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Size-differential feeding in Pinna nobilis L. (Mollusca: Bivalvia):Exploitation of detritus, phytoplankton and zooplankton

John Davenport a, Daria Ezgeta-Bali�c b, Melita Peharda b,*, Sanda Skeji�c b, �Zivana Nin�cevi�c-Gladan b,Slavica Matijevi�c b

a School of Biological, Earth and Environmental Sciences, University College Cork, North Mall Campus, Distillery Fields, Cork, Irelandb Institute of Oceanography and Fisheries, �Setali�ste Ivana Me�strovi�ca 63, 21000 Split, Croatia

a r t i c l e i n f o

Article history:Received 12 July 2010Accepted 29 December 2010Available online 5 January 2011

Keywords:bivalvestomach contentphytoplanktonzooplanktonendangered speciesAdriatic Sea

a b s t r a c t

The endangered fan shell Pinna nobilis is a large bivalve mollusc (<120 cm shell length) endemic to theMediterranean that lives one-third buried in soft substrata, generally in shallow coastal waters. Wehypothesised that P. nobilis of different sizes would ingest different food sources, because small fan shellswill inhale material from closer to the substratum than do large fan shells. We studied stomach contentsand faeces of 18 fan shells, 6 small (mean 23.0 cm length), 6 medium-sized (mean 41.5 cm length) and 6large (mean 62.7 cm length) living in a small area of a low-energy coastal detritic bottom characterisedby mud, sand and macroalgae at Mali Ston Bay, Croatia. We found that all P. nobilis ingested copiousquantities of undetermined detritus (probably at least 95% of ingested material), phytoplankton, microand mesozooplankton and pollen grains. Large P. nobilis stomach contents showed a preponderance ofwater column calanoid copepods, while small fan shells had higher numbers of bivalve larvae. All fanshells took in high numbers of harpacticoid copepods that are benthonic, feeding on microbialcommunities of detritus and benthic vegetation. There was also a significant selection of phytoplanktonspecies, some apparently occurring between inhalation and ingestion. The stomach contents of smallP. nobilis had a higher organic matter content than either medium-sized or large fan shells; this indicatedthat small fan shells ingested detritus of higher organic content than did larger P. nobilis. As the faeces ofall P. nobilis had similar organic matter content, this also indicates higher assimilation efficiencies insmall fan shells. The demonstration of differential dietary selectivity by different sized animals hasimplications for future trophic studies of this endangered species. This study also provides the firstdemonstration of predation on zooplankton by P. nobilis.

� 2011 Elsevier Ltd. All rights reserved.

1. Introduction

The endangered fan mussel or fan shell, Pinna nobilis Linneaus,1758, is a large bivalve mollusc (<120 cm shell length), endemic tothe Mediterranean, that commonly lives in seagrass meadows asshallow as 0.5 m deep, but can be found as deep as 60 m and inunvegetated areas (Zavodnik et al., 1991; Butler et al., 1993). Pinnanobilis shells are buried by up to a third of their length in thesubstratum, with the byssus attached to stones or roots of seagrasses, especially Posidonia oceanica (Linnaeus). The posterior endof the shell projects into the water column. The species isa suspension feeder, taking inwater through the inhalant syphon atthe posterior end of the body.

Previous studies have analysed different aspects of Pinna nobilisbiology and ecology, including spatial distribution, habitat use andpopulation structure (e.g. �Sileti�c and Peharda, 2003; Centoducatiet al., 2007; Rabaoui et al., 2008; Katsanevakis, 2009; Katsanevakisand Thessalou-Legaki, 2009; Coppa et al., 2010), influence of hydro-dynamic forces on population structure (Garcia-March et al., 2007),associated epifaunal communities (Addis et al., 2009; Rabaoui et al.,2009), age and growth (Richardson et al., 1999, 2004; Garcia-Marchand Marquez-Aliaga, 2007; Katsanevakis, 2007; Rabaoui et al.,2007), shell gaping behaviour (Garcia-March et al., 2008), shell bio-mineralization (Marin and Luquet, 2005), enzymatic activities (Boxet al., 2009) and genetic structure (Katsares et al., 2008). However,relatively little information is available concerning the diet ofP. nobilis (Cabanellas-Reboredo et al., 2009; Cabanellas-Reboredoet al., 2010). Recently Cabanellas-Reboredo et al. (2009) reportedthat d13C and d15N stable isotope analysis of fan mussels from sea-grass meadows indicates that water column organic matter (POM),

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

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sedimentary organic matter (SOM), seagrass fragments and theirepiphytes (EPoL) are all potential food sources for P. nobilis. Theyfound that EPoL was most important food source, followed byPOM > SOM > seagrass fragments, but there were some seasonalvariations.

Different methods are used for estimating trophic position andthe food sourcesofmarineorganisms, but themost commononesareanalysesof tissue fattyacids, stable isotope compositionandstomachcontents (e.g. Kharlamenkoet al., 2001; LehaneandDavenport, 2002,2006; Xu and Yang, 2007; Dang et al., 2009). Fatty acid analysis relieson the knowledge that prey fatty acid markers can be followedthrough food web since they are incorporated into the predators’tissues relatively unchanged (for detailed review see Dalsgaard et al.,2003). Analyses of d13C and d15N stable isotopes provide knowledgeof organisms’ trophic position and sources of food. Predators areusually d15Nenrichedby 3e4& comparedwith their prey,while d13Cenrichment is less (0.5e1&: e.g. Post, 2002;Michener and Kaufman,2007). The third method, that we employed here, consists of micro-scopic analysis of stomach contents and provides instantaneousinformation about the organisms’ diet. It permits detailed taxonomicanalysis of prey (e.g. Sidari et al., 1998; Lehane and Davenport, 2002,2006; Alfaro, 2006). In the case of Pinna nobilis, all of the above listedmethods are equally constrained (especially in terms of replication)by the limitations imposed on the destructive collection of a strictlyprotected endangered species (European Council Directive 92/43/EEC; Annex IV).

For a long time bivalve molluscs were considered to be exclu-sively herbivorous, with phytoplankton as the main component intheir diet. However, several studies during the last fewdecades haverevealed bivalves to be omnivores (e.g. Stuart et al., 1982; Cranfordand Grant, 1990; Langdon and Newell, 1990; Davenport et al.,2000; Lehane and Davenport, 2002, 2006). These studies identi-fied the importance of other food sources, including detritus,bacteria and even zooplankton in their diet. As there have been noprevious studies of Pinnanobilisdiet using stomach content analysis,

we used this method for determination of its diet during the time ofthe spring phytoplankton bloom (as this was likely to be a time ofmaximum food item diversity andmaximum fallout of seston to thebenthos). Because of the wide variation in P. nobilis shell size, andtheir posture that involves two thirds of the shell projecting into thewater column, it seemed likely that smaller fan mussels would bemore influenced by sediment and detritus, while larger animalswould be more dependent upon the water column above. Wetherefore investigated stomach contents in small,mediumand largeP. nobilis living in a sheltered area (where wave action was negli-gible) to investigate this possibility.

2. Methodology

2.1. Study sites and sample collection

Samples of Pinna nobilis were collected from Mali Ston Bay,Croatia (Lat 42�5104800, Long 17�4100000) on March 18th 2010 bySCUBA at depths of 2e4 m from an area with a diameter of about20 m (Fig. 1). The biotope of this area corresponds to a Mediterra-nean ‘biocenosis of the coastal detritic bottom’ (c.f. Klein andVerklaque, 2009), featuring a mixture of soft and sandy substrata,stones, shells, encrusting coralline algae, and red and green mac-roalgae. This area is extremely sheltered and rich in detritus. Thearea includes large individuals excluded in wave-exposed areas(Garcia-March et al., 2007).

Water temperature and salinity were measured with a hydro-graphic probe system (YSI Professional Plus). Zooplankton andphytoplankton were collected from the water columnwith a small,fine plankton net (mesh size 20 mm) which was hauled verticallythrough about 3.5 m from about 0.5 m above the bottom to thesurface. The sample was fixed in 2% glutaraldehyde solution.

A total of 18 fan mussels were collected e 6 from each of threesize classes. Pinna nobilis were collected one at a time and theirshell lengths were measured immediately after collection. Fan

Fig. 1. Map of the Adriatic Sea and Mali Ston Bay. Solid circle indicates sampling site.

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shells classified as ‘small’ had mean shell lengths of 23.0 � 3.26 cm(range: 18.5e26.5 cm), mean shell length of ‘medium’mussels was41.5 � 5.47 cm (34e49 cm), while mean length of ‘large’ musselswas 62.7 � 4.8 cm (56e69 cm). These size categories were entirelydiscrete. Each shell was carefully opened by cutting the adductormuscles (posterior adductor first). An incision was made witha scalpel through the stomach wall within 5 min of collection (c.f.Davenport et al., 2000) and the stomach contents drained intoa plastic container and preserved with an equal volume of 100%ethanol. Subsamples of faeces were also collected from the rectumand preserved with 100% ethanol.

2.2. Analysis of samples

All samples were processed within two weeks to avoid use offormalin. In the laboratory, samples were first analysed undera binocular photomicroscope (Olympus SZX 12) and observedanimals were classified within broad taxonomic categories ofzooplankton. In addition, pollen grains of Aleppo pine (Pinus hale-pensisMiller, 1768) were identified and counted. All zooplankton ina subsample of thewater column net sample (12.5% of total sample)were counted and classified into taxonomic categories. Countedvalues were then recalculated for the entire water column andabundance was expressed as the number of individuals per cubicmetre (ind. m�3). Due to a relatively large volume of preservedstomach contents (up to 60 ml) zooplankton analysis was per-formed on stomach contents’ subsamples. All animals were coun-ted in a subsample and the counts multiplied by the subsampleproportion of the whole. For all small Pinna nobilis the subsamplewas 50% of the whole stomach contents volume; for medium-sizedfan shells 12.5% (except in the case of one animal where it was 25%)and for all large individuals 6.25%. To standardise for differences instomach volumes, data for zooplankton taxa were calculated astheir % contributions to total zooplankton content.

For phytoplankton analysis of the water column, a subsample of2 ml was analysed by inverted microscopy (Olympus IX 51) usingthe Utermöhl method (Utermöhl, 1958) and datawere presented ascell numbers m�2 (Nin�cevi�c-Gladan et al., 2008). For stomachcontent analysis of phytoplankton, a subsample of 0.5 ml from eachstomachwas examined and abundances were obtained by countingthe number of cells in this aliquot. Phytoplankton samples werecharacterised to species or genus level. The relative percentagecontribution of a given species or genus was defined as the fractionof this taxon in the total cell number of the subsample.

For analysis of organic matter content, subsamples of bothstomach contents and faeces from all animals were each filteredonto Whatman GF/F glass microfibre filters using a vacuum pump,dried at 80 �C for 24 h, weighed and then ashed at 450 �C for 6 h

before cooling in a desiccator and final weighing. Organic mattercontents of these subsamples (determined by difference) wereexpressed as percentages of dry mass.

Data obtained from stomach contents were analysed accordingto fan mussel shell size class. Prior to the analysis, data were testedfor homogeneity of variance using Levene’s test and, if necessary,log (x þ 1) transformation. Analysis was performed using para-metric ANOVA or non-parametric KruskaleWallis test. ANOVA wasalso used for testing differences in contribution of organic matter tostomach contents and faeces. Post hoc Tukey and non-parametricManneWhitney U comparisons were employed if significantdifferences were found. For multivariate analysis of stomachcontents, the PRIMER software package was employed (PlymouthMarine Laboratories, UK; Clarke and Warwick, 1994). Percentagecontribution data for zooplankton and phytoplankton were trans-formed using log (x þ 1) and the BrayeCurtis similarity matrix wasused to generate 2-dimensional ordination plots with the non-metric multidimensional scaling (nMDS) technique. The ANOSIM1-way test was applied for testing differences in stomach contentsbetween different sized Pinna nobilis (Clarke and Warwick, 1994).The critical probability value was set at 0.05.

3. Results

3.1. Site and sample data

The temperature recorded at the surface of the water column onthe day of collection was 11.4 �C, while at a depth of 4 m it was13.5 �C. Corresponding salinity values were 23.3 and 37.6 respec-tively, indicating surface inflow of freshwater.

3.2. Zooplankton

Calanoidcopepods(2964ind.m�3)and their larvae (3769 ind.m�3)dominated in the plankton net sample, though there were appre-ciable numbers of bivalve larvae (1663 ind. m�3) and tintinnids(628 ind. m�3). Other taxa, occurringmuch less frequently, includedharpacticoid copepods (55 ind.m�3), gastropod larvae (22 ind.m�3),unidentified eggs (11 ind. m�3) and hydromedusae (11 ind. m�3).The ratio between adult calanoid and harpacticoid copepods was54:1. In addition, 375 pine pollen m�3 were noted.

Zooplankton taxadetermined from the fan shell stomachcontentsincluded: calanoid copepods, harpacticoid copepods, unidentifiedcopepod fragments, copepod nauplii, gastropod and bivalve larvae,tintinnids, unidentified eggs, and amphipods. Percentage contribu-tions of zooplankton taxa in Pinna nobilis stomach contents are giveninTable1.Harpacticoid copepodswere relatively farmore common instomachcontent samples than inthewatercolumnandoutnumbered

Table 1Percentage contribution of zooplankton taxa to total zooplankton numbers per stomach sample. S, M and L refer to small, medium and large specimens of Pinna nobilisrespectively. Mean values � standard deviation; range of values indicated in parentheses.

Taxon S M L ANOVA

Calanoid copepods 1.5 � 2.3 (0e5) 8.8 � 7.7 (0e18) 16.0 � 3.4 (12e20) F ¼ 8.82; p ¼ 0.003a

S < LHarpacticoid copepods 9.5 � 3.8 (5e16) 10.5 � 15.0 (0e36) 22.0 � 12.7 (0e33) F ¼ 2.16; p ¼ 0.150Copepod fragments 25.5 � 12.0 (9e40) 22.8 � 6.9 (15e33) 24.2 � 18.7 (7e59) F ¼ 0.06; p ¼ 0.943Copepod nauplii 3.3 � 4.1 (0e10) 8.8 � 5.7 (3e19) 22.0 � 16.0 (5e50) F ¼ 5.41; p ¼ 0.017

S < LGastropods 5.7 � 7.6 (0e20) 1.8 � 4.5 (0e11) 0 F ¼ 1.92; 0.181Bivalve larvae 48.7 � 19.9 (20e76) 39.3 � 17.2 (11e58) 12.8 � 6.1 (5e20) F ¼ 8.54; p ¼ 0.003

S ¼ M > LTintinnids 1.0 � 2.5 (0e6) 2.0 � 3.6 (0e9) 1.0 � 2.5 (0e6) F ¼ 0.24; p ¼ 0.791Unidentified eggs 4.5 � 5.4 (0e13) 5.3 � 12.1 (0e30) 1.8 � 2.9 (0e6) F ¼ 0.33; p ¼ 0.726

a Data have been transformed using log (x þ 1) prior to ANOVA.

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calanoid copepods. Calanoid: harpacticoid copepod ratios were 0.16,0.84 and 0.73 for small, medium and large fan shells, respectively.Large fan shells had a much greater proportion of calanoid copepods(p¼0.003) andcopepodnauplii (p¼0.017) in their stomachs thandidsmall fan shells, indicating a greater reliance on water columnorganisms. In contrast, small fan shells had ingested proportionatelyfar more bivalve larvae (p ¼ 0.003). No other zooplanktonic taxashowed significant differences among the P. nobilis size classes.

Results of a one-way ANOSIM test showed that there werehighly significant differences among zooplankton taxon percentagecontribution in stomach contents of the three size classes of Pinnanobilis (Global R ¼ 0.376, p ¼ 0.001) (Fig. 2). Most pronounceddifferences were noted between large and small fan shells(R ¼ 0.744, p ¼ 0.002). Between medium and small individuals thecorresponding value of Rwas 0.263 (p ¼ 0.043), while there was nosignificant difference in stomach content composition betweenlarge and medium P. nobilis (R ¼ 0.144, p ¼ 0.087). The dispersednature of points on the MDS plot, indicating much variation inzooplankton stomach contents, is also present within each sizeclass of P. nobilis. Spatial dispersal of data was especially evident forsmall and medium-sized fan shells, while large P. nobiliswere morehomogeneous in terms of zooplankton content in their stomachs.

3.3. Phytoplankton

The phytoplankton composition of the sea water sample takenconcurrently revealed 29 phytoplankton taxa, out of which 22 werediatom species and 7 were dinoflagellates (Table 2). The most abun-dant diatom species in the water column were Hemiaulus hauckii(14.79� 106 cell m�2) and Pseudo-nitzschia spp. (4.05�106 cellm�2).

The phytoplankton species composition and contribution recor-ded from all sampled stomach contents consisted of a total of 63 taxaderived from five classes: Bacillariophyceae (Diatoms), Dinophyceae,Prymnesiophyceae (Coccolithophorids), Euglenophyceae andChrysophyceae (Table 3). Most diversewere diatoms,with 36 speciesbeing recorded, while dinoflagellates were represented by 24species. Diatoms also dominated in terms of percentage contributionto stomach contents, and this was especially the case for large Pinnanobilis (Fig. 3).

The numbers of phytoplankton taxa recorded in stomachcontents of individual Pinna nobilis ranged from 10 to 26. Withrespect to fan shell size class, the smallest numbers of taxa were

Fig. 2. nMDS plot of proportional occurrence and taxonomic composition ofzooplanktonic organisms per stomach for three size classes of Pinna nobilis (L e large,M e medium, S e small). Stress 0.18.

Table 2Phytoplankton taxonomic composition in water column (cell m�2 � 104) and instomach contents of Pinna nobilis.

Phytoplankton taxa Water (cells m�2 � 104) Stomachs

Bacillariophyceae (Diatoms)1. Achnantes longipes þ2. Asterionellopsis glacialis 26.4 þ3. Bacteriastrum delicatulum þ4. Chaetoceros affinis 24.4 þ5. Chaetoceros atlanticus þ6. Chaetoceros curvisetus 65.1 þ7 Chaetoceros dydimus 26.48. Chaetoceros eibenii þ9. Chaetoceros peruvianus þ10. Chaetoceros sp. 238.111. Cerataulina pelagica 26.4 þ12. Climacosphaenia moniligera þ13. Coscinodiscus sp. 2.0 þ14. Cylindrotheca closterium þ15. Dactyliosolen fragilissimus þ16. Diploneis sp. þ17. Hemiaulus hauckii 1479.4 þ18. Hemiaulus sinensis 132.2 þ19. Grammatophora sp. þ20. Guinardia flaccida þ21. Leptocylindrus danicus 54.9 þ22. Licmophora abbreviata þ23. Licmophora flabellata 2.0 þ24. Melosira nummuloides þ25. Melosira sp. 4.1 þ26. Navicula spp. 4.1 þ27. Neocalyptrella robusta 6.1 þ28. Nitzschia longissima 4.1 þ29. Pennatae indeterm 6.1 þ30. Paralia sulcata þ31. Pleurosigma angulatum þ32. Pleurosigma sp. þ33. Proboscia alata 2.0 þ34. Pseudo-nitzschia spp. 404.9 þ35. Skeletonema costatum 16.236. Striatella unipunctata 4.137. Thalassionema nitzschioides 0.4.1 þ38. Thalassiothrix frauenfeldii 4.1 þ39. Thalasiosira sp. þ40. Triceratium sp. þDinophyceae (Dinoflagellates)1. Alexandrium minutum þ2. Alexandrium sp. þ3. Ceratium furca 14.2 þ4. Ceratium fusus 4.1 þ5. Ceratium horridum 2.0 þ6. Ceratium macroceros þ7. Ceratium trichoceros þ8. Ceratium tripos þ9. Cochlodinium sp. þ10. Dinophysis caudata 4.1 þ11. Dinophysis fortii 6.1 þ12. Dinophysis rotundata þ13. Dinophysis sp. þ14. Diplopsalis sp. þ15. Gymnodinium sp. þ16. Prorocentrum compressum þ17. Prorocentrum micans þ18. Prorocentrum miniumm þ19. Prorocentrum triestinum þ20. Podolampas palmipes þ21. Protoperidinium leonis þ22. Protoperidinium crassipes 2.023. Protoperidinium tuba þ24. Protoperidinium sp. þ25. Scrippsiella trochoidea þChrysophyceae1. Hermesinum adriaticum þPrymnesiophyceae1. Coccolithophoridae sp. þ

(continued on next page)

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recorded in small fan shells (15.8 � 3.3), while 19.0 � 3.7 and19.0 � 3.1 taxa were recorded in stomachs of medium and large fanshells, respectively. Results of a one-way ANOSIM test indicatedthat there was a highly significant difference in phytoplanktoncomposition of stomach contents amongst the three size classes ofP. nobilis (Fig. 4a; global R ¼ 0.505, p ¼ 0.001). Most pronounceddifferences were noted between large and small shells (R ¼ 0.870,p ¼ 0.002). The difference between large and medium fan shellswas also highly significant (R ¼ 0.400, p ¼ 0.004), while therewas no statistically significant difference in stomach contents

phytoplankton between medium and small fan shells (R ¼ 0.152,p¼ 0.087). As with the zooplankton data, therewas a high dispersalof points on the MDS plot for small and medium fan shells, indi-cating high variability in phytoplankton stomach contents betweenthe sampled individuals.

The taxon composition of dinoflagellates in Pinna nobilis stom-achs was mainly based on accumulation of the toxic genusDinophysis spp. (Dinophysis fortii Pavillard, 1923). Highly significantdifferences were found in the contribution of this genus to stomachcontents with respect to the size of the fan shell. Small P. nobilis hadsignificantly more Dinophysis spp. in their stomachs than didmedium and large individuals (Table 3, Fig. 4b, H ¼ 11.44,p ¼ 0.003). Significant differences were also noted betweendifferent sized P. nobiliswith respect to the percentage contributionof the large diatom Hemiaulus hauckii Grunow, 1882 (Fig. 4c;H ¼ 11.61, p ¼ 003; S < M < L).

Table 2 (continued )

Phytoplankton taxa Water (cells m�2 � 104) Stomachs

Euglenophyceae1. Eutreptia lanowii þ

þ Indicates presence.

Table 3Percentage contribution of phytoplankton taxa to phytoplankton stomach content samples. S, M and L refer to small, medium and large specimens of Pinna nobilis respectively.Mean values� standard deviation; range of values indicated in parentheses. Differences in the distributions of phytoplankton taxa amongst different sized P. nobilis tested withANOVA and KruskaleWallis as appropriate.

Phytoplankton taxa S M L ANOVA/KeW

Bacillariophyceae (Diatoms)Achnantes longipes 0.3 � 0.5 (0e1.1) 0 0Asterionellopsis glacialis 0 0.1 � 0.1 (0e0.4) 0Bacteriastrum delicatulum 0 0.1 � 0.9 (0e2.2) 0.1 � 0.3 (0e0.6)Chaetoceros spp. 0.8 � 1.1 (0e2.7) 0.7 � 1.2 (0e3.0) 2.0 � 1.4 (0e4.1)Cerataulina pelagica 2.9 � 1.4 (1.6e5.0) 0.9 � 0.9 (0e2.1) 0.2 � 0.3 (0e0.7) F ¼ 11.58, p < 0.001

S > M ¼ LClimacosphaenia moniligera 0.1 � 0.2 (0e0.4) 0.1 � 0.1 (0e0.3) 0Coscinodiscus sp. 0.3 � 0.7 (0e1.7) 0.2 � 0.2 (0e0.4) 0.1 � 0.1 (0e0.3)Cylindrotheca closterium 0 1.3 � 1.8 (0e4.7) 0.1 � 0.1 (0e0.3)Dactyliosolen fragilissimus 0 0.1 � 0.3 (0e0.9) 0.2 � 0.2 (0e0.5)Diploneis sp. 1.2 � 0.8 (0e2.5) 1.2 � 2.2 (0e5.7) 0.6 � 0.6 (0e1.5)Hemiaulus hauckii 31.0 � 23.6 (1.9e58.7) 61.8 � 23.5 (24.5e85.9) 85.6 � 5.3 (77.5e90.5) H ¼ 11.61, p ¼ 0.003

S < M < LGrammatophora sp. 2.2 � 4.4 (0e10.9) 1.6 � 3.0 (0e7.7) 2.0 � 1.9 (0.2e5.6)Guinardia flaccida 0.2 � 0.4 (0e1.1) 0.6 � 0.8 (0e2.1) 0.2 � 0.3 (0e0.6)Leptocylindrus danicus 0 3.1 � 7.7 (0e18.9) 0Licmophora spp. 0.7 � 1.3 (0e3.3) 0.3 � 0.8 (0e1.9) 0.1 � 0.1 (0e0.3)Melosira spp. 2.3 � 3.7 (0e8.7) 0.7 � 1.1 (0e2.2) 0.1 � 0.2 (0e0.5)Navicula spp. 4.5 � 9.3 (0e23.3) 1.9 � 2.1 (0.3e5.7) 0.3 � 0.3 (0e0.7)Neocalyptrella robusta 0.2 � 0.4 (0e1.1) 0.2 � 0.3 (0e0.9) 0.2 � 0.2 (0e0.6)Nitzschia longissima 0 0.5 � 0.8 (0e1.9) 0.1 � 0.1 (0e0.3)Pennatae indeterm 4.7 � 2.2 (1.2e6.6) 1.8 � 1.3 (0.5e3.8) 0Pleurosigma spp. 1.0 � 0.6 (0e1.7) 0.8 � 0.6 (0e1.7) 0.2 � 0.2 (0e0.6) F ¼ 4.12, p ¼ 0.038

S > LProboscia alata 0 0.4 � 0.8 (0e1.9) 0Pseudo-nitzschia spp. 3.0 � 2.8 (0e6.1) 1.3 � 1.6 (0e3.5) 0.5 � 0.5 (0e1.2)Thalassionema nitzschioides 2.8 � 1.7 (1.2e5.4) 1.8 � 2.8 (0e7.2) 1.1 � 0.6 (0.7e2.3)Thalassiothrix frauenfeldii 0 0 0.2 � 0.4 (0e1.1)Thalasiosira sp. 0.1 � 0.3 (0e0.7) 0.3 � 0.3 (0e0.7) 0.1 � 0.1 (0e0.3)Triceratium sp. 0.2 � 0.4 (0e1.1) 0.2 � 0.4 (0e0.9) 0

Dinophyceae (Dinoflagellates)Alexandrium sp. 0.3 � 0.5 (0e1.1) 0.2 � 0.3 (0e0.6) 0.1 � 0.1 (0e0.3)Ceratium spp. 0 0.2 � 0.2 (0e0.5) 0.5 � 0.4 (0e0.9)Cochlodinium sp. 0.3 � 0.6 (0e1.6) 0 0Dinophysis spp. 30.8 � 17.0 (4.7e50.4) 7.8 � 7.5 (0.6e21.6) 1.3 � 0.9 (0.5e2.8) H ¼ 11.44, p ¼ 0.003

S > M > LDiplopsalis sp. 0 0.1 � 0.1 (0e0.4) 0Gymnodinium sp. 0 0.2 � 0.3 (0e0.9) 0Prorocentrum spp. 8.1 � 5.6 (0e16.3) 8.3 � 6.5 (2.6e17.9) 2.8 � 1.7 (1.3e5.9)Podolampas palmipes 0.2 � 0.4 (0e1.1) 0 0Protoperidinium spp. 0 0.4 � 0.8 (0e1.9) 0.2 � 0.2 (0e0.6)Scrippsiella trochoidea 0.5 � 0.7 (0e1.9) 0.2 � 0.3 (0e0.7) 0

PrymnesiophyceaeCoccolithophoridae spp. 0.6 � 1.4 (0e3.3) 0.6 � 1.1 (0e2.8) 1.2 � 1.2 (0.3e3.7)

EuglenophyceaeEutreptia lanowii 0.8 � 1.7 (0e4.3) 0.2 � 0.4 (0e1.1) 0

ChrysophyceaeHermesinum adriaticum 0 0 0.1 � 0.1 (0e0.2)

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3.4. Organic matter content of stomach contents and faeces

The data for organic matter content of stomach and faecalsamples (Table 4) reveal highly statistically significant differencesin ingested food quality amongst the fan shells of different sizes. Itis evident that the small fan shells ingestedmaterial of much higherorganic content than large animals (with medium-sized fan shellsingesting material of intermediate organic value). The imagesshown in Fig. 5 demonstrate that detritus greatly dominated thevolume of stomach contents. Takenwith the data shown in Table 4,this indicates that the detritus ingested by smaller fan shells isorganically much richer than that ingested by larger individuals.

4. Discussion

Stomach contents analysis revealed that Pinna nobilis ingesteda wider range of potential food resources (detritus, phytoplanktonand zooplankton) than previously thought. Visually, it is apparentthat detritus makes up the great bulk, probably more than 95% byvolume, of the ingested material in P. nobilis of all three size classes(Fig. 5), which is consistent with the stable isotope studies ofCabanellas-Reboredo et al. (2009). Clearly, phytoplankton andzooplankton are likely to be relatively unimportant in terms ofoverall energy uptake. Pinna also ingested pine pollen grains, butlimited faecal analysis (Ezgeta-Bali�c, personal observation) indi-cates that these pass through the gut undigested.

Comparisons between stomach sample organic matter contentsof Pinna nobilis of different sizes revealed highly significantlydifferent values. A priori this can be due to two reasons that are notmutually exclusive. First, it may be that the smaller fan shells inhaleparticulate material with higher organic matter contents than dolarger fan shells, because they are closer to the substratum wheredetritus settles and is enriched by bacterial and fungal action (e.g.Tenore, 1983). Second, it is possible that the processing of partic-ulate material by gills and palps is affected by fan shell size, so thatthe inhaled material does not differ, but the ingested material does.Liang and Morton (1988) showed that pinnid bivalves have unique“rejection channels” that run from the labial palps, via the mantlesurface, to the junction between gills and mantle close to theexhalant current. These may well be involved in particle selection,and, in the light of the present investigation, merit further study.Overall, this appears to be the first demonstration of differences inage/size-dependent food quality by a bivalve mollusc.

As hypothesised, our data revealed significant differences inrelative frequency of intake of different planktonic organisms withrespect to size class of Pinna nobilis collected from Mali Ston Bay.

Large fan shells project much further into thewater column than dosmall fan shells and this probably explains many of these differ-ences. They ingested proportionately much greater quantities ofcalanoid copepods and diatoms (especially large Hemiaulushauckii), that were characteristic of water column plankton, thandid small fan shells. Conversely, the relative intake of bivalve larvaeand dinoflagellates (especially Dinophysis fortii) was significantlygreater in small fan mussels. Throughout, the findings for medium-sized P. nobilis tended to be intermediate between those for smalland large fan shells, confirming a highly significant pattern ofdifferential food item intake. Particularly interesting was thefinding that harpacticoid copepods were much more common (in

Fig. 3. Proportions of dinoflagellates and diatoms in stomach samples of 18 Pinnanobilis (L e large, M e medium, S e small).

Fig. 4. a) nMDS plot of stomach phytoplankton contents of three size classes of Pinnanobilis (L e large, M e medium, S e small). b) Percentage contribution of the dino-flagellate genus Dinophysis spp. to the stomach samples. c) Percentage contribution ofthe diatom Hemiaulus hauckii to the stomach samples. The larger the symbol, thegreater percentage contribution. Stress 0.11.

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stomachs of P. nobilis of all sizes) thanwould be expected from theirlow planktonic numbers in water column. Harpacticoids arebenthonic and common both on benthic vegetation and upondetritus; in both cases they largely browse on microbial films (e.g.Rieper, 1982; De Troch et al., 2001). It is possible that some har-pacticoids were intercepted when travelling between benthicplants, but given the numbers (and the quantities of detritusingested) it is far more likely that they were incidentally ingestedwith inhaled detritus.

This study provides the first demonstration of predation onzooplankton by Pinna nobilis. There is now plentiful evidence thata variety of taxonomically distant bivalve molluscs (freshwater and

marine mussels, cockles, oysters, scallops) ingest micro and meso-zooplankton and assimilate carbon from them (e.g. Davenport et al.,2000; Lehane and Davenport, 2002, 2004; Wong et al., 2003a,b;Alfaro, 2006; Porri et al., 2008; Troost et al., 2008a,b, 2009), thuscontributing to bentho-pelagic energetic coupling. Mussels andoysters (Mytilus edulis Linneaus, 1758, Mytilus galloprovincialisLamarck 1819, Perna perna (Linnaeus, 1758), Perna canaliculus(Gmelin,1791) and Crassostrea gigas (Thunberg,1793)) have attractedmost study, and it is evident that they cannibalise their own larvae atsome periods of the year (Lehane and Davenport, 2004; Alfaro, 2006;Porri et al., 2008; Troost et al., 2008a), aswell as consuming the larvaeof other species. In some cases as many as 50% of potential settlingmussel larvae are consumed by adult mussels, with significantimplications for recruitment and population dynamics (Porri et al.,2008). Pinna nobilis, especially small specimens, consumed largenumbers of bivalve veliger larvae at the time of our study (springbloom). Mali Ston Bay is a premier Croatian bivalve aquacultureregion, with substantial numbers of oysters (Ostrea edulis Linneaus,1758) and mussels (M. galloprovincialis) being reared close to thesampled fan shells. It is likely that theywere the sourceof theveligers.Because fan shells occur in low numbers, it is unlikely that theymakea significant contribution to overall bivalve larval mortality in areaswhere thereare farmorenumerouscannibalisticoystersandmussels.However, they clearly have substantial highly localised effects andcontribute to the chaotic dynamics of inshore zooplankton commu-nities (c.f. Doveri et al., 1993; Vaughn and Allen, 2010).

Although it was not part of this study, subsamples of faeces wereinspected for the presence of zooplankton. Entire or parts ofzooplanktonic organisms present in faecal material includedbivalve larvae, harpacticoid copepods, copepod fragments, tintin-nids, gastropods and unidentified eggs (Ezgeta-Bali�c, personalobservation). Overall, there was little evidence of whole copepodmaterial in faecal samples, and only bivalve shells (empty) and pinepollen grains (apparently undigested) occurred in the faeces of 6Pinna nobilis (2 specimens from each size class). These findingsindicate that digestion of zooplankton had taken place.

Significant differences between compositions of ingestedphytoplankton in different size classes of Pinna nobilis were alsodetected. These are less easy to interpret than the zooplankton data.However, diatoms are generally larger (especiallywhen occurring inchains) than dinoflagellates and it is noteworthy that large P. nobilisingested fewer dinoflagellates and more diatoms than did small fanshells (Fig. 3, Table 3). This suggests that size-related differences inthe geometry/morphology of food capture/processing structures(gills, labial palps, pallial organs) might be important. Pinna nobilisexhibits a greater adult size range than almost all other extantbivalves and could be a useful species to elucidate such differences.Some of the differences in quality of P. nobilis phytoplanktonic foodand its taxonomic composition are likely to be due to selectionbetween inhalation and ingestion, where organism size is unlikelyto be a factor. The diatom Pseudo-nitzschia spp. was very common inthe net plankton (Table 2), but very rare in the stomachs of allP. nobilis (Table 3). Pseudo-nitzschia spp. produces neurotoxicdomoic acid (Amzil et al., 2001; Cusack et al., 2002). The rarity ofthis genus in the stomach contents of P. nobilis, suggests possiblerejection before ingestion, but themechanism involved is unknown.

Table 4Organic matter content (% mass) of stomach and faecal samples in Pinna nobilis of different size categories: S, M and L refer to small, medium and large fan shells respectively.Mean values � standard deviation; range of values indicated in parentheses. NS indicates no significant difference.

Sample S M L ANOVA

Stomach 97.2 � 6.8 (83.3e100.0) 74.3 � 16.7 (50.0e100.0) 54.6 � 10.2 (40.9e70.0) F ¼ 19.06, p < 0.001S > M > L

Faeces 18.8 � 8.0 (5.7e30.0) 17.5 � 4.5 (14.0e26.3) 22.0 � 5.9 (16.8e33.3) F ¼ 0.79, p ¼ 0.472NS

Fig. 5. Images of Pinna nobilis stomach contents. Note that detritus greatly dominatesall images. a) Bivalve D-larva arrowed. b) Upper arrow indicates pine pollen grain,lower arrow indicates bivalve larva. c) Arrow indicates benthic diatom. d) Upper arrowindicates dinoflagellate, lower arrow indicates gastropod larva. e) Arrow indicatescalanoid copepod nauplius. f) Arrow indicates harpacticoid copepod. g) Arrow indi-cates diatom. h) Arrow indicates fragment of macroalga. Scale bar 100 mm.

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In reports on the feeding of the mussel Mytilus edulis, manyauthors have failed to demonstrate differential retention ofphytoplankton species by the gills (Cucci et al., 1985; Bougrier et al.,1997; Rouillon and Navarro, 2003). Diatom cells are protected byrigid siliceous frustules, but in spite of their rigid nature, it has beenfound that these organisms are more accessible to mechanicaltreatment of digestion than are flagellates enclosed by a moreflexible cell wall (Rouillon and Navarro, 2003). On the other hand,less digestible flagellates would be kept recirculating in suspension,thus lengthening their residence time inside the stomach (Brillantand MacDonald, 2000). It is unclear and contradictory, however,why the small specimens of Pinna nobilis accumulate more dino-flagellates (mostly thecate Dinophysis species) with respect todiatoms than do large specimens, which prefer diatoms (other thansimple size selection as suggested above). Sidari et al. (1998) foundthat Mytilus galloprovincialis preferentially selected dinoflagellatesrather than diatoms in the mussel stomach. They described theability of mussels to open the Dinophysis thecae and thereby digesttheir cellular contents more easily than other thecate dinoflagellateorganisms (e.g. Protoperidinium). Similar results were obtained byBuley (1936) for Mytilus californianus (Conrad, 1837) and AndresenLeitao et al. (1984) forM. edulis. Selection of phytoplankton speciesand its utilisation for nutrition, especially in relation to size ofbivalve, clearly requires further research.

All stomachs studied contained Aleppo pine (Pinus halepensis)pollen grains, which were also found in faeces. It seems probablethat these were ingested incidentally with other seston. The outercoat of the pollen grain is highly resistant to degradation bydigestive enzymes (Heslop-Harrison, 1971). Few studies have beenconducted on the nutritional importance of pollen to aquaticanimals. For example, studies performed by Britson and Kissel(1996) showed that pine and oak pollen had no nutritive signifi-cance to frog tadpoles. Similarly, under laboratory conditions, aftera three-week experimental period, mussels (Mytilus gallopro-vincialis) fed on pine pollen did not differ in their condition index incomparison with mussels held in control tanks (Peharda, personalobservation).

5. Conclusions

Overall, the results of this study confirmed our hypothesis thatPinna nobilis of different sizes, living in low-energy, detritus-richenvironments, can have markedly different diets (in terms oforganic content and composition of ingested zooplankton andphytoplankton), even when living within a few metres of eachother. This has substantial implications for further study, particu-larly those investigations that involve the analysis of stable isotopesor fatty acids to elucidate the uptake of organic matter from thecomplex environment of the near-bottom water column and theassociated detrital material, and its subsequent incorporation intothe tissues of P. nobilis.

As Pinna nobilis status as an endangered and protected species,scientists must respect it as much as we expect other stakeholders(e.g. fishers, developers) to do, in order to achieve the species’sustainable management. Future trophic investigations thereforeneed to incorporate these findings into their experimental designs.

Role of the funding source

Funding for this study was provided by the “Unity ThroughKnowledge Fund” (UKF) under a grant programdesigned to supportyoung researchers. UKF had no direct involvement in study design,collection, analysis and interpretation of data, or in writing of themanuscript. Permission for publishing this material was obtainedfrom the funding organisation.

Acknowledgements

This research was financed by support from the Croatian ‘UnityThrough Knowledge’ grant 3A “Bivalve feeding, competition andpredationewhat is at play”. Permission for collection of specimensof Pinna nobiliswas obtained from relevant national authorities andall work conducted complied with national Croatian law.

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