comparing ecological effects of two different types of pollution using multivariate techniques

16
P.S.Z.N. I: Marine Ecology, 14 (2): 113-128 (1993) 0 1993 Paul Parey Scientific Publishers, Berlin and Hamburg Accepted: October 30,1991 ISSN 0173-9565 Comparing Ecological Effects of two Different Types of Pollution Using Multivariate Techniques ARTEMIS NICOLAIDOU~, ARGYRO ZENETOS~, MARIA ANTONIEITA PANCUCCI~ & NOMIKI SIMBOURA~ 1 Zoological Laboratory, University of Athens, Paoepistimiopolis, GR - 15784, Greece. 2 National Centre for Marine Research, HeIlinikon, GR - 16604, Greece. With 6 figures and 1 table Key words: Multivariate analysis, organic pollution, solid wastes. Abstract. The effects of pollution by organic wastes were compared with those caused by dumping of coarse metalliferous residues on the benthic faunas in two areas in Greece. The efficiency of several univariate and multivariate methods in describing these effects was evaluated. Both types of pollution caused a decline in the number of species and diversity, except when dumping of solid wastes took place on finer sediments. There, the above parameters increased due to the increased heterogeneity of the sediment. Pollution by organic matter resulted in increased densities of opportunistic species. Conversely, lack of organic matter in the solid wastes did not enhance settlement of opportunists, with the exception of two species which were thought to benefit indirectly from the slag. The effects of organic pollution were described successfully by all mathematical methods used, while diversity and species abundance curves were not very adequate in describing solid waste pollution. Classification was not very helpful in distinguishing between polluted and clean sites, while ordination proved useful in separating polluted and unpolluted stations as well as the two different types of pollution. Problem Various industrial solid wastes are dumped into the sea as an economical method of disposal. These have received very little attention with regard to disturbance of marine benthic communities. The effects on the bottom fauna of china clay deposits have been studied in Cornwall by HOWELL & SHELTON (1970) and PROBERT (1975). BAMBER (1983) examined the impact of fly ash on benthos off the Northumberland coast, while BOURCIER (1969), BOURCIER & ZIBROWIUS (1973), and BLACKMAN & WILSON (1973) have studied the effects of “red mud” - the residual waste from the extraction of aluminum from bauxite. Brief mention of biological effects of mine waste disposal is made by GOYEITE & NELSON (1977) for an area in British Columbia and by WONG et al. (1978) for an area in Hong Kong. The environmental impact of marine and coastal mines is reviewed by ELLIS (1987). U.S. Copyright Clearance Center Code Statement: 0173-9565/93/1402-0113$02.50/0

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P.S.Z.N. I: Marine Ecology, 14 (2): 113-128 (1993) 0 1993 Paul Parey Scientific Publishers, Berlin and Hamburg

Accepted: October 30,1991

ISSN 0173-9565

Comparing Ecological Effects of two Different Types of Pollution Using Multivariate Techniques ARTEMIS NICOLAIDOU~, ARGYRO ZENETOS~, MARIA ANTONIEITA PANCUCCI~ & NOMIKI SIMBOURA~

1 Zoological Laboratory, University of Athens, Paoepistimiopolis, GR - 15784, Greece. 2 National Centre for Marine Research, HeIlinikon, GR - 16604, Greece.

With 6 figures and 1 table

Key words: Multivariate analysis, organic pollution, solid wastes.

Abstract. The effects of pollution by organic wastes were compared with those caused by dumping of coarse metalliferous residues on the benthic faunas in two areas in Greece. The efficiency of several univariate and multivariate methods in describing these effects was evaluated. Both types of pollution caused a decline in the number of species and diversity, except when dumping of solid wastes took place on finer sediments. There, the above parameters increased due to the increased heterogeneity of the sediment. Pollution by organic matter resulted in increased densities of opportunistic species. Conversely, lack of organic matter in the solid wastes did not enhance settlement of opportunists, with the exception of two species which were thought to benefit indirectly from the slag. The effects of organic pollution were described successfully by all mathematical methods used, while diversity and species abundance curves were not very adequate in describing solid waste pollution. Classification was not very helpful in distinguishing between polluted and clean sites, while ordination proved useful in separating polluted and unpolluted stations as well as the two different types of pollution.

Problem

Various industrial solid wastes are dumped into the sea as an economical method of disposal. These have received very little attention with regard to disturbance of marine benthic communities. The effects on the bottom fauna of china clay deposits have been studied in Cornwall by HOWELL & SHELTON (1970) and PROBERT (1975). BAMBER (1983) examined the impact of fly ash on benthos off the Northumberland coast, while BOURCIER (1969), BOURCIER & ZIBROWIUS (1973), and BLACKMAN & WILSON (1973) have studied the effects of “red mud” - the residual waste from the extraction of aluminum from bauxite. Brief mention of biological effects of mine waste disposal is made by GOYEITE & NELSON (1977) for an area in British Columbia and by WONG et al. (1978) for an area in Hong Kong. The environmental impact of marine and coastal mines is reviewed by ELLIS (1987).

U.S. Copyright Clearance Center Code Statement: 0173-9565/93/1402-0113$02.50/0

114 NICOLAIDOU, ZENETOS, PANCUCCI & SIMBOURA

Conversely, numerous papers have been published on the biological effects of organic enrichment in the marine environment. With reference to benthic communities, PBRks & BELLAN (1972) summarize the impact of organic pollu- tion in benthic populations, and PEARSON & ROSENBERG (1978) examine the succession in macrobenthic communities in relation to organic enrichment of the marine environment.

Multivariate analyses have been often used in community ecology (GAUCH, 1982) to delimit communities and to describe trends in them, but only recently have they begun to be used in environmental pollution studies (BLOOM, 1980; MRZA & GRAY, 1981; GRAY et al., 1988; HEIP et al., 1988; PAPATHANASSIOU & ZENETOS, in press).

The aim of this paper is to compare some of the most recently developed graphicaYdistributiona1 and multivariate techniques with those traditionally used in describing the effects of pollution by organic matter and solid waste in benthic communities. It also tests the sensitivity of these methods in distinguish- ing the ecological effects of the two different types of pollution.

Material and Methods

The benthos off Larymna was studied as part of the assessment of the environmental impact of dumping in the area (NICOLAIDOU et at., 1989). The present study takes six stations into consider- ation (Fig. 1). They were chosen to include two polluted stations (station 5 in the centre of the spoil patch and station 9 at its border), two clean stations (2 and 3) with similar sediment sue composition

Fig. 1. Sampling sites.

Comparing pollution effects by multivariate techniques

Table 1. Environmental parameters and community indices.

sta- depth sediment slag sand organic C no. of no. of diversity evenness tions m type Yo Yo YO species indiv.

.0.2m-2 .m-z

115

2 3 5 9 7 8 E F Y Z

58 51 75 80 84 85 36 31 72 85

muddy sand muddy sand

sand muddy sand

mud mud

muddy silt muddy sand muddy sand muddy sand

3.4 89 0.3 81 0 62 0.3 81

97.6 95 1.2 25 47.1 61 0.6 33 0 1 1 19 0 3 0.9 28 0 33 5.1 6 0 43 3.6 24 0 71 2.3 80 0 62 1.3 95

1595 1625 970 370 430 295

2926 12342 2505 1910

5.503 5.291 2.461 4.056 2.497 4.169 0.926 2.551 4.893 5.821

0.895 0.861 0.546 0.829 0.606 0.894 0.358 0.557 0.773 0.886

as the polluted ones, and two clean stations (7 and 8) with finer sediments. The last two stations were included because dumping also took place on fine sediment.

In the innermost part of Saronikos Gulf, the benthos was studied in relation to the nutrient and oxygen conditions (ZENETOS & BOGDANOS, 1987; FRILIGOS & ZENETOS, 1988). Here, four stations were chosen at different distances from the sewer outfall; they show a gradient of organic carbon in the sediment (Table I).

In both locations, two samples per station were taken with a 0.1m2 Van Veen grab, sieved through a 1 mm sieve, stained with Rose Bengal, and preserved in 4 % formalin.

The sediment analysis was carried out by the geological laboratory of the National Centre for Marine Research, Athens. The pipette method was used and the nomenclature is after FOLK (1954). The diversity of the fauna was calculated by the SHANNON-WIENER diversity index using the logz basis (SHANNON & WEAVER, 1963). The Principal Component Analysis (PCA) and the Multidimen- sional Scaling (MDS), based on Bray-Curtis similarity, were performed using the software package “PRIMER developed in the Plymouth Marine Laboratory, U.K. For the Correspondence Analysis the method of BENZECRI et al. (1973) was used. In the analyses, species found only at one station and in numbers lower than three individuals were excluded from the calculations. The data were transformed by Y = log (X + 1). The package “PRIMER was also used to plot the distribution of individuals among species (in geometric abundance classes) (GRAY & MIRZA, 1979; PEARSON et al., 1983) and the K-dominance curves (LAMBSHEAD et nl., 1983; CLARKE, 1990).

The depth and sediment characteristics of the sampling stations are shown in Table 1, which also summarizes the number of species, number of individuals, and diversity at each station. In Larymna, 157 species were found. The lowest number of species, 19, was found in the clean Station 7 with muddy sediment and the highest in the clean sandy Stations 2 and 3. The last two stations also had the greatest number of individuals, 1595 and 1625 indiv. e r n - * , respectively. The lowest number of individuals, 295 indiv. was found at Station 8. The diversity was highest at the clean sandy stations, followed closely by Station 9 at the edge of the polluted patch. Lowest diversity was observed at the polluted sandy Station 5 and at the clean but muddy Station 7.

It is clear that in Larymna, the diversity was influenced both by pollution and sediment particle size. Figure 2 shows the diversity plotted against the percen-

116 NICOLAIDOU, ZENETOS, PANCUCCI & SIMBOURA

Fig. 2. Relation between diver- sity and percentage of sand in the sediment. 2

\ W .z 0 -

E

*z 3 *Y

9

5

0 20 40 60 80 100

x sand

tage sand (coarse fraction) in the sediment: the finer stations 7 and 8 clearly had the lowest diversity among the clean stations. €onversely, between stations with approximately similar sediments (e. g., E and F; Y and Z ) , the highest diversity was observed at the cleaner stations (F and Z , respectively).

The abundance of individual species remained generally low, mostly below 50 indiv. - m-2, over the whole sampling area of Larymna. The most abundant were the cirratulid polychaete Thuryx rnurioni at Station 7 (200 indiv. * m-*) and the bivalve Kellyetlu miliuris (590 indiv. - m-2) at Station 5 . In the present survey, the latter species was only found in the polluted Stations 5 and 9, as was the bivalve Leptuxinus ferruginosus. Some species absent in the polluted stations were not found in large numbers when present elsewhere.

In the area of Saronikos, 137 species were found. The station closest to the outfall had only 6 species, while the largest number, 95 species, was observed at Station Z , farthest from the outfall. The diversity increased with increasing distance from the pollution source and ranged from 0.9 at Station E to 5.8 at the farthest Station Z (Fig. 2). The maximum number of individuals (12342 indiv. . m-’) was at Station F, immediately outside the highly polluted zone. Many species were missing from the polluted stations, while others were found there, either exclusively or in very large numbers. These species include: Cupitellu cupituta, with a maximum density of 689 indiv. . m-2, Cirrutulus cirratus (4344 indiv. . m-*), Polydoru untennutu (2266 indiv. - Prionospio mulmgreni (1266 indiv. . m-2), Scolelepis fuliginosu (2378 indiv. - m-2), and Scolelepis girurdi (2700 indiv. . m-2). Most of the above species have been described by BELLAN (1967) as indicators of organic pollution.

Comparing pollution effects by multivariate techniques 117

:I 50

0

"j\ 10 , I , i

0

I 111 v VII IX

I\, ,@,I,[,, ;/,,,,,,,(r:,, , ,,,w I 111 v VII IX I 111 v VII IX I L\ 111 v MI IX I Ill v VII IX

geomelric abundance classes

Fig. 3. Distribution of individuals among species. Percentage of species in each abundance class, where: 0 < 1; I : 1; I1 : 2-3; 111 : 4-7; IV: 8-15; V : 16-31; VI : 32-63; VII : 64-127; VIII : 128-255; IX : 256-511.

1 10

species rank

Fig. 4. Plot of the k-dominance curves for abundance at all stations.

118 NICOLAIDOU, ZENETOS, PANCUCCI & SIMBOURA

3

axis 1

Fig. 5. Position of stations on axes 1 and 2 derived from Principal Component Analysis.

D

Fig. 6. Non-metric Multidimensional Scaling (MDS) plot in two dimensions for the benthic com- munities at all stations.

Comparing pollution effects by multivariate techniques 119

A list of all the species encountered in both areas is given in the Appendix. The distribution of species per geometric abundance class is shown in Fig. 3.

In Larymna the lines show no great difference between clean and polluted coarse stations. In all stations the majority of species occur in the first 4 abundance classes, and the highest classes represented are between IV and VI. Only station 5 has an additional abundance class, although it does not contain a great percentage of species. Quite similar curves are produced for the fine Stations 7 and 8; their main difference from the previous set of stations is that here most species have single occurrences, so the decline in the first three abundance classes is much more rapid.

In Saronikos Gulf the abundance distribution curves reflect the horizontal gradient of organic carbon in the sediment. The clean stations Y and Z bear a high percentage of species represented by a few specimens, with the highest abundance class present being class VIII. In the more polluted stations the contribution of rare species decreases, with the highest abundance class being X.

The k-dominance curves in Fig. 4 show an apparent difference in the patterns of the highly polluted stations. The situation is much clearer for the Saronikos area, where the curves of the more polluted stations are more elevated. In Larymna the non-polluted but fine station 7 has a pattern similar to the polluted coarse station 5, while the coarse polluted station 9 joins the clean stations.

The Principial Component Analysis, applied to both sets of data from Larymna and Saronikos together, failed to distinguish between clean and polluted stations. Although the coarse clean stations are ordinated at higher scores on axis 2, the fine clean stations are placed together with the polluted ones. (Plot of stations on axes 1 and 2 is shown in Fig. 5.)

Correspondence analyses applied to the same data (graphs not plotted here) was sufficient only to isolate extremely different stations. Thus, the organically enriched stations E and F had low scores on axis 1 as opposed to all the other stations, while station 5, with its high slag content, was separated from the rest on axis 3.

The picture produced by the MDS (Fig. 6) is much clearer. The clean stations are on the lower left side of the diagramme, the polluted ones towards the upper right. In addition, there is a distinction between fine and coarse clean stations and between the two different types of pollution.

Discussion

Although there were differences in the physical environment at each site, the data obtained seemed sufficient for at least a preliminary comparison between the effects of the two types of pollution. In Saronikos Gulf, the increase in organic carbon in the sediment coincided with an initial increase in the numbers of species; this was followed by a drastic decline in the most polluted stations. The number of specimens also increased initially, reaching a maximum coincid- ing with the maximum of opportunistic species and dropping again at the heavily polluted stations. Some species which were present in low numbers, if at all, in the clean stations increased under low levels of organic pollution (station F) and

120 NICOLAIDOU, ZENETOS, PANCUCCI & SIMBDURA

were eliminated again in the heavily polluted station (E). This relation has been described in many other cases of organic pollution by PEARSON et al. (1983). Such a change in the number of species and individuals conforms to the model proposed by PEARSON & ROSENBERG (1978). At even higher levels of organic pollution (ROSENBERG, 1980), oxygen becomes depleted, the redox potential discontinuity rises in the sediment, and the sulfur ion concentration increases. The induced stress successively kills most of the species, leaving those adapted to reduced oxygen conditions as the last survivors. Also, in the most enclosed part of Saronikos Gulf, in Elefsis Bay, the water becomes stratified later in the summer and anoxic conditions occur. This leads to mass mortality, with some areas becoming completely azoic (ZARKANELLAS, 1979; FIULIGOS & ZENETOS, 1988).

The effects of solid waste dumping in Larymna were not as dramatic. The dumped residue is believed to have principally a mechanical effect on benthic animals, either killing them by burial or making the environment too unstable for most species to survive (CARTER, 1975). Here, the number of species and specimens also decreased in the highly polluted area compared with stations having sediments of similar particle size composition. Dumping on finer sedi- ments, however, leads to an increase in the number of species and individuals and in diversity. This is due to the admixture of coarse dumping material with the underlying fine sediments: mixed sediments have higher diversity than homogeneous coarse or fine sediments (see review by GRAY, 1974). Sediment modification by dumped material has implications concerning the use of diver- sity in environmental impact assessments. A reduced diversity has been con- sidered as one of the ecosystem stress symptoms by RAPPORT ef al. (1985) and SCHINDLER (1987), and GRAY (1989) mentions several examples to that effect. Concerning pollution by solid wastes in particular, BOURCIER (1969) and PROB- ERT (1975) recorded decreases in diversity due to dumping of industrial solid wastes, although in their case the dumped material was finer than the native sediment.

Diversity indices have been recommended by STIRN (1981) as a good measure for the detection and assessment of all forms of marine pollution. The same author stresses, however, that comparisons should be made over a uniform environment. It seems justified to suggest that diversity be used with caution in assessing effects of pollution by solid wastes.

In Larymna, as opposed to Saronikos, there was no spectacular increase in density of the opportunistic species usually found in organically enriched or disturbed areas. The presence of opportunistic species such as Capifella capitusa and the spionids Polydora, Prionospio, and Scolelepis in polluted areas has been attributed more to their life-history strategy (r-selection) than to their increased tolerance (GRAY, 1979). CHESNEY & TENORE (1985) found that the size of laboratory populations of C. cupifata reflected the nutrient levels available, and GREMARE ef ul. (1989) showed that the whole population cycle, including reproduction and secondary production, was driven by food availability. Tsw- TSUMI (1987) even suggested that large amounts of organic matter are a physiological prerequisite in order for C. capitafu to maintain individual and population growth. C. cupituta has been found to recolonize areas defaunated by disturbances other than organic pollution, but perhaps the conditions in such

Comparing pollution effects by multivariate techniques 121

areas were not as oligotrophic as in Larymna. This must certainly be true in the case of recolonization after a red tide (SIMON & DAUER, 1977) and an oil spill (SANDERS et al., 1980), where sources of carbon were made available. In the absence of organic matter in Larymna, there was little incentive for most opportunistic species to colonize. Two species, however, K. miliaris and L. fer- ruginosus, did increase in polluted Larymna sites. It is speculated that the same factor, i. e. food availability, may be responsible here. A number of Lucinacea (SPIRO et al., 1986; DANDO & SOUTHWARD, 1986; KUZNETSOV & OHTA, 1989), to which the above species belong, are known to obtain a substantial proportion of their nutrition from autotrophic symbionts. It is possible that certain symbiotic bacteria use inorganic compounds found in the tailings for chemosynthesis. One possible pathway would be the oxidation of FeS in the tailings; this would release the Fe found abundantly in the shells of the two species in Larymna. This matter merits further investigation.

The absence of opportunistic species in Larymna was reflected in the species abundance curves. The basic difference in the curves of the polluted sites only involved a drop in the number of rare species, not an increase of high abundance classes as was evident in the Saronikos area. Thus, this method was less sensitive in detecting solid waste pollution than pollution by organic matter. Similar conclusions were also drawn by RYGC (1986), who reported that toxic pollution by copper in the sediment did not cause deviation from the log normal distribution. Perhaps the method is not applicable in oligotrophic areas to detect pollution other than that by organic matter.

Similarly, the k-dominance curves were more sensitive in the organically enriched area of Saronikos.

The multivariate methods are known to have greater sensitivity and general- ity than univariate methods (GRAY et al., 1990; WARWICK & CLARKE, 1991). From the three ordination techniques applied here, the MDS was better in distinguishing polluted and clean stations as well as the two different types of pollution. It is suggested that the initial application of the MDS is a reasonable approach in situations where discrimination of various types of pollution over a varied environment is desired. On the other hand, the complementary use of univariate methods such as diversity indices and graphicaVdistributiona1 methods, including k-dominance curves and geometric abundance classes, would help to quantify the observed stress.

Summary

Several univariate and multivariate statistical methods were used to compare the effects of organic pollution on the benthic fauna with those caused by dumping of coarse metalliferous residues. Organic pollution was studied in Saronikos Gulf in the vicinity of the Athens sewer outfall, while the effects of tailings were examined at Larymna in the N.Evoikos Gulf; both sites are in Greece.

Organic pollution in Saronikos caused a decline in the number of species and diversity and an increase in the density of opportunistic species such as Capitella capitata, Cirratulus cirratus, Polydora antennata, Prionospio rnalmgreni,

122 NICOLAIDOU, ZENETOS, PANCUCCI & SIMBOURA

Scolelepis fuliginosa, and Scolelepis girardi. At the dumping site in Larymna the number of species and individuals also decreased with increased level of pollution, except when the coarse wastes were dumped over finer sediments. In the latter case, the above parameters increased due to sediment heterogeneity.

The low level of organic carbon in Larymna did not increase the number of opportunistic species. The density of two otherwise rare molluscan species - the bivalves Kellyella miliaris and Leptaxinus ferruginosus - did increase there. It is speculated that these bivalves obtain their nutrition from symbiotic auto- trophic bacteria which in turn are favoured by the inorganic compounds found in the tailings.

The absence of oppurtunistic species at the dumping site was reflected in the species abundance curves; they proved unsuitable to detect pollution by solid wastes in this oligotrophic area.

Similarly, the k-dominance curves were sensitive only in the organically enriched area of Saronikos.

Of the three ordination techniques applied (Principal Component Analysis, Correspondence Analysis, and Multidimensional Scaling), the MDS was better in distinguishing polluted and clean stations as well as the two different types of pollution.

Acknowledgements

The authors are grateful to Prof. J. S. GRAY for his useful suggestions and correction of the original manuscript and to an unknown referee for his constructive criticism.

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Appendix

Larymna Saronikos

Polychaeta Acesta sp. Ampharete aculifrons (HESSLE) Ampharetidae sp. Amphicteis gunneri (SARS) Amphictenidae sp. Ancistrosyllis sp. Anobothrus gracilis (MALMGREN) Anfinoe sp- Aricidea capensis DAY Aricidea claudiae LAUBIER Aricidea fauveli HARTMAN Aricidea sp. Armandia cirrosa FILIPPI Asychis biceps SARS Asychis goroi ( I z u u ) Bhawania reyssi KATZMANN, LAUBIER & ~ M O S Capitella capitafa (FABRICIUS) Cauleriella alata (SOUTHERN)

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Chaetopteridae sp. Chaetozone setosa MALMGREN Chone duneri MALMGREN Chone filicaudata SOUTHERN Cirratulus cirratus (MULLER) Cirratulus filiformis KEFERSTEIN Cirrophorus branchiatus EHLERS Cirrophorus sp. Clymenura clypeata (SAINT-JOSEPH) Cossura coasta KITAMORI Dasybranchus caducus GRUBE Ditrupa arietina (MULLER) Drilonereis filum (CLAPAREDE) Ehlersia cornuia RATHKE Eteone longa (FABRICIUS) Euclymene lumbricoides QUATREFAGES Euclymene oerstedi CLAPAREDE Eunice vittata (DELLE CHIAJE) Euratella salmacidis (CLAPAREDE) Eusyllis sp. Exogone verugera (CLAPAREDE) Glycera convoluta KEFERSTEIN Glycera rouxii AUDOUIN & M. EDWARDS Glyceridae sp. Glycinde normanii (MALMGREN) Goniada maculata OERSTED Harmothoe lunulata (DELLE CHIAJE) Harmothoe sp. Hesionidae sp. Hyalinoecia bremenii FAUVEL Hyalinoecia fauveli RIOJA Hyalinoecia tubicola (0. F. MULLER) Hydroides norvegica GUNNERUS Inermonephthys inermis (EHLERS) Lagis koreni (MALMGREN) Lanice conchilega (PALLAS) Laonice cirrata (SARS) Lepidasthenia maculata Dons Loimia medusa (SAVJGNY) Lumbrineris fragilis (0. F. MULLER) Lumbrineris gracilis EHLERS Lumbrineris impatiens CLAPAREDE Lumbrineris emandibulata mabiti F!AMOS Lumbrineris latreilli (AUDOUIN & M. EDWARDS) Lygdamis murata (ALLEN) Magelona minuta ELIASON Malacoceros fuliginosa (CLAPAREDE) Malacoceros girardi QUATREFAGES

Maldanidae sp. Marphysa belli (AUDOUIN & M. EDWARDS) Marphysa kinbergi MCINTOSH Marphysa sanguinea (MONTAGU) Mellina palmata GRUBE Myriochele heeri MALMCREN Neanthes caudata (DELLE CHIAJE) Nematonereis unicornis (GRUBE)

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Nephthys hystricis MCINTOSH Ninoe armoricana GLEMAREC Notomastus latericeus SARS Onuphis eremita AUDOUIN & M. EDWARDS Orbinia cuvieri AUDOUIN & M. EDWARDS Owenia fusiformis DELLE CHIAJE Paradoneis armata GLEMAREC Paradoneis lyra (SOUTHERN) Paralacydonia paradoxa FAWEL Paraonis sp. Paraprionospio pinnata (EHLERS) Pectinaria auricoma (0. F. MULLER) Pectinaria sp. Phyllodocidae sp. Pilargis verrucosa SAINT-JOSEPH Pista crisrata (MULLER) Podurke pallida CLAPAREDE Poecilochaetus serpens ALLEN Polydora antennata CLAPAREDE Polydora flava CLAPAREDE Praxillella gracilis (SARS) Prionospio cirrifera WIREN Prionospio ehlersi FAUVEL Prionospio malgremi CLAPAREDE Prionospio sp. Prionospio steenstrupi MALMGREN Pseudocapitella incerta FAUVEL Pseudo fabriciola sp . Pseudomystides limbata nigrolineata RIOJA Subellidae sp. Sarsonuphis quadricuspis (SARS) Scalibregma inflatum RATHKE Schistomeringos rudolphi (DELLE CHIAJE) Seprula concharum LANGERHANS Sigambra parva (DAY) Sphuerosyllis pirifera CLAPAREDE Spio decoratus BOBRETZKY Spiochaetopterus costarum (CLAPAREDE) Spiophanes bombyx (CLAPAREDE) Spiophanes kroyeri GRUBE Syllidae sp. Syllis brevipennis GRUBE Tachytrypane jeffreysii MCINTOSH Tuuberia gracilis (TAUBER) Tauberia multibranchiata HARTMAN Tuuberia reducta (HARTMAN) Tuuberia sp. Terebellides stroemi SARS Tharyx heterochaeta (LAUBIER) Tharyx marioni (SAINT-JOSEPH)

Mollusca Abra alba (W. WOOD) Abra longicahs (SCACCHI)

Abra nitida (MULLER) Acanthocardium paucicostata (C. B. SOWERBY) Culyptruea chinensis (LINNAEUS)

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Cingula proxima (ALDER) Clausinella fasciata (DA COSTA) Corbula gibba (OLIVI) Cuspidaria costelata (DESHAYES) Cylichna cylindracea (PENNANT) Dentalium sp. Dentalium vulgare DA COSTA Diplodonta brocchi (DESHAYES) Falcidens gutturosus KOWALEVSKY Gastropoda sp. Glans aculeata (POLI) Gouldia minima (MONTAGU) Hiatella arcrica (LINNAEUS) Isocardia sp. Kellyella miliaris (PHILIPPI) Leptaxinus ferruginosus (FORBES) Lepton nitidum TURTON Lima loscombei SOWERBY Loripes lacteus (LINNAEUS) Macoma balaustina (LINNAEUS) Montacuta substriata (MONTAGU) Musculus rnarmoratus (FORBES) Myriea spinifera (MONTAGU) Neolepton obliguatum (MONTEROSATC Nucula hanleyi WINCKWORTH Nucula nucleus (LINNAEUS) Nucula sulcaia BRONN Nucula turgida WINCKWORTH Nuculana fragilis (CHEMNITZ) Nuculana pella (LINNAEUS) Parvicardium scabrum (TURTON) Philine catena (MONTACU) Philine scabra (MULLER) Rissoa sp. Scissurella costata D’ORBIGNY Tellimya ferruginosa (MONTAGU) Tellina donacina LINNAEUS Tellina nitida POLI Tellina serrata BROCCHI Thracia papyracea (POLI) Thyasira alleni CARROZZA Thyasira jlexuosa (MONTAGU) Timoclea ovata (PENNANT) Venerupis luscens (LOCARD)

Crustacea Alpheus sp. Amphipoda sp. Anthura gracilis (MONTAGU) Apseudes sp. Brachiura sp. Callianassa subterranea (MONTAGU) Corophium rotundirostre STEPHENSEN Cumacea sp. Cumopsis sp. Decapoda sp. Dexamine spinosa (MONTAGU)

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Eurydice spinigera HANSEN Coneplax rhomboides (LINNAEUS) Harpinia pectinata SARS Isopoda sp. Leptocheirus hirsutimanus (BATE) Leptocheirus mariae KARAMAN Leptochelia savigny (KROYER) Leucothoe spinicarpa SARS Lophogaster tipicus SARS Macrura sp. Microdeutopus siationis DELLA VALLE Mysidacea sp. Ostracoda sp. Pantopoda sp . Phtisica marina SCABBER Processa sp. Pseudoniphargus sp. Stenothoe sp.

Echinodermatn Amphipholis squamata (DELLE CHIAJE) Amphiura jiliformis (0. F . MULLER) Amphiura sp. Asterina sp . Echinoideu juv. sp. Labidoplax digitata (MONTAGU) Leptopentacta elongata (DUBEN & KOREN) Ocnus planci (BRANDT) Ophiura albida (FORBES) Ophiura sp . Ophiuroidea juv. sp.

Miscellanea Actiniaria sp. Anthozoa sp . Aspidosiphon muelleri DIESING Brachionopoda sp . Foraminifera sp. Gastrotricha sp. Golfingia sp. Hydrozoa sp. Nematoda sp. Nemertinea sp . Oligochaeta sp. Onchnesoma steenstrupi KOREN & DANIELSSEN Phascolion strombi (MONTAGU) Phascolosoma granulatum LEUCKART Phoronis muelleri SELYS LONGCHAMP Podocoryna carnea SARS Porifera sp. Sipunculoidea sp .

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