e-mail: msim@ncmr.gr
Abstract
A general scheme for approaching the objective of Ecological Quality Status (EcoQ) classification of
zoobenthic marine ecosystems is presented. A system based on soft bottom benthic indicator species and
related habitat types is suggested to be used for testing the typological definition of a given water body in the
Mediterranean. Benthic indices including the Shannon-Wiener diversity index and the species richness are
re-evaluated for use in classification. Ranges of values and of ecological quality categories are given for the
diversity and species richness in different habitat types. A new biotic index (BENTIX) is proposed based on
the relative percentages of three ecological groups of species grouped according to their sensitivity or tolerance
to disturbance factors and weighted proportionately to obtain a formula rendering a five step numerical scale
of ecological quality classification. Its advantage against former biotic indices lies in the fact that it reduces
the number of the ecological groups involved which makes it simpler and easier in its use. The Bentix index
proposed is tested and validated with data from Greek and western Mediterranean ecosystems and examples
are presented. Indicator species associated with specific habitat types and pollution indicator species, scored
according to their degree of tolerance to pollution, are listed in a table. The Bentix index is compared and
evaluated against the indices of diversity and species richness for use in classification. The advantages of the
BENTIX index as a classification tool for ECoQ include independence from habitat type, sample size and
taxonomic effort, high discriminative power and simplicity in its use which make it a robust, simple and
effective tool for application in the Mediterranean Sea.
Fig 1: Flow diagramme of typology and classification processes using benthic invertebrate fauna.
Terrigenous Muds (VTC) biocoenoses disturbance and stress, are considered as forms
originally is described from the Circalittoral of pressure or pollution. Many authors have
zone 1. However, in Greek ecosystems it is summarised the adaptive strategies towards
usually met also in closed gulfs of shallower pollution into three (GRAY, 1979) four
depths encountered in 20-30m. So, for the (SALEN-PICARD, 1983) and five ecological
purpose of this work it shall be called as the groups according to their sensitivity to an
habitat of muds. Generally, the scheme increasing stress gradient (HILY, 1984;
adopted for the classification of habitats into GLÉMAREC, 1986; MAJEED, 1987;
types is based on the factors of depth, type of GRALL & GLÉMAREC, 1977; BORJA et
substrate, and phytal cover. al., 2000). Among these authors BORJA et al.,
(2000) proposed a biotic index receiving
c) Development of a Biotic index (BENTIX) continuous values as a function of the relative
Soft bottom macrobenthic communities abundance of the ecological groups present.
respond to environmental disturbance or stress The formula of BORJA et al., (2000) was based
by means of different adaptive strategies. on the percentages of five ecological groups
GRAY (1981a) considers that pollution effects weighting their contribution with use of
can be separated into two categories: different factors. The concept of the new
disturbance and stress, but in this work this Bentix index lies in the reduction of the
distinction is not taken into account and both ecological groups involved in the formula, in
1 Circalittoral is defined as the bathymetric zone with upper limit the lowest extent of the marine angiosperms
(around 35m) and with lowest (deepest) limit the lowest extent of sciaphilic algae (70-120m).
the sediment is azoic (all groups zero). were tested using data from various sites with
Numeric values between 2 and zero are non- known environmental pressures.
existent in the scale because if GI is zero the The Bentix index applies to all kind of
Bentix index is 2. A classification system of soft marine soft bottom benthic data. A refinement
bottom macrozoobenthic communities is of the upper limits of the scale is required in
proposed based on the Bentix index and the case only of a type of habitat which is
including five levels of ecological quality (table considered as physically stressed as is the
3). The boundaries between classes were set habitat of muds. In this case the nature of the
keeping equal distances among classes limited substratum with high percentage of fine
only by the two extremes of the scale (2-6) and particles favours the accumulation of organic
matter. In addition the circulation regime in work are mean values from a number of
muddy very sheltered bays and the replicates within a site and from a number of
morphological conditions naturally favour the sites within the same geographic area and
accumulation of nutrients and the stratification habitat type.
of the water column. Thus the benthic fauna
is normally dominated by some tolerant e) A total of 26 data sets (Table 2) covering 32
species, typical of mud (scored with 2) reducing geographic areas within Greece and the
the Bentix index even if the conditions are Mediterranean (Algeria, Lyon gulf, Turkish
undisturbed by human activities. Aegean coasts) are used in order to test and
A possible refinement of the limits of the validate the methods proposed. The data
Bentix scale for use in the muddy habitats originate from published documents, NCMR
would change the moderate class range from technical reports and/or unpublished data in
2.5-3.5 to 2.5-3, the good quality class from 3.5- the possession of the authors, communicated
4.5 to 3-4 and the high quality class from 4.5-6 data from colleagues all over the
to over 4. This suggestion was based on tests Mediterranean etc. The data was used and run
using benthic data from coastal muddy habitats in its analytical format referring to the standard
with known environmental pressures. sample size unit.
status are structured with GI representing less the derived EcoQ level in the three types of
than 13% of the fauna, GII over 30% and GIII habitats.
over 50% reaching 100%. For moderate quality To validate the Bentix index some water
status GI species represent less than 30%, GII quality parameters as the Particulate organic
over 13% and up to 88% and GII may reach Carbon concentration in seawater (POC), the
75% of the fauna. In the good quality status the Dissolved Oxygen concentration near the
contribution of GI sensitive species rises to over bottom (DO) and the percentage Organic
38%, GII is between 37 and 57% and GII is less Carbon content of the sediment (OC), were
than 15%. Finally high quality status is plotted against the Bentix index in the sampled
characterised by GI over 68%, GII around 30% stations (Fig. 4). The values of the abiotic
and GIII contributes less than 4%. parameters used in the scatter diagramms are
the mean annual values of the year 2000 (table
b) Validation of the method 4).
To validate the new tool of Bentix index a As seen in Figure 4a the index increases
Greek area was chosen that presents various with Dissolved Oxygen increasing and the DO
types of habitats and levels of quality status: reaches the maximum value of 4.97 ml/l
Saronikos Gulf. corresponding to the maximum value of the
Saronikos gulf receives the pressures of Bentix (4.27) and high EcoQ. The Spearman
organic pollution mainly originating from the rank correlation between DO and the Bentix
Psittalia central outfall of Athens metropolitan is statistically significant (p<0.01). The
area (NCMR, 2001a). The area, (including the Particulate Organic carbon concentration in
innermost very enclosed Elefsis Bay) presents seawater on the other hand shows a decrease
all levels of water quality and three types of with the increase of the index (Fig. 4b) but this
habitats, namely muddy sand, sandy mud and negative relationship is not statistically
mud. In December 2000, 24 stations were significant. The concentration of the Organic
sampled using a box corer with 0.1m2 sampling Carbon in the sediment (OC) shows a similar
surface. The stations are located in Saronikos pattern with POC (negative relationship with
gulf with increasing distance from the site of the Bentix index, although again not
station S7 in Psittalia where there is the outfalls statistically significant) reaching the lowest
of the sewage primary treatment plant (Fig. value of 0.35% in the highest EcoQ station with
3). Table 4 shows the values of the biological the Bentix index reaching the highest value of
indices, namely the community diversity (H’), 4.95 (Fig. 4c). In conclusion, the water and
the evenness of distribution J (PIELOU, 1969), sediment quality attributes are directly
the species richness (S), the Bentix index and reflected to the Bentix index.
87
Fig. 5: Trends in species richness (S) in the 5 ecological classes in shallow muddy sands related to an oil
spill in S. Evvoikos Gulf.
Table 5
Range of species variety (S) and community diversity (H’)
for different sampling units and habitat types.
Sampling surface S min H’ min Polluted S max H’ max Reference
0.05m2 5.3 0.78 coarse sands 88.5 5.79 Coarse sands
0.1m2 3.3 0.78 deltaic 124 6.06 Coarse sands
0.2m2 11.8 1.21 sandy muds 126 6.30 Muddy sands
0.5m2 28 1.82 fine sands 187 6.68 Muddy sands
studied are plotted in combination with the values of 5.46 and 5.52 respectively ranks them
Bentix index showing also the EcoQ according to the high EcoQ. This is explained by the fact
to the Bentix in increasing order. It is apparent that H’ encompasses both species richness and
that the community diversity is lower in the evenness and may be high due to increased
muddier sediments compared with the same species richness (S=71 in S26B and S=78 in
quality level coarser sediments (muddy sand, S16B) while at the same time some tolerant
sandy muds). The same is also valid for the species reach fairly high densities i.e. Eunice
species richness. Generally the biological vittata reaches densities of 7.34% and 11.8%.
indices values and especially those of the This situation may be evident in the reduction
diversity index are relevant with the values of of the evenness index (J=0.88 in S16B) and is
the Bentix index having lower values in the often encountered in intermediate levels of
lower level quality status. disturbance showing sometimes elevated
However there appear some differences in species richness. From this example it is evident
the results of the two methods, ie. stations S26B that the Bentix reflects better the EcoQ than
and S16B (Table 4) are classified according to the diversity index does, as the change in the
Bentix to the good EcoQ, while the diversity species composition is better expressed.
b) Application of the methods in a Western is evident that the Bentix index values
Mediterranean area differentiate among stations reflecting the
To apply the Bentix index in the Western lower EcoQ of station 2, while the diversity
Mediterranean and compare it with the results indices values give comparable results among
of the diversity indices, a set of data (MASSÉ, stations.
1971) coming from the Bay of Prado (Gulf of
Lion) was used. These macrozoobenthic data Discussion
was collected from the infralittoral well sorted
fine sands or shallow sands habitat. The values Although it is not yet well established it
of the Bentix index, the biological indices H, J seems that specific types of habitats or
and S, and the corresponding EcoQ in the two ecosystems are common throughout the
stations studied are given in table 8. Station 1 Mediterranean ecoregion and that the
is mentioned as most exposed, and more pure corresponding communities can be classified
(greater self purification capacity) than station into types which are similar in their basic
2, which is more exposed to the river structure and composition throughout the
"Huveaune" outputs representing a source of Mediterranean. Of course there are species
pollution from urban and industrial wastes. It that present local patterns of distribution within
Effectiveness
Dependence on external factors Reflection of community attributes
Robustness
Index Habitat Sample Taxon. S Evenness Species
Type size effort sensitivity
them as tools for the classification of benthic size distribution may be more reliable
communities into ecological quality classes. (REIZOPOULOU et al., 1996).
As seen in Table 9 the Bentix index The biological index of H’ gives a good
proposed is a very robust and adequately description of the community structural and
effective tool in classifying benthic biotic aspects. However, only if used in
communities into ecological quality classes. combination with the Species richness, the
Its robustness lies in the fact that it is largely evenness index, and maybe the faunistic data,
habitat type and sample size independent and so as to highlight the dominance of opportunistic
thus has a potential for global application. Its species, gives a safe description of the
effectiveness in discriminating between community structure and composition. Besides,
ecological classes is based on its ability to reflect its high dependence on external factors renders
the faunal composition in relation with the the index inconvenient for use in a benthic
resistance of species to disturbance factors. community ecological classification scheme.
Limitations of the use of the Bentix index
are met in the case of transitional waters Acknowledgements
(estuaries and lagoons) where the natural
conditions favour the presence of tolerant We would like to thank the anonymous
species in very high densities. In this case reviewers for their contribution in the
undisturbed lagoons or estuaries may appear improvement of the paper and the Chief Editor
with low quality status if the Bentix index is Dr. E. Papathanassiou for motivating us to
used. Other indices such as the geometric body produce this work.
Sandy muds
CODE SPECIES EG REGION
(percentage abundance %)
Pol Drilonereis filum 1
Pol Levinsenia gracilis 2 Catalan coasts
Pol Paralacydonia paradoxa 2 Catalan coasts
Pol Schistomeringos rudolphi 3 Amvrakikos (12.4)
Pol Scoloplos armiger 2 French Medit. coasts
Pol Sigambra parva 1 Amvrakikos (26.4)
Pol Sternaspis scutata 2 Strymonikos, Izmir, Diavlos Oreon (21.2),
Kerkira (2.2)
Mol Corbula gibba 3 Izmir Bay, Atalanti (10)
Mol Hiatella arctica 1 Pagassitikos (13)
Mol Monia patelliformis 1 Pagassitikos (12)
Mol Myrtea spinifera 2 Strymonikos
Mol Mysella bidentata 2 Diavlos Oreon (8.3), Atalanti (29)
Mol Timoclea ovata 2 Kavala gulf, French coasts
Ech Amphiura chiajei 2 Kavala gulf, Geras (4.3)
Ech Amphiura filiformis 2 Adriatic, Catalan, Kerkira (1.3), Patraikos
Sip Aspidosiphon kowalevskii 1 Strymonikos
Sip Aspidosiphon muelleri 1 Kavala gulf
Muddy sands
CODE SPECIES EG REGION
(percentage abundance %)
Pol Aponuphis bilineata 1
Pol Aponuphis brementi 1 Crete
Pol Aricidea catherinae 1 Crete
Pol Chaetozone setosa 3 Amvrakikos (11.8), Pagassitikos (26)
Pol Chone duneri 1 Crete, Geras (1.2)
Pol Clymenura clypeata 1 Sporades (18.3), Geras (1.1)
Pol Cossura soyeri 2 Crete
Pol Diplocirrus glaucus 2
Pol Dirtupa arietina 2 Crete
Pol Euchone rosea 1 S. Evvoikos, Geras (10)
Pol Euclymene palermitana 1 Strymonikos
Pol Eunice vittata 2 S. Evvoikos
Pol Goniada maculata 1 Geras (1), Catalan coasts
Pol Heteromastus filiformis 3 Strymonikos
Pol Levinsenia gracilis 2 Crete, Pagassitikos (10)
Pol Lumbrineris gracilis 1 Crete
Pol Lumbrineris latreilli 2 S. Evvoikos, Amvrakikos (15.3), Sporades (16),
Geras (19)
Pol Magelona minuta 1 Crete
Pol Micronephtys maryae 1 Crete
Pol Monticellina dorsobranchialis 2 Crete, Pagassitikos (16)
Pol Nephtys hombergi 2 French Medit., Catalan coasts, Strymonikos
Pol Notomastus latericeus 2 Crete, Sporades (17.5), Geras (9.4)
Pol Paralacydonia paradoxa 2 Catalan coasts
Pol Prionospio banyulensis 1 SE Attica coasts (11)
Pol Pseudoeliocapitella fauveli 2 Crete
Pol Rhodine loveni 1 Crete
Pol Schistomeringos rudolphii 3 Amvrakikos (4.2) Geras (6)
Pol Sphaerosyllis taylori 1 S. Evvoikos
Pol Spiophanes kroyeri 2
Mol Corbula gibba 3 Geras (4.4), Catalan coasts
Mol Tellina distorta 2 Strymonikos
Mol Thyasira flexuosa 3 Crete
Mol Timoclea ovata 2 Pagassitikos (3.6)
Cru Corophium volutator 3 Amvrakikos (15.3)
Sip Onchnesoma steenstrupi 1 S. Evvoikos, SE Attica (5.2), Pagassitikos (10), Crete
Sip Aspidosiphon muelleri 1 Amvrakikos (18.3)
Midlittoral sands
Pol Ophelia bicornis 1 Thermaikos, Strymonikos
Pol Scolelepis squamata 2 Thermaikos
Mol Donacilla cornea 1 Thermaikos, Strymonikos
Cru Eurydice affinis 1 Strymonikos
Coralligenous
CODE SPECIES EG REGION
(percentage abundance %)
Pol Adyte pellucida 1
Pol Brania pusilla 1
Pol Dorvillea rubrovittata 1 Chalkis
Pol Euchone rosea 1 Kalamitsi (Ionian)
Pol Eurysyllis tuberculata 1
Pol Exogone rostrata 1
Pol Glycera tesselata 1
Pol Haplosyllis spongicola 1
Pol Paleanotus debile 1
Pol Pholoe minuta 2
Pol Pionosyllis dionisi 1 Diavlos Oreon (2.8)
Pol Polyphysia crassa 2 Chalkis
Pol Pontogenia chrysocoma 1
Pol Prionospio banyulensis 1
Pol Serpula concharum 1 Chalkis
Lagoons
CODE SPECIES EG REGION
(percentage abundance %)
Pol Aricia foetida 2 Orbetello lagoon (Tyrrhenian Sea),
Pol Armandia cirrosa 1 Orbetello lagoon (Tyrrhenian Sea),Gialova lagoon
(Ionian Sea-Greece), Mesolongi lagoon (8),
Papas (8.6)
Pol Capitella capitata 3 Gialova lagoon (Ionian Sea-Greece),
Mesolongi lagoon (13), Papas (5.7)
Pol Ficopomatus enigmaticus 3 Orbetello lagoon (Tyrrhenian Sea),
Mesolongi lagoon (11)
Pol Hediste diversicolor 3 Logarou (6.89)
Pol Heteromastus filiformis 3 Gialova lagoon (Ionian Sea-Greece), Papas (6.9)
Pol Hydroides dianthus 3 Papas (19.9)
Pol Hydroides elegans 3 Orbetello lagoon (Tyrrhenian Sea),
Pol Leptonereis glauca 1 Orbetello lagoon (Tyrrhenian Sea),
Pol Malacoceros fuliginosus 3 Mesolongi lagoon (49)
Pol Microspio mecznicowianus 2 Logarou (8.1)
Pol Nainereis laevigata 2 Papas (15.7)
Pol Neanthes caudata 3 Orbetello lagoon (Tyrrhenian Sea), Mesolongi
lagoon (2.3)
Pol Nephtys hombergi 2 Logarou (11.7)
Pol Ophiodromus pallidus 2 Mesolongi lagoon (17)
Pol Perinereis cultifera 1 Gialova lagoon (Ionian Sea-Greece)
Pol Phyllodoce rubiginosa 1 Orbetello lagoon (Tyrrhenian Sea),
Pol Pomatoceros triqueter 3
Pol Spio decoratus 3 Orbetello lagoon (Tyrrhenian Sea), Papas(4)
Pol Syllis gracilis 2
Pol Protoaricia oerstedii 2 Papas (1.6)
Mol Abra alba 2 Mesolongi lagoon (Greece) (19)
Mol Abra ovata 2 Orbetello lagoon (Tyrrhenian Sea),Gialova lagoon
(Ionian Sea-Greece), Papas (32), Logarou (67)
Mol Bittium reticulatum 2 Gialova lagoon (Ionian Sea-Greece)
Mol Cerastoderma glaucum 2 Orbetello lagoon (Tyrrhenian Sea), Papas (14.2),
Logarou (15)
Mol Cerithium vulgatum 1 Gialova lagoon (Ionian Sea-Greece)
Mol Cyclope neritea 1 Gialova lagoon (Ionian Sea-Greece), Logarou (0.36)
Mol Hydrobia acuta 2 Gialova lagoon (Ionian Sea-Greece)
Mol Hydrobia ventrosa 2 Logarou (5.7)
Mol Loripes lacteus 2 Papas (48)
Mol Mytilaster minimus 1 Orbetello lagoon (Tyrrhenian Sea), Papas (7.2)
Mol Parvicardium exiguum 1 Logarou (1.57)
Deltas
CODE SPECIES EG REGION
(percentage abundance %)
Pol Cossura soyeri 2
Pol Ficopomatus enigmaticus 3
Pol Hediste diversicolor 3 Evros Delta
Pol Heteromastus filiformis 3 Strymonikos (4)
Pol Neanthes succinea 2
Pol Scolaricia typica 1
Pol Spio decoratus 3 Evros Delta, Strymonikos (18.6)
Mol Abra ovata 2 Evros Delta
Mol Hydrobia acuta 2 Evros Delta
Mol Spisula subtruncata 2 Strymonikos (81)
Cru Corophium orientale 1 Thermaikos, Strymonikos
Cru Gammarus aequicauda 1 Evros Delta
ANNEX II:
List of tolerant species with scoring number, examples of occurrence (with percentage abundance)
and ecological traits.
Instability indicators-Pollution indicators
Codes Species EG Region Ecological
(percentage abundance %) preferance
Pol Aphelochaeta marioni 2 Algeria, Kerkira (1,4) Mud
Pol Aricidea fauveli 2 Mud
Pol Capitella capitata 3 Thermaikos (225 ind/m2),
Saronikos (18), Papas (15.9)
Pol Capitellides giardi 3
Pol Capitomastus minimus 3 euryhaline,
muddy sands
Pol Caulleriella alata 2 Sand