Mar Biol (2009) 156:2149–2160

DOI 10.1007/s00227-009-1245-7

ORIGINAL PAPER

Prevalence, patterns, and eVects of shell damage on Geukensia demissa in South Carolina estuarine habitats

Rachel Hillard · Keith Walters

Received: 27 January 2009 / Accepted: 18 June 2009 / Published online: 4 July 2009© Springer-Verlag 2009

Abstract Shelled molluscs frequently exhibit a record ofdamage on exterior surfaces that can evidence past preda-tion attempts and may aVect survival and growth. In SouthCarolina populations of the ribbed marsh mussel, Geukensiademissa, >90% of the individuals and up to 60% of thetotal shell area are damaged. A trend toward greateramounts of damage occurred on mid-marsh compared tooyster reef mussels from the barrier beach side of inlets.Shell damage eVects on survivorship and shell and tissuegrowth were assessed seasonally during multi- and single-season Weld experiments. Mussels from a common mid-marsh site were divided into size classes (»50 or 70 mm),treated to create two damage levels (undamaged and dam-aged), and replaced within mid-marsh exclusion cages tominimize additional shell damage. In both multi- and sin-gle-season experiments increased shell damage resulted insigniWcantly greater mortality. Linear shell growth wasunaVected by increased damage, but 50 mm mussels grewtwice as fast. Shell mass increased 16–50% in the multi-season and single-season winter period, but decreased 7–12% during the single-season summer period. Tissue masssigniWcantly decreased 31–43% in 50 mm damaged mus-sels, but increased by 33% for 70 mm mussels in bothmulti-season and the single-season winter period experi-ments. Shell damage did reduce tissue mass 43% in 70 mmsingle-season summer mussels. Experimental results indi-cate shell damage from a simulated increase in predationcan aVect negatively both survival and growth of marsh

mussels. Seasonal timing of shell damage and initial musselsize also inXuenced the eVects of sublethal predation onshell and tissue growth. The previously unrecognized impor-tance of sublethal predation and the resultant signiWcantnegative eVects of shell damage on survival and growth willaVect the distribution and population dynamics of G. dem-issa in coastal marshes and will inXuence the overall contri-bution of ribbed mussels to estuarine ecosystems.

Introduction

Shell damage or the loss of the outer periostracum layers iscommon in marine bivalves (Lomovasky et al. 2005; Schejterand Bremec 2007). Suspected causes of damage includepredation (Hughes and Seed 1981; Alexander and Dietl2001; Ramsay et al. 2000, 2001), burrowing (Alexanderand Dietl 2001; Ramsay et al. 2000, 2001; Lomovaskyet al. 2005), harvesting (Ramsay et al. 2000, 2001; Schejterand Bremec 2007), and erosion (Kesler and Bailey 1993;Day et al. 2000). A majority of the causes are either speciesspeciWc (e.g., harvesting commercial species) or commonacross a number of species (e.g., burrowing) and do notexplain observed taxa or spatial diVerences in shell damage.However, failed decapod predation is a leading cause ofdamage in many bivalves and could account for diVerentpatterns in damage across taxa or habitats. Availability(e.g., time of inundation in intertidal habitats), size, andmechanical ease of crushing or opening bivalves all canaVect the success or failure of crab predators (Elner andHughes 1978; Hughes and Seed 1981; Seed and Hughes1995; Caro and Castilla 2004). The chips, scrapes andgouges on outer shell surfaces are evidence of failed preda-tion attempts (Seed and Hughes 1995; Lomovasky et al.2006) and may or may not increase the odds of future

Communicated by F. Bulleri.

R. Hillard · K. Walters (&)Department of Marine Science, Coastal Carolina University, P.O. Box 261954, Conway, SC 29588, USAe-mail: kwalt@coastal.edu

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successful predation (Vermeij 1982) and/or aVect bivalvesurvival and growth.

Failed decapod predation will damage shells, but theprevalence and possible eVects of damage on bivalve survi-vorship and growth remain understudied. In an eVort tomimic damage from dredging, LoosanoV and Nomejko(1955) removed portions of new and older shell edges andsigniWcantly reduced the length of American oysters, Cras-sostrea virginica. Damaged oysters immediately acceler-ated growth to compensate for the loss, but ultimatelyresumed typical shell growth rates (LoosanoV and Nomejko1955). Nontrophic eVects of the deposit feeding crab, Chas-magnathus granulatus, on the stout razor clam, Tagelusplebeius, increased the frequency of shell damage (Lom-ovasky et al. 2006). Although related to disturbance and notpredation, razor clams repaired damage eVects and grewslower in the presence of crabs (Lomovasky et al. 2006).Results suggest that sublethal shell damage can aVect thegrowth of bivalves.

The ribbed marsh mussel, Geukensia demissa, is a pre-dominant Wlter-feeding bivalve within intertidal estuarinesites frequented by numerous decapod predators. Geuken-sia demissa typically are found from low to high intertidalmarsh elevations often attached to the roots, rhizomes, andstems of Spartina alterniXora (Lent 1967; Lutz andCastagna 1980; Kraus and Crow 1985). In South Carolina,mussels also are found in intertidal oyster reefs and bothlow-marsh and reef mussels experience increased tidalinundation and an increased availability of food (Kuenzler1961). The increased food availability enables mussels togrow faster and reach sexual maturity sooner compared tomid- and high-marsh individuals (Bertness 1980; Borreroand Hilbish 1988; Franz 1996, 1997, 2001). The longerlow-marsh inundation times also increase the risk of preda-tion from resident and transient marsh species (Hughes andSeed 1981; Brousseau 1984; Lee and Kneib 1994; Seed andHughes 1995; Hughes and Grabowski 2006). Decapodcrustaceans including the blue crab, Callinectes sapidus,and other xanthids (e.g., Panopeus herbstii) are major pre-dators on ribbed mussels within marshes (Hughes and Seed1981; Lee and Kneib 1994; Seed and Hughes 1995). Crabsuse chelae and/or mandibles to extract or dislodge mussels,chip or crush the shell, and eventually cut the adductormuscle (Hughes and Seed 1981; Seed and Hughes 1995,1997; Caro and Castilla 2004). The chipping at a shell willleave scalloped marks while scissoring produces cleftmarks (Hughes and Seed 1981; Seed and Hughes 1995;Alexander and Dietl 2001). The damage characteristicallyfound on G. demissa shells in both living (Seed and Hughes1997) and dead assemblages (Alexander and Dietl 2001)includes both scallop and cleft marks, and the frequency ofmarks suggests failed predation attempts by crabs are com-mon (Alexander and Dietl 2001).

Although previous indications suggest ribbed musselsexhibit shell damage consistent with sublethal decapod pre-dation, the prevalence and ecological consequences of shelldamage have not been identiWed. Natural diVerences intidal inundation will aVect both mussel growth and avail-ability to predators. Failed predation and resulting shelldamage could result in mussels allocating more energy toshell repair instead of shell and/or tissue growth. Reducedgrowth in G. demissa does result in both a greater risk offuture predation and a reduction in reproductive output(Kuenzler 1961; Brousseau 1984; Franz 1996, 1997, 2001;Smith and Jennings 2000). The objectives of this studywere to examine the prevalence and patterns of visible shelldamage within living Weld populations of mussels relativeto tidal elevation and habitat. Yearly and seasonal eVects ofsimulated shell damage on G. demissa mortality andgrowth also were determined in Weld experiments.

Materials and methods

Damage prevalence and patterns

The prevalence and patterns of shell damage were deter-mined within Weld populations of G. demissa collectedfrom mid-marsh and oyster reef habitats in March to May2006 within two ocean-dominated South Carolina estuar-ies: Hog Inlet (33°50�2�N, 78°36�4�W) and Murrells Inlet(33°33�6�N, 70°2�56�W). Collections fortuitously occurredafter any local winter season (ca. November to March) mor-tality and before the typical seasonal increases in musselrecruitment or decapod predation took place. Marsh andreef habitats were selected from both mainland and barrierisland sides within each inlet. Mainland habitats were onthe far western side of each inlet and barrier island habitatswere on the landward side of barrier beaches. Mid-marshsites were within <1 m tall S. alterniXora stands and reefcollection sites were within intertidal oyster reefs fringingthe low marsh. Oyster reefs in South Carolina typicallyoccupy low intertidal elevations between the furthest extentof S. alterniXora and the beginning of subtidal waters.

Shell damage was measured on 50 mussels of varioussizes collected haphazardly from within unrecorded habi-tats along a 50–100 m reach of shoreline. In the Weld,length (umbo to shell margin), width (lateral axis), andheight (valve to valve) of each mussel were measured to thenearest 0.1 mm using digital calipers. Images of the rightand left valves also were captured with a digital camera andlater processed to determine total shell area and total area ofshell damage using image analysis software (Pro Plus,v.4.5.1.22). Damage was deWned as any area where theperiostracum was visibly removed exposing the innercalcite layers of the shell.

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Survival and growth experiments

Shell damage eVects on survival and growth of musselswere assessed in two Weld experiments conducted fromJanuary to September 2007 in the mid-marsh at Hog Inlet,South Carolina (33°51�0.5�N, 78°35�12�W). Multi-season,8 months, and single-season experiments, two 4-monthperiods, were conducted (see below). Mussels for eachexperiment were collected in January or May from mid-marsh sediments at Vereen State Park, South Carolina(33°52�27�N, 78°35�33�W). Individuals were collectedfrom Vereen Park because of site accessibility and the pres-ence of suYcient numbers of G. demissa with minimumshell damage. Transplanting mussels from Vereen Park toHog Inlet sites also minimized possible confounding eVects(e.g., site adaptation) that could reduce chances of detectingtreatment eVects if mussels solely from Hog Inlet were usedin experiments. Vereen Park is along the Atlantic Intra-coastal Waterway approximately 2.5 km north of Hog Inlet.

Relatively undamaged mussels from Vereen Park weretransported to the lab, numbered (Floy Tag®), maintained inaerated and frequently changed seawater from the collectionsite, and processed in under 3 days before being placed in theHog Inlet mid-marsh Weld location. Additional samples foreach size (n = 50) and damage treatment (n = 25 per treat-ment) also were collected and immediately frozen at ¡20°Cfor later processing to determine shell and tissue mass in Weldmussels. Shell length, width, and height initially were mea-sured to the nearest 0.01 mm and collected mussels weredivided into two size classes (n = 100 each): medium (mean50 mm, range 42–60 mm) and large (mean 70 mm, range 65–79 mm). Medium mussels are within the size range where bothblue crabs (Callinectes sapidus) and mud crabs (Panopeusherbstii) are able to consume G. demissa (Seed andHughes 1995). Mussels ¿ 50 mm can be consumed by crabsduring a single predation event (Hughes and Seed 1981; Seedand Hughes 1995) and may be less likely to exhibit shelldamage from failed predation (Seed and Hughes 1997).Larger mussels (À50 mm) may experience a size refugerequiring multiple predation events to consume (Paine 1976;Hughes and Seed 1981; Seed and Hughes 1995, 1997) andincrease the possibility of observing shell damage. The rapidgrowth of medium relative to large mussels (Kuenzler 1961;Bertness 1980; Lutz and Castagna 1980; Brousseau 1984)also suggests 50 mm mussels may allocate more energy togrowth and therefore are better able to repair shell damage.

Mussels from each size class were divided into two shelldamage treatment levels: no additional damage (undam-aged) and an additional level of shell damage (damaged).All collected mussels had existing levels of shell damageand the damage treatment standardized the amount of newbut not the total damage area. The damage treatmentremoved an extra 20% of the shell surface which was

consistent with the average amount observed on Weld col-lected mussels (see “Results”). Damage was created bysanding oV the outer layers of shell until the inner calcitelayer was exposed using a rotary tool (Dremel®). A numberof techniques to mimic crab predation initially were tried(e.g., scraping shell with channel lock pliers), but only sand-ing produced the required levels of shell damage in theshortest time possible. Both valves on all mussels were pho-tographed and the initial total shell area and damage weremeasured using image analysis software (ImageJ, v.1.38).

The Weld site was selected based on observed patterns inshell damage and reported growth rates. Mid-marsh comparedto oyster reef mussels generally had greater amounts of shelldamage (see “Results”). Mid- to high-marsh G. demissapopulations also have slower growth rates compared to low-marsh mussel populations (Lent 1967; Lutz and Castagna1980; Franz 1996, 1997, 2001). Greater shell damage andslower growth rates suggest that mid-marsh mussels mayexperience greater ecological eVects from shell damagecompared to mussels from other marsh locations.

Mussels (n = 5) from the same size and damage treat-ment were placed in 10 mm Vexar® mesh cages (50 cm talland 12 cm in diameter). Cages (n = 10 per size and damagetreatment) were placed within holes excavated in the sedi-ment between S. alterniXora culms. Each cage was Wlledwith excavated sediment up to the level of the sedimentsurface to enable mussel burial (Lent 1968, 1969; Franz1997). The use of cages facilitated recollection of numberedmussels and minimized additional predation attempts andpossible shell damage.

The eVects of size class and shell damage treatments wereexamined in multi- and single-season experiments. Geuken-sia demissa typically experience variable growth rates withboth rapid (summer) and slow (winter) growing periods(Brousseau 1984; Borrero and Hilbish 1988; Franz 1996,1997, 2001). The multi-season, 8 months experiment wasconducted from January to September (winter + summer)and integrated the eVects of seasonal diVerences in growthrates. Potential seasonal diVerences in mussel responses toshell damage were examined in the single-season experi-ment that consisted of two 4-month treatment periods: Janu-ary to May (winter) and May to September (summer).Experimental mussels for the summer treatment periodagain were collected from Vereen Park in May and pro-cessed as described above. January and May Weld collectedmussels were compared to account for any potential diVer-ences in the initial conditions of experimental mussels.

At the end of each experimental treatment period cagedmussels were returned to the lab and frozen at ¡20°C priorto being processed. Final shell length, width, and heightwere measured and each valve, except mussels collected inwinter from the single-season experiment, again was photo-graphed. Along with the initially frozen samples of January

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and May Weld collected mussels, individuals were dissectedto remove all tissue from the shell and dried at 60°C to aconstant shell and tissue dry mass. Average monthlygrowth rates were determined for mussel size class anddamage treatments by calculating the mean change (Wnal–initial) in shell length and mass, tissue mass, and damagearea relative to the length of the experiment (8 or 4 months).Rates were not standardized to initial sizes because of thelimited variation among mussels within a size class and alack of signiWcant correlations between initial and Wnalmeasurements.

Statistical analyses

Hierarchical log–linear models and a backward eliminationapproach were used to test the dependence or independenceof various categorical variables (Feinberg 2007, Quinn andKeough 2002). To analyze spatial patterns in shell damage,the dependence of damage categories (present, absent) oninlet sides (barrier island, mainland) and habitat sites (mid-marsh, reef) was determined for Weld collected musselsfrom Murrells and Hog Inlet. In multi- and single-seasonexperiments, the dependence of survivorship (alive, dead)and growth categories (positive, negative) on shell damage,size class, and season treatments also were determinedwhere appropriate. The change in likelihood goodness-of-Wt was used to evaluate which factors to include andproduce the simplest explanatory model (Feinberg 2007;Quinn and Keough 2002).

Field collected mussels from initial samples in Januaryand May were analyzed to generate a best-Wt, shell dimen-sion by shell or tissue mass regression in order to calculateshell and tissue mass for mussels used in survival andgrowth experiments (Quinn and Keough 2002). In all casesshell length and a power equation proved the best Wt for thedata. Estimated constants and regression coeYcients wereused to calculate initial shell and tissue dry mass for mus-sels deployed in experiments. Changes in shell and tissuemass for experimental mussels were calculated as thediVerence between Wnal, measured and initial, estimatedmass values.

The total and/or change in shell length and mass, tissuemass, and shell damage area were analyzed using analysisof variance (ANOVA) models (Quinn and Keough 2002).The signiWcance of inlet (Hog, Murrells), side (barrierisland, mainland), and habitat (reef, mid-marsh) eVects onthe percent of shell damage in Weld collected mussels wasanalyzed with a blocked, one-way ANOVA. Inlet (block)and habitat were considered random eVects, representingonly two of many possible inlets or habitats. Habitat eVectswere tested over the side error mean square, each side rep-resenting habitat replicates sampled within an inlet, andindividual mussels were considered subsamples collected

within each habitat on a side. In both multi- and single-sea-son experiments, initial shell length and the percentage ofshell area damaged were analyzed to substantiate damagetreatments and assure unexpected size or seasonal diVer-ences did not confound the experimental design. Changes(Wnal–initial) in shell length, and tissue and shell dry masswere analyzed with a blocked, nested ANOVA to deter-mine the signiWcance of treatment eVects. Size class (50,70 mm) was blocked for both multi- and single-seasonexperiments. The multi-season model included damagetreatment and cage within damage treatment eVects and thesingle-season model included season (winter, summer),damage within season, and cage within damage within sea-son eVects. Model designs for ANOVAs were selected, inpart, to provide conservative tests for each treatment eVectand when possible to avoid confounding by testing forupper level treatment eVects (e.g., damage levels) overamong mussel error (Quinn and Keough 2002; Underwood1997). Dead, missing, or negatively growing mussels wereexcluded from analyses of growth, but were analyzed inlog-linear models (see above) to assess diVerences in survi-vorship (alive, dead) and growth categories (positive, nega-tive). Negatively growing individuals did not occur in themulti-season experiment and only were a small fraction(18%) of all mussels in the single-season experiment. Alldata used in ANOVA models were tested for assumptions(e.g., normality, homogeneity). If violations were identi-Wed, appropriate transformations (e.g., arcsine square root,fourth root) were applied. All statistical analyses were runusing SPSS (v.11–14).

Results

Damage prevalence and patterns

Shell damage was common with on average 90% of allcollected mussels exhibiting some amount of damage(Table 1). Within Murrells inlet, the proportion of musselsdamaged depended on habitat (�2 = 19.1, df = 1, P < 0.001)but not on side (�2 = 0.005, df = 1, P > 0.05). All MurrellsInlet mid-marsh mussels were damaged but 10% of oysterreef mussels were undamaged. Damage prevalence withinHog Inlet depended on a side by habitat interaction eVect(�2 = 5.3, df = 1, P < 0.025). All barrier island, but only70% of mainland mid-marsh mussels were damaged.

The overall average amount of shell surface area dam-aged on Weld collected mussels was 20 § 2%, and damageamounts varied across inlets, sides, and habitats (Fig. 1).The percentage of shell damage was signiWcantly diVerentbetween inlets (F1,394 = 4.43, P < 0.04) but not betweenhabitats (F1,1 = 0.31, P > 0.05). Although not signiWcant,mussels from mid-marsh habitats tended to have more

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damage, averaging 29 § 3% of shell area removed, com-pared to oyster reef mussels that had on average only11 § 1% of the shell area removed. Barrier island musselsalso appeared to have a greater percentage of shell damagecompared to mainland side mussels within each inlet(Fig. 1), but the study’s sampling design did not permitdetecting a signiWcant side eVect with existing data.

Multi-season survivorship and growth experiment

An initial comparison of mussels deployed within cagesindicated both size and damage diVerences but no

confounding treatment eVects. Shell length was signiW-cantly diVerent between medium and large size treatments(F1,163 = 1817.6, P < 0.001), but not between damagedand undamaged treatments (F1,18 = 0.7, P > 0.05) or cages(F18,163 = 0.8, P > 0.05). Experimental procedures eVec-tively randomized the diVerent sized mussels among dam-age treatments and cages. The percentage of shell damagewas signiWcantly diVerent between damage (F1,18 = 430.9,P < 0.001) and size treatments (F1,163 = 32.6, P < 0.001),but not between cages (F18,163 = 1.7, P > 0.05). Shells of70 mm compared to 50 mm mussels exhibited a greateramount of damage even if not treated, but the technique ofsanding shells produced a consistent increase in the percentof shell damage within size classes.

Combined mortality for all mussel treatments during themulti-season experiment was <10%. Mortality depended onshell damage (�2 = 5.1, df = 1, P < 0.025) but was indepen-dent of size class (�2 = 0.5, df = 1, P > 0.05). For both sizeclasses the mortality of damaged compared to undamagedmussels was greater (Fig. 2). On average mortalityincreased 4–10% or 3–6 times in damage treatments(Fig. 2).

Size was the only factor that aVected the linear growth ofshells (Fig. 3a). As expected based on previous studies,shell growth was signiWcantly diVerent between 50 and70 mm mussels (F1,163 = 240.2, P < 0.001). All mussels inthe multi-season experiment increased in length, but the

Table 1 The percentage of mussels collected with some amount of shell surface damage from oyster reefs (Reefs) and mid-marsh (Marsh) habitatswithin barrier island and mainland sides at Murrells and Hog Inlets, SC

Inlet Murrells Hog

Side Mainland Barrier Island Mainland Barrier Island

Habitat Reef Marsh Reef Marsh Reef Marsh Reef Marsh

Percent damaged 88 100 86 100 76 68 94 100

Fig. 1 The percent area of shell damage (mean + SE) on mussels col-lected from oyster reef and mid-marsh habitats within barrier islandand mainland sides at Hog and Murrells Inlet, SC

Inlet SidesBarrier Mainland

0

10

20

30

40

50

60

70Murrells Inlet

Hog Inlet

Shel

l Dam

age

Are

a (%

)

0

10

20

30

40

50

60

70

ReefMid-Marsh

Fig. 2 The mean (+SE) percent mortality for mussels from the multi-season (8 months) survivorship and growth experiment

Size Class50 mm 70 mm

Mus

sel M

orta

lity

(%)

0

5

10

15

20UndamagedDamaged

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50 mm size class (1.8 mm/months) grew twice as fast as the70 mm size class (0.8 mm/months). Shell damage did notaVect linear shell growth (F1,18 = 0.074, P > 0.05). A sig-niWcant cage eVect (F18,163 = 2.4, P < 0.002), unexpectedgiven the random distribution of damage treatments amongcages described above, likely reduced the ability to detect adamage eVect on linear shell growth.

Shell mass growth was aVected by size and damagetreatments (Fig. 3b). Length was a signiWcant predictor ofinitial shell dry mass (Table 2) and enabled calculation ofshell mass growth rates for both damaged and undamaged

mussels. Mussel size (F1,161 = 6.7, P < 0.015) and shelldamage treatments (F1,18 = 7.7, P < 0.015) signiWcantlyaVected changes in shell mass. Shell mass increased twiceas much over the multi-season experiment for 50 mm (45–50%) compared to 70 mm mussels (20–26%). Damaged(0.41–0.38 g/months) compared to undamaged shell mass(0.34–0.29 g/months) also increased at a signiWcantly fasterrate (Fig. 3b).

Mussel tissue mass only was aVected by size treatments(Fig. 3c). Again, shell length was a signiWcant predictor ofinitial tissue dry mass (Table 2) and enabled calculation oftissue growth rates. Size class (F1,160 = 30.1, P < 0.001) butnot damage treatments (F1,18 = 1.0, P > 0.05) signiWcantlyaVected changes in tissue dry mass. Increases in tissue bio-mass were slower for 50 mm, damaged (36.4 mg/months)compared to undamaged mussels (53.1 mg/months), butfaster for 70 mm, damaged (34.2 mg/months) compared toundamaged mussels (24.7 mg/months). A signiWcant diVer-ence in tissue growth among cages within damaged andundamaged treatments (F18,160 = 1.8, P < 0.002) likelyaVected the ability to detect diVerences between damagetreatments.

Seasonal survivorship and growth experiment

Comparisons of mussels initially deployed in the single-season experiment indicated no uncontrolled eVects. Shelllengths were signiWcantly diVerent only between size treat-ments (F1,288 = 3318.8, P < 0.001), and not between dam-age (F2,36 = 1.8, P > 0.05) or season treatments (F1,2 = 0.5,P > 0.05), or cages (F36,288 = 1.3, P > 0.05). The initial sizeof mussels did not confound damage, season, or cageeVects. The percent of shell area removed was signiWcantlydiVerent between size (F1,288 = 21.8, P < 0.001) and dam-age treatments (F2,36 = 322.9, P < 0.001), but not betweenwinter and summer seasons (F1,2 = 0.2, P > 0.05) or cages(F36,288 = 1.3, P > 0.05). Damage treatments were distinctand did not vary between seasons or among cages.

Mussel mortality was dependent on damage (�2 = 4.1,df = 1, P < 0.045) but not on season (�2 = 1.3, df = 1,P > 0.05) or size treatments (�2 = 0.1, df = 1, P > 0.05).Mortality was 2.5£ greater in damaged compared toundamaged mussels for combined seasons and size classes(Fig. 4). Although not signiWcantly dependent on season,shell damage increased mortality 8–10% in winter but notin summer. Mussel mortality generally was low betweenseasons and only ranged from 1 to 6 individuals. Mortalitybetween size classes was slightly greater in 70 mm (7%)compared to 50 mm mussels (4%) regardless of shell dam-age (Fig. 4).

A majority of the mussels in the single-season experi-ment grew in length and/or mass, but some actuallydecreased in size (Table 3). A negative change in shell

Fig. 3 The mean (+SE) total change in a shell length, b shell drymass, and c tissue dry mass for mussels from the multi-season survi-vorship and growth experiment

∆∆ S

hel

l Len

gth

(m

m)

0

2

4

6

8

10

12

14

16

Undamaged

Damaged

Size Class

50 mm 70 mm

∆∆ D

ry T

issu

e M

ass

(mg)

0

100

200

300

400

500

∆∆ D

ry S

hel

l Mas

s (g

)

0

1

2

3

4

a

b

c

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length, shell or tissue dry mass occurred in ·18% of allmussels and size typically decreased in large mussels dur-ing the winter (Table 3). Changes (increase, decrease) inshell length depended on size by damage (�2 = 5.5, df = 1,P < 0.020) and season eVects (�2 = 31.4, df = 1, P < 0.001);shell dry mass depended on season by size (�2 = 5.3, df = 1,P < 0.025) and season by damage eVects (�2 = 10.1, df = 1,P < 0.001); and tissue dry mass depended on season by size(�2 = 18.6, df = 1, P < 0.001), season by damage (�2 = 19.8,df = 1, P < 0.001), and size by damage eVects (�2 = 5.8,df = 1, P < 0.020). Negative growth in shell length and drymass and tissue dry mass in marsh mussels depended onseason, size and shell damage treatments.

Seasonal and size treatments aVected the rate of linearshell change in mussels with positive growth (Fig. 5a).Linear shell growth was signiWcantly diVerent between sizeclasses (F1,261 = 255.2, P < 0.001) and seasons (F1,2 = 755.8,P < 0.001), but not damage treatments (F2,36 = 2.9,P > 0.05) or cages (F36,261 = 0.6, P > 0.05). Shell growthrates were greater in summer compared to winter forboth medium (3.3 vs. 0.4 mm/months) and large mussels(1.8 vs. 0.1 mm/months). Relative to size and irrespectiveof damage, 50 mm compared to 70 mm mussels weregrowing ca. 4£ faster in winter and 2£ faster in summer.

Damage treatments aVected changes in shell dry mass(Fig. 5b). Shell length was a signiWcant predictor of initialshell dry mass for both January and May damagedand undamaged mussels (Table 2). The growth in shelldry mass was signiWcantly diVerent between size class(F1,246 = 6.6, P < 0.015), season (F1,2 = 18.6, P = 0.05), anddamage treatments (F2,36 = 7.2, P < 0.005). Cage eVects(F36,246 = 1.5, P < 0.05) also were signiWcant but did notconfound interpretation of major treatment eVects. Duringwinter months shell mass increased up to 2£ as much indamaged compared to undamaged mussels (Fig. 5b). The

Fig. 4 The mean (+SE) percent mortality for mussels from the single-season (winter, summer) survivorship and growth experiments

Summer

Size Class50 mm 70 mm

Per

cent

Mor

talit

y (%

)

0

5

10

15

20

Winter

0

5

10

15

20UndamagedDamaged

Table 2 The length–mass power equation regressions generated for January and May subsamples of damaged and undamaged mussels immediately frozen and not used in survival and growth experiments

Date Treatment Dry tissue mass (Y) Dry shell mass (Y)

January Undamaged Y = 0.0042(length)2.8 Y = 1.2 £ 10¡5(length)3.2

F1,48 = 356.3, P < 0.001 F1,48 = 835.9, P < 0.001

R2 = 0.881 R2 = 0.946

Damaged Y = 0.110(length)1.9 Y = 2.46 £ 10¡5(length)2.9

F1,45 = 147.5, P < 0.001 F1,45 = 1052.6, P < 0.001

R2 = 0.766 R2 = 0.959

May Undamaged Y = 0.007(length)2.7 Y = 1.6 £ 10¡4(length)2.6

F1,47 = 181.3, P < 0.001 F1,48 = 441.6, P < 0.001

R2 = 0.794 R2 = 0.900

Damaged Y = 0.002(length)3.0 Y = 1.0 £ 10¡4(length)2.6

F1,48 = 456.9, P < 0.001 F1,48 = 996.5, P < 0.001

R2 = 0.905 R2 = 0.954

Regression coeYcients and constants were used to estimate initial shell (g) and tissue (mg) dry mass for yearly (January) and single-season experimental mussels (January and May)

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2156 Mar Biol (2009) 156:2149–2160

eVects of shell damage were reversed during summermonths when the growth of undamaged mussels of bothsizes was slightly but signiWcantly greater than damagedmussels (Fig. 5b). In general, shell growth was greater dur-ing the summer for all except damaged, 70 mm musselswhose summer and winter growths were similar (Fig. 5b).Although the total summer growth of 50 mm versus 70 mmindividuals was similar, 50 mm mussels were adding shellmass at an »20% greater rate.

Treatment eVects on tissue growth paralleled changes inshell mass (Fig. 5c). Again, shell length was a signiWcantpredictor of initial tissue dry mass for damaged and undam-aged mussels collected in both January and May (Table 2).Tissue growth was signiWcantly diVerent between size class(F1,235 = 958.7, P < 0.001), season (F1,2 = 55.7, P < 0.020),and damage treatments (F2,36 = 5.8, P < 0.010). A signiW-cant cage eVect (F36,235 = 1.7, P < 0.015) did not confoundinterpretation of major treatment eVects. Shell damage hadless eVect in winter but a greater eVect in summer on tissuecompared to shell growth (Fig. 5b, c). Summer tissuegrowth was reduced by ca. 25% in damaged mussels(Fig. 5c). As for shell mass, tissue growth generally was 2–4£ greater during summer versus winter months. The rela-tive growth rates for the diVerent sized mussels in summerwere 20–50% greater in 50 mm compared to 70 mm indi-viduals.

Discussion

Shell damage was both common and extensive in SouthCarolina populations of G. demissa and varied across therange of intertidal habitats sampled. On average, ¸90% ofmussels and up to 60% of the surface area of each shell wasdamaged. A greater percentage of mid-marsh (92%) com-pared to oyster reef mussels (86%) exhibited some shelldamage. Within Hog Inlet all mid-marsh mussels from thebarrier island side were damaged, but only 70% of mainland

mussels were damaged. Mid-marsh (up to 60%) comparedto reef mussels (only up to 20%) tended to have a greaterpercentage of shell damaged. The percentage of shelldamage also appeared greater on barrier island (31%) com-pared to mainland sides (6%) and within Murrells (20%)compared to Hog Inlet (17%). DiVerences in the prevalenceand extent of shell damage may be explained by variationin the possible sources of shell damage.

Failed attempts by predators are one of the likely causesof shell damage in bivalves. Chelate predators (e.g., deca-pods) can chip and scar outer shell layers in an attempt toopen and consume bivalve prey. If the predation attempt isunsuccessful, exterior damage to the shells is not repairedand remains a record of past predation events. Possible rea-sons for unsuccessful predation attempts range from timelimitations to cost-beneWt evaluations (Elner and Hughes1978; Hughes and Seed 1981; Seed and Hughes 1995,1997; Caro and Castilla 2004). For example, a particularlywell-defended bivalve (e.g., thick shell) may require moretime to open than is available to the predator. Within inter-tidal habitats, elevation combined with tidal height deter-mine the maximum time available for a predation event.The greater frequency and duration of inundation withinlow-marsh elevations does increase predator-induced mor-tality in G. demissa (Bertness and Grosholz 1985; Kneib1995). The degree of tidal coverage also should inXuencethe prevalence and extent of shell damage from failed orinterrupted predation events.

A number of decapod species (e.g., P. herbstii, C. sapi-dus) commonly prey on G. demissa in both lab (Hughesand Seed 1981; Lee and Kneib 1994; Seed and Hughes1995) and Weld studies (Lin 1990). In North Carolina andGeorgia marshes G. demissa mortality is greater along thelow-marsh edge compared to the mid-marsh interior (Lin1990; Walters 2009.). Although successful predation isgreater in low-marsh mussel populations, evidence of failedpredation or shell damage in our study suggests that tidalinundation is not the only factor aVecting crab predation onmussels. Mid-marsh mussels inundated less frequently andfor shorter durations tended to have greater levels of shelldamage compared to low-intertidal reef mussels. Reducedlevels of shell damage within oyster reefs could indicate allpredation attempts are successful, but southeastern musseldensities, 143–468 ind. m¡2 on reefs (Walters and Coen2009) versus 1–422 ind. m¡2 in the mid-marsh (Kuenzler1961; Stiven and Kuenzler 1979; Bertness 1980; Borrero1985; Stiven and Gardner 1992; Newell and Krambeck1995), do not suggest increased predation success on reefs.Mussels on reefs typically are buried in the sedimentbetween or under oyster clumps that potentially reducepredator accessibility (e.g., Seitz et al. 2001). Also, densemussel populations in low-marsh elevations outside of reefs

Table 3 The percentage of mussels that decreased in either shelllength or dry mass or tissue dry mass for season (winter, summer),size (medium = 50 mm, large = 70 mm) and damage treatments(U = undamaged, D = damaged) in the single-season survivorship andgrowth experiment

Winter Summer

Medium Large Medium Large

U D U D U D U D

Shell length 8.0 2.0 10.0 37.0 0.0 0.0 2.0 0.0

Shell dry weight 8.0 2.0 59.0 14.0 0.0 4.0 0.0 2.0

Tissue dry weight 17.0 28.0 31.0 9.0 0.0 2.0 2.0 29.0

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are uncommon in South Carolina (Walters pers obs.),unlike the dense mussel reefs that can form in the low-marsh of northern states (Franz and Tanacredi 1993; Franz1996, 1997, 2001). Similar to subtidal oyster reefs in NorthCarolina (Grabowski 2004; Hughes and Grabowski 2006),South Carolina intertidal reefs may act as an eVectiverefuge from mussel predators.

DiVerences in shell damage between inlets also may reX-ect diVerences in predator accessibility. The greater extentof shell damage in Murrells compared to Hog Inlet, only57 km apart, could result from inlet diVerences in crab den-sities. Murrells Inlet is approximately twice as large with

greater landscape complexity (e.g., more tidal creeks) com-pared to Hog Inlet (Wright, personal communication). Thelarger size and greater complexity would suggest MurrellsInlet supports a larger crab population. However, commer-cial and recreational crabbing is more common in MurrellsInlet, potentially reducing overall crab numbers. Resolutionof the exact contribution that diVerences in crab densitiesmake to the observed variation in shell damage betweeninlets requires more accurate estimates of crab stocks thancurrently exists.

As an alternative to failed predation attempts, shell dam-age on G. demissa may result from mechanical, chemical or

Fig. 5 The mean (+SE) total change in a shell length, b shell dry mass, and c tissue dry mass for mussels from single-season survivorship and growth experiment

Winter

Size Class

50 mm 70 mm

0

100

200

300

400

500

Winter

0.0

0.5

1.0

1.5

2.0

2.5

3.0

Winter

0

5

10

15

20Undamaged

Damaged

Summer

∆ Sh

ell D

ry M

ass

(g)

0.0

0.5

1.0

1.5

2.0

2.5

3.0

Summer

∆ Shel

l Len

gth

(mm

)0

5

10

15

20

Summer

Size Class

50 mm 70 mm

∆ Tis

sue

Dry

Mas

s (m

g)

0

100

200

300

400

500

b

c

a

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2158 Mar Biol (2009) 156:2149–2160

physiological processes in the sediments eroding the outershell layers. Erosion around the umbo, or portion of theshell most often buried in the sediments, was suggested toexplain observed damage in South Carolina populations ofG. demissa (Brousseau 1984; Borrero 1985). How erosioncould remove multiple layers of shell even in the smallestor most juvenile mussels was not explained, and in at leastone study exposed shell portions not buried in the sedimentalso exhibited shell loss (Borrero 1985). If erosion alonecaused shell damage, time of exposure in the sedimentswould mean that the older the mussel the greater the area ofshell damage. Observed diVerences in shell damage amongdiVerent sized mussels and also the diVerences betweeninlets all suggest that erosion, although a possible explana-tion for some shell loss, is not the major cause of shell dam-age in G. demissa.

Shell damage in G. demissa had consequential eVects onmussel mortality and growth. Although overall rates werelow (2–13%), mortality was consistently greater for dam-aged mussels in both yearly and single-season experiments.Linear shell growth was unaVected by shell damage, how-ever, medium-sized mussels grew twice as fast as the largemussels in both multi- and single-season experiments. Shelldamage caused a 16–50% increase in shell mass except inseasonal summer mussels. In the single-season experiment,summer damage decreased shell mass by 7–12%. Wintershell damage decreased tissue mass for medium mussels by31–43%, but increased tissue mass by 33% in large musselsin both multi- and single-season experiments. Summerdamage reduced tissue mass by 43% for large mussels inthe single-season experiment. The observed negative eVectsof shell damage on G. demissa survival and growth suggestsublethal predation could have a major impact on musselpopulations and, by extrapolation, the overall dynamics ofsoutheastern estuarine systems.

Numerous population studies of G. demissa exist(Brousseau 1984; Bertness and Grosholz 1985; Borrero1985; Borrero and Hilbish 1988; Franz and Tanacredi1993; Nielsen and Franz 1995; Franz 1996, 1997, 2001),but few quantify Weld rates of either predatory or non-pred-atory mortality (Stiven and Kuenzler 1979; Seed 1980;Borrero 1985; Bertness and Grosholz 1985; Borrero andHilbish 1988; Lin 1989, 1990). In a New England saltmarsh, 0.8–9.3% of the entire mussel population sampledhad died from non-predatory mortality (Bertness and Gros-holz 1985). For juveniles (<30 mm), predators accountedfor up to 33% of low-marsh losses and 0% of mid-marshloses over a 6-month period (Bertness and Grosholz 1985).Reported non-predatory mortality in southeastern com-pared to northeastern habitats is slightly greater but typi-cally <20% per year (Borrero and Hilbish 1988; Waltersand Coen 2009). In contrast, southeastern predation onmussels can be intense ranging from estimates of 8 to 16%

per day in North Carolina marshes (Lin 1989, 1990) to 7.7–19.3% per month in South Georgia (Walters 2009).Although predators across the East Coast of the US appearto account for greater mussel losses than mortality from anynon-predatory source, in the southeast mortality from shelldamage contributes 0.5–25% per year to overall mortalityrates.

Shell damage to G. demissa also has signiWcant negativeconsequences for both shell and tissue growth. The eVectsof damage depended on both size and season. For example,the shell mass of mussels damaged in winter increased 20–100% but decreased 6–13% in summer. Unrepaired shelldamage could lead to an increased probability of mortalityfrom either predators or physiological stress. Mussels withunrepaired shell damage are more vulnerable to futurelethal predation (Hughes and Seed 1981). Blue crabsactively will select mussels with weakened shells, increas-ing the chances of successfully cracking open and consum-ing the mussel (Hughes and Seed 1981; Seed and Hughes1995, 1997). Unrepaired damage also could increase mor-tality by aVecting the ability of mussels to thermoregulate,increasing physiological stress and the likelihood of death(e.g., Helmuth 1998; Jost and Helmuth 2007).

Seasonal and size diVerences in the eVects of shell dam-age indicated mussels will alter the energy expended onshell and tissue growth. Winter damage resulted in an 18%decrease in 50 mm but stimulated 70 mm tissue growth. Insummer damage reduced 70 mm tissue growth by 46%.Food availability, predation and reproductive activity allmay explain seasonal diVerences in the eVects of shell dam-age. If damage occurs in the winter mussels may allocatelimited energy supplies that result from seasonal reductionsin food availability toward shell repair. During the summerwhen food supplies are greater energy may be allocatedmore toward linear shell growth and repair to counteract anincreased chance of predation, and reproduction, typically asummer occurrence. Smaller mussels are easier for deca-pods to open and reaching a larger size or refuge can reducethe chance of predatory mortality (Paine 1976; Hughes andSeed 1981; Bertness 1984; Eggleston 1990; Hughes andSeed 1995; Kneib 1995; Reusch and Chapman 1997; Smithand Jennings 2000). In 50 mm mussels, the choice to getlarge and reach a potential predator size refuge appearsselected over the needs for shell repair and tissue growth.Linear shell growth rates were at least double in 50 mm(7.0–13.7 mm/month) compared to70 mm mussels (0.4–1.8 mm/month). Ultimately, the summertime reduction intissue growth may have a negative eVect on reproduction in50 mm mussels because tissue mass and reproductive out-puts are positively correlated (Brousseau 1984; Franz 1997).

Varying seasonal patterns in growth and reproductiveoutput also are implicated as possible reasons for bivalvereductions in size and/or mass that result in negative

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growth. Spawning, annual weight cycle changes and starva-tion all can cause G. demissa to lose tissue and shell massthroughout the year (Brousseau 1984; Borrero and Hilbish1988; Franz 1997). South Carolina populations of G. dem-issa experience major monthly Xuctuations in size andmass, especially tissue mass (Borrero and Hilbish 1988). Inour study, shell length or mass or tissue mass declined in·18% of the mussels. Negative growth primarily occurredin single- and not multi-season experiments. Apparentlymussels are able to compensate for short term (4 months),negative growth over longer periods (8 months) ultimatelyresulting in positive growth rates.

Shell and tissue mass and growth rates in G. demissagenerally decrease with increasing tidal elevation (Jordanand Valiela 1982; Bertness and Grosholz 1985; Borrero1985; Stiven and Gardner 1992; Franz and Tanacredi 1993;Franz 1997). Mid- to high-marsh growth rates are <50%that in the low-marsh (Borrero 1985; Franz 1997). Shortertidal inundation periods and less access to food for mid-marsh mussels potentially result in reduced growth rates(Franz 1997). In our study, a greater percentage of mussels(92%) and a greater amount of shell damage (2–54%)occurred within mid-marsh sites. Greater sublethal preda-tion rates (this study) combined with decreased mass andreduced food availability (Franz 1997) suggest mid-marshmussels may exist in a suboptimal or fringe habitat. Mid-marsh populations actually may represent sinks suppliedfrom low-marsh sources.

Sublethal shell damage in G. demissa populationsaVects both the survivorship and growth of individualmussels. Damage slightly but signiWcantly increased mus-sel mortality. Although damage did not reduce lineargrowth, increases in shell mass were reduced during thesummer. Sublethal damage also reduced tissue growth ofboth medium and large mussels dependent on the season.Varying changes in shell mass by season indicated mus-sels were able to partition energy between the diVerentneeds for repair and growth, and possibly reproduction.Although food availability typically is reduced in winter,more energy may be available for shell repair than in sum-mer when energy is allocated toward both growth andreproduction. Partitioning energy also is dependent onmussel size (age). The reduced tissue growth in mediummussels suggests smaller individuals do not have a largeenough energy reserve to simultaneously repair shell dam-age while increasing tissue mass. Reductions in tissuemass and reproductive outputs may not allow individualmussels to maintain eVectively a sustainable population.The individual consequences of sublethal predation likelywill aVect both population and community dynamics ofG. demissa, a critical species in southeastern estuarinemarshes.

Acknowledgments We would like to thank E. Trott, T.K. Austin,J. Kanes, A. Puzzo, M. Lawrence, and the 2006 CCU Advanced Pop-ulation Biology class for Weld support; Dr. E. KoepXer for use of ImagePro Plus software and Dr. E. Wright for GIS data; and Drs. F. Bulleri,E. Burge, J. Hutchens, E. ProYtt, and 3 anonymous reviewers forsuggestions and comments on the manuscript. Financial support wasprovided in part by the National Fish and Wildlife Foundation andCCUs Coastal Marine and Wetland Studies graduate program. Thisstudy complied with current laws of the USA.

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