Polychaetes as environmental indicators revisited

Marine Pollution Bulletin 50 (2005) 1153–1162 www.elsevier.com/locate/marpolbul

Review

Polychaetes as environmental indicators revisited Adriana Giangrande *, Margherita Licciano, Luigi Musco Department of Biological and Environmental Sciences and Technology, University of Lecce, Marine Biological Station, 73100 Lecce, Italy

Abstract The utilization of polychaetes in descriptive ecology is reviewed in the light of recent research especially concerning the biota hard bottom environments. Polychaetes, often linked in the past to the concept of opportunistic species able to proliferate after an increase in organic matter, have played an important role especially with regard to impacted soft-bottom habitats. Increased knowledge of the group, suggests that not only opportunistic species can be utilised as indicators, so that these organisms can be disengaged from the old concept of opportunistic taxa. Moreover, recent researches conducted on this group allowed demonstrating as surrogacy is not always applicable. Among polychaetes inhabiting hard bottom environment, the analysis of family Syllidae appears particularly promising. Studied conducted in our laboratory demonstrated as syllid species decrease in abundance or completely disappear under varying sources of negative impact. The distribution of species also appeared indicative in underlying effects of marine protected areas (MPA) functioning, or in describing different climatic areas within biogeographical sectors. It is obvious that good results can only be obtained on the basis of good taxonomic resolution. We suggested that, in monitoring studies, operational time could be optimized not only by working at a higher-level on the whole invertebrate data set, but by also selecting a particularly indicative group and working at fine level. Ó 2005 Elsevier Ltd. All rights reserved. Keywords: Polychaetes; Syllidae; Monitoring; Global changes; Surrogacy; Mediterranean sea

1. Introduction Polychaetes play an important role in the functioning of benthic communities (Hutchings, 1998). This is not only because they often are the numerically dominant macrobenthic taxon, but also because of the diversity of feeding modes they exhibit. This is especially true of soft-bottom habitats, where the distribution of species is mainly linked to the sediment particle size (Gambi and Giangrande, 1986). They have been shown to be good indicators of species richness and community patterns in benthic invertebrate assemblages (Fresi et al., 1983; Olsgard and Somerfield, 2000; Sparks-McConkey and Watling, 2001;

*

Corresponding author. E-mail address: [email protected] (A. Giangrande).

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Van Hoey et al., 2004), and have recently been proposed as surrogates for marine biodiversity (Olsgard et al., 2003). Polychaetes have been extensively used in coastal studies for monitoring purposes especially in soft-bottom habitat (Crema et al., 1991; Elias, 1992; Grall and Gle´marec, 1997; Solis-Weiss et al., 2004). Among benthic groups, polychaetes are, in fact, one of the best indicators of environmental disturbance, since this taxon contains both sensitive and tolerant species in a gradient from pristine to heavily disturbed habitats (Pocklington and Wells, 1992). However, polychaete assemblages have rarely been utilized in hard bottom monitoring programmes (Bellan, 1980, 1984; Bellan et al., 1988), although they are abundant and well studied also concerning this habitat, where the substrate type and algal cover seem to be the main factors structuring assemblages and determining the presence or absence of species (Abbiati et al., 1987; Giangrande, 1988; Sarda`, 1991).

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1.1. Monitoring with macrobenthos: A brief history Monitoring with benthic invertebrates has mainly followed the so-called ‘‘indicator species’’ approach, qualitative, based on the presence–absence of taxa sensitive to perturbations, or quantitative, based on numerical or taxonomic abundance. The qualitative approach was based on the definition of opportunistic taxa, mainly polychaetes. Studies involving communities progressively replaced the biology of single indicator species, the effect of stress being easier to measure by utilizing multispecies assemblages, and examining changes in abundance of sets of species. In the assessment of coastal environmental quality through a quantitative approach, the abundance, biomass and species richness of zoobenthos have been widely utilised parameters (Gray, 1989; Eaton, 2001), especially in soft-bottom communities (Clarke, 1993; Harkantra and Rodriguez, 2004; Kress et al., 2004). In these studies the macrobenthos is typically studied, and polychaetes are widely used (Samuelson, 2001). Effect of stress on the population levels includes: increase in production, especially linked to eutrophication processes; reduction in diversity and an increase of dominance by opportunistic species; decreasing number of species coupled with increasing number of individuals. Since these opportunistic forms are typically small sized species with short life cycles, a decreasing biomass is also observed (Pearson and Rosenberg, 1978; Gray, 1989). Over the years a number of methods and techniques have been developed such as Abundance/Biomass comparison curve technique (Warwick, 1986), or geometrical class distribution of species plot (Gray and Mirza, 1979), which also allows an objective selection of groups of indicator species (Gray and Pearson, 1982). Multivariate methods have been shown to be more sensitive than univariate or graphical ones in discriminating between sites or times (Warwick and Clarke, 1991). In this kind of study the identification of organisms at species level within communities represents the greatest constraint in terms of both time and costs, so that a reliable use of a reduced taxonomic resolution was an important development in the practical assessment of environmental changes. Some studies have shown that little information is lost by working at higher taxonomic level (e.g. Family or even Phylum), and there are theoretical reasons and empirical evidence that in this way community responses to human perturbations may be easily detected (Warwick, 1988, 1993; Olsgard and Somerfield, 2000; Olsgard et al., 1997, 1998; Mistri and Rossi, 2000, 2001). This approach, called Taxonomy Sufficiency (TS), completely bypasses the importance of indicative species. Numerous studies have shown, however, the loss of information following this surrogacy approach, especially when if applied to biodiversity measurement (Gray et al., 1990; Warwick et al., 1990; Roy et al., 1996; Bianchi and Morri, 2000; Giangrande, 2003; Terlizzi et al., 2003; Giangrande et al., in press).

One of the reasons for the functioning of this approach could be that species are more affected than higher taxa by both natural variability and seasonal cycle. The natural variability is in fact one of the critical points in evaluating the effects of anthropogenic activities both on populations and multispecies assemblages. Further development in monitoring led in fact to the identification of an appropriate sampling design capable of measuring a specific effect and to tease it apart from natural variation (Underwood, 1996; Benedetti-Cecchi, 2001). The first experimental design for assessment of environmental impacts was based on the comparison between the putatively impacted area and a single reference area, and this was not appropriate for isolating the impact from other sources of spatial and temporal variation occurring in these assemblages. The evolution of this approach was a procedure adding a time series and an increase replication in the number of reference areas (Underwood, 1991, 1992, 1993). Most of these studies were carried out on artificial hard substrates as these were easier to investigate and substrates could be returned to the labs for detailed studies. The difficulty in investigating natural hard substrates, linked to the large amount of replicates needed in these types of studies, encouraged reduced taxonomic resolution. 1.2. Polychaetes in the monitoring field: Opportunistic species When referring to opportunistic species of polychaetes, one immediately thinks of Capitella capitata, the most common taxon found in high organic enriched sediments (Zajac and Whitlatch, 1982). The definition of opportunistic species follows an old concept (Cognetti and Taliercio, 1970; Cognetti and Varriale, 1971; Bellan, 1967) still popular with some monitoring programmes (Amaral et al., 1998; Go´mez Gesteira and Dauvin, 2000; Samuelson, 2001). According to Pearson and Rosenberg (1978) and Gle´marec and Hily (1981), opportunistic polychaetes species are selected in relation to their capability to proliferate after increases in organic matter. Such species mainly belong to the Capitellidae, Cirratulidae, and Spionidae families. Some authors also have referred to different polluted areas by the presence of species belonging to these families (Bellan, 1984; Bellan et al., 1988). Opportunistic species are pioneer forms dominating the initial stages of succession after disturbance. In many cases only one or two opportunistic species have been found to dominate the early phases of succession (Dauer and Simon, 1976; Zajac and Whitlatch, 1982). As in the common opportunistic taxa, life-history traits of C. capitata give it the capability to build up dense populations rapidly. It seems that during early stages of colonization this species can reach very high densities without suffering from intraspecific competition (Whitlatch and Zajac, 1985). It is also well known that C. capitata is a complex of sibling species (Grassle and Grassle, 1974), as well as the Polydora ciliata

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complex (Manchenko and Radashevsky, 1998), and probably many of the other small opportunistic polychaetes, thus rejecting the claim that many of such species are in fact ‘‘cosmopolitan species’’. These forms may also experience high speciation and extinction rates (Cognetti and Maltagliati, 2000). 2. Hard bottom polychaetes; not only opportunistic species Excluding studies on fouling, marine invertebrates inhabiting natural hard bottoms have rarely been utilized for monitoring (Marchini et al., 2004; Le Hir and Hily, 2002). This is largely due to the difficulty in sampling procedures and number of taxa found in the infralittoral fringe. Hard substrates are colonized by both vagile and sessile organisms (solitary and colonial), so it is difficult to choose appropriate taxon for such monitoring programs. Moreover, as stated before, the application of the correct experimental design in the identification of environmental impact in habitats which vary naturally, also involves great number of spatial and temporal replicates (Underwood, 1993, 1996; Chapman et al., 1995). Therefore, often monitoring studies in these environments are carried out considering only macroscopic encrusting organisms, and involving non-destructive sampling by permanently marked quadrates or transects resurveyed visually or photographically (Fraschetti et al., 2001; Terlizzi et al., 2005). However, other than conspicuous encrusting organisms easily detectable, rocky shores are also characterised by mat-like habitats with an extremely diverse assemblage of small cryptic vagile invertebrates (Kelaher et al., 2001), whose response to changes in environmental conditions is largely unknown (Moore, 1972). This is probably due to the difficulty of quantitative sampling and extraction of vagile organisms, which makes problematic the comparison among different substrates. It is for this reason that vagile invertebrates have up to now been considered unsuitable for monitoring. However, within this compartment, some representative groups can be selected as indicative organisms. In this context polychaete taxon seems to be an appropriate candidate. Hard-bottom vagile polychaetes have been well investigated within Mediterranean area, even though without involving an appropriate experimental design (Bellan, 1969, 1971; Fresi et al., 1983, 1984; Abbiati et al., 1987; Giangrande, 1988; Somaschini, 1988; Sarda`, 1991; Alos, 1999; Lo´pez and Vie´itez, 1999; Tena et al., 2000; Fraschetti et al., 2002; Giangrande et al., 2003, 2004), and rarely utilized for monitoring (Bellan, 1980, 1984; Bellan et al., 1988). Among polychaete families colonizing hard substrata, Syllidae is one of the most diverse and well known from a taxonomic point of view, numbering about 667 taxa distributed in a large array of habitats, especially on hard bottom littoral fringe (San Martı´n, 2003). Syllids have been proved to be very useful as indicator taxon, even if they react in an opposite way to what usually observed in other polychaetes families. They were found to be highly sensi-

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tive to pollution or other kind of stress, decreasing in number of species and individuals or completely disappearing (Giangrande et al., 2004; Musco et al., 2004). Opportunistic forms seem to be very rare in this group, as an example we found a taxon identified as Syllis cfr hyalina, which was the only polychaete present at a site influenced by high temperature water discharge, and reaching a very high density (10,000 individuals in 20 cm2; unpublished data). Another taxon often collected in stressed environments is S. gracilis, which was demonstrated to be a complex of sibling species (Cognetti and Maltagliati, 2000). Finally, Autolytus benazzii, and Anoplosyllis edentula (recorded as Syllides edentula) are also reported having opportunistic features (Cognetti and Varriale, 1971; Cognetti and Maltagliati, 2000), and Syllis prolifera is considered a species which increases in abundance with increasing environmental stress (Bellan, 1980; Giangrande, 1988). 2.1. ‘‘Negative’’ impact indicators In a study conducted during the building of the Cerano Power-Station, along the South Adriatic coast some important changes were observed in species composition and abundance of Syllidae relatively to a putatively affected area (Musco et al., 2004). In this area, located South of the Power station, where the algal mat of Cystoseira remained apparently unaltered, syllid assemblages revealed heavy modification compared to the northern reference site which were not affected and characterized by comparable algal cover (Fig. 1). Syllid species seem to respond to disturbance rapidly with changes mainly occurring at shallow depths. The most involved species, Brania pusilla, Salvatoria clavata, Eusylllis lamelligera and species belonging to the genus Exogone, which typically colonise shallow sites, completely disappeared in the impacted site, while population of Syllis prolifera markedly declined. It was supposed that the decline of both number of specimens and species was due to the high sedimentation rate occurred at the southern site. The Power Station building induced in fact water turbidity that was transported following the main current towards Southern area. A visible increasing of sedimentation was observed within the substrate during the sampling phase, but unfortunately sediment load was not measured. Up to now no studies were actually focused on the influence of sedimentation rate on hard substrate vagile invertebrates. The prevalent opinion is that ‘‘high’’ sediment loads are detrimental to the overall diversity of rocky coast organisms through inhibition of recruitment and mortality of less tolerant species and/or through enhancement of spatial dominance by a few tolerant space monopolizing species (Airoldi, 2003). An investigation focused on the influence of sedimentation on syllid colonization is at present in progress on our laboratory. Another example of syllid sensitivity comes from a study conducted in shallow hard substrates along the Ionian Sea on the effects of a sewage discharge on biodiversity (Terlizzi et al., 2002). The analysis of syllids within polychaetes

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Fig. 2. Investigation of effects from seawage discharge on Syllid assemblage. (a) Map of the study area. Sampling were carried out at 5 m depth, sites were approximately 100–300 m apart. At the putatively impact location (I), one site was about 10 m from the outfall, the remaining two (controls) (C1 and C2) were on its right and left, respectively. (b) Cluster analysis (Bray Curtis Similarity PRIMER, Plymouth Laboratory). Three replicates (A, B, C) were considered for each sampling site. Fig. 1. Investigation of Cerano Power station building impact along the South Adriatic Coast. (a) Map of the study area with indicated 2 sampling transects (A, B) each one composed by three stations located at 1, 15 and 25 m depths. (b) Trends of number of species (lines) and number of individuals (bars) in the stations.

revealed how, also in this case, they were the best descriptors of environmental changes discriminating the impacted sites (Fig. 2). In Fig. 2b the diagram relative to the cluster analysis is reported, where the impacted site (I) is compared with two not impacted ones (reference sites indicated as controls C1 and C2) and where three replicates were considered for each site. A quite marked separation is present between the replicates of the impacted sites and that of the controls. The number of species decreased from 40 (controls) to 16 (impact), and the number of individuals from 925 to 418. This decrease in species richness involved especially rare taxa. Within Syllis genus the number of species decreased from 21 to 17 proceeding from the controls to the impacted area. Most of the species such as S. armillaris, S. gerlachi, S. rosea, S. pulvinata and S. prolifera, decreased in number of individuals. By contrast S. gracilis and S. krohni showed an inverse trend, increasing in abundance at the impacted site. Between them, only the former is already reported for stressed environment. The decreasing in abundance of S. prolifera in the impacted site ap-

pears quite strange because this species is often reported as typical of stressed environments (Bellan, 1980; Giangrande, 1988). As a whole, no actual opportunistic forms were detected in the impacted site as far as the syllid assemblage, because also species increasing in abundance did not show an increase similar to that usually observed for typical opportunistic forms. Completely different was the trend observed for the rest of polychaete assemblage at the studied area. A change in species composition between reference sites and impacted one was observed, with very few species abundant and often exclusive to the impact site, so that a decrease of species number coupled with an increase of abundance was observed, that is the typical trend usually observed also in soft-bottom polychaetes under disturbance. The species collected at the impacted site were mainly Platynereis dumerilii and Polyophthalmus pictus, which are considered opportunistic forms in rocky-shore habitats (Bellan, 1980). 2.2. ‘‘Positive’’ impact indicators A recent study carried out along the South Adriatic coast (Fig. 3), has shown as hard bottom vagile polychaetes

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more probably affected by non-selective predation. Moreover this effect seems not to be present in the endolithic species of the genus Lysidice (Eunicidae) (Giangrande et al., 2004). High predation rate was already hypothesized as a factor explaining the assemblage structure of polychaetes inhabiting Posidonia sea grass bed (Gambi et al., 1995). In this environment, characterised by the presence of a large number of Crustacea, some of which potential predators of worms, the polychaete assemblage is often characterized by a high number of species with very few individuals. It is obvious, however an appropriate experimental design is needed to assess the influence of predation rate on polychaetes assemblages. Fig. 3. Map of the three investigated sites along the Apulian coast (South Adriatic Sea) with different human impact. Explanations are in the text.

were good indicators of different environmental conditions and as the same conclusions can be drawn by considering only the Syllidae component (Giangrande et al., 2004). Three sites exhibiting comparable habitats in terms of type of substratum, but different human impact have been analysed. The Otranto site, an area least influenced by human impact and recently included in a list of European Marine Biodiversity Research Sites selected because of its pristine status (BIOMARE, www.pml.ac.uk/biomare/ site.htm), had intermediate values of density and number of polychaete species. The Cerano area, largely affected by industrial pollution, showed the lowest number of species and abundance. Finally Torre Guaceto, an already functioning marine protected area (MPA), which can be influenced by the ‘‘positive impact’’ (protection), showed no high variation in number of species, but the highest density value. The differences among the three sites was, also in this case, higher at shallower depths, which are most influenced by human activities, while the deepest samples appeared more homogeneous. Diversity index was instead lowest at Cerano, and higher and with similar values in the other two sites. Therefore, diversity seems to remain a good indicator that an area is being influenced of a ‘‘negative impact’’. In this area the subfamily Exogoninae (Syllidae) seems to be the taxa mostly exhibiting this negative impact. The increase in polychaete abundance observed at the protected site (Torre Guaceto) could be due to a ‘‘trophic cascade’’ effect (Pinnegar et al., 2000) which can be explained as follow: protection can increase the abundance of species predating on small fishes, which in turn feed on small invertebrates. A similar effect was at another Mediterranen MPA by Badalamenti et al. (1999) and Milazzo et al. (2000), who suggested that changes in abundance more than changes in diversity could be indicator of the effect of protection. The hypothesis of low predation rate can be corroborated by the observation that the species, which exhibit larger numbers of individuals at Torre Guaceto, are those already more abundant at the other sites, and therefore

2.3. Bioclimatic indicators Syllidae were found to be good biogeographic and bioclimatic descriptors within the Mediterranean basin (Musco and Giangrande, in press). These authors, inferring syllid distribution in some Mediterranean stretches of coast, demonstrated how species distribution mainly follows a bioclimatic (ecological) rather than biogeographical pattern. These assumptions lead to hypothesize syllid distribution a suitable mean of describing not only environmental changes in space, but also at temporal scale. The present distribution of syllids can be used to test the Mediterranean tropicalization hypothesis. It is well known, in fact, that the average temperature of the surface of the sea is increasing (Bethoux et al., 1990; Hughes, 2000) and that the response of marine biota is already visible, involving rapid alteration of structural biodiversity (Bianchi and Morri, 1993, 1994; Bianchi, 1997, 2004; Hughes, 2000; Go´mez and Claustre, 2003; Grubelic et al., 2004). Distribution and phenology of ‘‘sentry’’ species, invertebrates with short life cycle, as syllids are, may be good indicators of changes warning before macroscopical changes occur. Accurate data sets of taxa suitable to be considered indicators are needed in order to compare the present situation with the past one to be able to document changes in biodiversity and the composition of communities. A revised list of syllid species was therefore used for a temporal comparison on the stretches of coast where both past and present data were available. The changes of bioclimatic categories in relative values between past and present data are shown in Fig. 4, where an increase of species typical of warm regions was observed considering the whole Mediterranean area (M). This could be an indication of changes in global environmental conditions (e.g. a rise in temperature). However, when the different stretches of coasts analysed were considered, differences were not so marked, especially along the Iberian coast which showed the least change in composition between the past and present situation. The trend towards warmer composition in the whole Mediterranean could also be explained by the concentration of recent studies mainly in warmer areas previously poorly investigated. It is probably for this reason that a

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Fig. 4. Temporal comparison between Syllidae bioclimatic category distribution in some coastal lines (SP Spanish Coast from 1989 to 2003; IT Italian Coast from 1995 to 2003; LS Levant Sea from 1995 to 2003) and in the whole Mediterranean basin (M) from 1995 to 2003. D = distribution of categories of species added (%) deriving from the difference from past and present data. C = species distributed in cold waters (Arctic, subArctic, Antarctic, sub-Antarctic species); TC = species distributed in temperate cold waters (mainly European North Atlantic species); T = species distributed in temperate waters (mainly Iberian Atlantic species); TW = species distributed in temperate warm waters (Subtropical species or those widely distributed between tropical and temperate zones), W = species distributed in warm waters (Inter-tropical species), and E = euryterm species.

prevalence of species characteristic of warm areas was detected among the syllid species added to the Mediterranean fauna. However, the general trend arising from the analysis of Mediterranean Syllidae, does not exclude a true indication of a general change of the Mediterranean biota towards a tropicalization. It is interesting to note as some syllid, mainly characteristic of temperate cold areas, are not still mentioned in recent lists (i.e. Exogone fauveli, E. brevipes, Autolytus alexandri, A. rubrovittatus, Paratyposyllis peresi, Salvatoria tenuicirrata, Trypanosyllis gigantea). A survey in the areas where these species were previously collected is in progress to verify their actual disappearance. As a whole, however, it is a matter of fact that most of the new records after the year 1995 belong to warmer categories. In either cases, climatic changes or more southern location of investigations, syllids revealed highly descriptive capabilities and therefore can be proposed as indicators of large-scale ecological changes. 3. Polychaetes and surrogacy The knowledge of Systematics and Phylogeny appears of paramount importance in researches dealing with conservation or management issues. However, the use of surrogates should be limited also within ecological approaches such as routine analysis of biodiversity measurements for monitoring purposes. In the biodiversity analysis Warwick and Clarke (1995) and Clarke and Warwick (1998, 2001) introduced the Taxonomic distinctness index (TD), based on the taxonomic relatedness of the species in a given sample. In this method

the distance can be visualized as the length of the path connecting the species traced through a Linnean or phylogenetic classification of the full set of species involved. The local biodiversity is compared to an expected value derived from a master species list for the group of organisms under investigation in that area or habitat. TD is measured for any specific group and habitat type. Possible human impact can be checked by considering if a putatively impacted locality has a ‘‘lower than expected taxonomic diversity’’. According to Warwick and Clarke (1995) the TD decreases with increasing stress, and represents an univariate index of community perturbation more sensitive than species Diversity. This means that a method to quantify biodiversity became a method to measure stress, to be used in monitoring and routinal ecological analysis. In contrast, the Taxonomy Sufficiency (TS), conceived for routine analysis (Ellis, 1985) was later utilized to quantify the biodiversity (Balmford et al., 1996, 2000), and this has already been deeply criticised (Giangrande, 2003; Terlizzi et al., 2003; Giangrande et al., in press). One of the most serious and not yet properly addressed limitations of the surrogacy approach is the lack of consideration given to processes of sympatric speciation, which have been shown to occur frequently in the marine environment (Hellberg, 1998) thus leading to the presence of great number of species within some genera as a result of a high intra-area radiation. This is what can occur in most of the Syllidae genera, whose contribution to local biodiversity is not negligible. Sympatric speciation pattern is often reduced or absent in short evolutionary time habitats, e.g. brackish waters or in other stressed environments. This is probably one of the reasons why the TS in environments such as lagoons, may actually work (Mistri and Rossi, 2000, 2001). In stressed habitats selection is already appreciable at high taxonomic level, because very few species belonging to different groups are able to colonize these habitats. Colonization of brackish water, for instance, is a rare event, which historically happened independently in different groups. Furthermore, as stated above, brackish water species are not particularly prone to speciation due to short evolutionary time allowed by the environment. Therefore the analysis at family level approached by the TS gives the same results as using the species level. As an example some Mediterranean habitats (lagoons, soft bottoms, hard bottoms) were compared in number of polychaetes families and species (Table 1), after computation of the ratio species/families. Comparing three coastal brackish water lakes located along the Tyrrhenian Sea (Latium, Italy) (Gravina and Giangrande, 1984) the ratio is low and quite constant, ranging from 1.5 to 1, on account of the paucity of number of closely related species. In these habitats with increasing stress (in this case low salinity present in the Fondi lake) only four species belonging to four different families were present.

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Table 1 Comparison of polychaetes diversity at different taxonomic levels in some Mediterranean biotopes Brackish water No. of families No. of species Ratio

Caprolace Lake (salinity 30&, low organic load) 17 (89%) 27 (64%) 1.5

Sabaudia Lake (salinity 30&, high organic load) 10 (52%) 13 (30%) 1.3

Soft-bottom

Latium coast (high trophic input)

No. of families No. of species Ratio

27 (93%) 91 (94%) 3.5

Tuscany coast (low trophic input) 24 (82%) 52 (54%) 2.1

Hard-bottom (similar depth and algal cover) No. of families No. of species Ratio

South Adriatic coast

Tyrrhenian coast

17 (74) 108 (71%) 6.4

20 (81%) 110 (72%) 5.5

Hard-bottom No. of families No. of species Ratio

Torre Guaceto (protected site) 17 (89%) 108 (86%) 6.4

Otranto (pristine site) 16 (84%) 84 (67%) 5.3

Comparing soft-bottom areas along the Tyrrhenian coast submitted to different trophic input from rivers (Gambi and Giangrande, 1986), the ratio is higher, ranging from 3.5 to 2.1. In this case, considering the family level lead to a loss of information. The highest ratio is, however, observed for hard bottom environments, which often are colonized by a great number of closely related species. This is particularly true considering species belonging to the family Syllidae. On hard bottom, values ranged from 6.4 to 4.6 and resulted quite similar comparing different areas with similar environmental conditions, but located in different basins (Tyrrhenian Sea and Adriatic Sea) (Giangrande, 1988; Giangrande et al., 2003). The last example reported in Table 1 concerns the decrease of the species/family ratio with increasing pollution coming from the comparison of different hard bottom polychaete assemblages from the same geographical area, but submitted to a different human impact. Utilised data are the same previously reported in the discussion of ‘‘positive’’ human impact and coming from Torre Guaceto, Otranto and Cerano analyses (Fig. 3) (Giangrande et al., 2004). In this case, it is clear that the TS method is not useful, it means that working at family level lead to a great loss of information. Selection due to stress seems in fact to act on the number of species and not on the number of families. Even at generic level Syllidae are not indicative! The conclusion from the present analysis is that only the brackish waters are the environments where the TS can be applied. 4. Concluding remarks From the reported examples it is evident how hard bottom polychaetes can be highly indicative of different environmental situations thus leading to consider these

Fondi Lake (salinity 20% ) 4 (21%) 4 (10%) 1

Total 19 42

29 96

23 153 Cerano (polluted site) 14 (74%) 65 (52%) 4.6

19 126

organisms for a future utilization as indicators in monitoring approaches. In particular, the analysis of Syllidae species distribution appears a very sensitive index. Species belonging to this family decrease in abundance or completely disappear under different sources of negative impact (pollution, high sedimentation rate), so they do not respond to the ‘‘classical scheme’’ which considers polychaetes indicative only by the presence of opportunistic taxa (Cognetti and Taliercio, 1970; Bellan, 1984). Syllidae were also found to be indicative of protection effects (Giangrande et al., 2004), or in describing different bioclimatic areas within biogeographical sectors (Musco and Giangrande, in press). As concerns this last point, their utilization has been suggested also in assessing climatic changes within the Mediterranean area. However, although this hypothesis appears extremely interesting, available data are at present too scant and only further researches could give more indications. The reported results have been obtained on the basis of a good taxonomic resolution. The importance of taxonomy in the ecological field and its re-evaluation was already stressed by several authors (Altaba, 1997; Boero, 2001; Giangrande, 2003; Giangrande et al., in press). Syllids can be appropriate candidates in ecological researches because they are not only very sensitive to disturbance, but also a taxonomically well-known polychaete family (Licher, 1999; San Martı´n, 2003, 2005). Probably any group of invertebrates could be indicative if analyses were conducted at finer taxonomic level. The importance of taxonomy in ecological fields is also underlined in discussing the use of surrogacy considering the whole polychaete taxon. Surrogacy seems not to be applicable in most of the environments. The comparison of polychaete diversity in different biotopes also revealed soft-bottom habitats more diverse at family level than hard-substrates. By contrast, the high

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richness in number of polychaete species inhabiting hard substrates (mainly Syllidae) is a matter of fact, especially if compared with the number of species colonizing softbottom environment. This is simply due to the fact that the general morpho-functional polychaete design is more adapted for living within sediment, where the group evolved (Fauchald, 1974; Giangrande and Gambi, 1998), than within the algae. Few families have adapted this design to live on hard substrates, among them Syllids are the most representative. The number of species is higher on hard bottom, because of niche partitioning also due to the high degree of competition here existing. Within Syllidae a great number of congeneric species can be commonly found in the same restricted area also leading to a probable niche overlapping (redundancy hypothesis sensu Walker, 1992). The life-style of Syllidae seems also to favour the development of a capacity for asexual reproduction, a feature usually present in sessile organisms (Schroeder and Hermans, 1975), as a probable response to the high competition rate. However, few data on syllid feeding requirement are available (Giangrande et al., 2000), in order to infer intra-interspecific competition and implication for the allocation of energy (Belovski, 1997). A significant increase in size coupled with decreasing density of individuals was observed from not impacted to impacted sites (unpublished data), and this can be an interesting point to investigate, also considering that the size structure of invertebrate assemblages was proposed as an index to be used in monitoring approaches (Basset et al., 2004). In conclusion our suggestion is that in monitoring studies operational time could be optimized not only by working on the whole invertebrate data set utilising surrogacy, but also working at finer level on a selected indicative group. This approach, apart from Mediterranean Syllidae (Giangrande et al., 2004; Musco et al., 2004; Musco and Giangrande, in press), was already utilized by Olsgard et al. (2003), who proposed Terebellidae species in North Atlantic soft-bottom environments, as indicators and surrogate for marine biodiversity. Also in this case the work was possible thanks to the contribution of one of the major specialists in Terebellidae taxonomy. References Abbiati, M., Bianchi, C.N., Castelli, A., 1987. Polychaete vertical zonation along a littoral cliff in the west Mediterranean. P.S.Z.N. Marine Ecology 8, 33–48. Airoldi, L., 2003. The effects of sedimentation on rocky coast assemblages. Oceanography and Marine Biology: An Annual Review 41, 161– 236. Alos, C., 1999. Anelidos poliquetos del Cabo de Creus (NE de Espana). Faces de Corallina elongata Ellis & Solander y de Cystoseira mediterranea (J. Feldmann). Miscellanea Zoologica 14, 17–27. Altaba, C.R., 1997. Documenting biodiversity: the need for species identifications. Trends in Ecology and Evolution 12, 358–359. Amaral, L.C.Z., Mogardo, E.H., Salvador, L.B., 1998. Polyquetas bioindicadores de poluic¸ao organica em praias paulistas. Revista Brasiliana de Biologia 58 (2), 307–316.

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