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Marine Environmental Research 108 (2015) 91e99

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Marine Environmental Research

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Endoliths in Lithophaga lithophaga shells e Variation in intensityof infestation and species occurrence

Melita Peharda a, *, Barbara Calcinai b, Sanja Puljas c, Stjepko Golubi�c d, Jasna Arapov a,Julien Th�ebault e

a Institute of Oceanography and Fisheries, �Setali�ste Ivama Me�strovi�ca 63, 21000 Split, Croatiab Polytechnic University of Marche, Department of Life and Environmental Sciences, Via Brecce Bianche, 60131 Ancona, Italyc Faculty of Science, University of Split, Teslina 12, Split, Croatiad Boston University, Biological Science Center, 5 Cummington Street, Boston, MA 02215-2406, USAe Universit�e de Brest, Institut Universitaire Europ�een de la Mer, Laboratoire des Sciences de l'Environnement Marin (LEMAR UMR6539 UBO/CNRS/IRD), rueDumont d'Urville, 29280 Plouzan�e, France

a r t i c l e i n f o

Article history:Received 8 March 2015Received in revised form4 May 2015Accepted 9 May 2015Available online 12 May 2015

Keywords:Coastal zoneMarine ecologyAdriatic SeaMediterraneanSclerochronologyEutrophication

* Corresponding author.E-mail address: melita@izor.hr (M. Peharda).

http://dx.doi.org/10.1016/j.marenvres.2015.05.0020141-1136/© 2015 Elsevier Ltd. All rights reserved.

a b s t r a c t

Pronounced differences with respect to the extent of infestation and the degree of Lithophaga lithophagashell damage inflicted by euendolithic taxa at two sites in the Adriatic Sea representing different pro-ductivity conditions, are described. Shells collected from the eastern part of Ka�stela Bay, which ischaracterized by higher primary productivity, have significantly more shell damage then the shellcollected from a site on the outer coast of the island of �Ciovo exposed to the oligotrophic Adriatic Sea. Thepresence of endoliths and their perforations were detected in different layers of the shell, includingsolidly mineralized parts of the skeleton and within the organic lamellae incorporated into the shell.Phototrophic endoliths were not observed in the specimens. The most serious damage to L. lithophagashells was the boring clionaid sponge Pione vastifica, which was more common in shells collected fromKa�stela.

© 2015 Elsevier Ltd. All rights reserved.

1. Introduction

The European date mussel Lithophaga lithophaga (Linnaeus,1758) is an actively boring endolithic bivalve inhabiting mostlyshallow waters along the entire Mediterranean coast (Fisher et al.,1987; Poppe and Goto, 2000). The species lives inside galleriesbored in calcareous rock by glandular secretions from the mantle(Morton and Scott, 1980). It is an ecologically important speciesbecause of its characteristic limestone penetrating life style as wellas due to concerns about illegal harvesting that necessarily involvesthe destruction of the coastal habitats it occurs in.

Although subject of several studies, the ecology of L. lithophaga isstill poorly known. Studies conducted on this species primarilyexamined those aspects of L. lithophaga biology related eitherdirectly or indirectly to fisheries, because L. lithophaga is regarded asa food source. These include analyses of its population structure and

settlement (�Simunovi�c and Grubeli�c, 1992; Galinou-Mitsoudi andSinis, 1995, 1997a; Devescovi and Ive�sa, 2008), reproduction (Valliet al., 1986; �Simunovi�c et al., 1990; Galinou-Mitsoudi and Sinis,1994, 1997b; Jaafar Kefi et al., 2014) and different aspects of tissuecontamination (Dujmov and Su�cevi�c, 1990; Deudero et al., 2007;Jaafar Kefi et al., 2012a, 2012b; Ozsuer and Sunlu, 2013). More than20 years ago, however, Fanelli et al. (1994) warned that the recoveryof exploited stocks of L. lithophagamaybe slow. L. lithophaga exhibitshigh variation in growth rates between individuals and can live forover 54 years (Galinou-Mitsoudi and Sinis, 1995; Peharda et al.,unpublished data). Several recent studies have addressed theanthropogenic impact on L. lithophaga habitat (e.g. Fanelli et al.,1994; Devescovi et al., 2005; Paravicini et al., 2010; Guidetti, 2011).

Due to its longevity as well as its size of up to 90 mm,L. lithophaga itself presents an available substratum for settlementof other organisms. In recent studies Jaafar Kefi et al. (2012a, b)observed boring annelids and sipunculids in the shells ofL. lithophaga and linked these observations with disturbances inshell growth. In addition to organisms settling on the outer shellsurface of bivalves, the settlement and impact of macro- andmicro-

M. Peharda et al. / Marine Environmental Research 108 (2015) 91e9992

boring organism has been described for a number of species(Kaehler andMcQuaid,1999; Radtke and Golubic, 2005; �Curin et al.,2014). Micro-boring organisms or euendoliths (Golubi�c et al., 1981)penetrate carbonate substrata by either chemical or mechanicalmechanisms, and are able to disrupt them by forming numerousboreholes, tunnels and galleries. When settling on mollusc shells,they can cause substantial damage (Kaehler and McQuaid, 1999;Thomas, 2000; Trigui El-Menif et al., 2005; �Curin et al., 2014).

Eundoliths comprise different taxa including cyanobacteria(Webb and Korrûbel,1994; Kaehler andMcQuaid,1999), green algae(Radtke and Golubic, 2005), fungi (Golubi�c et al., 2005), sponges(Rosell and Uriz, 2002), polychaetes (Moreno et al., 2006; Riascoset al., 2008), as well as other bivalves (Schiaparelli et al., 2005).Shells of Lithophaga, likeothermolluscs, containmineral andorganicmatrices (Kobayashi and Samada, 2006), which are penetrated byeuendoliths and may in part serve as an energy source to them.

Biotic and abiotic factors strongly influence bioerosion. How-ever, bioerosion rates are not constant over time and space anddepend, among other factors, on invertebrate and fish grazing,sedimentation, nutrient concentration, eutrophication levels (Risket al., 1995) and on substratum density and mineralogy(Sch€onberg, 2002; Calcinai et al., 2007, 2008). It may vary, more-over, in accordance with the variability inherent in larval recruit-ment and to the successional phases of the boring community(Hutchings, 1986). Several studies have demonstrated that bio-erosion by both micro- and macro-borers is enhanced by an in-crease in nutrients and particulate organic matter (POM) (Rose andRisk, 1985; Hallock and Schlager, 1986; Hallock, 1988; Holmes,2000; Fabricius, 2005). Carreiro-Silva et al. (2005, 2009, 2012)have clearly demonstrated that inorganic nutrients strongly con-trol the erosion rates caused by micro-borers such as cyanobacteriaand green algae. According to Highsmith (1980), boring bivalves aremore abundant in areas with higher plankton productivity. Themain objectives of the present study were to: (i) describe the in-tensities of euendolith infestation of L. lithophaga shells in theAdriatic Sea, at two sites representing different productivity con-ditions; (ii) identify the euendolithic taxa and (iii) explain thepossible causalities if differences in euendolith infestation wereapparent. The main goal of this project, however, was to evaluatethe potential of L. lithophaga as an archive of data on variations inenvironmental conditions, especially with reference to marinepollution and different levels of primary production.

2. Materials and methods

Individual specimens of L. lithophagawere collected on 2nd July2013 and 20th June 2014 by SCUBA on two sites in the Adriatic Sea:The first site (Site 1) was located on the south-eastern side of theisland of �Ciovo (43.483611�N, 16.365556�E) and L. lithophaga werecollected from 2 to 3 m depth here. The second site (Site 2) waslocated on the eastern part of Ka�stela Bay (43.535833�N,16.448056�E), where L. lithophaga were collected from 1 to 2 mdepth. Although the two sampling sites are geographically close,they are ecologically different. Site 1 is located in an un-populatedarea exposed to the open waters of the Adriatic Sea, and is char-acterized by oligotrophic conditions. In contrast, Site 2 is located inKa�stela Bay in the vicinity of urban, agricultural and industrialprocesses with water quality characterized by increased eutrophi-cation (Nin�cevi�c Gladan et al., 2010). In order to obtain data on theproductivity of the sampling sites, water samples were collectedtwice each month over a one year period from the surface layer todetermine chlorophyll a concentrations (chl a). Exceptions wereAugust and November 2013 when only one sample was collected.Samples (400 mL) were filtered through a glass microfibre filter(Whatman GF/F) and then frozen at �18 �C to await analysis. Chl a

was extracted in 90% acetone, and fluorescence was measured us-ing a TURNER TD-700 fluorometer and determined using themethod of Strickland and Parsons (1972). Differences in chl a con-centrations between sites were analysed using a paired t-test. Priorto the analysis, data were tested for homogeneity of variance usingLevene's test and log transformed.

After collection, L. lithophaga individuals were brought to thelaboratory where their tissues were separated carefully from theshell and shells were either preserved in 4% formaldehyde or left toair dry to be stored for later laboratory analysis. Shell size wasselected at random for analysis and ranged from 30.6 to 93.6 mmfor Site 1 (mean ± st.dev. ¼ 61.84 ± 13.29, N ¼ 83) and from 42.0 to91.0 mm for Site 2 (mean ¼ 66.90 ± 10.32 mm, N ¼ 103).

Shell structure was observed using petrographic thin sections.Calcite is present just below the periostracum, while the inner shelllayer is composed of aragonite (Harper unpublished data). Euendo-lith infestationwasdetectedmacroscopicallybychanges ineither thelocal thickening of the shells or by discoloration (white appearance)on the internal shell surface. Euendolith infestation intensity wasassignedanumberona subjective scale, ranging from0 to5modifiedfrom �Curin et al. (2014), where 0 described visually uninfected shellsand 5 heavily infected ones (Fig. 1). Each shell was assigned anidentificationnumberandphotographed fromthe insideandoutside.The photographs were saved and catalogued for later analysis. Thedegree of infestationwas related to shell size and location.

The presence of microbial euendoliths was analysed using threedifferent approaches: (i) exposing euendoliths by dissolving theshell; (ii) assessing the abundance of borings by direct SEM offractured shells and (iii) replicating the micro-borings in poly-merizing resins (Golubi�c et al., 1970, 1975).

(i) Fragments of six shells collected in July 2013 from Site 2 wereplaced in 10% hydrochloric acid (HCl) in order to remove thecarbonate substratum. Following decalcification, organicparts of the shell and endoliths were placed on microscopeslides and observed using light microscopy (Axio ZeissImager M1). In addition, fragments of ten shells collectedfrom Sites 1 and 2 in June 2014 were analysed using theabove procedures.

(ii) Dry shell fragments of six L. lithophaga shells collected in July2013 were prepared for scanning electron microscopy (SEM).In order to reveal changes in shell structure, shell fragmentswere examined with and without etching; these shell frag-ments were both freshly fractured and/or treated with 2%hydrochloric acid (HCl). The treated samples were washed intap water and dried; the samples were placed on stubs,sputter coated with gold and observed using a Philips XL 20SEM. These pictures were taken to test how endoliths influ-ence the formation of shell layers in infested and non-infested individuals and their distributions inside the shell.

(iii) Resin casts of the micro-borings were prepared, followingGolubi�c et al. (1970), from the shell fragments of six shells.Shell fragments were embedded in EMBed-812 (EMS Catalog#14120) under a vacuum. Following polymerization, thesamples were sectioned with a diamond saw and treatedwith 2% HCl solution for a few minutes followed byfrequently changed hypochlorite bleach for several days toremove inorganic and then organic parts of the shell.Exposed resin casts of micro-borings were sputter coatedwith gold and observed by SEM.

3. Results

Pronounced differences were observed in chl a concentrationsbetween sampling sites (paired t¼ 5.94, p < 0.001). At Site 1 (�Ciovo)

Fig. 1. Categories of euendolith infestation of Lithophaga lithophaga shell: A. Shell classified as slightly damaged disturbances visible only in area near umbo (category 1); B. Damagevisible in the area near umbo as well as toward the central part of the shell (category 2); C. White patches visible in different parts of the shell (category 3); D. The shell is deformed,most of the inner surface covered in patches (category 4); E. Heavily infested and fragile shell (category 5). Scale bar is 1 cm in all photographs.

M. Peharda et al. / Marine Environmental Research 108 (2015) 91e99 93

chl a values ranged from 0 to 1.09 mg/m3 (mean ±-st.dev ¼ 0.29 ± 0.25 mg/m3). The lowest values were recorded inJuly and August, 2013, while the highest ones were in midDecember, 2013 and at the beginning of January, 2014 (Fig. 2). AtSite 2 (Ka�stela), the chl a values were significantly higher andranged from 0.12 to 1.54 mg/m3 (mean ± st.dev ¼ 0.83 ± 0.42 mg/m3). High chl a values were recorded over an extended period fromMarch to June, 2014.

Changes in the colour and the occurrence of white patches andblisters on the interior surface of shells collected in 2013 have beenused for evaluating the extent of the endolith impact onL. lithophaga. Over 94% of the analysed individuals from Site 1 hadsome alterations in shell structure that could be attributed toendoliths, whereas at Site 2 most shells were damaged heavily andonly one shell was obtained that had no macroscopically visiblealterations.

Shells collected from the two study sites differed significantlywith respect to the degree of damage by euendolith infestation(Fig. 3). At the oligotrophic Site on �Ciovo, 52 shells (out of 83collected) could be classified with damage within the categories 1and 2, 80 were classified under the category 3, while only 3 wereclassified as heavily damaged under category 4; no shells were

Fig. 2. Chlorophyll a concentrations (mg/m3) at �Ciovo location (Site 1, grey bars) andKa�stela bay (Site 2, black bars). Data collected twice per month in a period from July2nd 2013 and June 20th 2014.

damaged to the level of the category 5. In contrast, at Site 2, inKa�stela Bay, characterized by more eutrophic conditions, the situ-ation was reversed. Only 8 shells (out of 103 collected) were clas-sified as slightly damaged (categories 1 and 2), 19 were classifiedunder category 3, while 75% were classified under categories 4 and5. In fact, at that site, the dominant classification categorywas 5 andaccounted for 40% of the collected shells.

The presence of endoliths and their perforations was detected indifferent layers of the shell, including solidly mineralized parts ofthe skeleton and within organic lamellae incorporated into theshell. Damage to the periostracum is assumed to be largely me-chanical, however, patches of periostracum discoloration observedat low magnification indicated the effect of some bacterial infec-tion. Upon dissolution of the shell and microscopic investigation,the discolored patches showed a rough surface and loosened per-iostracal fibres, indicating destructive enzymatic activity, but thepresence of bacteria that may have caused such damage at the timeof collection was not observed (see Hook and Golubi�c, 1990).

The presence of euendoliths and their perforations was detectedin different layers of the shell, frequently located in the layerimmediately below the periostracum (Fig. 4, arrow), but also insolidly mineralized regions as evident from SEM images of frac-tured surfaces (Fig 5, arrow). They appear to be boring both theorganic and inorganic parts of the shell. Tubular borings replicatedin resin are observed by SEM as a planar networks, distributedparallel to the periostracum (Fig. 6A), or spread over the surfaces ororganic lamellae (Fig. 6B). Their distribution could be observedafter the resin replicas are exposed by dissolving the shell car-bonate around them. The organic lamellae may be loosened usinghypochlorite bleach. The tunnels are irregular in outlines, repeat-edly branched and variable in diameter between 0.8 and 2 mm. TheResin replicas of boring networks are clearly distinct from repli-cated structural pores of the shell, which are straight, runperpendicular to the shell surface and are an order of magnitudenarrower then the microboring tunnels. In contrast, the micro-borers are consistently associated with organic lamellae in the shelland often distributed inside the lamella (Fig. 7A) or growing alongthe lamellar surface (Fig. 7B). The appearance of these micro-borings in terms of filament diameters, branching and their dis-tributions in the shells was similar in specimens collected fromboth sites. Their distributions along andwithin the organic lamellae

Fig. 3. Incidence of shell damage by euendoliths in L. lithophaga shells collected at �Ciovo location (Site 1) and Ka�stela bay (Site 2) by the categories of infestation intensity (see Fig. 1).

Fig. 4. Petrographic section of L. lithophaga shell observed under polarized microscopeshowing the appearance of different shell layers. Arrow indicates periostracum. Scalebar 200 mm.

Fig. 5. SEM image of fractured L. lithophaga shell showing m

M. Peharda et al. / Marine Environmental Research 108 (2015) 91e9994

and the absence of photosynthetic pigments support the assump-tion that these microborers are organotrophic and of probablefungal affinity. Those endoliths that are distributed just below theperiostracum have been observed both by light microscopy and onSEM images (Fig. 7).

Differences were observed with respect to coloration, withsamples from Ka�stela (Site 2) being characterized by periodicbrown widening. The fungal traces of either Polyactina araneolaRadtke 1991 (produced by the fungus Conchyliastrum enderiZebrowski) or Flagrichnus profundus Wisshak and Porter, 2006(produced by the chytrid fungus Schizochytrium), were observedonly in shells collected from Site 1 at �Ciovo (Fig. 8). The traces wereunfortunately incomplete and did not include completemorphology needed to distinguish between the above taxa. Pho-totrophic endoliths were not observed in the analysed specimens.None of the above microbial euendoliths produced any seriousimpact on shell structure.

The most serious damaging impact on the shells of L. lithophaga,which also accounted for the substantial difference between thetwo compared sites was due to the presence and boring activity ofthe clionaid sponge Pione vastifica, which was common in shellscollected at Site 2 (Ka�stela). Pionewas not observed in L. lithophagasamples collected from Site 1 (�Ciovo). This species was observedboth by SEM and light microscopy. The damage caused toL. lithophaga shells was extensive, as illustrated in Fig. 8. This

icroboring infestation (white arrow). Scale bar 50 mm.

Fig. 6. SEM image of resin-casts microboring in L. lithophaga, caused most likely byeuendoliths of fungal affinity. Specimens were slightly etched in hydrochloric acid andtreated with sodium hypochlorite. A. Network of euendolith traces that appears to bejust below the periostracum in side view. B. Network of traces in plane view. Scale barsare 10 mm long.

Fig. 7. SEM image of L. lithophaga shell dissolved in hydrochloric acid revealing organiclayers with euendoliths. A. Organic lamella with euendolith traces within and on top ofthe structure; scale bar 100 mm. B. Microboring casts over the surface of an organiclamella; scale bar 10 mm.

M. Peharda et al. / Marine Environmental Research 108 (2015) 91e99 95

sponge initially excavated the shell and remained close to the outersurface, connecting itself to water through papillary channels. Thesponge galleries then expand deeper and may be located indifferent parts of the shells, including outer, middle and inner shelllayers (Fig. 9A, B). Clionaid sponges remove carbonate in smallchips leaving concave traces of individual ‘bites’ (Fig. 9C). Thecontact interface between the sponge and shell carbonate showsthat the process of surface carbonate removal involves dissolution,leaving fine etch-marks that replicate the network of the inter-crystalline boundaries.

The bivalve Rocellaria dubia (Pennant, 1777) was observedboring L. lithophaga shells collected at both sites (Fig. 10). Only 3(4%) of L. lithophaga shells collected from �Ciovo contained endolithR. dubia, however, whereas 38 (37%) of those collected from Ka�stelacontained this endolithic bivalve in their shells. Furthermore, a totalof seven L. lithophaga from Ka�stela contained two or three R. dubiain their shells. Due to its shell length, that can be >5 mm, and therelatively thin shell of L. lithophaga, R. dubia boreholes extendthrough all shell layers of its host and cause pronounced distur-bances to shell structure.

4. Discussion

In the present study, pronounced differences in shell damagewith respect to sampling site has been identified, with shellscollected from the eastern part of Ka�stela Bay, which is character-ized by more eutrophic conditions, showing more damage. Due tothe relatively slow water renewal time in Ka�stela Bay, especially

during warmer parts of the year, there is a limited exchange ofmarine organisms, including potential endoliths, between the twosampling sites. According to Zore-Armanda (1980), the averagewater renewal time in Ka�stela Bay varies with respect to environ-mental conditions, from about one month to as short as five days inperiods with strong wind conditions. During the warm period ofthe year (July to September) wind forcing is relatively weak andfreshwater inflow is low, due to which the renewal time is longerespecially in the eastern part of the bay (Zore-Armanda, 1980)where our sampling site was located. These conditions are alsoresponsible for increased coastal primary production that remainslocalized in an overall oligotrophic sea. Such pronounced differencein environmental conditions produce different selective pressureon organisms including endoliths and their hosts.

Two common morphs of calcium carbonate occur in bivalveshells, namely aragonite and calcite (Carter, 1980). According toHarper (unpublished data) both calcite and aragonite are present inL. lithophaga shells: calcite occurring in a layer immediately belowthe periostracum while the aragonite is present in the inner shelllayer. The periostracum is the layer of sclerotinized protein, whichcovers the exterior of the calcified shell of all bivalve species, and isof variable character (Harper, 1997). According to the same author,particularly thick periostracum is characteristic of bivalves thatchemically bore into hard substrata and those that burrow deeplywithin the sediment. For species that chemically bore into a sub-stratum, a thick periostracum serves as protection from their ownboring secretions (Taylor and Kennedy, 1969).

It is generally assumed that abrasion and/or corrosion duringboring activity damage the periostracum and the underlying shell.

Fig. 8. SEM image of fungal trace found penetrating the shell of L. lithophaga. Prepa-ration as resin casts etched out by hydrochloric acid. Scale bar 20 mm.

Fig. 9. The boring sponge Pione vastifica in the shells of L. lithophaga collected inKa�stela bay. A. Shell fragment with a large borings caused by the sponge that extendingthrough all shell layers; scale bar 1 mm; B. Detail of A, showing sponge spicules in thecollapsed sponge tissue; scale bar 200 mm; C. Resin-cast sponge “bites”; scale bar10 mm.

M. Peharda et al. / Marine Environmental Research 108 (2015) 91e9996

In spite of that, no fatal shell damage seems to occur in boringmytilids and it is possible that organic sheets, often observed in theinner shell layers, prevent lethal damage (Owada, 2009). Thisauthor, who analysed two species of Lithophaga, Lithophaga anti-llarum and Lithophaga nigra, did not find evidence of organic sheetsin the inner shell layer. In contrast, we found significant numbers oforganic lamellae embedded in the L. lithophaga shell and revealedby etching of petrographic sections of the shell by hydrochloricacid.

There are few studies looking at the energetic cost of replacingshell loss due to erosion. According to Day et al. (2000), compen-sation for shell erosion is an ongoing process involving a long-termcost. Molluscs may continually lay down shell to counter erosionand such compensatory deposition may increase with age. Thin-ning due to erosion may also make shells fragile, with potentiallylethal consequences. The energetic cost of replacing shell loss dueto erosion has been overlooked in previous research on molluscanenergy budgets, although several studies have shown that shellbreakage incurs a significant short-term cost and may reducegrowth. According to Kaehler and McQuaid (1999) endoliths have astrong effect on the allocation of energy in molluscs. These authorsshowed that infested Perna perna (Mytiloidea) had heavier shellsthan uninfected ones. Similarly, Barthel et al. (1994) found slightlyhigher weight of heavily perforated Chlamys islandica shells prob-ably due to repairs of perforation by carbonate. Similar response tufungal attack has been described in hermatypic corals (Further-more, Kaehler and McQuaid (1999) showed that infested musselsallocated less energy to reproduction). The impact of endoliths ongrowth, condition index and reproductive capacity of L. lithophagashould be examined in future studies. Endoliths present in theshells of L. lithophaga reflect a limestone boring life style of theirhost. L. lithophaga is a known suspension feeding organism and soare the most damaging endoliths, including the boring sponge, P.vastifica and the boring bivalve R. dubia. The microbial euendolithsobserved were almost exclusively organotrophes of fungal affinity,which managed to parasitize the organic components of the shellbut inflicted little damage to the host. The absence of phototrophiceuendolithic cyanobacteria and algae, which are known to inflictserious structural damage to non-boring mytilids (�Curin et al.,2014) is due to the circumstance that the micro-borers in theshells of Lithophaga can be considered to live in almost aphoticconditions. Although these shells were collected in shallow habi-tats, there is limited light penetration into holes made byL. lithophaga.

P. vastifica is an excavating sponge widespread in the Mediter-ranean and North Atlantic Ocean. It produces red, dull-orange,

coloured small papillae (<1 mm in diameter) and small erosionchambers (Rützler, 2002). This species can excavate variouscalcareous substrata, but it is frequently recorded in mollusc shells.Barthel et al. (1994) have shown that the population of the edible C.islandica is infested heavily by P. vastifica; nearly 90% of the studiedscallops being bored by this sponge. In contrast to other findings,however, P. vastifica seems not to decrease the development ofC. islandica mainly because this species showed a higher growthrate in comparison to the lowgrowth rate of P. vastifica. Consideringthe low growth rates of L. lithophaga, however, any infestation byP. vastificamay strongly damage the shell of this species and pose asignificant hazard to the host. Excavating sponges have been

Fig. 10. L. lithophaga shell with boring of Rocellaria dubia passing through all shell layers. A siphonal holes of R. dubia on external shell surface of L. lithophaga, B. shell disturbancesassociated with R. dubia presence and visible on the inner shell surface of L. lithophaga (white arrow). Scale bar 1 cm.

M. Peharda et al. / Marine Environmental Research 108 (2015) 91e99 97

identified as potential threats to pearl oysters in Australia (Fromontet al., 2005) and Mexican Pacific coral reefs (Bautista-Guerreroet al., 2014).

The high infestation of L. lithophaga shells in Ka�stela Bay due tothe presence of P. vastifica may be the result of locally high level oforganic pollution as well as of higher influx of inorganic nutrientsand the associated increase in primary production. These condi-tions are known to encourage any boring community, especiallyfavouring filter-feeding macro-boring organisms (Hallock andSchlager, 1986; Hallock, 1988; Tribollet and Golubic, 2005). It isalso known that high bioerosion rates may occur in pristine envi-ronmental conditions (Hutchings et al., 2004). In those cases it isthe grazing activity that promotes microbial bioerosion (Tribolletet al. 2011). Many other factors may influence the levels oferosion, e.g. epilithic algal cover and overfishing (Risk et al., 1995;Hutchings et al., 2004). These various aspects have been studiedmainly in tropical habitats, especially in coral reefs (Tribollet et al.2011). According to Jaafar Kefi et al. (2012a,b), disturbances recor-ded in L. lithophaga shells from Bizerta (Tunisia) also appear relatedto local environmental conditions. The site investigated wasexposed to organic and industrial discharges from the city ofBizerta, including the town itself, industrial units bordering thelagoon as well as the boat traffic. The authors also hypothesizedthat the above exposures could increase the vulnerability of thebivalve to shell infestation by burrowing invertebrates leading tonoticeable morphological malformations. The geological impact ofthe interplay of dissolved inorganic nutrients and particulateorganic matter in water with the abundance and diversity of bio-erosion agents was conceptually defined as Paleotrophodynamics(Wisshak, 2012).

R. dubia, one of the most common boring bivalve species in theeastern Adriatic Sea was documented to occur at depths of up to40 m in Rijeka Bay in the north-eastern Adriatic (Hrs-Brenko et al.,1998). This species bores into limestone and shells of variousbivalve species using mechanical (abrasion by the shell) andchemical (etching secretions) means (Morton et al., 2011). Althoughit can bore into various bivalve species, R. dubia is uncommon inspecies that are endobenthic in soft substrata such as, for example,

Venus verrucosa. According to Trigui El-Menif et al. (2005) only 0.4%of V. verrucosa collected in Tunis had R. dubia present in their shells.In a recent study of endoliths in Modiolus barbatus shells from theAdriatic Sea, �Curin et al. (2014) observed R. dubia occurred in >40%of sampled M. barbatus shells that were collected from Mali StonBay (bivalve aquaculture area). In this study, R. dubiawas identifiedin 4% of L. lithophaga shells collected at �Ciovo, and in 37% of shellsfrom Ka�stela bay. Variations in infestation observed between thesites can be explained by differences in nutrient conditions, Ka�stelaBay being eutrophic (Nin�cevi�c Gladan et al., 2010). This is inagreement with Highsmith (1980), who observed a significantpositive relationship between plankton primary productivity andbioerosion activity.

Over the past decade, the shells of long-living bivalves havebeen utilized as archives of environmental data (Reynolds et al.,2013; Sch€one, 2013; Bu�seli�c et al., 2015). Sclerochronology,through investigation of morphological changes (increment width;Butler et al., 2013.) as well as geochemical composition (Sch€one andGillikin, 2013) has enabled reconstruction of marine environmentalconditions and their variability. Caution, however, is necessarywhen interpreting growth increment widths as well as shellelemental composition when dealing with species, such asL. lithophaga, that are highly infested with endoliths. In such cases,the main drivers of inter-annual variations in increment widths aremost likely influenced by infestations with endolithic organisms, orby the corresponding shell repair, rather than by variations inenvironmental conditions such as seawater temperature or pro-ductivity. Furthermore, the presence of endolithic organisms andtheir secondary precipitates may distort the measured stableisotope record and trace element composition (Nothdurft andWebb, 2009).

Acknowledgements

This research was funded through the Croatian-French Program“Cogito”, project “Lithophaga lithophaga (Bivalvia; Mytilidae),archive of environmental changes in the Mediterranean”. Dr Eliz-abeth Harper performed mineralogical analysis of the shell. The

M. Peharda et al. / Marine Environmental Research 108 (2015) 91e9998

authors are grateful to Ivica Matijaca, Igor Isajlovi�c, Daria EzgetaBali�c, Toni Ma�s�ce and Cl�emence Royer for logistical help withsample collection. International collaborationwas promoted by theAlexander-von-Humboldt Foundation, Bonn and Hanse Institutefor Advanced Studies, Delmenhorst, Germany. Special thanks to DrMaxWisshak and Prof Brian Morton for providing suggestions thatimproved the quality of the manuscript.

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