58 (2007) 156–162www.elsevier.com/locate/seares

Journal of Sea Research

Repaired shell damage in the commercial scallop Zygochlamyspatagonica (King & Broderip, 1832), Argentine Sea

Laura Schejter ⁎, Claudia Bremec

CONICET, Consejo Nacional de Investigaciones Científicas y Técnicas, Buenos Aires, ArgentinaINIDEP, Instituto Nacional de Investigación y Desarrollo Pesquero, Laboratorio de Bentos, Paseo Victoria Ocampo 1,

B7602HSA, Mar del Plata, Argentina

Received 8 May 2006; accepted 27 February 2007Available online 19 March 2007

Abstract

We present an overview of repaired shell damage in the scallop Zygochlamys patagonica in the commercial beds of theArgentine Sea. Presence of scars was registered in 11962 scallops, ranging from 20 to 90 mm total height, from the fishing groundsin 2003 and also in 1995 (pre-fishery condition). Values of percentage of scarring (presence) were variable in all areas. Samplescollected in 1995 showed the highest percentage of scars. As the highest records of scarring were registered in pre-fisheryconditions, it is not possible to regard these marks as absolute indicators of anthropogenic disturbance caused by trawling activities.Moderate and severe damage was mostly recorded in individuals of commercial size (≥55 mm). This indicates not only thefragility of smaller scallops, but also the accumulation of damage in older specimens, probably more resistant to damage because oftheir thicker shells. The selective removal of commercial individuals could explain in part our results that indicate a higherpercentage of repaired shell damage in 1995, when the average size of the population was also higher. Future investigations areneeded to assess effects of scarring at different shell sizes (ages) and relate these to levels of survival in Patagonian scallops thrownback into the sea during processing on board.© 2007 Elsevier B.V. All rights reserved.

Keywords: Repaired shell damage; Scars; Zygochlamys patagonica; Fishing disturbance; Argentine Sea

1. Introduction

Conspicuous scars in shells are detected in manymolluscs. They are the result of a sub-lethal damage thathas subsequently been repaired. Several studies haveattempted to establish the factors that could producerepair of shell damage in different species (Checa,1993; Gaspar et al., 1994; Ramsay et al., 2000; Green-field et al., 2002; Cadée, 1999; Alexander and Dietl,

⁎ Corresponding author. CONICET, Consejo Nacional de Investi-gaciones Científicas y Técnicas, Buenos Aires, Argentina.

E-mail address: schejter@inidep.edu.ar (L. Schejter).

1385-1101/$ - see front matter © 2007 Elsevier B.V. All rights reserved.doi:10.1016/j.seares.2007.02.005

2001; Lomovasky et al., 2005 and references therein).Trawling and dredging activities are mentioned asimportant causes of shell scarring in the gastropodBuccinum undatum (Mensink et al., 2000), and in thebivalves Arctica islandica (Witbaard and Klein, 1994),Glycymeris glycymeris (Kaiser et al., 2000; Ramsayet al., 2000, 2001; Ramsay and Richardson, 2000),Ensis siliqua (Gaspar et al., 1994) and Ensis arcuatus(Robinson and Richardson, 1998). Ramsay et al. (2000)suggested that scarring in Glycymeris glycimeris couldbe used to differentiate between severely fished andlightly fished areas. It has also been suggested thatmarks on scallop shells provide information on the

Fig. 1. Zygochlamys patagonica beds in the Argentine Sea.

Table 1Scale used for the visual assessment of shell scars

Score Description

0 No scars1 Mild damage: 1 or 2 small scars2 Moderate damage: usually 1 larger scar, and also small scars3 Severe damage: several large scars, sometimes deforming

the shell

157L. Schejter, C. Bremec / Journal of Sea Research 58 (2007) 156–162

frequency of past fishing activities, and therefore couldbe used as indicators of the stock status (Caddy andDefeo, 2003). However, trawling and dredging activi-ties are not the only causes of shell scarring, and in manyspecies certainly not the major cause. Predation, bur-rowing processes, parasitism and physical events arealso important causes (Checa, 1993; Gaspar et al., 1994;Cadée, 1999; Alexander and Dietl, 2001; Richardson,2001; Ramsay et al., 2001; Lomovasky et al., 2005;Silina, 2006 and references therein). Unfortunately, it isnot always possible to ascertain what was the cause ofthe observed scars (Ramsay et al., 2000).

The Patagonian scallop Zygochlamys patagonica(King & Broderip, 1832) is distributed in the MagellanicBiogeographic Province, and it is the target species of arecent fishery in Argentina that started in 1996, alongthe 100 m isobath (Lasta and Bremec, 1998).

Repaired shell damage was always detected duringroutine monitoring cruises of the fishing grounds in theArgentine Sea. In the present paper we present results ofvisual inspection of shell scarring on Z. patagonica

from samples collected in 2003 in five beds, after sevenyears of commercial trawling. We compare and discussthese results with data regarding scallops collected in thesame areas in 1995, a year before the scallop fisherystarted.

2. Materials and methods

Scallops from Zygochlamys patagonica beds, situat-ed between 39° and 42° 30′ S on the 100 m isobath(Fig. 1), were examined in order to detect scarring on theshells. Samples came from a total of 67 sites. 2003

Fig. 2. An illustration of the damage scales used: 0, no damage; 1, mild damage; 2, moderate damage; 3, severe damage.

158 L. Schejter, C. Bremec / Journal of Sea Research 58 (2007) 156–162

samples were taken during the INIDEP monitoringcruises carried out in June and November, using a non-selective dredge in the SAO, SWSAO, Valdés, Tango Band Reclutas beds. Additionally, we analysed scallopsfrom three samples collected in Reclutas, one in SAO,one in SWSAO, two in Valdés and three in Tango Bbeds during exploratory cruises in 1995, before thescallop fishery started.

Epibionts were removed to facilitate the visualinspection of scars on shells. Presence of scars wasrecorded and the frequence (%) of occurrence in eachsample was estimated. Differences between areas wereassessed by examining the overlap between confidenceintervals (Schenker and Gentleman, 2001; Payton et al.,2003) of the scarring condition in % average. Althoughconservative, this method is useful as the information

Table 2Sampled area, number of Patagonian scallops analysed, average ofscarring (%), standard deviation and coefficient of variation in thestudy area in the commercial beds in 2003 and 1995 (pre-fishedcondition of the commercial beds) in the Argentine Sea

Area Mumberof scallops

Average ofscarring (%)

SD CV (%)

2003Reclutas 2837 20.66 0.74 3.58Sao 535 11.03 1.32 12.00SW Sao 5006 13.68 0.46 3.38Valdes 1093 22.32 1.13 5.04Tango B 887 15.34 1.20 7.801995Reclutas 488 37.15 1.92 5.17Sao 245 60.00 3.13 5.21SW Sao 195 29.70 3.27 11.02Valdes 293 63.30 2.81 4.45Tango B 383 46.22 2.54 5.50

needed to carry out a more appropriate procedure (suchas a statistical model or test) is unavailable.

The percentage of repaired shell damage in thedifferent size classes was also estimated from sub-samples from all scallop beds and both periods (1995and 2003). A qualitative scale for the visual assessmentof the shell damage was developed following Ramsayand Richardson (2000) in order to estimate the severityof the injuries suffered by the scallops (Table 1). Fig. 2illustrates scallop shells belonging to all scale catego-ries. To avoid subjectivity on damage level during vi-sual inspection (Ramsay and Richardson, 2000), allinspections were carried out by the same observer.Since the Z. patagonica fishery works with a commer-cial scallop size of Nor=55 mm we used this size tomake comparisons between shell damage proportionsin 1995 and 2003. Size structure of scallops in differentbeds and study periods are presented (INIDEP DataBase, Project Vieira Patagónica).

Fig. 3. Average of scarring (%) in the various Zygochlamys patagonicabeds. Bars show the confidence intervals calculated.

Fig. 4. Percentage of scallops with repaired shell damage in the varioussize categories and in both periods (1995 and 2003).

159L. Schejter, C. Bremec / Journal of Sea Research 58 (2007) 156–162

3. Results

A total of 11962 scallops, ranging from 5 to 90 mmtotal height, were sampled. Scallops N20 mm total shellheight were found to have scars. For a general analysiswe recorded single, multiple and/or deeper marks thatdeformed the shell (Table 1, Fig. 2) as a positive sign ofrepaired shell damage. These marks were very differentfrom gastropod drill holes or common growth ringsregistered in Zygochlamys patagonica. Table 2 sum-marises the number of tows and number of scallopssampled per bed and the percentage of scarred scallops.Average of scarring (%) during 2003 was similar in allstudy beds, although values were variable within eachbed; in general, mean values were b20%. The scallopscollected in 1995 showed the highest values of scarring(%), always ≥30%, reaching 63% in the Valdés bed.Differences between the same areas in 1995 and 2003were analysed by comparing the confidence intervals(Fig. 3). As shown in Fig. 3, the non-overlap of theconfidence intervals between the 1995 and 2003 samplesin the same bed (and as a whole) indicates differencesbetween these two scarring conditions.

In subsamples of 443 (1995) and 336 (2003) scallopsbelonging to all study beds repaired shell damage wasestimated for all size categories (Table 3, Fig. 4).Scallops N40 mm presented proportionally more scarsthan those b40 mm. No differences between the twostudy periods were detected considering the percentageof scallops with repaired shell damage. Although thesize structure of the whole population in 1995 and 2003is not reflected in the size structure of the subsamples,the proportions of repaired shell damage for each size

Table 3Scallops with repaired shell damage (all size categories) consideringthe damage scale from 0 (no damage) to 3 (severe damage), in bothstudy periods

Size/score

1995 2003

0 1 2 3 0 1 2 3

b15 7 0 0 0 0 0 0 015–19 1 0 0 0 0 0 0 020–24 8 0 0 0 1 0 0 025–29 19 2 0 0 8 3 0 030–34 19 2 0 0 13 2 0 035–39 24 7 5 1 8 3 3 140–44 21 13 8 0 19 5 5 045–49 21 9 15 1 14 16 16 250–54 20 13 21 5 23 10 21 155–59 20 12 40 7 43 7 18 360–64 12 12 17 6 22 3 18 465–69 6 7 20 8 9 5 12 8N69 9 1 12 12 3 0 3 4Total 187 78 138 40 163 54 96 23

category based in these subsamples could be applied tothe whole population (Cochran, 1977). Scallop sizedistribution (in %) per bed and total (INIDEP Data Base,Project Vieira Patagónica) for the two study periods isgiven in Fig. 5. It indicates (except in the Reclutas bedwhere abundant recruits were found in1995) that themean scallop population size was considerably higherin 1995. Higher levels of shell damage (moderate andsevere) were detected mostly in scallops having a com-mercial size during both study periods (Fig. 6, Table 3).

4. Discussion

We found scars on Zygochlamys patagonica shells inall samples from both sampling periods. In contrast towhat we expected, we registered the highest values ofscarring in pre-fishery conditions, when there were nodisturbances by scallopers. The scallop fishing activityincreased from 1996 to 2003, and removed 37000 t and43000 t of commercial (Nor=55 mm) and non-commercial sizes (discarded scallops b55 mm), respec-tively (Mario Lasta, pers. comm.). Witbaard and Klein(1994) found less shell scarring on Arctica islandicashells in areas intensively trawled and attributed theirresults to a higher mortality of individuals damaged afterthe trawling event. Vermeij (1983, in Alexander andDietl, 2001) hypothesised that some bivalves could havelow frequencies of shell repair because leakage ofmetabolites from damaged and/or marginally exposedmantle edges increased predator detection by means ofchemical molecules, allowing the prey to be eaten evenwhen the fractured valves are closed. Although thePatagonian scallops showed high survival rates (nearly96%) after a single trawling event (Bremec et al., 2004),the experiments were performed with non-damagedindividuals, not exposed to predators. The consequencesof repeated trawling on scallops with different levels ofshell damage or on fragile recruits and young specimensare unknown. Recovery of the scallops from a sub-lethal

Fig. 5. Scallop size structure (in %) per bed and total (taken from INIDEP Data Base, Project Vieira Patagónica) in 1995 and 2003.

160 L. Schejter, C. Bremec / Journal of Sea Research 58 (2007) 156–162

injury depends not only on the level of damage, but alsoon their own protection against predators and scaven-gers after the injury and during the shell reparation time.The lower frequency of repaired shell damage registered

Fig. 6. Percentage of commercial and non-commercial scallops(≥55 mm and b55 mm, respectively) with the levels of damageconsidered, from 0 (no damage) to 3 (severe damage).

at the fishing grounds during 2003 could be partiallyrelated with the fragility and vulnerability of this scal-lop, characterised by its thin shell (Zelaya and Schejter,2001).

It is remarkable that the Patagonian scallop popula-tion average size was 60–65 mm in 1995 and 55 mm in2003 (INIDEP Data Base, Project Vieira Patagónica, S.Campodónico, pers. comm.). The selective removal ofcommercial individuals could in part explain theseresults, as the majority of bigger scallops with thickershells always presented repaired shell damage (mostlymoderate and severe damage), and this fraction of thepopulations was more abundant in 1995. In contrast,smaller scallops presented principally no damage ormild damage, with fewer scallops showing moderatedamage, and only exceptionally severe damage. Scal-lops b40 mm could be more vulnerable to shell damageand probably do not recover from moderate or severedamage, but only from minor damage, as our resultsshow. The fraction of the medium and bigger (thicker)scallops that remains on the bottom could probablyrecover from their injuries, but smaller specimens

161L. Schejter, C. Bremec / Journal of Sea Research 58 (2007) 156–162

probably die from the injuries, because of predators andscavengers, or because of their low shell repair capacity.

Scallops collected in 1995 had not been exposed toscallop fishery. However, scallop fishing grounds over-lap with areas in the Argentine Sea where demersal fishhave been long been exploited (Cousseau and Perrota,1998; Bezzi et al., 2000; Sánchez and Bezzi, 2004).This activity, although not assessed, could have disturb-ed benthic organisms in various ways. However, thesetrawling events target demersal fishes and do not in-tensively exploit scallop patches. Moreover, scallopsof all sizes, not only those b55 mm, are discarded dur-ing demersal fishery. In consequence, the shell damagefound in scallops collected in 1995 could be attributednot only to predation but also to several trawling eventsnot related with scallop fishery. It is also possible thatbigger (older) scallops accumulate scars of shell repairduring their longer lifetime, and hence only big scallopspresent moderate or severe damage.

Richardson (2001) and Ramsay et al. (2001)discussed the difficulty of identifying with certaintygrowth breaks arising from fishing disturbance, predatorattacks and the bivalves’ own natural activities (mainlyburrowing behaviour). This latter origin of scars isimprobable in Zygochlamys patagonica, which presentsa high number of filter-feeding invertebrates encrustingboth shells (Schejter and Bremec, 2006). Trophic studiesby means of stable isotope analysis indicate that somegastropods and echinoderms do prey on Patagonianscallops (Botto et al., 2006). In any case, their feedingstrategy (Ciocco and Orensanz, 2001) would not damagethe shells. We think that fishes could potentially causeshell damage, as scallops form the diet of some species(Callorhynchus callorynchus, Congiopodus peruvianus,Pseudopercis semifasciata) in Patagonia (Ciocco andOrensanz, 2001; González, 2002). Additionally, twonotothenioids from theMalvinas Islands (Patagonotothenand P. ramsayi) are known to feed on discarded damagedPatagonian scallops (Laptikhovsky, 2004), and rests offishery discards were recently found during gut contentanalysis of P. ramsayi (J. Pello, pers. comm.).

In conclusion, we found higher levels of scarringunder the pre-fishery conditions. The scallop fisheryremoves the fraction of the population (larger indivi-duals) with high probability of repaired shell damage.The higher percentage of scarring in 1995 can beexplained by the average scallop size, remarkablyhigher in all beds than in 2003, excluding Reclutas.Regarding the specimens of smaller sizes, thrown backinto the sea during processing on board, futureinvestigations are needed to properly assess levels ofsurvival.

Acknowledgements

We would like to thank Ángel Marecos and MónicaDi Pace for help with the sampling, Daniel Hernándezfor statistical assistance, Silvana Campodónico forproviding the data base of scallop size frequencies,and Gerhard C. Cadée and two anonymous reviewerswhose critical suggestions contributed to improving thismanuscript. This work was partially supported by grantsAntorchas Foundation n° 13900–13, FONCyT Pict2003, 01–15080 and CONICET PIP 5009. This isINIDEP Contribution N° 1430.

References

Alexander, R.R., Dietl, G.P., 2001. Shell repair frequencies in NewJersey bivalves: a recent baseline for tests of escalation withtertiary mid-Atlantic congeners. Palaios 16, 394–371.

Bezzi, S., Akselman, R., Boschi, E. (Eds.), 2000. Síntesis del estado delas pesquerías marítimas argentinas y de la cuenca del Plata. Años1997–1998, con una actualización de 1999. Publicaciones espe-ciales INIDEP, Mar del Plata. 388 pp.

Botto, F., Bremec, C., Marecos, A., Schejter, L., Lasta, M., Iribarne, O.,2006. Identifying predators of the SW Atlantic Patagonian ScallopZygochlamys patagonica using stable isotopes. Fish. Res. 81, 45–50.

Bremec, C.S., Lasta, M.L., Hernández, D., 2004. Survival of Pata-gonian scallop (Zygochlamys patagonica, King & Broderip, 1832)after the size selection process on comercial fishing vessels. Fish.Res. 66, 49–52.

Caddy, J.F., Defeo, O., 2003. Enhancing or restoring the productivityof natural populations of shellfish and other marine invertebrateresources. FAO Fish. Tech. Paper, vol. 448. 159 pp.

Cadée, G.C., 1999. Shell damage and shell repair in the Antarctic limpetNacella concina from King George Island. J. Sea Res. 41, 149–161.

Checa,A., 1993.Non-predatory shell damage in recent deep-endobenthicbivalves from Spain. Palaeogeogr. Palaeoclimatol. Palaeoecol. 100,309–331.

Ciocco, N.F., Orensanz, J.M., 2001. Depredación. In: Maeda-Martínez, A.N. (Ed.), Los Moluscos Pectínidos de Iberoamérica:Ciencia y Acuicultura. McGraw-Hill, México, pp. 267–283.

Cochran, W.G., 1977. Sampling proportions and percentages, In:Cochran, W.G. (Ed.), Sampling Techniques, 3rd ed. Wiley & Sons,New York, pp. 50–72.

Cousseau, M.B., Perrota, R.G., 1998. Peces Marinos de Argentina:Biología, distribución y pesca. Publicaciones Especiales INIDEP,Mar del Plata. 163 pp.

Gaspar, M.B., Richardson, C.A., Monteiro, C.C., 1994. The effects ofdredging on shell formation in the razor clam Ensis siliqua fromBarrinha, Southern Portugal. J. Mar. Biol. Assoc. UK 74, 927–938.

González, R., 2002. Alimentación del salmón de mar Pseudopercissemifasciata (Cuvier, 1829) en el Golfo San Matías. IBMP Ser.Publ., vol. 1, pp. 23–34.

Greenfield, B.K., Lewis, D.B., Hinke, J.T., 2002. Shell damage in saltmarsh periwinkles (Littoraria irrorata (Say, 1822)) and resistanceto future attacks by blue crabs (Callinectes sapidus (Rathbun,1896)). Am. Malacol. Bull. 1–2, 141–146.

Kaiser, M.J., Ramsay, K., Richardson, C.A., Spence, F.E., Brand, A.R.,2000. Chronic fishing disturbance has changed shelf sea benthiccommunity structure. J. Anim. Ecol. 69, 494–503.

162 L. Schejter, C. Bremec / Journal of Sea Research 58 (2007) 156–162

Laptikhovsky, V.V., 2004. A comparative study of diet in three sym-patric populations of Patagonotothen species (Pisces: Notothenii-dae). Polar Biol. 27, 202–205.

Lasta, M., Bremec, C., 1998. Zygochlamys patagonica in the ArgentineSea: A new scallop fishery. J. Shellfish Res. 17, 103–111.

Lomovasky, B.J., Gutierrez, J.L., Iribarne, O.O., 2005. Identifyingrepaired shell damage and abnormal calcification in the stoutrazor clam Tagelus plebeius as a tool to investigate its ecologicalinteractions. J. Sea Res. 54, 163–175.

Mensink, B.P., Fischer, C.V., Cadée, G.C., Fonds, M., Ten Hallers-Tjabbes, C.C., Boon, J.P., 2000. Shell damage and mortality in thecommon whelk Bucciunum undatum caused by beam trawlfishery. J. Sea Res. 43, 53–64.

Payton, M.E., Greenstone, M.H., Schenker, N., 2003. Overlappingconfidence intervals or standard error intervals: what do they meanin terms of statistical significance? J. Insect Sci. 3 (34) (6 pp.).

Ramsay, K., Richardson, C.A., 2000. Techniques for assessingrepaired shell damage in dog cockles Glycymeris glycymeris L.J. Shellfish Res. 19, 927–931.

Ramsay, K., Kaiser, M.J., Richardson, C.A., Veale, L.O., Brand, A.R.,2000. Can shell scars on dog cockles (Glycymeris glycymeris L.) beused as an indicator of fishing disturbance? J. Sea Res. 43, 167–176.

Ramsay,K., Richardson, C.A.,Kaiser,M.J., 2001. Causes of shell scarringin dog cockles Glycymeris glycymeris L. J. Sea Res. 45, 131–139.

Richardson, C.A., 2001. Molluscs as archives of environmental change.Oceanogr. Mar. Biol. Ann. Rev. 39, 103–164.

Robinson, R.F., Richardson, C.A., 1998. The direct and indirect effectsof suction dredging on a razor clam (Ensis arcuatus) population.ICES J. Mar. Sci. 55, 970–977.

Sánchez, R.P., Bezzi, S.I. (Eds.), 2004. El Mar Argentino y sus re-cursos pesqueros. Tomo 4. Los peces marinos de interés pesquero.Caracterización biológica y evaluación del estado de explotación.Publicaciones especiales INIDEP, Mar del Plata. 359 pp.

Schejter, L., Bremec, C., 2006. Benthic richness in scallop beds -Zygochlamys patagonica (King and Broderip, 1832) as primarysettlement substrate. J. Shellfish Res. 25 (1), 305.

Schenker, N., Gentleman, J.F., 2001. On judging the significance ofdifferences by examining overlap between confidence intervals.T.A.S. 55, 182–186.

Silina, A.V., 2006. Tumor-like formations on the shells of Japanesescallops Patinopecten yessoensis (Jay). Mar. Biol. 148, 833–840.

Vermeij, G.J., 1983. Traces and trends of predation, with specialreference to bivalved animals. Palaeontology 26, 455–465.

Witbaard, R., Klein, R., 1994. Long-term trends on the effects of thesouthern North Sea beamtrawl fishery on the bivalve molluscArctica islandica L. (Mollusca, bivalvia). ICES J. Mar. Sci. 55,99–105.

Zelaya, D., Schejter, L., 2001. Shell composition of Zygochlamyspatagonica (King & Broderip, 1832) along a latitudinal gradient.13th Int. Pect. Work., Coquimbo, p. 175.