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Sewage pollution and extinction risk: an endangeredlimpet as a bioindicator?
F. ESPINOSA*, J.M. GUERRA-GARCÍA and J.C. GARCÍA-GÓMEZLaboratorio de Biologı́a Marina, Dpto. Fisiologı́a y Zoologı́a, Facultad de Biologı́a, Universidad de
Sevilla, Avda Reina Mercedes 6, 41012, Sevilla, Spain; *Author for correspondence (e-mail:
free@us.es; phone: +34-954557100; fax: +34-954233480)
Received 6 January 2005; accepted in revised form 9 September 2005
Key words: Harbour, Monitoring, Patella ferruginea, Patellogastropods, Pollution, Sewage outfall,
Siphonaria
Abstract. The mollusc Patella ferruginea, endemic to the Mediterranean, is the most endangered
marine species on the list of the European Council Directive 92/43/EEC and it is under serious risk
of extinction. In spite of the low abundances and restricted distribution of this limpet, important
populations have been found in the harbour of Ceuta, north Africa. The main objective of the
present study was to characterise, for the first time, the effects of sewage pollution on P. ferruginea
and related limpet species, and to evaluate the potential value of these limpet assemblages as
bioindicators, using univariate and multivariate analyses. Physicochemical parameters and limpets
were sampled in nine stations located at 0, 1, 2, 4, 8, 16, 32, 64 and 128 m away from the discharge
point of a sewage effluent in Ceuta harbour. The stations closer to the outfall (0, 1, 2, 4 and 8) were
characterised by higher values of turbidity, phosphate and ammonia in the water column, and
organic matter, faecal coliforms and faecal Streptococci in sediments. A total of six limpet species
were found and studied (Patella ferruginea, P. caerulea, P. nigra, P. rustica, P. ulyssiponensis and
Siphonaria pectinata); the number of limpet species increased with increasing distance from the
outfall, while diversity and evenness reached the highest values at intermediate sites. Siphonaria
pectinata and P. caerulea were the most resistant and abundant species, while P. ferruginea was the
most sensitive species to sewage pollution, only found at stations from 32 to 128 m. The distri-
bution of this endangered limpet seems mainly affected by the pollution gradient, and not by the
competition with the remaining limpets. The results of this study should be taken into account in
future programmes of management and conservation of P. ferruginea.
Introduction
The limpet Patella ferruginea Gmelin, 1791, endemic to the Mediterranean, isthe most endangered marine species on the list of the European CouncilDirective 92/43/EEC on the conservation of Natural Habitats and of WildFauna and Flora, 1992 (Ramos 1998), and it is, presently, under serious risk ofextinction (Laborel-Deguen and Laborel 1991; Templado and Moreno 1997).Although its relative abundance in Palaeolithic and Neolithic deposits indicatesa former distribution in the Western Mediterranean Basin (East coast of Italy,Mediterranean France, Iberian Peninsula, Morocco, Tunisia and the WesternMediterranean islands), today its Mediterranean range has progressively con-tracted to a few restricted areas (Cretella et al. 1994; Templado 1996) probably
Biodiversity and Conservation (2007) 16:377–397 � Springer 2006DOI 10.1007/s10531-005-3014-3
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due to human pressure (Aversano 1986; Laborel-Deguen and Laborel 1991).Although the species is threatened with extinction, important populations havebeen found recently inside the harbour of Ceuta, Strait of Gibraltar (Guerra-Garcı́a et al. 2004a, b); Ceuta harbour is environmentally unique, differingsubstantially from other conventional harbours, since it is located between twobays connected by a channel which increases the water movement and ex-change and contributes to the maintenance of rich and diverse communities ofmarine invertebrates (Guerra-Garcı́a and Garcı́a-Gómez 2005). Little is knownabout the biology and ecological preferences of P. ferruginea; this species has avery low growth and reproductive rate, reaching sexual maturation at 2–3 years (Guerra-Garcı́a et al. 2004a). It is a protandric species with oocytes of142–170 lm (Unpublished data) and this limpet feed mainly on cyanobacteriaand the algae Ralfsia spp. and Rissoella spp.In the harbour of Ceuta, P. ferruginea coexists with five other limpet species:
Patella caerulea Linnaeus, 1758, Patella nigra da Costa, 1771, Patella rusticaLinnaeus, 1758, Patella ulyssiponensis Gmelin, 1791 and Siphonaria pectinata(Linnaeus, 1758). Patella nigra is also an endangered limpet, however, unlikeP. ferruginea, P. nigra is not suffering a clear regression and populations seemto be increasing (Templado et al. 2004). Recent morphological and molecularstudies seems to indicate that P. nigra should be transferred to the genusCymbula, as Cymbula safiana Lamark, 1819 (see Ridgway et al. 1998;Koufopanou et al. 1999). Taking into account that there is a sewage outfallinside the harbour of Ceuta, the present study explores how this sewage effluentis affecting the limpet assemblages in general andPatella ferruginea in particular.Due to their ecological importance, as well as sedentary life, molluscs have
assumed a major role in monitoring contaminants worldwide (Boening 1999;Feldstein et al. 2003). They are abundant, sedentary and easy to collect, whichmakes them ideal for biomonitoring (Bresler et al. 2003a, b). Furthermore, incomparison with other marine environments, access to intertidal ecosystems isusually easier, and these ecosystems are more amenable to management thanopen ocean and sublittoral benthic habitats. Additionally, the composition ofsessile communities is particularly useful as baseline for ecological monitoringbecause such organisms are unable to avoid disturbances in the marine envi-ronment and thus, the composition of the community reflects their commonhistory (Fa et al. 2002).Differences in physical and biological conditions are the main cause of
variation in marine communities, both in time and space (Pain and Levin 1981;Dayton 1984; Sousa 1984), and, consequently, environmental gradients areimportant in determining the structure of assemblages (Bishop et al. 2002).Some of these gradients originate as anthropogenic perturbations. One of themost serious, and increasingly common, sources of disturbance in marinecommunities is the discharge of sewage effluents (Gerlach 1981; Gray 1982).These effluents are often discharged via outfalls into shallow subtidal habitats,and can result in significant effects on marine biota, involving changes incytology and physiology at the individual level that are ultimately manifested
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as alterations in the community structure (Littler and Murray 1975). There arefew studies describing the effects of sewage on macro-benthic assemblagesliving on hard substrata (Terlizzi et al. 2002). Furthermore, according toUnderwood (1997), some authors have analysed differences between an im-pacted location and a single control, with evident problems of pseudoreplica-tion and consequently confounding in the logical interpretation of results.Additionally, along the Mediterranean coasts, despite a large amount ofdomestic and industrial sewage discharged to the sea (UNEP 1989), there arefew published accounts of the effects of sewage effluents on the macrobenthos(see Terlizzi et al. 2002).The objectives of the present study are to characterise the effect of a sewage
effluent on density, size and assemblages of the patellid community inhabitingthe rocky intertidal shores of the harbour of Ceuta, North Africa, with specialattention to the endangered P. ferruginea, and to explore the value of thesepatellid molluscs as bioindicators of sewage pollution.
Material and methods
Study area
The harbour of Ceuta (35�53¢ N, 5�18¢ W) is one of the most important in theStrait of Gibraltar, because of its situation relative to Europe and Africa(Figure 1). There are no river discharges directly into the harbour and, unlikeother harbours in this region of the Mediterranean, industrial activity adjacentto the harbour of Ceuta is absent. Consequently, the contamination inside theharbour is derived from the sewage effluents of urban influence, antifoulingpaints and accidental oil spills during the loading and dumping involved inshipping operations. Although the sediments are moderately polluted in theharbour of Ceuta (Guerra-Garcı́a et al. 2003), this harbour has a unique designwith two opposing entrances and a channel, which increases water exchangemaintaining high oxygen levels in the water column. Under these unusualconditions (polluted sediments but oxygen saturation), the communities of theharbour of Ceuta are characterised by rich and diverse macrobenthic com-munities. The number of species is unusually high when compared with othermore conventional enclosed harbours of nearby areas which do not have twoopposing entrances or a channel (see Guerra-Garcı́a and Garcı́a-Gómez2004a–c, 2005; in press).Inside the harbour there is a sewage outfall located close to a leisure resort.
The study was conducted during summer (August 2002), which coincides withthe maximum peak of tourist activity. Raw sewage is discharged onto the shorearea through a pipeline with a rectangular section measuring 135 · 75 cm.Although the outfall is discharging throughout the whole year, it is especially
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active during the summer months, discharging every day. The outfall terminusis located in the intertidal area, composed of sandstone artificial rocks.
Sampling methods
A total of nine sites were selected for this study. The first station (Site 0) wasthe ‘outfall site’ and the remaining stations were located at 1, 2, 4, 8, 16, 32, 64and 128 m away along a transect (see Figure 1). The presence of the sewageeffluent involves a gradient, and sampling is usually conducted in spatial scaleand regularly (May 1985; Foe and Knight 1987; Lopez-Gappa et al. 1990;Zmarzly et al. 1994); however, sampling at regular intervals from a disturbanceusing a single spatial scale is not necessarily appropriate (Bishop et al. 2002).We used herein a logarithmic scale (log2) to explore more carefully the areaclose to the outfall since communities inhabiting this area are the most affectedby the sewage pollution.
Limpet samplingIn each station, the density of limpets was measured by counting the number ofspecimens found in a 1 m wide transect located from the zero tidal level to theupper level of the intertidal in which limpets were present. At site 0, coincidentwith the outfall, no limpets were found. The size of each limpet was estimatedby measuring the shell length (see Guerra-Garcı́a et al. 2004a). The species
Figure 1. Map of the study area in the harbour of Ceuta, North Africa. Arrow indicates the
sewage discharge point, and the gross continuous line the 128 m transect. Sampling sites from 0 to
128 m along the transect are indicated.
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were identified ‘in situ’ when possible; if the species could not be properlyvisually identified due to epiphytic alga or fauna, the limpet was removed foridentification in the laboratory.
Physico-chemical analysisIn addition to the limpet study, several physico-chemical parameters weremeasured in the water column and sediments in each sampling stations.Water samples were taken in the nine stations. Free and total ammonia,
nitrate, nitrite, phosphate and pH were measured using colorimetric methodsbased on analytical test Seachem�, and dissolved oxygen using the kitD.O.Azoo�. Turbidity was measured in nephelometric turbidity units (ntu)using a turbidimeter Hanna HI 93703.Sediments were also collected at the nine sites, at 4 m depth and 20 m away
from the coast. Analysis were conducted using the finest fraction of the sedi-ment (diameter less than 0.063 mm) (see Guerra-Garcı́a and Garcı́a-Gómez2005)). Sediment samples were conserved in sterile containers until their arrivalat the laboratory where they were frozen. The organic content was analysed byashing samples of sediment to 500 �C for 6 h and re-weighing (mean values ofthree replicates of 2 g each) (see Estacio et al. 1997). Phosphate and nitratewere measured using UV visible spectrophotometry followingMétodos oficialesde análisis para aguas residuales y suelos (1986). Hydrocarbons were measuredby extraction and FT-IR spectrophotometry (see Estacio et al. 1997). Thefaecal coliforms were measured as the coliforms which fermented lactose in amedium M-FC with production of acid and gas at 44.5 �C during 24 h. Formeasuring the faecal Streptococci, agar m Enterococcus at 35 �C during 48 hwas used. The results of microbiological analyses were expressed as colonialformers units (cfu) per gram of sediment.
Statistical analysis
The total number of species, the Shannon–Wiener diversity index (Shannonand Weaver 1963) and the Pielou’s evenness index (Pielou 1966) were calcu-lated for each station based on the abundances of patellid species.The affinities among stations were established through cluster analysis using
the UPGMA method (unweight pair–group method using arithmetic averages)(Sneath and Sokal 1973), based on the Bray–Curtis similarity index for thelimpet species matrix and on the Euclidean distance for the environmentalmatrix. Abundance data of the limpet species were double square root trans-formed so that the ensuing classification and ordination were not determinedonly by the most dominant species (Clarke and Green 1988); environmentaldata were transformed using log (x+1) (see Guerra-Garcı́a and Garcı́a-Gómez2001). In order to confirm the results of the cluster, Principal ComponentAnalyses were used for the ordination of stations based on the physico-chemical data measured in water and sediment, and a MDS (non-metric
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multidimensional scaling) was used for biological data. To test the ordination,the stress coefficient of Kruskal was employed (Kruskal and Wish 1978). Toexplore the relationships among environmental measures and the patellidassemblages, a canonical correspondence analysis (CCA) was applied. Rela-tionships between multivariate biological structure and environmental vari-ables were also examined using the BIO-ENV procedure (Clarke andAinsworth 1993). Percentage of similarity analysis (SIMPER) (Clarke 1993)was used to determine the species involved in grouping of the different stations.Possible differences in limpet abundances and sizes between the groups
defined by ordination and classification analyses based on physicochemicalparameters, were tested using Kruskal–Wallis test, since normality (Shapiro–Wilk test) and/or homogeneity of variances (Levene test) were not passed, andconsequently ANOVA parametric tests could not be carried out.Univariate and multivariate analyses were carried out using BMDP (Dixon
1983), PRIMER (Clarke and Gorley 2001) and the PC-ORD (McCune andMefford 1997).
Results
Physicochemical parameters
Table 1 includes the values of physicochemical parameters measured in waterand sediments. In the water column, a clear trend could be observed fornutrients. The concentrations of ammonia and phosphate were at least oneorder of magnitude higher in the stations located near the outfall than in theremaining stations further away. The highest values of turbidity and pH werealso recorded near the sewage outfall. On the other hand, oxygen showed thelowest values in the first 16 m, while in stations located at 32, 64 and 128 maway from the outfall, the oxygen concentrations were higher, reaching9.0 mg/l. With regard to the sediment, both faecal coliforms and Streptococciwere more abundant in the stations closer to the outfall; the same trend wasobtained for hydrocarbons (Table 1) and for organic matter (Figure 2).However, phosphate and nitrate did not show a clear pattern, and concen-trations of phosphate were often higher in the stations more distant from theoutfall.The PCA plot obtained using the physicochemical parameters of the water
column reflected similar gradients to the PCA elaborated with the sedimentvariables, although the former showed more clearly the gradient produced bythe outfall (Figure 3). The first axis of the PCA ordination using water columnmeasures, explained 59.1% of the total variance and the percentage of varianceexplained by axis 1 of the PCA based on the sediment measures was 43.4%.The PCA analyses, consequently, confirmed the trend of a pollution gradientfrom the outfall point. Cluster analyses also supported this ordination andshowed clearly that stations could be separated into two groups according to
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Table
1.
Values
obtained
forvariablesmeasuredin
thewatercolumnandsedim
entattheninesamplingsitesalongthetransect.n.a:data
notavailable.
Sites
Watercolumn
Sedim
ent
Freeammonia
(ppm)
Totalammonia
(ppm)
Nitrate
(ppm)
Nitrite
(ppm)
Phosphate
(ppm)
Oxygen
(mg/l)
pH
Turbidity
(ntu)
F.coliform
s
(cfu/g)
F.Streptococci
(cfu/g)
Phosphate
(ppm)
Nitrate
(ppm)
Hydrocarbons
(ppm)
02.50
3.50
0.2
0.10
3.5
6.0
8.2
35.42
416.94
268.36
12.50
3.50
1.0
0.50
3.5
6.5
8.2
15.06
9134
5.35
7.13
76.67
20.50
3.00
0.2
0.10
2.5
5.0
8.7
10.69
3119
4.89
20.37
78.82
40.15
2.00
0.2
0.10
2.0
7.0
8.0
5.19
18
230
5.20
3.19
119.78
80.15
2.00
0.2
0.10
3.0
5.0
7.9
2.19
2108
9.24
6.35
85.69
16
0.01
0.15
0.2
0.05
1.0
5.0
8.1
0.85
015
8.38
8.59
23.51
32
0.01
0.15
0.2
0.05
0.2
9.0
8.1
1.10
015
17.02
17.92
32.64
64
0.01
0.15
0.2
0.05
0.2
9.0
8.1
0.86
07
14.53
14.26
52.70
128
0.01
0.15
0.2
0.05
0.2
9.0
7.9
0.88
1n.a.
9.40
16.77
70.69
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the physicochemical parameters both in the water column and sediments. Onegroup (from now on referred to as near sites) was formed by the sites located inthe first 8 m of the transect, and the second group (from now on referred to as
Figure 2. Percentage of organic matter measured in the nine sampling sites along the transect.
Mean values and standard deviations are included.
Figure 3. PCA (left) and Cluster (right) plots, based on the physicochemical parameters measured
in the water column and sediment.
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further away sites) included the remaining sites (from 16 to 128 m) (Figure 3).These two groups of stations shown by the physicochemical data (near sites vsfurther away sites) were used in further comparisons between density and sizeof specimens, as well as for SIMPER analysis.
Biological data
The limpets Siphonaria pectinata (Basommatophora) and Patella caerulea(Patellogastropoda) were present in all the sampled sites, although the densitieswere significantly higher in the further away sites than in the near sites(S. pectinata, K = 5.4, p
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in sediment, according to the BIO-ENV. Including extra variables the signifi-cance of the correlation decreased, although the values were also significant(Table 3). Taking into account that eight stations only were sampled, themaximum number of variables which we could included in the CCA analysiswas seven; consequently, we selected the seven variables which, independently,showed the best correlation coefficients with the biotic data in the BIO-ENVanalysis: turbidity, free ammonia, total ammonia, nitrite, phosphate, organic
Figure 4. Number of individuals and size of each limpet species at the sampled stations along the
transect. Mean values and standard deviations are included for size.
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matter in sediment, and phosphate in sediment. The first axis of the CCAanalysis (Figure 8, Table 4) mainly correlated with the organic matter of thesediment, but also with the concentrations of total ammonia, turbidity andphosphate (both in water and sediment). Axis 1 separated Patella ferrugineaand P. rustica from the remaining species. These two limpets were associatedwith the further away sites (32, 64 and 128 m), characterised by lower con-centrations of ammonia, phosphate in water, organic matter in sediment andlower values of turbidity. On the other hand, the axis 2 separated the stations 1
Figure 4. Continued
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and 2 -and the species Siphonaria pectinata and Patella caerulea-, from thestations 4, 8 and 16 -and the species P. nigra and P. ulyssiponensis-, based on theconcentrations of free ammonia, which correlated significantly with the axis 2.
Discussion
Physico-chemical data
The present study showed moderate concentrations of nutrients (mainlyammonia and phosphates) in the water column close to the outfall. These
Figure 5. The relative contribution in percentage of individuals of each limpet species at the
sampling sites. See also Figure 4.
Figure 6. Species richness (S), Shannon–Wiener diversity (H¢) and Pielou evenness (J) of thepatellid community in each station.
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concentrations were considerably higher than those measured in other areasof the harbour of Ceuta and adjacent waters (see Guerra-Garcı́a 2001),which indicates the urban influence of sewage effluent. The oxygen con-centrations near the outfall (5–7 mg/l) were lower than in the sites 32, 64and 128 m (9 mg/l). Several studies have recently pointed out the impor-tance of oxygen in the water column on macrofaunal assemblages (Saı́z-Salinas 1997; Guerra-Garcı́a and Garcı́a-Gómez 2005). Our data are inagreement with Littler and Murray (1975) that recorded values of 5.5 mg/l
Figure 7. Cluster and MDS analysis based on the abundance of patellid species.
Table 2. Average abundances of the species from sites located closer to the outfall (N) and further
away (F).
Species Abund. N Abund. F Av. Dis. Ratio Dis. (%) Cum. Dis (%)
Patella rustica 0.75 18.00 9.13 2.18 23.40 23.40
Patella caerulea 11.00 94.00 7.77 2.49 19.90 43.30
Siphonaria pectinata 17.25 115.25 7.01 4.59 17.97 61.27
Patella ferruginea 0.00 5.50 6.75 1.64 17.29 78.57
Patella ulyssiponensis 0.50 2.50 4.23 1.13 10.83 89.39
Patella nigra 6.50 5.75 4.14 1.10 10.61 100.00
Species are listed in order of decreasing contribution to the average dissimilarity (Av. Dis.) between
the two groups. The ratio indicates Dis/Standard deviation. The total average dissimilarity between
groups is 39%.
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in an outfall point located in San Clemente Island, California, and values of7–8 mg/l, 30 m away. Mean values of turbidity measured inside Ceuta’sharbour are about 0.62 ntu (CEDEX 2000); however, the values measuredin this study near the effluents reached 35 ntu. These high values of tur-bidity, due to the presence of solids and organic matter in suspension mayhave direct negative effects since these can clog the gills of marine organ-isms, such as limpet molluscs. In this sense, Marshall and McQuaid (1989)compared the survival rate of a pulmonate limpet (Siphonaria capensis)with a prosobranchia limpet (Patella granularis) in the presence of sand andlow oxygen concentrations, and found a higher survival of the pulmonatelimpet possibly due to the different breathing strategy. This fact couldexplain the presence of S. pectinata very close to the effluent outfall in thepresent study. Furthermore, Branch (1981) pointed out that siltation may bemore important than salinity in excluding limpets from estuaries.
Biological data
There is a lack of studies dealing with the abundance of patellids in areasaffected by sewage disposal. Bishop et al. (2002) found higher densities of the
Table 3. Summary of results from BIO-ENV analysis.
k Best variable combination
1 Turbity 0.871 F. ammonia 0.870 T. ammonia 0.866 Nitrite 0.828
2 Turbidity 0.944 Turbidity 0.923 F. ammonia 0.893 T. ammonia 0.893
Phosphate T. ammonia T. ammonia Cu
3 T. ammonia 0.946 T. ammonia 0.929 F. ammonia 0.907 F. ammonia 0.907
Turbidity Phosphate T. ammonia T. ammonia
O.M. Turbidity Turbidity O.M.
4 F. ammonia 0.960 T. ammonia 0.951 T. ammonia 0.946 F. ammonia 0.927
T. ammonia Nitrite Nitrate T. ammonia
Turbidity Turbidity Turbidity Phosphate
O.M. O.M. O.M. Turbidity
5 F. ammonia 0.956 T. ammonia 0.953 T. ammonia 0.945 F. ammonia 0.939
T. ammonia Nitrite Nitrate T. ammonia
Phosphate Phosphate Phosphate Oxygen
Turbidity Turbidity Turbidity Turbidity
O.M. O.M. O.M. O.M.
6 F. ammonia 0.950 T. ammonia 0.944 T. ammonia 0.943 F. ammonia 0.937
T. ammonia Nitrite Nitrate T. ammonia
Phosphate Phosphate Phosphate Phosphate
Turbidity Turbidity Turbidity pH
O.M. O.M. O.M. O.M.
Phosphate (sed) Phosphate (sed) Phosphate (sed) Phosphate (sed)
Combinations of variables, k at a time, giving the highest rank correlations between biotic and
environmental similarity matrices are shown with the value of the weighted Spearman rank cor-
relation coefficient; text in bold type indicate the best combination overall.
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Figure 8. Graphic representation of the stations, limpet species and environmental measures with
respect to the first two axes of the canonical correspondence analysis (CCA).
Table 4. Summary results of the canonical correspondence analysis.
Axis 1 Axis 2 Axis 3
Eigenvalue 0.11 0.06 0.01
Species–environment correlation 0.99 0.99 0.99
Percentage of species variance 58.3 30.8 6.7
Correlation with environmental variables
Free ammonia (ppm) – 0.72* –
Total ammonia (ppm) 0.79* – –
Nitrite (ppm) – – –
Phosphate (ppm) 0.89** – –
Turbidity (ntu) 0.76* – –
OM sed. (%) 0.98*** – –
Phosphate sed. (ppm) � 0.89** – –
*p
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limpet Patelloida latistrigata in sites further away from an outfall; Tabladoet al. (1994) found significant lower densities of Siphonaria lessoni near anoutfall point. In the present study, for the six limpet species recorded, thelowest abundances were found close to the outfall, and sites 1 and 2 weredominated by Siphonaria pectinata, which was the most resistant species to thesewage pollution. On the other hand,P. ferruginea was most sensitive to theeffluent, and was absent in regions of low oxygen concentrations, and highconcentrations of ammonia, phosphate and turbidity in the water column. Thislimpet is the most endangered marine invertebrate in the Western Mediterra-nean rocky shores. It has been traditionally considered a K-strategist, associ-ated with clean waters, a long life cycle and a lower reproductive rate (seeGuerra-Garcı́a et al. 2004a). Although several important populations ofP. ferruginea have been found recently in the harbour of Ceuta (Guerra-Garcı́aet al. 2004a, b), the presence of this species on the Iberian Peninsula is ex-tremely reduced; the most recent cites of P. ferruginea in the Iberian Peninsulaare reported by Garcı́a-Gómez (1983) who recorded several individuals inAlgeciras Bay, and Moreno (1992), who found two specimens in Cabo de Gata.It is especially interesting that other species, such as P. nigra and P. ulyssi-ponensis were more abundant in intermediate sites. These higher abundancescould be due to enrichment effects (sensu the Intermediate Disturbance andDynamic Equilibrium Hypotheses) and should be considered at least aspotential components of community structure through e.g. competitive effects.It is also interesting that P. rustica was the greatest contributor to dissimilarity.It is an upper-shore species, usually found well above the other limpet speciesstudied, and may indicate the possible influence of dessication pressures alongthe vertical gradients.For the dominant species, S. pectinata and Patella caerulea, the specimens
near the discharge point were significantly larger than the individuals locatedfurther away. A combination of several factors (such as the higher inputs oforganic matter and the lower intraspecific and interspecific competition due tolower densities) could explain this pattern. High growth rates in areas affectedby organic enrichment have been recorded for Patella vulgata (Hatton 1938;Fischer-Piette 1948; Lewis and Bowman 1975) and S. pectinata (Voss 1959).Bastida et al. (1971) measured a higher growth rate for S. lessoni inside aharbour area. Liu and Morton (1998) found larger specimens of Patelloidasaccharina and Patelloida pygmaea in polluted areas in comparison tounpolluted sites, and Tablado et al. (1994) recorded higher growth rates inspecimens of S. lessoni placed near sewage outfall than specimens placed innon-polluted areas.Multivariate analysis showed that turbidity, ammonia and phosphate in
the water column, together with the organic matter in sediment, were theparameters that mainly explained the limpet assemblages. Recent studiesfocused on marine communities of Algeciras Bay, also located in the Strait ofGibraltar, have shown that turbidity is one of the factors negatively affectingthe distribution of benthic assemblages (Sánchez-Moyano et al. 1998).
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Effects of sewage effluents
The results of the present study, based on the limpet assemblages, showed a cleargradient of environmental perturbation from the sites near the sewage outfall tothe further away sites. As pointed out by Pearson and Rosenberg (1978), theeffects of a sewage effluent are most pronounced in the vicinity of the outlets anddecrease progressively with increasing distance from the discharge points.Raffaelli and Hawkins (1996) pointed out that most of the small volumes ofeffluent discharge have ecological effects in the first 10 m away from the outfall.Littler and Murray (1975), in a study conducted in San Clement Island, Cali-fornia, indicated pollution effects inside the first 30 m from the effluent, andnormal communities from 90 m away. Terlizzi et al. (2002) provided evidencethat sites located about 100–300 m apart from an outfall located in Apuliancoast, Italy, were similar to each other and they differed from the site locatedin close proximity to the sewage. Lopez-Gappa et al. (1993) found pollutioneffects on intertidal communities 50–100 m away from effluents from the cities ofNecochea and Quequén (Argentina). In the present study, natural conditionswere completely re-established at 64 m from the discharge point.
Conclusions and environmental implications
The physicochemical parameters measured both in the water column andsediment showed a clear perturbation due to the presence of the sewage effluentinside the harbour. However, the effect on limpet assemblages is restricted, andfrom 32–64 to 128 m from the point of discharge ‘normal’ conditions arere-established. From a methodological point of view, the use of log2 can beuseful to select and locate the sampling sites in this kind of study, focused onenvironmental gradients.Furthermore, limpet assemblages can be used as a tool to evaluate the
environmental state of the coast, without the need of using the whole com-munity which would be more time consuming and would require higher costs.In this sense, authorities and government institutions are increasinglydemanding quick and effective environmental studies in coastal areas. This factprecludes developing series of data based on complex matrices of varioustaxonomic groups whose identifications requires great effort and time. A short-term spatial study dealing with only several easy-to-identify limpet species canyield similar results to those obtained with costly physico-chemical analysis.Although further studies are necessary to investigate the ecological prefer-
ences and responses to pollution of the endangered mollusc Patella ferruginea,this study represents a first approach, showing that this limpet is sensitive tosewage pollution, specially to the increase of turbidity, ammonia and phos-phate, and the decrease of oxygen concentrations in the water column. Theseinitial results should be taken into account in future studies of management
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and conservation of P. ferruginea. Furthermore, the present work showed thatthe highest densities of P. ferruginea were measured at 32 and 64 m away fromthe outfall, coinciding with the highest densities of other limpets; therefore, thistrend indicates that the main problem for P. ferruginea is the degree of pol-lution, and not interspecific competition with other limpets. This fact should bealso taken into consideration in future programmes of reintroduction orresettling of this endangered limpet.
Acknowledgements
Special thanks are due to our colleagues Alexander Roi González, CristinaHuertas and Aurora Ruiz for helping during sampling. The present work wasfunded by the Asamblea de Ceuta, Autoridad Portuaria de Ceuta, and a PhDscholarship FPU AP-3556-2001 (to F. Espinosa) from the Ministry of Edu-cation and Culture of Spain.
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