Download - Phytoplankton Composition of the Stomach Contents of the Mussel Mytilus

Transcript
Page 1: Phytoplankton Composition of the Stomach Contents of the Mussel Mytilus

BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, researchlibraries, and research funders in the common goal of maximizing access to critical research.

PHYTOPLANKTON COMPOSITION OF THE STOMACH CONTENTS OF THEMUSSEL MYTILUS EDULIS L. FROM TWO POPULATIONS: COMPARISONWITH ITS FOOD SUPPLYAuthor(s) :G. ROUILLON, J. GUERRA RIVAS, N. OCHOA, and E. NAVARROSource: Journal of Shellfish Research, 24(1):5-14. 2005.Published By: National Shellfisheries AssociationDOI: 10.2983/0730-8000(2005)24[5:PCOTSC]2.0.CO;2URL: http://www.bioone.org/doi/full/10.2983/0730-8000%282005%2924%5B5%3APCOTSC%5D2.0.CO%3B2

BioOne (www.bioone.org) is a a nonprofit, online aggregation of core research in the biological, ecological, andenvironmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published bynonprofit societies, associations, museums, institutions, and presses.

Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance ofBioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use.

Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries orrights and permissions requests should be directed to the individual publisher as copyright holder.

Page 2: Phytoplankton Composition of the Stomach Contents of the Mussel Mytilus

PHYTOPLANKTON COMPOSITION OF THE STOMACH CONTENTS OF THE MUSSELMYTILUS EDULIS L. FROM TWO POPULATIONS: COMPARISON WITH ITS FOOD SUPPLY

G. ROUILLON,1* J. GUERRA RIVAS,1 N. OCHOA2 AND E. NAVARRO1

1Departamento de Genética, Antropología Física y Fisiología Animal, Facultad de Ciencia yTecnología. Universidad del País Vasco/Euskal Herriko Unibertsitatea. Apdo. 644–48080, Bilbao,España; 2Laboratorio de Ecología Acuática, Facultad de Ciencias Biológicas. Universidad NacionalMayor de San Marcos, Ciudad Universitaria, Avda. Venezuela, cuadra 32 s/n Lima, Perú

ABSTRACT Seasonal data on phytoplankton composition of seston and stomach contents of the mussel (Mytilus edulis Linnaeus,1758) from two contrasting sites, an estuarine mud flat and a rocky open shore, were compared to ascertain: (a) the extent to whichdifferential characteristics of both sites affect this composition and (b) the degree of similarity between stomach contents andmicroalgal composition of seston of these sites as an index reflecting the complex processes of selection taking place within thefeeding-digestive system of mussels. Individuals and water samples were collected monthly from November 2001 to December 2002,when salinity, temperature, and total and organic particulate matter concentration were also recorded in the water column. Preservedsamples of seston and stomach contents were analyzed by inverted microscopy according to the Utermöhl method. Phytoplankton cellswere counted and the different species grouped, taxonomically and, according to the habitat, into pelagic and tychopelagic. These dataserved to compute abundance (total cell count) and frequency index. Relative abundances of each group were compared for similaritybetween sampling sites and stomach and water samples in each site. Similarity analyses were performed using the index of Bray-Curtis,significant differences between samples being determined by the non parametric test of ANOSIM. Results of this test for thecomparison between water and stomach contents resulted in significant differences: R � 0.68 in the estuary and R � 0.75 in the openshore area. Stomach contents presented a reduced average number of species (n � 6 in mussels from both sites) and a greaterproportion of tychopelagic forms for comparison with the water samples (n � 20 and 24 in the estuary and open shore, respectively).Maximum phytoplankton density in water samples occurred in the May to October period, the group responsible for this incrementbeing the diatoms. The stomach contents of marine mussels displayed two peaks of phytoplankton concentration in May (caused bythe dinoflagellate Ensiculifera sp.) and in July (caused by the diatoms Pseudo-nitzschia pungens and Licmophora sp.). In the case ofstomach contents of estuarine mussels, a single peak of abundance was recorded in the month of May and was mainly produced byEnsiculifera sp. To conclude, the main result coming from these comparisons is the increased abundance of dinoflagellates in thestomach contents relative to the corresponding seawater samples in the estuarine and open shore media. This result is discussed in thelight of previous data concerning the differential utilization of species of phytoplankton by bivalve molluscs.

KEY WORDS: phytoplankton, food supply, stomach content, mussels, Mytilus edulis

INTRODUCTION

Marine coastal areas are characterized by great space-temporalfluctuations in both phytoplankton abundance and specific com-position. In the temperate area, dominant species of phytoplanktonexhibit seasonal variations and a natural succession between phy-toplankton groups that accompany the occurrence of blooms (Berg& Newell 1986, Varela 1996). Superimposed on these long-termcycles, short-term pulses of microphytobenthos resuspensioncaused by wind- and tide-driven currents are also relevant re-garding the chlorophyll concentration and microalgal compositionof the seston (Roman & Tenore 1978, Baillie & Welsh 1980,Muschenheim 1987, Grant et al. 1990, de Jonge & van Beusekom1992, Newell & Shumway 1993). This stands particularly true forsoft-bottomed shallow tidal flats common to estuaries and shel-tered areas of the coast, where tidal variability of chlorophyllconcentration can exceed the seasonal range (Grant et al. 1993,Smaal & Haas 1997). Hummel (1985) studying the diatom com-position of the water column above a tidal mud-flat in the WaddenSea reported a greater presence of benthic species at the mostlandward sampling points for comparison with deeper points. Con-sequently, microalgal composition at these sites would appear, toa great extent, affected by short-term tidal changes in contrast withthe open shores where seasonal variability would be dominant.

This fact constitutes one of the sources of spatial variation alongthe coast.

Mussels Mytilus edulis Linnaeus, 1758 are conspicuous inhab-itants of both open-shore and estuarine habitats where they formimportant populations. The interaction of mussel populations withphytoplankton as food source has long been documented. For ex-ample, Blanton et al. (1987), van der Veer (1989) and Hickman etal. (1991) reported that phytoplankton blooms were accompaniedby increased growth and production and improved condition indexof various mussel species in culture plots. All these observationssupport the idea that mussels generally rely on phytoplankton astheir main food supply.

However, different species of phytoplankton seems to behavein a different way as regards its food value for bivalves underculture conditions (Epifanio 1979, Enright et al. 1986, Laing &Millican 1986). When available, field observations appear to con-firm the above extremes: Beukema and Cadee (1991) comparedthe patterns of growth of Macoma balthica Linnaeus, 1758 withthe patterns of abundance of different phytoplankton componentsover 15 y, to conclude faster growth and better condition associ-ated with higher abundance of diatoms for comparison with yearswhen flagellates were dominant. Given that, the ability exhibitedby several bivalves (mussels included) for the preferential utiliza-tion of species of phytoplankton (Cucci et al. 1985, Shumway et al.1985, Bougrier et al. 1997, Rouillon & Navarro 2003) should beconsidered a useful mechanism ensuring a complete exploitationof this resource under the conditions of variability prevailing in themarine coastal habitat.*Corresponding author. E-mail: [email protected]

Journal of Shellfish Research, Vol. 24, No. 1, 5–14, 2005.

5

Page 3: Phytoplankton Composition of the Stomach Contents of the Mussel Mytilus

In dealing with this phenomenon of differential utilization, auseful approach under field conditions would be the comparison ofgut contents, and the water column or superficial sediments, interms of phytoplankton species composition. Using these proce-dures, Kamermans (1994) reported that species composition in gutcontents of various epifaunal and infaunal bivalves living in mudflats resembled more the composition of the water column thanthat in superficial sediments, but no evidence of selective feedingcan be concluded from her data. Shumway et al. (1987) andMuñetón-Gómez et al. (2001) also reported similar patterns ofseasonal variation of species composition in seawater and stom-achs of Placopecten magellanicus Gmelin, 1791 and Spondylusleucacanthus Broderip 1833, respectively. However, Ciocco andGayoso (2002) observed that stomach content composition ofribbed mussels (Aulacomya atra Molina, 1782) did not reflect theoccurrence of diatom blooms recorded in the area of study.

The present study compares seasonal data on phytoplanktoncomposition of seston and stomach contents of mussels (M. edulis)sampled along a year. The study was conducted at two sites pre-senting different characteristics, a muddy flat in an estuary and arocky shore from an exposed beach, to ascertain (a) the extent to

which spatial differences in phytoplankton composition reflect theparticular conditions of both sites, specially in which concerns tothe balance between pelagic and tychopelagic microalgae and (b)the degree of similarity between stomach contents of mussels fromthe two sites and the microalgal composition of the water columnat these sites as an index reflecting the possible occurrence ofdifferential retention, ingestion, and selective digestion of speciesof phytoplankton within the feeding apparatus of mussels.

MATERIALS AND METHODS

Two sampling sites were chosen to represent open shore andestuarine habitats: a rocky area at Atxabiribil beach (43°23�29�LN;02°59�28�LW) and a muddy-flat in the Ría de Plencia (43°24�39�LN; 02°56�52�LW), respectively (Fig. 1). Water temperatureand salinity were recorded each time with a LF330/SET StandardConductivity Cell (TetraCon 325, Germany).

Sampling was performed during the ebb tide from a point situ-ated approximately 3 m. above the chart datum. Mussels recentlyemerged (<30 min.) and superficial water samples were collectedmonthly at these two sites, from October 2001 to December 2002,in the case of water samples and from November 2001 to October2002 in the case of mussels. Water samples (5 L.) were dividedinto two aliquots, for particulate seston analysis and phytoplanktoncomposition, respectively.

Total particulate matter and organic content of seston weredetermined by standard procedures: Known volumes of watersampled were filtered on ashed and preweighed glass-fiber filtersthat were then rinsed with seawater-isotonic ammonium formatedried at 100°C for 48 h, weighed, ashed at 450°C for 6 h andweighed again. The increment of dry weight and the subsequentweight loss on ignition experienced by these filters, both dividedby the volume filtered, represented the total particulate matter(TPM: mg L−1) and particulate organic matter (POM: mg L−1),respectively; organic content (f) was the ratio of POM to TPM.

Phytoplankton Composition of Water Samples

Water samples were immediately fixed by the addition of glu-taraldehyde to the sample to give a final concentration of 1%.Quantitative analysis was made following a modification of themethod of Utermöhl (Hasle 1978): 50 mL of water were allowedto settle for 36–48 h in a combined chamber and cylinder. Iden-tification and counting followed under an inverted microscope(Nikon, phase contrast DIAPHOT). The aliquot counted repre-sented a 5% of total chamber volume. Identification of phytoplank-ton species was performed to the closest taxon possible accordingto the following references: Cupp (1943), Balech (1988), Ricard(1987), Tomas (1993; 1996), Van den Hoek et al. (1995).

Microalgal species were grouped, according to the habitat, intwo categories: pelagic and tychopelagic, the latter including bothintermediate and benthic non-adhering forms (Gailhard et al.2002).

TABLE 1.

Range of environmental variables in the two sampling sites, measured over a 14 month period.

Site Name Habitat Temperature °CSalinity

S‰TPM

mg � 1−1Organic Content

fCells Density

(N° � ml−1)

Plencia estuary Estuarine 10.2–22.5 18.0–30.0 4.036–43.44 0.115–0.216 15.4–662.8Atxabiribil beach Marine (open-shore) 11.0–21.5 32.6–35.2 1.785–17.755 0.109–0.521 12.53–746.18

Figure 1. Map of the study area. Sampling sites are indicated

ROUILLON ET AL.6

Page 4: Phytoplankton Composition of the Stomach Contents of the Mussel Mytilus

Stomach Content Analysis

Mussels collected in the field were immediately preserved in afixative mixture made up of formaldehyde and glutardialdehyde inthe proportion 3:2, diluted with filtered seawater to a final con-centration of 5%. This mixture is assumed to simultaneously en-sure optimal preservation of animal tissues (formaldehyde) andfeatures of phytoplankton cells (glutardialdehyde). Gapping ofvalves observed after 10–15 min exposure of mussels to the fixa-tive allowed access to the mussels’ soft tissues, stomach contentsincluded. Mussels that did not gape were discarded; this circum-stance only occurred 1 mo (June).

In the laboratory, valves were separated apart to allow stomachcontents collection by means of a hypodermic syringe. After re-cording the volume collected, the stomach content was added to100 mL of glutardialdehyde 1% and 50 mL of it were allowed tosettle for 36–48 h in a combined chamber and cylinder. A fivepercent of chamber volume was analyzed under the inverted mi-croscope following Utermöhl method.

Cell density or abundance was obtained by dividing the numberof cells counted in an aliquot by the aliquot volume. Relativedensity of a given species or group of species was defined as thefraction this species or group represent of the total cell numberfrequency index of a species or group is defined as the number ofsamples presenting this species or group divided by the total num-ber of samples.

Statistical Analysis

We used 3 replicates for water samples and 3 individuals toanalyze of stomach contents per site and per month. Given the

differences in cell density between water and stomach samples,statistical comparisons were based on relative density values (per-centage of cell number) to obviate the concentration factor thataffects the stomach contents. According to Clarke and Warwick(2001), these data were normalized by means of square root trans-formation before performing similarity analysis using the Bray-Curtis index, significant differences between samples being deter-mined by the non parametric test of similarity (ANOSIM) usingPRIMER v5 software (Clarke & Gorley 2001).

RESULTS

Density of phytoplankton cells in the water column fluctuatedbetween broad limits along the year, but the range was very similarin both the sites (15.4–662.8 cell.mL−1 in the estuary and 12.53–746.18 cells.mL−1 in the open shore). This contrasts with signifi-

TABLE 2.

Summary of ANOSIM results.

Samples Factors R P

Marine vs. estuarine water Month 0.956 0.001*habitat 0.931 0.001*

Marine water versus stomach contents Month 0.796 0.001*Compartment 0.77 0.001*

Estuarine water versus stomach contents Month 0.683 0.001*Compartment 0.653 0.001*

* Significant differences

Figure 2. Seasonal variation of phytoplankton abundance of the main taxonomic groups. Note that the scale is divided by 105 in the case ofstomach content of mussels.

PHYTOPLANKTON IN STOMACH CONTENT OF MUSSELS 7

Page 5: Phytoplankton Composition of the Stomach Contents of the Mussel Mytilus

Figure 3. Dendrogram for hierarchical clustering of water samples.

Figure 4. Cell density of 10 more abundant species. Black bars correspond to pelagic species, white bars correspond to tychopelagic species. d,indicates dinoflagellates species.

ROUILLON ET AL.8

Page 6: Phytoplankton Composition of the Stomach Contents of the Mussel Mytilus

cantly higher values of total particulate matter and lower organiccontents found in the estuary for comparison with the open shore.Average temperatures were slightly higher in the estuary. Salinitymean values were 25.4‰ in the estuary and 33.8‰ in the openshore (Table 1).

Seasonal Variation of Phytoplankton Abundance and Composition in

the Water Column

Temporal variation of abundance of the different phytoplank-ton groups is compared between estuarine and open shore watersamples in Figure 2a and b. Data for the estuarine area suggests theexistence of 2 blooms, in spring (April to June) and autumn (lateSeptember). Two centric diatoms (Chaetoceros costatus and Lep-tocylindrus danicus), and C. costatus and the pennate diatom As-terionellopsis glacialis appeared as the main species responsiblefor the spring and autumn peaks, respectively (Fig. 2a). In the openshore (Fig. 2b), the onset of the period of high abundance wasdelayed to May and the two spring and autumn peaks tended tomerge in this area giving rise to a period of high abundance thatextended from May to early October. This period was character-ized by the following succession of species: Skeletonema costatum(centric diatom) and L. danicus, that formed a first peak, followedby C. costatus forming a second peak, and Pseudo-nitzschia pun-gens (pennate diatom) a third peak of abundance.

Results of a two-layout analysis of similarity based on compar-ing the abundance of different phytoplankton species (ANOSIM)between sampling dates and sites (estuarine vs. open-shore) aresummarized in Table 2. According to these results, phytoplank-

ton composition was dissimilar in both the seasonal comparison (R� 0.956) and when comparing estuarine and marine waters (R �

0.931).Results from ANOSIM performed on water samples were ex-

pressed as dendrograms of similarity (Fig. 3). Season appears asthe main component allowing differentiation of two groups sharinga similarity <30% and constituted, approximately, by the samplesfrom spring–summer on one side and the rest of seasons on theother. Analogously, two secondary groups constituted by autumnand winter samples shared <45% of similarity. Site origin of watersamples was a less discriminating component, although similaritybetween estuarine and open shore samples was never >55%. Thehighest values corresponded to comparisons of samples taken inthe same month, and particularly in the summer season due to thesimultaneous occurrence in both media of blooms dominated bythe pelagic centric diatoms: C. costatus, L. danicus, S. costatum,and Chaetoceros curvisetus.

Figure 4a and b compares the 10 most abundant species (high-est cell density) between estuarine and open shore samples. Allthese species were diatoms and about 40% of more abundant dia-toms were centric species, which contributed more (15% to 20%)than any other group to total abundance. As to the habitat, pelagicgroup constituted 60% to 80% of most abundant species, comparedwith 10% to 30% of tychopelagic.

Species more abundant do not necessarily represent the com-monest species. Consideration of the frequency index computedfor the 10 commonest species found in water samples (Fig. 5a,b)was aimed to provide complementary information, that can be

Figure 5. Frequency index of the 10 commonest species. Legends as in Fig. 4.

PHYTOPLANKTON IN STOMACH CONTENT OF MUSSELS 9

Page 7: Phytoplankton Composition of the Stomach Contents of the Mussel Mytilus

summarized as follows: (a) The totality of the 10 most frequentspecies were also diatoms, but in this case 90% of species werepennates (b) 60% of species recorded were common to both areas,these species also presenting a high frequency index (0.745–0.938). Two centric chain-forming diatoms, Stephanopysis turris(estuarine) and Guinardia delicatula (open shore) and 6 pennatediatoms: Gyrosigma fasciola, Navicula elegans, Synedropsis sp.(estuarine) and Climacosphenia sp., Licmophora sp, and Pseudo-nitzschia pungens (open shore) accounted for the main differencesbetween both sites.

Phytoplankton in Stomach Contents: Comparison With the

Food Supply

The patterns of monthly variation of phytoplankton abundancein the stomach contents of estuarine and marine mussels was char-

acterized by a peak in May contributed by the dinoflagellate En-siculifera sp. A secondary peak in July, composed of Pseudo-nitzschia pungens (pelagic pennate) and Licmophora sp. (tycho-pelagic, pennate) was only apparent in the stomach of marinespecimens (Fig. 2c,d).

Results of two-layout ANOSIM tests (Table 2) comparing phy-toplankton composition in stomach contents and water indicatedsignificant differences for both estuarine and open shore habitats(R > 0.5). Dendrograms of similarity (Fig. 6) showed that waterand stomach content samples were grouped apart, particularly inopen shore samples where similarity in composition of both groupswas <20%. In general, similarity between water samples and theircorresponding stomach content was always <20%, with the excep-tions of April in the estuary (>60%) and November to Decemberin the open shore (>40%).

Main contribution to phytoplankton abundance in stomach con-tents corresponded with the dinoflagellate Ensiculifera sp., which

Figure 6. Dendrogram for hierarchical clustering of water and stomach samples from estuarine and open-shore sites.

ROUILLON ET AL.10

Page 8: Phytoplankton Composition of the Stomach Contents of the Mussel Mytilus

was accounted for by 56% and 30% of total cell density in estua-rine and open shore mussels, respectively. None of the remainingmicroalgal species, belonging to a diversity of groups (diatoms,dinoflagellates, naked flagellates, chlorophyta, and coccoli-phorids), contributed more than 10% (Fig. 4c,d). The proportion ofpelagic among the 10 most abundant species of phytoplanktondecreased from 60% or 80% in water samples form the estuary andopen shore sites, respectively, to 40% in stomach contents.

Diatoms and dinoflagellates were the most frequent microalgalgroups in the stomach contents of mussels, irrespective of thesampling area. Presence of centric diatoms increased from 10% ineither samples to 20% or 50% in stomachs of open shore andestuarine mussels (Fig. 5c,d).

DISCUSSION

Fernández (1990) and Varela (1996), described phytoplanktonpatterns in the Cantabrian Sea as typical from temperate seas, (withcharacteristically low density or biomass in winter) spring blooms,and summer stratification inducing a high primary productivityduring these periods. Sporadic small blooms during autumn havealso been described. In this work, we registered high microalgalabundance from May to October and a near-monthly succession offew species blooms. Present results thus appear to corroborate theearlier mentioned pattern, except that the onset of high-densityperiods was delayed to late spring and extended to the autumn,without a clear decline of phytoplankton abundance during thesummer as that reported by Elosegui et al. (1987) in an area closeto our study sites. These differential features were particularlymarked in the estuary. Labry et al. (2001) recorded a winter phy-

toplankton bloom in water samples from the Gironde plume in thenorth of the Bay of Biscay in contrast with our lowest record ofabundance during this season.

Total phytoplankton abundance presented similar seasonaltrends in the two places of study; however frequency and relativedensity of microalgal species differed between estuarine and openshore sites. These differences concern mainly to the habitat of thespecies, particularly diatoms. Benthic microalgae are abundant inshallow sediments and non-adhering species may be easily resus-pended (Baillie & Welsh 1980, de Jonge 1985, Asmus & Asmus1993), so that a greater presence of benthic and intermediate spe-cies of phytoplankton (here collectively designed as tychopelagic)could be expected in samples taken from the estuary. Indeed, 42%of diatoms density corresponded to tychopelagic species in theestuary, compared with 35% in the open shore (Fig. 7a,b).

The species composition recorded in gut contents differed fromthat from the water surrounding the mussels in 2 respects: (a) Anincrease of cell density corresponding to the tychopelagic group ofdiatoms in stomach contents for comparison with water samplescan be observed, irrespective of the sampling site (Fig. 7). In viewof results reported by various authors working with different spe-cies of bivalves (Davis & Marshall, 1961, Shumway et al. 1987,Newell et al. 1989, Kamermans 1994) this could be considered arather general rule and would be attributed to the possibility thatdiet available in the near bottom included a greater proportion ofresuspended microphytobenthos compared with the water columnabove. Muschenheim & Newell (1992) analyzed data of chloro-phyll and carbon concentration and direct cell count in the water at3–5 cm above a mussel bed, to conclude that mussels fed prefer-

Figure 7. Relative abundance (annual average values) of diatoms from different habitats

PHYTOPLANKTON IN STOMACH CONTENT OF MUSSELS 11

Page 9: Phytoplankton Composition of the Stomach Contents of the Mussel Mytilus

entially a high concentration of resuspended benthic diatoms. (b)The distribution of taxonomic groups of microalgae differedgreatly as a consequence of the increased presence of dinoflagel-late and chlorophyta in stomach contents compared with watersamples (Fig. 8). Particularly dinoflagellates, that constitute a mi-nor component in water samples, may reach, on average, 25% or30% of microalgal abundance in stomachs of estuarine and openshore mussels, respectively. It could be argued that the stomachcontents reflected the phytoplankton composition of the water col-umn above the mussel beds 2–3 h before the specimens weresampled. However, the possibility this temporal shift might ac-count for the differences recorded is remote, because preliminaryreports on tidal variation of phytoplankton composition in the areaof study revealed minor differences (own unpublished results).Moreover, the enrichment of stomach fluids in dinoflagellates andchlorophyta, in detriment of the major group of diatoms, has beenbroadly reported in different species of bivalves (Loret et al. 2000,Muñetón-Gómez et al. 2001, Ciocco & Gayoso 2002, Rouillon etal. 2002). The process seems to be a selective one because Rouil-lon (1998) reported, in the scallop Argopecten purpuratus La-marck 1719 that the abundance of dinoflagellates increased in thestomach contents, but the species diversity of this group decreased

in the stomach compared with that in the immediate habitat. In thiswork the abundance of dinoflagellates inside the mussels is mainlybased on the noticeable accumulation of Ensiculifera sp. cells inthe May to June interval, when seawater did not record a specialpresence of these species. This selectivity could be on the basis ofthe extraordinary capacity of accumulation exhibited by differentbivalves in coincidence with short-lasting dinoflagellate blooms(Shumway et al. 1987, Shumway et al. 1994, Sidari et al. 1998),and acquires special relevance with the occurrence of episodicdisease outbreaks associated with the blooming of toxic species.

Concerning the mechanisms underlying the increased presenceof dinoflagellates and chloropyta within the stomach contents ofmussels from both populations, two hypothesis are at least pos-sible: (1) these microalgae could be ingested in preference to dia-toms through the differential retention in the ctenidia and/or se-lection during the pseudofeces forming process; (2) they would befar more resistant to extracellular digestion remaining longerwithin the gut and being preferentially voided with the feces. Thefact that mussels remained emerged for �30 min before collectionmight have reinforced this effect.

If not fully conclusive, available evidence on the subject basedmainly on flow cytometry seems to support the second possibility:

Figure 8. Relative abundance (annual average values) of the main taxonomic groups of phytoplankton in water and stomach samples.

ROUILLON ET AL.12

Page 10: Phytoplankton Composition of the Stomach Contents of the Mussel Mytilus

In a series of experiments with seven species of bivalves fed amixture of microalgae (a dinoflagellate, a diatom, and a crypto-monad flagellate), Shumway et al. (1985) and Cucci et al. (1985)found that most species accumulated dinoflagellate cells in thefeces, although diatoms were also abundant in two cases. Cioccoand Gayoso (2002) reported the presence of two dinoflagellatespecies in the stomachs of A. atra mostly as intact cells, whichsuggest they are not assimilated by the ribbed mussel. Comparingthe relative abundance of two microalgae (a diatom and a nakedflagellate) in the diet, stomach contents, and feces, Rouillon andNavarro (2003) have demonstrated the preferential digestion of thediatom by the mussel M. edulis. This interpretation would be con-sistent with the reported long-term correlation between naturalabundance of diatoms and growth of bivalves (Beukema & Cadee1991, see Introduction).

However, the preferential rejection of diatoms in the pseudofe-ces have also been documented (Shumway et al. 1985, Bougrier etal. 1997), pointing to an alternative mechanism for increasing the

relative abundance of other phytoplankton groups in the ingesteddiet under the conditions of high seston concentration that can beassumed during the occurrence of blooms.

Precise knowledge of characteristics of natural diets availableto bivalve populations, particularly the phytoplankton composi-tion, is of prime importance as regards the understanding of growthand dynamics of these populations (Beukema & Cadee 1991).Comparison of stomach content and seston compositions in termsof frequency and abundance of phytoplankton species constitutes arealistic approach to this subject. However, results are very oftendifficult to interpret because of the various levels of selectioninteracting across the feeding processes of bivalves. Controlledfeeding experiments with natural diets are currently underway atour laboratory, in order for these issues to be readily undertaken.

ACKNOWLEDGMENTS

This work was supported through the Research Group ProjectUPV 154.320-G07/99. G. R. was founded by an AECI grant.

LITERATURE CITED

Asmus, H. & R. M. Asmus. 1993. Phytoplankton-mussel bed interactionsin intertidal ecosystems. In: R. F. Dame, editor. Bivalve filter feedersin estuarine and coastal ecosystem processes. Berlin: Springer-Verlag.pp. 57–84.

Baillie, P. W. & B. L. Welsh. 1980. The effect of tidal resuspension on thedistribution of intertidal epipelic algae in an Estuary. Estuar. Coast.Mar. Sci. 10:165–180.

Balech, E. 1988. Los dinoflagelados del Atlántico Sudoccidental. Madrid:Publ. Espec. Nº 1 IEO. 310 pp.

Berg, J. & R. I. E. Newell. 1986. Temporal and spatial variations in thecomposition of seston available to the suspension feeder Crassostreavirginica. Estuar. Coast. Shelf Sci. 23:375–386.

Beukema, J. J. & G. C. Cadee. 1991. Growth rates of the bivalve Macomabalthica in the Wadden Sea during a period of eutrophication: relation-ships with concentrations of pelagic diatoms and flagellates. Mar. Ecol.Prog. Ser. 68:249–256.

Blanton, J. O., K. R. Tenore, F. Castillejo, L. P. Atkinson, F. B. Schwing &A. Lavin. 1987. The relationship of upwelling to mussel production inthe rias on the western coast of Spain. J. Mar. Res. 45:497–511.

Bougrier, S., A. J. Hawkins & M. Héral. 1997. Preingestive selection ofdifferent microalgal mixtures in Crassostrea gigas y Mytilus edulisanalysed by flow cytometry. Aquaculture 150:123–134.

Ciocco, N. F. & A. M. Gayoso. 2002. Microalgal food of the ribbed musselAulacomya atra (Molina, 1782) in Golfo Nuevo (Patagonia, Argen-tina). J. Shellfish Res. 21(2):497–501.

Clarke, K. R. & R. N. Gorley. 2001. PRIMER v5: user manual/tutorial.Plymouth, England. Primer-E Ltd. 91pp.

Clarke, K. R. & R. M. Warwick. 2001. Change in marine communities: anapproach to statistical analysis and interpretation, 2nd ed. Plymouth,England: Primer-E Ltd.

Cucci, T., S. Shumway, R. C. Newell, R. Selvin, R. Guillard & C. Yentsch.1985. Flow cytometry: a new method for characterization of differen-tial ingestion, digestion and egestion by suspension feeders. Mar. Ecol.Prog. Ser. 24:201–204.

Cupp, E. 1943. Marine plankton diatoms of the west coast of NorthAmerica. Bulletin of the Scripps Institution of Oceanography. Los An-geles: University of California Press. 221pp.

Davis, R. L. & N. Marshal. 1961. The feeding of the bay scallop,Aequipecten irradians. Proc. Nat. Shellfish Assoc. 52:25–29.

Elosegui, A., J. Pozo & E. Orive. 1987. Plankton pulses in a temperatecoastal embayment during the winter-spring transition. Est. Coast. &Shelf Sci. 24:751–764.

Enright, C. T., C. F. Newkirk, J. S. Craigie & J. D. Castell. 1986. Evalu-

ation of phytoplankton as diet for juvenile Ostrea edulis L. J Exp. Mar.Biol. Ecol. 96:1–13.

Epifanio, C. E. 1979. Growth in bivalve molluscs: nutritional effects of twoor more species of algae in diets fed to the American oyster Crassos-trea virginica (Gmelin) and the hard clam Mercenaria mercenaria.Aquaculture 18:1–12.

Fernández, E. 1990. Composición, distribución y producción del fitoplanc-ton en el Cantábrico Central. Ph.D thesis. Universidad de Oviedo.

Gailhard, I., Ph. Gros, J. P. Durbec, B. Beliaeff, C. Belin, E. Nezan & P.Lassus. 2002. Variability patterns of microphytoplankton communitiesalong the French coast. Mar. Ecol. Prog. Ser. 242:39–50.

Grant, J., M. Dowd, K. Thompson, C. Emerson & A. Hatcher. 1993.Perspectives on field studies and related biological models of bivalvegrowth and carrying capacity. In: R. F. Dame, editor. Bivalve filterfeeders in estuarine and coastal ecosystem processes. Berlin, Heidel-berg: Springer-Verlag. pp. 371–420.

Grant, J., C. T. Enright & A. Griswold. 1990. Resuspension and growth ofOstrea edulis: a field experiment. Mar. Biol. 104:51–59.

Hasle, G. R. 1978. The inverted-microscoped method. In: A. Sournia, edi-tor. Phytoplankton manual. United Nations education scientific. PageBrothers Ltd. 382 pp.

Hickman, R. W., R. P. White, J. Illingworth, J. L. Meredith-Young & G.Payne. 1991. The relationship between farmed mussels, Perna canali-culus, and available food in Pelorus-Kenepuru Sound, New Zealand,1983–1985. Aquaculture 99:49–68.

Hummel, H. 1985. Food intake of Macoma baltica (Mollusca) in relationto seasonal changes in its potential food on a tidal flat in the DutchWadden Sea. Neth. J. Sea Res. 19(1):52–76.

de Jonge, V. N. 1985. The occurrence of “epipsammic” diatom popula-tions: a result of interaction between physical sorting of sediments andcertain properties of diatom species. Estuar. Coast. Shelf Sci. 21:607–622.

de Jonge, V. N. & E. E. Van Beusekom. 1992. Contribution of resuspendedmicrophytobenthos to total phytoplankton in the Ems estuary and itspossible role for grazers. Neth. J. Sea. Res. 30:91–105.

Kamermans, P. 1994. Similarity in food source and timing of feeding indeposit-and suspension-feeding bivalves. Mar. Ecol. Prog. Ser. 104:63–75.

Labry, C., A. Herbland, D. Delmas, P. Laborde, P. Lazure, J. M. Froide-fond, A. M. Jegou & B. Sautour. 2001. Initiation of winter phytoplank-ton blooms within the Gironde plume waters in the Bay of Biscay. Mar.Ecol. Prog. Ser. 212:117–130.

PHYTOPLANKTON IN STOMACH CONTENT OF MUSSELS 13

Page 11: Phytoplankton Composition of the Stomach Contents of the Mussel Mytilus

Laing, I. & P. F. Millican. 1986. Relative growth and growth efficiency ofOstrea edulis L. spat fed various algal diets. Aquaculture 54:245–262.

Loret, P., A. Pastoureaud, C. Bacher & B. Delesalle. 2000. Phytoplanktoncomposition and selective feeding of the pearl oyster Pinctada marga-ritifera in the Takapoto Lagoon (Tuamoto Archipielago, FrenchPolynesia): in situ study using optical microscopy and HPLC pigmentanalysis. Mar. Ecol. Prog. Ser. 199:55–67.

Muñetón-Gómez, Ma del S., M. Villalejo-Fuerte & I. Gárate-Lizarraga.2001. Contenido estomacal de Spondylus leucacanthus (Bivalvia:Spondylidae) y su relación con la temporada de reproducción y laabundancia de fitoplancton en Isla Danzante, Golfo de California. Rev.Biol. Trop. 49(2):581–590.

Muschenheim, D. K. 1987. The dynamics of near-bed seston flux andsuspension-feeding benthos. J. Mar. Res. 45:473–496.

Muschenheim, D. K. & C. R. Newell. 1992. Utilization of seston flux overa mussel bed. Mar. Ecol. Prog. Ser. 85:131–136.

Newell, C. R. & S. Shumway. 1993. Grazing of natural particulates bybivalve molluscs: a spatial and temporal perspective. In: R. F. Dame,editor. Bivalve filter feeders in estuarine and coastal ecosystem pro-cesses. NATO ASI series, Vol. G 33. Heidelberg: Springer-Verlag. pp.85–148.

Newell, C. R., S. E. Shumway, T. L. Cucci & R. Sevin. 1989. The effectsof natural seston particle size and type on feeding rates, feeding selec-tivity and food resource availability for the mussel Mytilus edulis L. atbottom culture sites in Maine. J. Shellfish Res. 8:187–196.

Ricard, M. 1987. Diatomophycées. Atlas du phytoplancton marin, vol. II.Edition du Centre National de la Recherche Scientifique. Paris. 297 pp.

Roman, M. R. & K. R. Tenore. 1978. Tidal resuspension in Buzzards Bay,Massachusetts. I. Seasonal changes in the resuspension of organic car-bon and chlorophyll a. Estuar. Coast. Shelf Sci. 6:37–46.

Rouillon, G. 1998. Fitoplancton en el contenido estomacal de concha deabanico (Argopecten purpuratus, Lamarck 1719) de diferentes tallas encultivos suspendidos, Bahía Independencia, Pisco. Tesis para optar eltitulo de Biólogo. Universidad Nacional Mayor de San Marcos, Lima,Peru. 90 pp.

Rouillon, G. & E. Navarro. 2003. Differential utilization of species of

phytoplankton by the mussel Mytilus edulis. Acta Oecologica. 24:S299–S305.

Rouillon, G., J. Mendo & N. Ochoa. 2002. Fitoplancton en el contenidoestomacal de Argopecten purpuratus (Mollusca, Bivalvia) suspendida adiferentes profundidades en Bahía Independencia. In: J. Mendo & M.Wolf, editors. Memorias I Jornada Científica, Reserva Nacional Para-cas, Universidad Nacional Agraria La Molina. 244 pp.

Shumway, S., T. Cucci, R. Newell & C. Yentsch. 1985. Particle selection,ingestion, and absorption in filter-feeding bivalves. J. Exp. Mar. Biol.Ecol. 91:77–92.

Shumway, S., R. Selvin & D. Shick. 1987. Food resources related to habitatin the scallop Placopecten magellanicus (Gmelin, 1791): A qualitativestudy. J. Shellfish Res. 6(2):89–95.

Shumway, S., S. Sherman, A. Cembella & R. Selvin. 1994. Accumulationof paralytic shellfish toxins by surfclams, Spisula solidissima (Dill-wynm 1897) in the Gulf of Maine: seasonal changes, distribution be-tween tissues, and notes on feeding habits. Natural Toxins 2:236–251.

Sidari, I., P. Nichetto, S. Cok, S. Sosa, A. Tubaro, G. Honsell & R. DellaLoggia. 1998. Phytoplankton selection by mussel, and diarrhetic shell-fish poisoning. Mar. Biol. 131:103–111.

Smaal, A. & H. Haas. 1997. Seston dynamics and food availability onmussel and cockle beds. Estuar. Coast. Shelf Sci. 45:247–259.

Tomas, C. R. 1993. Marine Phytoplankton. A guide to naked flagellatesand Coccolithophorids. 1. Marine flagellates, In: J. Throndsen, editorand 2. Modern Coccolithophorids, In: B. Heimdal, editor. United King-dom: Academic Press. 263 pp.

Tomas, C. R. 1996. Identifying marine diatoms and dinoflagellates. 1.Diatoms, In: G. Hasle & E. Syvertsen, editors and 2. Dinoflagellates,In: K. Steidinger & K. Tangen, editors. United Kingdom: AcademicPress Inc. 598 pp.

van den Hoek, C., D. Mann & H. Johns. 1995. Algae: an introduction tophycology. Great Britain: Cambridge University Press. 623 pp.

van der Veer, H. W. 1989. Eutrophication and mussel culture in the West-ern Dutch Wadden Sea: impact on the benthic system: a hypothesis.Helgoland. Meerensunt. 43:517–527.

Varela, M. 1996. Phytoplankton ecology in the Bay of Biscay. Sci. 60:45–53.

ROUILLON ET AL.14