenaria, Spisula solidissima, and Tellina carpenteri, respectively;however, no umbonal preference was evident for Gemma gemma.Although chi-square goodness-of-fit analyses revealed significantly

different frequencies from the expected frequencies for all bivalveprey, region 4 was never drilled in any bivalve. Because this regioncouldbe single-handedlydriving theobserved significant differences,

analyses were run excluding region 4, revealing selectivity for region1 when feeding on M. arenaria, S. solidissima, and T. carpenteri;however, there was no preference for regions 1–3 in G. gemma

(Table 3). Valve selectivity in bivalve prey was not evident (Table 4).For gastropod prey, boreholes were found most often near

the aperture of Ilyanassa trivittata (64% in region 8) and

Littorina littorea (82% in region 1). However, boreholes in

cannibalized prey were most often located farther away fromthe aperture, with themajority (90%) of boreholes concentratedin regions 2 and 3 (55% and 35%, respectively).

DISCUSSION

The Foraging Ecology of Naticids: A Forensic Approach

Forensic-based studies of naticid foraging, including thecurrent study, often rely on the presence of a robust relationshipbetween moonsnail size and borehole diameter, such that

predator size can be reliably inferred from drilled shell remains(e.g., Kitchell et al. 1981, Dietl & Alexander 2000, Beal 2006,Chiba & Sato 2012). The laboratory results of the current study

confirmed this relationship for Lunatia heros, demonstratingthat larger moonsnails produced significantly larger boreholesthan smaller moonsnails. This relationship has been described

Figure 4. The frequency of drilled prey in given prey size classes (shell length in millimeters) across different predator size classes (outer borehole

diameter in millimeters) forLittorina littorea (n$ 192): 0–1.49mm (A), 1.5–2.99mm (B), 3–4.49mm (C), and 4.5–5.99mm (D);Lunatia heros (n$ 80):

1.5–2.99 mm (A), 3–4.49 mm (B), 4.5–5.99 mm (C), and 6–7.49 mm (D);Mya arenaria (n$ 93): 0–1.49 mm (A), 1.5–2.99 mm (B), 3–4.49 mm (C), and

4.5–5.99 mm (D); and Spisula solidissima (n$ 78): 0–1.49 mm (A); 1.5–2.99 mm (B); 3–4.49 mm (C); 4.5–5.99 mm (D); and 6–7.49 mm (E).

CLEMENTS AND RAWLINGS760

previously for L. heros by Vencile (1997), Weissberger andGrassle (2003), and Beal (2006), although these studies usedinner borehole diameter instead of OBD. The present analyses

also demonstrated that the relationship between moonsnail shelllength and OBD did not vary significantly across prey speciesdiffering in shell thickness and composition. Such consistency

across species is critical because it allows one to use drilled shellsto assess the prey selection of moonsnails within a prey species,across prey species, and across the entire ontogeny of L. heros.

Several assumptions must be made when inferring the diet of

moonsnails from analyses of beach-collected drilled shells.Chief among these is the assumption that moonsnails typicallyfeed by drilling hard-shell prey (see Visaggi et al. [2013] for

exceptions). This seems acceptable given that alternativemethods of predation by naticids, such as smothering, are likely

very rare (Visaggi et al. 2013). A second important assumptionis that beached shell collections provide an unbiased assessment

of the true diet of moonsnails. Although shell morphology and

the different hydrodynamics and entrainment of bored and

unbored valves can potentially affect the spatial distribution of

empty bivalve shells (Chattopadhyay et al. 2013), the forensic

approach undertaken here based on drilled shell remains alone

is likely to be reasonably independent of such taphonomic biases.

Right and left valves can also display opposite displacement

trajectories during hydrodynamic displacement (Chattopadhyay

et al. 2013), which could potentially drive any observed trends in

valve selectivity. Given the length of shoreline sampled and the

similar number of drilled right and left valves collected in this

study, valve trajectory does not appear to be a significant source

of taphonomic bias here. Wave energies could also lead to

differential size sorting of drilled shells between wave-exposed

and wave-sheltered beaches; however, given that the collections

spanned both environments and the data were pooled for the

size–frequency analyses, the results should be robust to such

confounds.

Taphonomic biases are more likely to occur in studies

assessing predation intensity across prey size classes, prey

species, or prey shell thicknesses, because drilled shells may be

removed from an assemblage disproportionally to undrilled

shells, giving inaccurate estimates of predation intensity (e.g.,

Roy et al. 1994, Klompmaker 2009). Likewise, shells of

different thicknesses may be differentially broken and/or re-

moved from an assemblage (Grey et al. 2006). Indeed, differ-

ential fragmentation of shells facilitated by boreholes may have

influenced these selectivity results. For example, when compar-

ing shells of a similar size, shells with larger boreholes may be

more susceptible to fragmentation than those with smaller

boreholes (Martinell et al. 2012). As such, small shells with

large boreholes may be common, but they break long before

washing ashore, hence producing the illusion of size selectivity

when one does not exist. Differential shell fragmentation is

unlikely to have strongly influenced the results of the current

study, however, given that this would be expected to be an issue

Figure 5. The relationship between prey shell length and the difference

between predator shell length and prey shell length for cannibalistic

predation events (n$ 80) based on collections from Port Morien beach.

The dashed line represents the arbitrary boundary of the gap in the

distribution, representing the minimum size differential between predators

and prey. Predator shell length was estimated from the predictive model

for estimating predator size from outer borehole diameter measurements.

Figure 6. The maximum prey size exploited by different size classes of moonsnails (represented by outer borehole diameters in millimeters) across 7 prey

species at Port Morien beach.

ONTOGENETIC CHANGES IN LUNATIA HEROS PREDATION 761

only for very small, fragile bivalve shells, such as those of smallMya arenaria, Spisula solidissima, or Tellina carpenteri.

Size Selective Predation in Naticids

A general feature of naticid predation is that larger snails

tend to feed on larger prey items, albeit not exclusively (e.g.,Edwards 1974, Alexander & Dietl 2001, Weissberger & Grassle2003, Morton 2008). This was also reflected in the current study

in which moonsnail shell length was related positively to preyshell length in all 7 prey species examined. Each relationshipwas species-specific, however, and varied in size-selective

strength (R2) across prey species. Similar results have beenreported elsewhere, in which selective strength varies acrossdifferent species of prey (Alexander &Dietl 2001), and different

combinations of predators and prey. In addition, selectivestrength can vary spatially and temporally for the same

predators and prey species (Kitchell et al. 1981, Alexander &Dietl 2001).

Comparisons of prey selectivity acrossmoonsnail size classes

documented a shift from small prey to larger prey with in-creasing predator size. This trend was apparent only for preytaxa with a large size range (Mya arenaria, Spisula solidissima,

Littorina littorea, and Lunatia heros), with larger predators alsoable to exploit a wider range of prey sizes. Weissberger andGrassle (2003) reported similar findings, suggesting that larger

naticids (L. heros and Neverita duplicata) can consume a widersize range of S. solidissima than smaller naticids. Althoughsmall prey items are occasionally preyed on by large predators,

Figure 7. Ontogenetic change in diet based on an examination of 7 common prey species ofLunatia heros collected fromPortMorien beach. Frequencies

were calculated independently for each prey species and were determined by summing the number of prey shells within each predator size class (as

represented by outer borehole diameter [OBD]) and dividing by the total number of specimens collected of that prey taxon. Prey are ordered from

smallest to largest according to maximum shell lengths (Abbott 1974, Rosenberg 2009) within their respective taxonomic class (4 bivalves and

3 gastropods, respectively): Gemma gemma (n$ 50), Tellina carpenteri (n$ 50), Mya arenaria (n$ 93), Spisula solidissima (n$ 78), Ilyanassa

trivittata (n$ 48), Littorina littorea (n$ 192), and Lunatia heros (n$ 80).

TABLE 2.

Results of chi-square goodness-of-fit analyses of Lunatia heros borehole site specificity for bivalve and gastropod prey.

n

Borehole position

df Chi-square P value1 2 3 4 5 6 7 8

Bivalves

Gemma gemma 50 14 16 20 0 — — — — 3 18.16 <0.001*

Mya arenaria 108 73 13 22 0 — — — — 3 113.56 <0.001*

Spisula solidissima 80 80 0 0 0 — — — — 3 240.00 <0.001*

Tellina carpenteri 95 70 10 15 0 — — — — 3 125.00 <0.001*

Gastropods

Ilyanassa trivittata 48 17 1 0 0 0 0 3 31 7 142.00 <0.001*

Littorina littorea 190 155 13 0 1 3 0 1 17 7 841.33 <0.001*

Lunatia heros 83 2 46 29 6 0 0 0 0 7 205.87 <0.001*

Observed frequencies were tested against expected frequencies chosen on the basis of equal frequencies of boreholes in each shell region (bivalves:

1–4, 25%; gastropods: 1–8, 12.5%). * P < 0.001.

CLEMENTS AND RAWLINGS762

high R2 values and the low frequency of large boreholes insmaller prey shells suggest that L. heros does select for

particular-size prey within a given prey species. Although it ispossible that larger moonsnails simply suffocate small prey andconsume them without drilling, these alternative modes of

predation appear rare (Visaggi et al. 2013) and are unlikely tomask selective predation in this instance. Zlotnik (2001)reported similar findings for an extinct naticid predator–preyassemblage from the Miocene, in which large predators selec-

tively drilled more energetically favorable (larger) prey than smallpredators. Furthermore, in the current study, size selectivity wasless apparent in smaller prey taxa with a narrower size range

(e.g., Tellina carpenteri, Ilyanassa trivittata, and Gemmagemma), because even small predators are able to exploit theentire size range of these prey species.

Size and Energy Maximization

The association between larger moonsnails and larger prey

items suggests there is an advantage for snails to consume largerprey items. Selecting prey with a greater tissue reward relative topredation effort is known to be advantageous for naticidgastropods (Kitchell et al. 1981, Anderson et al. 1991, Kelley

1991). The energy maximization premise (MacArthur & Pianka1966, Pyke et al. 1977) is one potential explanation for such size-selective predation. Cost–benefit analyses have shown that as

prey size increases, internal shell volume increases dispropor-tionately faster than shell thickness (Kitchell et al. 1981). Giventhat drilling rates are slow and dependent on shell thickness

(Kitchell et al. 1981, Boggs et al. 1984, Kabat 1990), larger preypresent a greater energetic reward per unit drilling time comparedwith smaller prey of the same species. Likewise, thinner shell prey

should be more energetically favorable than thicker shell prey ofthe same prey size/volume. As such, it would be beneficial forpredators to feed on larger prey items rather than smaller ones,and thinner shell prey relative to thicker shell prey of the same

tissue mass. Previous studies have reported that naticids tend tomake foraging decisions in concert with predictions of energymaximizationmodels (e.g., Kitchell et al. 1981, Boggs et al. 1984,

Kelley 1991, Zlotnik 2001). Grey et al. (2007) also demonstratedthat, among equal-size prey, Polinices lewisii preferred thin-shelled over thick-shelled Protothaca staminea in a laboratory

setting. Other aspects of naticid foraging and predation still needto be considered in more explicit detail in the context of energymaximization models, however, such as the energy expended in

prey capture, handling, andmanipulation of larger versus smallerprey (Kabat 1990). Likewise, size for size, different prey speciesmay mount different types of defensive responses to predation,resulting in different energetic costs for the predator. The

question still remains, however, as to why large predatorsoccasionally consume small prey items. This may reflect periodswhen large moonsnails are unable to adequately locate the most

energetically favorable prey taxa and consume suboptimal preyopportunistically (Kitchell et al. 1981, Dietl & Alexander 1997).

Size Constraints and Size Refuges

Although there appears to be an energetic advantage tofeeding on large prey items, smaller predators rarely do so. In

the current study, this was supported by the strength of therelationships between predator size and prey size (Fig. 3) as well asthe increase in maximum prey size exploited with increasing

moonsnail size for 4 prey species (Figs. 4 and 6). These observa-tions may be explained by nonoverlapping habitats of smallpredators and large prey. For instance, smaller predators may be

unable to burrow deeply enough to encounter large prey bur-rowed within the sediment (Weissberger 1999). Although possiblytrue for large, deeply burrowedMya arenaria, this seems unlikely

for most prey items of Lunatia heros, particularly epifaunalgastropod prey. More likely, larger prey items are too big forsmall predators to handle and subdue (Dietl & Alexander 1995,Chiba & Sato 2012). Chiba and Sato (2012) have suggested that

selective predation in Euspira fortunei (Reeve, 1855) may bedriven by size limits of exploitable prey that accompany the sizeof the predator�s foot. Given that naticids typically envelop their

prey entirely within their foot before drilling, small moonsnailsmay encounter physical constraints in handling, subduing, anddrilling large prey items.

Because the metrics used to define ‘‘size’’ in predators andprey may not be meaningful biologically, it can be difficult todefine a size of a given prey item that represents a critical limit fora given size of predator. Prey size is usually viewed in the context

of predator size, both of which are typically represented by shelllength. Based on this comparison, naticids are clearly able toconsume bivalves with similar or larger shell lengths than their

own, although the maximum size differential between predatorand prey can differ markedly among prey species (Kitchell et al.1981, Dietl & Alexander 1997). Kitchell et al. (1981) noted that

for Neverita duplicata, the maximum size of bivalve preyexploited relative to predator size (e.g., the maximum prey-to-predator size ratio) decreasedwith increasing predator size across

TABLE 4.

Results of chi-square analysis of Lunatia heros valve selec-tivity for bivalve prey.

n

Valve

df Chi-square P valueL R

Mya arenaria 108 54 54 1 0.00 1.000

Spisula solidissima 80 34 46 1 1.80 0.180

Tellina carpenteri 95 43 52 1 0.85 0.359

Observed frequencies were tested against theoretical expected frequen-

cies chosen on the basis of equal frequencies of boreholes in each valve

(left [L]/right [R], 50%).

TABLE 3.

Results of chi-square analysis of Lunatia heros borehole sitespecificity for bivalve prey excluding region 4.

n

Borehole

position

df Chi-square P value1 2 3

Gemma gemma 50 14 16 20 2 1.12 0.571

Mya arenaria 108 73 13 22 2 58.17 <0.001*

Spisula solidissima 80 80 0 0 2 16.00 <0.001*

Tellina carpenteri 95 70 10 15 2 70.00 <0.001*

Observed frequencies were tested against expected frequencies chosen

on the basis of equal frequencies of boreholes in each shell region (1–3,

33.3%). * P < 0.001.

ONTOGENETIC CHANGES IN LUNATIA HEROS PREDATION 763

4 bivalve species, suggesting that it becomes more difficult formoonsnails to exploit bivalve prey considerably larger than

themselves as predator and prey size increase. Interestingly, incontrast, when moonsnails prey on conspecific snails, a predatorsize advantage appears absolutely necessary across all size rangesof predators (Kitchell et al. 1981). Consequently, there appears to

be much more to consider in terms of prey vulnerability topredators than the metric of shell length alone.

ThemoonsnailLunatia heros is known to be able to consume

bivalve prey with a prey–predator size ratio (based on shelllengths) greater than 1.0 (Vencile 1997, Weissberger & Grassle2003, Beal 2006, the current study) (Fig. 3; symbols below the

dashed line. However, most prey taxa selected by L. heros in thecurrent studywere smaller in shell length than their correspondingpredators based on inferences fromOBDs (Fig. 3; symbols abovethe dashed line). This was particularly true for conspecific prey

items, but also for the vast majority of other gastropod prey(Ilyanassa trivittata and Littorina littorea) as well as gem clams(Gemma gemma). Of the 7 prey species examined, Mya arenaria

was the only species consumed most frequently by moonsnailssmaller than their respective prey item. Vencile (1997) and Beal(2006) provided evidence of 1:1 size matching between L. heros

and M. arenaria, suggesting that moonsnails typically selectsoftshell clam prey of comparable size with their own bodies.Although this was apparent at small predator–prey sizes in the

current study, moonsnails tended to drill M. arenaria larger thanthemselves with an increase in predator size. Ultimately, furtherwork is warranted to determine themaximum sizes of prey thatL.heros can exploit for different prey species, and to assess the

mechanism by which this predator is able to evaluate prey items,to determine whether or not to commence drilling, and to subdueand consume its prey successfully.

The importance of predator size relative to its prey isdemonstrated most convincingly in instances of cannibalismby Lunatia heros. Cannibalism is a common phenomenon in

L. heros and is recognized to be a predictable outcome ofselective predation based on the energy maximization premise(Kelley 1991). In 80 instances of L. heros feeding on conspecificsin the current study, the predator was larger than the prey item

in all but 2 cases, with predators in general having a 20 mm sizeadvantage over their conspecific prey (Fig. 3), although in somecases as little as a 3 mm difference in shell length was sufficient

(Fig. 5). Kitchell et al. (1981) reported that when two equal-sizeindividuals of the shark eye, Neverita duplicata, were confinedtogether, they battled each other repeatedly for dominance, but

without success. In contrast, when there was a marked sizedisparity between the snails, the smaller moonsnail was subduedimmediately by the larger predator. Further direct observations

of encounters between moonsnails may help to determine moreprecisely the minimum size difference between predator andprey in cannibalistic encounters, and how this varies acrossdifferent size classes of predators.

Some prey species are also able to reach sizes at which theyare no longer vulnerable to naticid predation. For instance, thebivalve Anadara ovalis (Bruguiere, 1789) appears to reach

a refuge from naticid predation along the northwestern Atlanticcoastline at shell lengths larger than 37 mm (Alexander & Dietl2001), whereas the size refuge is considerably larger for Spisula

solidissima at shell lengths larger than 120 mm (Dietl &Alexander 1997). Such refuges are often restricted to specifichabitats, geographic locations, and time periods. For instance,

Commito (1982) noted that Mya arenaria in Lubec, Maine,reached a size refuge from Lunatia heros at shell lengths greater

than 30 mm, as predators larger than 20 mm in shell diameterwere rarely found at this location. Subsequent work hasdemonstrated that such prey size refuges do not exist in otherhabitats or when larger size cohorts of predators are present

(Vencile 1997, Beal 2006). Although the current study was notdesigned to examine prey size refuges from L. heros, the sizedisparity between predator and prey suggests that size is not an

adequate refuge from predation for most of the prey examinedin this study. Given that L. heros can reach shell lengths of morethan 100 mm (Rosenberg 2009) and can feed on softshell clams

as large or larger than their own shell lengths (Fig. 3), large preymay still be vulnerable to predation at their largest sizes.Conversely, because Spisula solidissima can reach maximumsizes larger than L. heros (200 mm vs. 115 mm [Rosenberg

2009]), and tend to be drilled by moonsnails with greater shelllengths (at least for large prey sizes), it is likely that surfclamscan and do reach size refuges fromL. heros predation. Likewise,

based on these results, large moonsnails will only reach a sizerefuge from predation by conspecifics if, and only if, there areno moonsnails present that are larger than them. Further

studies examining both drilled and undrilled shells acrossdifferent size classes of prey species are now required to confirmwhether size refuges really do exist in these and other prey

species of L. heros.

Borehole Site Stereotypy

Site fidelity of boreholes is suggestive that drilling position isan important component of naticid predation. Borehole sitestereotypy has been noted in a variety of naticid species,

including Lunatia heros (e.g., Kelley 1991, Dietl & Alexander1997, Kingsley-Smith et al. 2003, Cintra-Buenrostro 2012), andwas documented in all 7 prey species examined in the current

study. In cases of cannibalism, L. heros exhibited a strongtendency to drill conspecifics in shell regions 2 and 3 (Table 4),supporting the results of Dietl andAlexander (1995), who notedthat themajority of naticid boreholes (attributed toL. heros and

Neverita duplicata) were located in regions 2 and 3 of L. herosand N. duplicata prey. In other gastropod prey, the results weredifferent, with Littorina littorea and Ilyanassa trivittata drilled

preferentially in regions 1 and 8, respectively, closer to the prey�saperture. These results may be a consequence of differences inhandling position required to subdue and drill different sized

gastropod prey successfully (Kabat 1990) or an artifact of preyshell morphology (Berg 1975, Dietl & Alexander 1995). Forpredation on bivalves, Dietl and Alexander (1997) determined

that L. heros preferred to drill over the umbo when feeding onSpisula solidissima—a result supported by the observations for3 of the 4 bivalve prey species, except Gemma gemma in thecurrent study. Differences in site selectivity have been noted for

other bivalve species. For instance, boreholes produced byPolinices pulchellus (Donovan, 1804) preying on Cerastodermaedule (Linnaeus, 1758) deviated slightly from the umbo as prey

size increased (Kingsley-Smith et al. 2003), and were found in thecenter of the shell (between regions 1 and 3 using our method)64%–73% of the time. Prey shape, shell thickness, relative sizes

of predators and prey, and the ways in which prey are handledbefore drilling could all play a role in borehole site specificity(Kitchell et al. 1981, Kabat 1990).

CLEMENTS AND RAWLINGS764

When preying on bivalves, naticids often prefer to drillthrough the umbo, which is surprising given that this is typically

the thickest region of the shell. However, given that the umbo isthe first part of a bivalve shell to be laid (i.e., outer adult umbo islaid during larval and juvenile stages), and highly solubleamorphous calcium carbonate is the predominant carbonate

mineral form deposited in larval and young juveniles (Weisset al. 2002), the umbo may be more susceptible to naticidpredation than other parts of the shell because naticids typically

secrete an acidic enzymewhen drilling. In fact, the umbo is oftenthe first part of the shell to dissolve in juvenile (e.g., Green et al.2009, Talmage & Gobler 2010) and adult (Haag 2012) bivalves

under acidic conditions. Furthermore, the umbo is the oldestpart of a bivalve shell and may have experienced a greaterdegree of erosion relative to younger parts of the shell (Haag2012). Alternatively, umbonal drilling may be reflective of

handling position of the prey during drilling, because drillingat the umbo enables the naticid�s foot to encompass the entireprey and restrict the prey from opening its valves, minimizing

handling time and the potential for prey escape (Kabat 1990).Future studies should make an attempt to isolate the mecha-nisms by which borehole site selectivity operates among naticid

gastropods.Although strong borehole site specificity at the umbo was

evident forMya arenaria, Tellina carpenteri, andSpisula solidissima,

boreholes in the small bivalve Gemma gemma were distributedbetween regions 1, 2, and 3. Given that G. gemma reachesa maximum shell length of 3.2 mm only, the mineral composi-tion of the shell may not differ substantially between the umbo

and the rest of the shell, or, alternatively, the handling positionrequired to minimize prey escape may allow for flexibility indrill site selection. Interestingly, Kitchell et al. (1981) reported

more ‘‘nonnormal’’ borehole sites in extremely large and smallprey sizes relative to a predator�s preferred size range, andattributed such nonnormality to altered manipulation of ex-

treme-size prey. However, this would not be expected to influenceborehole site specificity in small prey such as G. gemma, giventhat these bivalves were drilled by the smallest size classes ofLunatia heros (Fig. 7). The results for G. gemma are also in

contrast to those of other small bivalve species in this study (i.e.,T. carpenteri) in which L. heros did exhibit strong borehole siteselection for the umbo. In addition, borehole site selectivity has

been reported to increase with increasing predator size in extinctnaticid predator–prey systems (Miocene [Zlotnik 2001]), suggest-ing perhaps there is a learning component to drill site selection.

Further studies examining prey encounter and drilling behavior,along with ontogenetic analyses of borehole site specificity, areneeded to understand more completely this particular behavior

in L. heros. Although such analyses were attempted for preyspecies in this study, sample sizes within individual size classeswere too small to draw any firm conclusions.

Although borehole site stereotypy is a common feature of

naticid predation, valve selection among bivalve prey is muchmore variable among taxa. Although Lunatia heros did notdemonstrate valve selection in the current study, previous studies

have described naticid species that demonstrate left-valve spec-ificity (Rodrigues et al. 1987,Hasegawa& Sato 2009), right-valvespecificity (Anderson 1992, Chattopadhyay&Dutta 2013), or no

specificity at all (e.g., Taylor 1970, Kingsley-Smith et al. 2003,Casey & Chattopadhyay 2008). When valve specificity exists, ithas been attributed to the ways in which naticids capture and

manipulate their prey, potentially to minimize interference andescape during predation (Hasegawa & Sato 2009).

Ontogenetic Changes in Diet: Intraspecific Size Selectivity and

Interspecific Prey Selectivity

Ontogenetic changes in prey preferences and predatorybehavior are common in animal taxa and have been documentedacross a wide variety of taxonomic groups, including assassin

bugs (Cisneros & Rosenheim 1997), phytoseiid mites (Walzeret al. 2004), copepods (Kawabata 1991), brown trout (Sanchez-Hernandez et al. 2012), aquatic and terrestrial snakes (Lind 1990,

Lind &Welsh 1994, Savitzky & Burghardt 2000), tiger salaman-ders (Leff & Bachmann 1986), cownose rays (Fisher et al. 2011),sunfish (Mola mola [Nakamura & Sato 2014]), and thaididgastropods (Hart & Palmer 1987). The results of this study add

to this body of literature and suggest that the predatory ecologyof Lunatia heros changes across its life span from juveniles toadults associated with an increase in body size. To our knowl-

edge, such shifts in naticid predatory behavior have yet to bedocumented explicitly for this species.

Several naticid species are known to undergo dietary shifts in

early ontogeny (e.g., Bernard 1967, Page & Pedersen 1998, Culver&Lipps 2003,Reyment&Elewa 2003; but see Berg 1976). It is notyet known, however, if Lunatia heros also adopts a herbivorous

diet during its early life stages after metamorphosis beforeswitching to a predatory existence, similar to some species(Bernard 1967), or drills immediately or soon after settlementand metamorphosis like many others (Berg 1976, Kingsley-Smith

et al. 2005). Although the settlement size of many naticids has yetto be documented, Kingsley-Smith et al. (2005) found thatPolinices pulchellus settled to the benthos at a size of approxi-

mately 1 mm (shell length) and began drilling molluscan preywithin 3 days of metamorphosis. Larvae of L. heros hatch fromthe egg collar at sizes of 284 ± 47.5 mm(SD) and spend from8 days

to 6 wk in the plankton, but their size at settlement and meta-morphosis on the benthos has not been determined (Kenchingtonet al. 1998). Given that the smallest borehole found in the currentstudy (0.50 mm; Spisula solidissima) corresponded to a moonsnail

shell length of 1.67mm, it seems doubtful thatL. heros spends anytime as a transient herbivore upon settlement andmetamorphosis.Efforts should nowbemade to confirmor refute this by examining

the size and mode of feeding of newly settled juveniles of L. herosdirectly under laboratory and field conditions.

Understanding how prey preference and diet change across

a predator�s life span, from newly metamorphosed juvenile toadult, is essential to understanding community-wide effects ofpredators in various systems (Wollrab et al. 2013). Muricid

gastropods can shift between preferred prey species depending onprey abundance, and will remain selecting the latter prey specieseven if the former rebounds and becomes abundant again (e.g.,Wood 1968, Murdoch 1969). Hence, predators may become

conditioned to a particular type of prey over time (ingestiveconditioning) and may only shift dietary preferences if that preybecomes scarce. Although not reported for naticids, this type of

selective predatory behavior certainly warrants exploration.Models of predator-mediated coexistence have also histori-

cally neglected the incorporation of ontogenetic changes in diet.

Using theoreticalmodels,Wollrab et al. (2013) showed that smallchanges in diet between juvenile and adult predators can shiftmechanisms of predator-mediated coexistence among predators

ONTOGENETIC CHANGES IN LUNATIA HEROS PREDATION 765

and prey within an ecological community. Although these shiftscan potentially promote coexistence and biodiversity, they can

also introduce alternative states within ecological communities,in which slight disturbances can lead to depauperate communi-ties (Wollrab et al. 2013). Without the knowledge of dietarychanges across the ontogeny of naticid gastropods, assessments of

whole-community impacts of naticid predation have to assumeuniform predatory behavior across all sizes and ages of thesepredators. A failure to incorporate dietary shifts may therefore

underestimate the true impacts of naticid predation in theirrespective ecological communities.

Documenting changes in prey selection and predatory

behavior across the life span of an organism can be a challengingundertaking, which may explain why, for many taxa, suchinformation is lacking. Naticid gastropods are an exception tothe rule, however, given that they leave behind hallmark

boreholes in their hard-shell molluscan prey that can be linkedreliably to predator size. Consequently, through every step oftheir development, except perhaps during a transient herbivo-

rous phase evident in a select few species (Bernard 1967),moonsnails provide a wealth of evidence relating to their dietand feeding ecology. The study of naticids therefore provides

a very tractable system for examining ontogenetic changes indiet and exploring the community-wide ramifications of suchontogenetic shifts. The current study, focusing on 7 major prey

items within the diet of L. heros, has begun to accomplish this.Given that this species can exploit 20 molluscan species locally(Clements et al. 2013), the documented shifts in diet reportedhere now need to be extended to a broader range of prey species.

The reasons for undertaking this are more than just academic; L.

heros is an important predator in nearshore environments (e.g.,Commito 1982, Weissberger & Grassle 2003, Beal 2006, Clem-

ents et al. 2013), particularly for commercially important bivalvespecies. In addition, there is considerable interest in the fisherypotential of this species in Nova Scotia (Kenchington et al. 1998,Fisheries and Oceans Canada 1999), and if this species is to be

exploited commercially, it is critically important to understandthe effects of removing different life history stages for properecosystem management. Furthermore, differences in predator

size and prey assembly exist between intertidal and subtidalcommunities for L. heros (larger predators in subtidal commu-nities [Commito 1982]), which can lead to varying impacts of this

predator among ecological communities as well. Ultimately,a clear understanding of ontogenetic diet shifts in L. heros isnecessary for understanding the changing role of these predatorsacross their life span within the soft-sediment communities in

which they reside.

ACKNOWLEDGMENTS

The authors thank Dr. Andrew Hebda at the Nova ScotiaMuseum of Natural History for providing key information.

They also acknowledge Michelle Ellsworth-Power and Drs.David McCorquodale and Katherine Jones at Cape BretonUniversity for their assistance, and thank Kurt Simmons for

feedback on an earlier draft of this article. This project wasfunded through a CBURPGrant to T.A.R. and was conductedin partial fulfillment of the requirements for the Bachelor ofScience (Honors) degree in biology to J.C.C. at Cape Breton

University, Sydney, Nova Scotia.

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