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 con-
ducted 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 eects of marine protected areas (MPA) functioning, or in
describing dierent 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 select-
ing a particularly indicative group and working at ne level.
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 macro-
benthic 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 spe-
cies richness and community patterns in benthic inverte-
brate assemblages (Fresi et al., 1983; Olsgard and
Somereld, 2000; Sparks-McConkey and Watling, 2001;
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 Glemarec,
1997; Solis-Weiss et al., 2004). Among benthic groups,
polychaetes are, in fact, one of the best indicators of envi-
ronmental disturbance, since this taxon contains both sen-
sitive 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).
0025-326X/$ - see front matter 2005 Elsevier Ltd. All rights reserved.
doi:10.1016/j.marpolbul.2005.08.003
*
Corresponding author.
E-mail address: gianadri@ilenic.unile.it (A. Giangrande).
www.elsevier.com/locate/marpolbul
Marine Pollution Bulletin 50 (2005) 11531162
1.1. Monitoring with macrobenthos: A brief history
Monitoring with benthic invertebrates has mainly fol-
lowed the so-called indicator species approach, qualita-
tive, based on the presenceabsence of taxa sensitive to
perturbations, or quantitative, based on numerical or tax-
onomic abundance.
The qualitative approach was based on the denition of
opportunistic taxa, mainly polychaetes. Studies involving
communities progressively replaced the biology of single
indicator species, the eect of stress being easier to mea-
sure 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). Eect of stress on the population levels includes: in-
crease in production, especially linked to eutrophication
processes; reduction in diversity and an increase of domi-
nance by opportunistic species; decreasing number of spe-
cies 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 compari-
son 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 sen-
sitive than univariate or graphical ones in discriminating
between sites or times (Warwick and Clarke, 1991). In this
kind of study the identication 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 re-
duced taxonomic resolution was an important development
in the practical assessment of environmental changes. Some
studies have shown that little information is lost by work-
ing 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 perturba-
tions may be easily detected (Warwick, 1988, 1993; Olsgard
and Somereld, 2000; Olsgard et al., 1997, 1998; Mistri and
Rossi, 2000, 2001). This approach, called Taxonomy Su-
ciency (TS), completely bypasses the importance of indica-
tive 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; Gian-
grande et al., in press).
One of the reasons for the functioning of this approach
could be that species are more aected than higher taxa by
both natural variability and seasonal cycle. The natural
variability is in fact one of the critical points in evaluating
the eects of anthropogenic activities both on populations
and multispecies assemblages. Further development in
monitoring led in fact to the identication of an appropri-
ate sampling design capable of measuring a specic eect
and to tease it apart from natural variation (Underwood,
1996; Benedetti-Cecchi, 2001). The rst experimental de-
sign 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 refer-
ence areas (Underwood, 1991, 1992, 1993). Most of these
studies were carried out on articial hard substrates as
these were easier to investigate and substrates could be re-
turned to the labs for detailed studies. The diculty 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 eld: 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 denition of opportunis-
tic species follows an old concept (Cognetti and Taliercio,
1970; Cognetti and Varriale, 1971; Bellan, 1967) still popu-
lar with some monitoring programmes (Amaral et al.,
1998; Go mez Gesteira and Dauvin, 2000; Samuelson,
2001).
According to Pearson and Rosenberg (1978) and
Glemarec and Hily (1981), opportunistic polychaetes spe-
cies are selected in relation to their capability to proliferate
after increases in organic matter. Such species mainly be-
long to the Capitellidae, Cirratulidae, and Spionidae fami-
lies. Some authors also have referred to dierent 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 suering from intra-
specic 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
1154 A. Giangrande et al. / Marine Pollution Bulletin 50 (2005) 11531162
complex (Manchenko and Radashevsky, 1998), and prob-
ably 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 experi-
ence 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 diculty in sampling proce-
dures 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 dicult to choose
appropriate taxon for such monitoring programs. More-
over, as stated before, the application of the correct experi-
mental design in the identication of environmental impact
in habitats which vary naturally, also involves great num-
ber 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 qua-
drates 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 diculty of quantitative sampling and extraction of
vagile organisms, which makes problematic the compari-
son among dierent 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 con-
text 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 Vieitez, 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 dis-
tributed in a large array of habitats, especially on hard bot-
tom littoral fringe (San Mart 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-
tive to pollution or other kind of stress, decreasing in num-
ber of species and individuals or completely disappearing
(Giangrande et al., 2004; Musco et al., 2004). Opportunis-
tic forms seem to be very rare in this group, as an example
we found a taxon identied as Syllis cfr hyalina, which was
the only polychaete present at a site inuenced by high tem-
perature water discharge, and reaching a very high density
(10,000 individuals in 20 cm
2
; 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 ben-
azzii, and Anoplosyllis edentula (recorded as Syllides eden-
tula) 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 impor-
tant changes were observed in species composition and
abundance of Syllidae relatively to a putatively aected
area (Musco et al., 2004). In this area, located South of
the Power station, where the algal mat of Cystoseira re-
mained apparently unaltered, syllid assemblages revealed
heavy modication compared to the northern reference site
which were not aected and characterized by comparable
algal cover (Fig. 1). Syllid species seem to respond to dis-
turbance rapidly with changes mainly occurring at shallow
depths. The most involved species, Brania pusilla, Salvato-
ria clavata, Eusylllis lamelligera and species belonging to
the genus Exogone, which typically colonise shallow sites,
completely disappeared in the impacted site, while popula-
tion of Syllis prolifera markedly declined.
It was supposed that the decline of both number of spec-
imens 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 follow-
ing the main current towards Southern area. A visible
increasing of sedimentation was observed within the sub-
strate during the sampling phase, but unfortunately sedi-
ment load was not measured. Up to now no studies were
actually focused on the inuence 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 toler-
ant space monopolizing species (Airoldi, 2003). An investi-
gation focused on the inuence 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 eects of a sewage discharge on biodiversity (Terlizzi
et al., 2002). The analysis of syllids within polychaetes
A. Giangrande et al. / Marine Pollution Bulletin 50 (2005) 11531162 1155
revealed how, also in this case, they were the best descrip-
tors 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 com-
pared 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 pres-
ent 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 spe-
cies decreased from 21 to 17 proceeding from the controls
to the impacted area. Most of the species such as S. armil-
laris, S. gerlachi, S. rosea, S. pulvinata and S. prolifera, de-
creased in number of individuals. By contrast S. gracilis
and S. krohni showed an inverse trend, increasing in abun-
dance at the impacted site. Between them, only the former
is already reported for stressed environment. The decreas-
ing 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; Gian-
grande, 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 oppor-
tunistic forms. Completely dierent 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 abun-
dant and often exclusive to the impact site, so that a de-
crease of species number coupled with an increase of
abundance was observed, that is the typical trend usually
observed also in soft-bottom polychaetes under distur-
bance. 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
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.
Fig. 2. Investigation of eects from seawage discharge on Syllid assem-
blage. (a) Map of the study area. Sampling were carried out at 5 m depth,
sites were approximately 100300 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.
1156 A. Giangrande et al. / Marine Pollution Bulletin 50 (2005) 11531162
were good indicators of dierent 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 dierent human impact have been
analysed. The Otranto site, an area least inuenced 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 aected by
industrial pollution, showed the lowest number of species
and abundance. Finally Torre Guaceto, an already func-
tioning marine protected area (MPA), which can be inu-
enced by the positive impact (protection), showed no
high variation in number of species, but the highest density
value. The dierences among the three sites was, also in this
case, higher at shallower depths, which are most inuenced
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 indi-
cator that an area is being inuenced of a negative im-
pact. 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 eect (Pinnegar et al., 2000) which can be ex-
plained as follow: protection can increase the abundance
of species predating on small shes, which in turn feed
on small invertebrates. A similar eect 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 indica-
tor of the eect of protection.
The hypothesis of low predation rate can be corrobo-
rated by the observation that the species, which exhibit lar-
ger numbers of individuals at Torre Guaceto, are those
already more abundant at the other sites, and therefore
more probably aected by non-selective predation. More-
over this eect seems not to be present in the endolithic spe-
cies 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 preda-
tors of worms, the polychaete assemblage is often charac-
terized by a high number of species with very few
individuals. It is obvious, however an appropriate experi-
mental design is needed to assess the inuence of predation
rate on polychaetes assemblages.
2.3. Bioclimatic indicators
Syllidae were found to be good biogeographic and bio-
climatic 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 fol-
lows a bioclimatic (ecological) rather than biogeographical
pattern. These assumptions lead to hypothesize syllid dis-
tribution a suitable mean of describing not only environ-
mental 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, invol-
ving 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, inverte-
brates with short life cycle, as syllids are, may be good indi-
cators 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 situ-
ation 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 biocli-
matic categories in relative values between past and present
data are shown in Fig. 4, where an increase of species typ-
ical 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 dierent stretches of
coasts analysed were considered, dierences were not so
marked, especially along the Iberian coast which showed
the least change in composition between the past and pres-
ent situation.
The trend towards warmer composition in the whole
Mediterranean could also be explained by the concentra-
tion of recent studies mainly in warmer areas previously
poorly investigated. It is probably for this reason that a
Fig. 3. Map of the three investigated sites along the Apulian coast (South
Adriatic Sea) with dierent human impact. Explanations are in the text.
A. Giangrande et al. / Marine Pollution Bulletin 50 (2005) 11531162 1157
prevalence of species characteristic of warm areas was de-
tected 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 indica-
tion of a general change of the Mediterranean biota to-
wards 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, Paratypo-
syllis 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 cat-
egories. In either cases, climatic changes or more southern
location of investigations, syllids revealed highly descrip-
tive capabilities and therefore can be proposed as indica-
tors 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 mea-
surements for monitoring purposes.
In the biodiversity analysis Warwick and Clarke (1995)
and Clarke and Warwick (1998, 2001) introduced the Tax-
onomic 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 con-
necting the species traced through a Linnean or phyloge-
netic classication 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 specic 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 be-
came a method to measure stress, to be used in monitoring
and routinal ecological analysis. In contrast, the Taxon-
omy Suciency (TS), conceived for routine analysis (Ellis,
1985) was later utilized to quantify the biodiversity (Balm-
ford et al., 1996, 2000), and this has already been deeply
criticised (Giangrande, 2003; Terlizzi et al., 2003; Gian-
grande et al., in press).
One of the most serious and not yet properly addressed
limitations of the surrogacy approach is the lack of consid-
eration given to processes of sympatric speciation, which
have been shown to occur frequently in the marine environ-
ment (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 dierent groups
are able to colonize these habitats. Colonization of brac-
kish water, for instance, is a rare event, which historically
happened independently in dierent 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 computa-
tion 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 dierent families were
present.
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 = distribu-
tion of categories of species added (%) deriving from the dierence from
past and present data. C = species distributed in cold waters (Arctic, sub-
Arctic, 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.
1158 A. Giangrande et al. / Marine Pollution Bulletin 50 (2005) 11531162
Comparing soft-bottom areas along the Tyrrhenian
coast submitted to dierent 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 consider-
ing species belonging to the family Syllidae. On hard bot-
tom, values ranged from 6.4 to 4.6 and resulted quite
similar comparing dierent areas with similar environmen-
tal conditions, but located in dierent basins (Tyrrhenian
Sea and Adriatic Sea) (Giangrande, 1988; Giangrande
et al., 2003).
The last example reported in Table 1 concerns the de-
crease of the species/family ratio with increasing pollution
coming from the comparison of dierent hard bottom
polychaete assemblages from the same geographical area,
but submitted to a dierent human impact. Utilised data
are the same previously reported in the discussion of po-
sitive 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 use-
ful, 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 fami-
lies. 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 dierent
environmental situations thus leading to consider these
organisms for a future utilization as indicators in monitor-
ing approaches. In particular, the analysis of Syllidae spe-
cies distribution appears a very sensitive index. Species
belonging to this family decrease in abundance or com-
pletely disappear under dierent sources of negative impact
(pollution, high sedimentation rate), so they do not re-
spond to the classical scheme which considers polychae-
tes indicative only by the presence of opportunistic taxa
(Cognetti and Taliercio, 1970; Bellan, 1984).
Syllidae were also found to be indicative of protection
eects (Giangrande et al., 2004), or in describing dierent
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 eld 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 Mart n, 2003, 2005). Probably any
group of invertebrates could be indicative if analyses were
conducted at ner taxonomic level.
The importance of taxonomy in ecological elds 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 dierent bio-
topes also revealed soft-bottom habitats more diverse at
family level than hard-substrates. By contrast, the high
Table 1
Comparison of polychaetes diversity at dierent taxonomic levels in some Mediterranean biotopes
Brackish water Caprolace Lake
(salinity 30&, low organic load)
Sabaudia Lake
(salinity 30&, high organic load)
Fondi Lake
(salinity 20% )
Total
No. of families 17 (89%) 10 (52%) 4 (21%) 19
No. of species 27 (64%) 13 (30%) 4 (10%) 42
Ratio 1.5 1.3 1
Soft-bottom Latium coast (high trophic input) Tuscany coast
(low trophic input)
No. of families 27 (93%) 24 (82%) 29
No. of species 91 (94%) 52 (54%) 96
Ratio 3.5 2.1
Hard-bottom (similar depth
and algal cover)
South Adriatic coast Tyrrhenian coast
No. of families 17 (74) 20 (81%) 23
No. of species 108 (71%) 110 (72%) 153
Ratio 6.4 5.5
Hard-bottom Torre Guaceto (protected site) Otranto (pristine site) Cerano (polluted site)
No. of families 17 (89%) 16 (84%) 14 (74%) 19
No. of species 108 (86%) 84 (67%) 65 (52%) 126
Ratio 6.4 5.3 4.6
A. Giangrande et al. / Marine Pollution Bulletin 50 (2005) 11531162 1159
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 soft-
bottom 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 de-
sign 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 Sylli-
dae 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 fea-
ture usually present in sessile organisms (Schroeder and
Hermans, 1975), as a probable response to the high compe-
tition rate.
However, few data on syllid feeding requirement are
available (Giangrande et al., 2000), in order to infer
intra-interspecic competition and implication for the allo-
cation of energy (Belovski, 1997). A signicant 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 mon-
itoring approaches (Basset et al., 2004).
In conclusion our suggestion is that in monitoring stud-
ies operational time could be optimized not only by work-
ing on the whole invertebrate data set utilising surrogacy,
but also working at ner 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 sur-
rogate for marine biodiversity. Also in this case the work
was possible thanks to the contribution of one of the major
specialists in Terebellidae taxonomy.
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