Changes in benthic fish assemblages as a consequence of coastal works in a coastal lagoon: The Mar Menor (Spain, Western Mediterranean)

Marine Pollution Bulletin 53 (2006) 107–120 www.elsevier.com/locate/marpolbul

Changes in benthic fish assemblages as a consequence of coastal works in a coastal lagoon: The Mar Menor (Spain, Western Mediterranean) A. Pe´rez-Ruzafa *, J.A. Garcı´a-Charton, E. Barcala, C. Marcos Departamento de Ecologı´a e Hidrologı´a, Facultad de Biologı´a, Universidad de Murcia, 30100 Murcia, Spain

Abstract The benthic fish assemblage of the Mar Menor consisted of 37 species. Dominant species are: Gobius cobitis, Lipophrys pavo and Tripterygion tripteronotus on infralittoral rocks; Pomatoschistus marmoratus, Callionymus pussillus, Callionymus risso and Solea vulgaris on sandy bottoms and Gobius niger, Syngnathus abaster, Hippocampus ramulosus and Symphodus cinereus on Cymodocea nodosa–Caulerpa prolifera mixed beds. From 1985 to 1989 tourist development has led to the creation of new beaches and the installation of artificial rocky structures for retaining sediments. Dredging for the extraction of sand and subsequent pumping altered sediment characteristics causing a real stress leading to the substitution of typical sandy bottoms communities with Cymodocea nodosa by Caulerpa prolifera communities on mud. Soft bottom fish assemblages responded to changes in vegetation cover and substratum characteristics mainly changing the species composition, while artificial hard substrata contain a similar fish community than natural ones, harbouring even richer and more diverse assemblages. This positive effect of breakwaters should not obscure their likely negative effects on hydrodynamics and the subsequent changes of sediment quality and vegetation cover on the breakwatersÕ area of influence. Ó 2005 Elsevier Ltd. All rights reserved. Keywords: Fish assemblages; Coastal works; Coastal lagoons; Mediterranean

1. Introduction Coastal lagoons are dynamic ecosystems dominated by physical characteristics, such as shallowness, relative isolation and the presence of boundaries with strong physical and ecological gradients (Unesco, 1981). Most lagoons show frequent physical and chemical disturbances and fluctuations (Unesco, 1981) being considered as naturally stressed habitats (Barnes, 1980), belonging to the physically controlled ecosystems of Sanders (1968). Environmental stress conditions the structure of biological assemblages leading to rather complex interactions among physical, chemical and biological parameters and

*

Corresponding author. E-mail address: [email protected] (A. Pe´rez-Ruzafa).

0025-326X/$ - see front matter Ó 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.marpolbul.2005.09.014

processes (Gamito et al., 2005). Species respond to these situations through their life-history strategies, for example by having an increased reproductive effort through early reproduction, small and numerous offspring with large dispersive capability, short life span and small body size of adults, therefore providing a selective advantage in unpredictable or short-lived environments. Because of these characteristics, coastal lagoons usually are among those marine habitats with a highest biological productivity (Allongi, 1998). They play an important ecological role among the coastal zone ecosystems providing a collection of habitat types for many species (Ya´n˜ez-Arancibia and Nugent, 1977; Clark, 1998), functioning as nursery areas, and feeding grounds for marine estuarine opportunistic fishes that support important fisheries. Pe´re`s and Picard (1964) considered the Mediterranean lagoon system as a well differentiated and unique homogeneous assemblage, the so-called euryhaline and

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A. Pe´rez-Ruzafa et al. / Marine Pollution Bulletin 53 (2006) 107–120

eurythermal biocenoses. This consideration has been maintained by later authors as Augier (1982) or Gue´lorget and Perthuisot (1983). Species composition of adult fish assemblages in coastal lagoons has been well studied in the Mediterranean (Casabianca and Kiener, 1969; Lozano, 1969; Mathias, 1970; Paris and Quignard, 1971; Herve´ and Brusle, 1980, 1981; Ramos and Pe´rez-Ruzafa, 1985; Bouchereau et al., 2000; Mariani, 2001) and elsewhere ´ lvarez et al., 1986; Thorman, (Ya´n˜ez-Arancibia, 1985; A 1986; Stoner, 1986; Pollard, 1994; Vieira and Musick, 1994; Elliott and Dewailly, 1995; Whitfield, 1994, 1999; Ishitobi et al., 2000; Araujo and Costa de Azevedo, 2001; Garcı´a et al., 2001; Kupschus and Tremain, 2001; Paperno et al., 2001; Pombo et al., 2002). These works consider the fish assemblages as relatively homogeneous inside each lagoon, and usually lagoonal fishes are classified mainly according to their migratory behaviour (e.g. Whitfield, 1999). Variability between lagoons is attributed to the integration of a large set of biotic and abiotic factors (Ross and Epperly, 1985; Ya´n˜ez-Arancibia et al., 1985), and variability inside any single lagoon has been related to the confinement gradient sensu Gue´lorget and Perthuisot (1983); an indicator of the degree of marine influence on lagoon ecosystems (Mariani, 2001). Most lagoons are subject to human exploitation—through fishing or aquaculture, and tourism, with the associated urban, industrial or agricultural development—inducing changes that affect their ecology. Although the effects of disturbance on macrobenthic invertebrate community structure is well known (e.g. Koutsoubas et al., 2000), little is known on the effect of coastal works on fish assemblages in coastal lagoons. The Mar Menor lagoon, located in the Southeast of Spain (Fig. 1), is of social concern because of the large changes during recent decades with concomitant impact on its communities structure and dynamic (Pe´rez-Ruzafa, 1989, 1996; Pe´rez-Ruzafa et al., 1987, 1991). After the enlargement of El Estacio channel to make a navigation channel and a marina in the early 1970s, the lagoon is under a process of slow but continuous colonization by marine species (Pe´rez-Ruzafa, 1989; Pe´rez-Ruzafa et al., 1991). Some changes were produced by coastal works for tourism facilities (land reclamation, the opening or deepening and extending channels, urban development and associated wastes, building sporting harbours, etc.). In 1986, the Spanish Ministry of Public Works initiated a plan for artificial beach creation in the lagoon. Sand from shallow areas close to the northern part of La Manga (the sandy barrier enclosing the Mar Menor) was pumped into the shallow areas in the west coast of the Mar Menor. The stability of new beaches was reinforced by the installation of rocky breakwaters perpendicular to the coast. The present study analyzes the observed changes in fish assemblage structure as a consequence of disturbance produced by the dredging and pumping of sand, and by the introduction of artificial rocky substrata to maintain the new beaches and for building marinas in the Mar Menor lagoon.

Fig. 1. Location of the Mar Menor lagoon and sampling stations. Continuous line indicates pumping area for creation of new beaches (P), dotted line delimits dredging zones for extracting sand (D). Localities T9, T10, T16, T17, T22 and T23 include breakwaters.

2. Material and methods 2.1. Study site The Mar Menor is a hypersaline coastal lagoon, with a surface area of 135 km2 located on the Southwestern Mediterranean coastline (37°42 0 0000 North—00°47 0 0000 West) (Fig. 1) with a mean depth of 3.6 m and maximum over 6 m. The salinity of the lagoon waters range from 42 and 46 psu. The bed sediment grain size composition is predominantly muddy and sandy; with some areas of natural rocky bottoms around islands and some calcareous and volcanic outcrops. Muddy bottoms cover both the whole central area of the lagoon and those shallow bottoms showing a lower hydrodynamism being, at the same time, covered by a dense meadow of the algae Caulerpa prolifera

A. Pe´rez-Ruzafa et al. / Marine Pollution Bulletin 53 (2006) 107–120

or patches of the sea grass Ruppia cirrhosa. Sandy bottoms (with sand content up to 89%) are located on the margins of the basin and in the small bays surrounding the islands in which scarce patches of the phanerogame Cymodocea nodosa grow. The organic carbon content in the sediments of the Mar Menor is highly variable, ranging from less than 0.5% at sandy bottoms up to 8.6% in the Caulerpa prolifera areas (Pe´rez-Ruzafa, 1989, 1996; Pe´rez-Ruzafa et al., 1989). The fish fauna of the Mar Menor has been well studied (Lozano, 1969; Ramos and Pe´rez-Ruzafa, 1985; Pe´rezRuzafa, 1989; Barcala, 1999) and consists of 73 species. The most abundant species in benthic assemblages are: Gobius cobitis, Lipophrys pavo and Trypterigion tripteronotus on shallow infralittoral rocks; Pomatoschistus microps, Callionymus pussillus, Callionymus risso, Solea vulgaris and Solea lascaris on sandy bottoms and Gobius niger, Syngnathus abaster and Hippocampus ramulosus on Cymodocea nodosa–Caulerpa prolifera mixed beds. 2.2. Sampling design Fish assemblages were sampled at 24 sites (Fig. 1) by diving using visual census along transects 50–100-m long

109

and 1-m wide (Table 1). Replicates were taken at the three main substratum types (sandy bottoms, Caulerpa prolifera– Cymodocea nodosa mixed beds on muddy bottoms, and photophilic communities on rocky bottoms). Between 1985 and 1989, soft bottoms were sampled comparing the situations before and after dredging and pumping which took place in 1986 in areas affected and in control sites (Fig. 1). For their part, natural rocky bottoms were surveyed from 1987 to 1989 to be compared with artificial hard substrata (jetties and dykes designed to retain the sediment) once in place (i.e. without considering the situation prior to construction). To characterize sedimentary changes due to the anthropogenic actions, samples were taken by divers before and after the execution of coastal works in both the dredging and pumping zones, as well as in bottoms covered by sand and by Caulerpa prolifera meadows unaffected by the actions. Samples were stored and transported in darkness and cold in polyurethane bags. At the laboratory they were dried at room temperature. During this process they were stirred to break lumps, after they were sieved through a 2 mm mesh and the grabs (>2 mm fraction) were weighted. Grain size distribution in the <2 mm fraction was

Table 1 Census performed to study the fish assemblage at different locations for different treatments Natural rocky bottoms T1-R T2C-R T2D-R T2E-R T3-R T4-R T5-R T7-R T8-R

Type of bottom Rock Rock Rock Rock Rock Rock Rock Rock Rock

Breakwaters T10B-RD T10C-RD T16-RD T17-RD T22-RD T23-RD T9A-RD T9B-RD T9C-RD

Pumping zone T12A-S T12B-S T13-M T13-S T14-M T14-S T17-M T18A-M T18A-S T18B-M

Sand Sand Caulerpa Sand Caulerpa Sand Caulerpa Caulerpa Sand Caulerpa

Dredging zone T15-S T19A-S T19B-S T19C-S T20-S T21-CH T21-M T21-S T24-S T9C-M

Soft bottoms (controls) T10A-M T11A-M T11A-S T11B-M T11B-S T11C-M T11C-S T11D-S T11E-S T11F-S

Caulerpa Caulerpa Sand Caulerpa Sand Caulerpa Sand Sand Sand Sand

meadow on mud meadow on mud meadow on mud meadow on mud meadow on mud meadow on sand meadow on mud meadow on mud meadow on mud

Soft bottoms (controls) T11G-S T11H-S T15A-M T15B-M T1-M T2A-M T2B-M T4-M T4-S T6-S

Type of bottom Rock Rock Rock Rock Rock Rock Rock Rock Rock DO DO DO DO DO DI DI DI DI DI

Sand Sand Sand Sand Sand Chaetomorpha linum Caulerpa meadow Sand Sand Caulerpa meadow Sand Sand Caulerpa Caulerpa Caulerpa Caulerpa Caulerpa Caulerpa Sand Sand

meadow meadow meadow meadow meadow meadow

on on on on on on

mud mud mud mud mud mud

Location of transects is determined by the first number (up to two digits) after T and is shows at Fig. 1. Letters after the location number indicates different sites in the same locality. Letters after the hyphen correspond to indication of the type of substrate or vegetation cover (R: rock; RD: rock/dykes; S: sand; M: Caulerpa meadow; CH: Chaetomorpha linum; DI: located inside a dredged hole; DO: located outside dredged holes).

A. Pe´rez-Ruzafa et al. / Marine Pollution Bulletin 53 (2006) 107–120

110

determined by the Boyoucos hydrometer method (Day, 1965; Soil Conservation Service, 1973) after dispersion of clusters by mechanical agitation in a sodium-hexametaphosphate and Na2CO3 solution. Prior to the analysis, salts were removed by washing and centrifugation and organic matter by hydrogen peroxide treatment. Grain size classification was made according to the International Association for Soil Science (Duchaufour, 1975). Organic carbon was determined by the Walkley–Black method (Buchanan, 1984) and total nitrogen by the Kjeldahl method (Bremner, 1965). 2.3. Analysis of data The changes to the sediment characteristic variables of organic carbon, total nitrogen, and proportion of each grain size class, were compared among sites covered or not by vegetation, before and after pumping and dredging activities, by means of two-way analyses of variance. In addition, the analysis compared changes occurring inside the holes caused by dredges and in the areas surrounding these holes. Furthermore, possible differences in depth and hydrodynamism among sites were tested using ANOVA. At each site, hydrodynamism (as represented by wave exposure) was estimated according to Keddy (1983) as follows: X Wave exposure ¼ ðmean wind velocity22:5  wind frequency22:5  effective fetch22:5 Þ where the effective fetch (Fe) is the direct fetch (F), or distance in kilometres along which the wind blows from each direction, corrected by fetches at directions less than 45° using the equation, F e ¼ ½F ðaÞ  cos a þ F ðaþ22:5Þ  cosða þ 22:5Þ þ F ða22:5Þ  cosða  22:5Þ=½cos a þ 2  cosða þ 22:5Þ where a is equal to 0 for each Fe calculated. The values of wave exposure obtained at each site were corrected for measured depth at this point and estimated wave length for each wind conditions, as the effect of waves on the bottom depends on these parameters (Bretschneider, 1964; Pond and Pickard, 1978; Pe´rez-Ruzafa, 1989). Fish density is expressed as number of individuals 100 m2. For each species, its relative abundance and frequency of occurrence were estimated, classifying them as very frequent (f P 70%), frequent (40% 6 f < 70%), common (15% 6 f < 40%) and occasional species (f < 15%). Fish assemblage structure was expressed at each sampling site according to species composition, species richness, abundance and Shannon–Wiener diversity HÕ index (Margalef, 1974). To explore the variation of fish assemblages throughout the lagoon, a correspondence analysis (CA) (ter Braak and Prentice, 1988) using transformed abundance [ln (x + 1)] was performed using the CANOCO v. 3.15 package (ter

Braak, 1990). The results of the ordination analysis are displayed in a biplot after scaling the axes by adjusting the speciesÕ scores to the speciesÕ variance: the resulting scores are correlations between species and eigenvectors. Rare species were downweighted following the procedure offered by CANOCO in order to prevent their excessive influence on the ordination. Average values of fish assemblage variables (abundance, species richness and H 0 diversity) and the log-transformed data of abundance of the most frequent species (f P 15%) were compared between natural and artificial hard substrata using ANOVA. The effect of pumping and dredging on the fish assemblage inhabiting soft bottoms (colonised or not by Caulerpa prolifera) was assessed using two-way analyses of variance on the observed values of assemblage variables, as well as of abundance of the most frequent species, considering the spatial factor ‘‘Type of action’’ (with three levels, i.e. pumping, dredging and control sites), and ‘‘Time’’ (before vs. after) (n = 5). Both factors have been considered to be fixed. Prior to analyses, homogeneity of variances were tested using CochranÕs test. A posteriori SNK procedure was used to identify those means that were significantly different. As with the sediment variables, the fish assemblage was distinguished between changes occurring inside the holes caused by dredges, and in the areas surrounding these holes. In addition, as an indication of temporal changes, observed values were represented graphically against time before and/or after the execution of coastal works. Polynomial least-square regression curves were fitted on the resulting points in an attempt to describe temporal trends. 3. Results 3.1. Characterization of environmental changes Both pumping and dredging areas showed changes in habitat characteristics as the result of the works. Both areas were originally shallow, with depths lesser than 1.5 m, and sandy, with no vegetation cover or with scarce patches of Cymodocea nodosa. At the deeper limit of both areas, at depths higher than 1.5 m, dense Caulerpa prolifera meadows started to extend. After pumping operations, a slow recovery of shallow areas by Caulerpa prolifera patches was observed, this being more rapid in dredging areas, where 50% of the holes were densely colonized by Caulerpa prolifera or Chaetomorpha linum (Pe´rez-Ruzafa et al., 1991). Table 2 shows the main characteristics of the sediments for natural sandy bottoms, and muddy bottoms under Caulerpa prolifera meadows—both acting as controls during the ANOVA, and in localities affected by pumping of sands and by dredging. Before the activities, both dredging and pumping areas showed typical sandy bottoms dominated by coarse and fine sand and with low content of silt and clay. Organic matter was lower than 0.5%. These

234.5 281.6 444.0 8504.5 15,029.5 9517.5 4133.5 3527.4 7000.9 3423.8 5271.6 2406.7 7.6 0.0

Thirty-eight fish species have been recorded in the present study (Table 3). Except A. boyeri, all species show benthic habits but the benthic fish assemblage living in the Mar Menor is not homogeneous. The correspondence analysis (Fig. 5) shows that fish assemblages are spatially organized according to the three main lagoon sediment types. The first two ordination axes, which explain 41.3% of total variance in data, position sampling units according to the nature of the substrata and vegetation cover. The rocky bottom data, for both natural and artificial areas, are situated in the negative part of the first axis. Sandy bottom data are situated at the positive part of the first axis, including controls, pumping and dredging zones with sandy bottoms all together. Finally, data from Caulerpa prolifera meadows cluster at the positive part of the second axis.

4.0 3.5

Before

0.6

After

0.5

3.0 2.5 2.0 1.5 1.0 0.5 0.0

Total Nitrogen (%)

Organic Carbon (%)

SE Mean

1070.3 921.5 1368.0 46,591.6 36,836.0 54,396.0 38,481.4 44,625.4 32,337.3 10,583.4 20,522.0 2853.4 449.6 22,107.0 0.4 0.5 0.8 0.1 0.2 0.2 0.2 0.1 0.3 0.3 0.2 0.3 0.4 0.0

SE Mean

3.5 3.5 3.4 0.8 0.9 0.7 0.7 0.5 0.9 2.2 1.2 3.0 3.4 1.1 2.0 2.7 2.8 4.1 9.4 0.3 1.6 0.5 2.5 1.6 0.9 2.4 3.9 0.5

SE Mean

19.7 20.7 17.9 8.4 13.0 4.8 5.2 1.7 8.6 7.0 3.4 9.8 12.9 1.8 1.9 2.9 0.9 2.6 5.7 0.5 1.6 0.5 2.8 1.1 0.4 1.8 2.7 0.2

SE Mean

15.0 14.1 17.0 3.4 7.0 0.5 4.0 1.2 6.9 4.1 2.2 5.6 7.5 2.7 0.8 1.1 0.3 1.0 2.3 0.2 0.7 0.2 1.2 0.5 0.2 0.8 1.1 0.2 6.2 5.7 7.1 1.3 2.7 0.2 1.6 0.4 2.9 1.6 0.9 2.2 3.2 1.0 4.5 6.6 3.8 3.3 5.4 4.3 4.7 7.5 5.2 3.1 5.9 3.5 2.8 2.1

SE Mean SE

similarities respond to comparable conditions of hydrodynamics (expressed as estimated wave exposure) and depth (Table 2) and low vegetation cover. On the other hand, muddy bottoms under dense Caulerpa prolifera meadows were dominated by fine sand and showed higher percentage of silt and clay. Organic carbon is higher than 3% (p < 0.01 for all analysed variables except for C/N relationship). Wave exposure is significantly lower because the effect of the greater depth. Several variables showed significant (p < 0.05) or marginally significant (p < 0.1) effect of the interaction action * before/after. Mean organic carbon content increased both in pumping and dredging areas after actuations, reaching values higher than 1.5% (Fig. 2). Coarse and fine silt also shows marginally significant variations in the time after, increasing at pumping and dredging areas (Fig. 3). Clays also increased in affected areas (p < 0.05) (Fig. 3). Wave exposure decreased significantly in pumping and dredging areas as a consequence of the building of breakwaters and the increase in depth inside holes, respectively. Comparison in the dredging zone among holes produced by dredging and surrounding areas (Fig. 4) shows that the main changes take place inside holes, values being significantly higher in the case of organic carbon content (p < 0.001) and in the percentage of clay (p < 0.05).

38.1 39.5 35.2 15.0 18.2 12.4 37.1 42.9 31.2 51.7 52.2 51.4 47.1 39.8

Mean SE

5.9 8.4 7.9 8.0 16.0 4.3 5.7 7.5 9.2 4.7 6.6 6.4 9.6 2.9 21.0 20.0 22.9 71.9 59.1 82.2 52.4 53.8 50.9 35.6 41.4 31.1 29.4 54.7

Mean SE

4.9 7.4 3.3 4.9 5.3 7.7 2.1 0.6 4.1 0.6 1.0 0.8 1.4 1.5 15.8 13.7 19.9 10.8 5.5 15.0 3.8 1.3 6.4 1.5 1.5 1.4 2.2 2.7

Mean SE Mean

18.1 22.5 9.1 5.2 4.2 6.0 5.6 4.8 6.6 8.3 5.3 10.6 10.6 5.3

SE

0.1 0.1 0.0 0.0 0.0 0.0 0.1 0.0 0.1 0.0 0.0 0.0 0.1 0.0 0.2 0.3 0.1 0.0 0.0 0.0 0.5 0.0 1.0 0.3 0.1 0.5 0.8 0.1

0.4 0.4 0.3 0.0 0.0 0.0 0.1 0.0 0.3 0.1 0.1 0.1 0.2 0.1

Mean Mean

3.1 3.2 3.1 0.2 0.2 0.2 1.0 0.1 1.8 1.0 0.3 1.6 2.0 0.3 Caulerpa meadows Before After Sandy bottoms Before After Pumping area Before After Dredging area Before After Inside holes Outside holes

SE

C/N

9.0 13.5 1.4 0.7 0.7 0.9 0.7 0.4 1.4 1.1 1.1 1.2 1.3 2.0

Hydrodynamism Depth (m) Clay (%) Fine silt (%) Coarse silt (%) Fine sand (%) Coarse sand (%) Grabs (%)

111

3.2. Fish assemblage

Total nitrogen (%) Organic carbon (%)

Table 2 Mean and mean standard error (SE) of sediment variables at each treatment (pumping areas, dredging zones and controls) with indication of mean depth and wave exposure (see text for calculation methodology)

A. Pe´rez-Ruzafa et al. / Marine Pollution Bulletin 53 (2006) 107–120

Before After

0.4 0.3 0.2 0.1 0.0

CM

CS

P

D

CM

CS

P

D

Fig. 2. Organic carbon and total nitrogen content of sediments in control areas in Caulerpa meadows (CM), sandy bottoms (CS), pumping zone (P) and dredging areas (D), before and after the engineering works.

A. Pe´rez-Ruzafa et al. / Marine Pollution Bulletin 53 (2006) 107–120 8.0

Before

7.0

After

4

Organic Carbon (%)

Coarse Silt (%)

112

6.0 5.0 4.0 3.0 2.0 1.0 0.0

CS

20 18 16 14 12 10 8 6 4 2 0

P

1

D

Before

CM

CS

DI

DO

CM

CS

DI

DO

CM

CS

DI

DO

0.5

Total Nitrogen (%)

Fine Silt (%)

2

0

CM

After

0.4 0.3 0.2 0.1 0.0

CM

CS

P

D 25

25

Before After

20

Clay (%)

20

Clay (%)

3

15 10

15 10 5

5

0

0

CM

CS

P

D

Fig. 3. Grain-size content of sediments in control areas in Caulerpa meadows (CM), sandy bottoms (CS), pumping zone (P) and dredging areas (D), before and after the engineering works.

Fig. 4. Organic carbon, total nitrogen and clay content of sediments in control areas in Caulerpa meadows (CM) and sandy bottoms (CS) and in dredging areas inside holes (DI) and surrounding areas (DO), after the engineering works.

This group include controls and pumping and dredging zones census covered by Caulerpa meadows or by Chaetomorpha linum, both after dredging/pumping. The only exception is the data from the census T10-M (see Table 1) characterized by being covered with low density Caulerpa prolifera meadow on sand instead of mud and clustered with sand assemblages. Natural rocky bottom assemblages were characterized by the presence of a very frequent species, Gobius cobitis, representing 43% of total abundance, the frequent species Lipophrys pavo (27% of total abundance) and seven common species (Syngnathus abaster, Lipophrys dalmatinus, Tripterygion tripteronotus, Tripterygion melanurus, Hippocampus ramulosus, Gobius niger and Symphodus (Crenilabrus) cinereus). Eight species—Anguilla anguilla, Sparus

aurata, Diplodus vulgaris, Lithognathus mormyrus, Gobius paganellus, Lipophrys canevai, Mugillidae spp., and Atherina boyeri- were occasional species. On artificial rocky bottoms, Gobius cobitis and Lipophrys pavo were very frequent and Gobius paganellus, Gobius buchichi, Tripterygion tripteronotus and Parablennius sanguinolentus became frequent species. On sandy bottoms the dominant species was Pomatoschistus marmoratus, with 100% of frequency of occurrence and 83% of abundance. For their part, Callionymus risso, Callionymus pusillus, Syngnathus abaster and Hippocampus ramulosus were frequent species, while Solea vulgaris and mugillids were common. Finally, Gobius niger and Syngnathus abaster were very frequent species in Caulerpa prolifera beds. The former represented 49% of the total abundance and the latter 13%. Hippocampus

Table 3 Mean abundance (individual 100 m2), mean standard error (SE) and relative abundance (RA) of fish species, total mean abundance, species richness and diversity at the three different communities found in the Mar Menor and in artificial rocky bottoms, pumping areas (before and after actuations) and dredging zones (before and after actuations) Rocky bottoms Natural Mean

SE

RA

AANG

0.1

0.1

0.2

SABA STYP NOPH HRAM

1.0

0.6

2.0

0.5

0.3

1.0

SSCR

Caulerpa meadows

Pumping areas

Controls

Controls

Before

Mean

Mean

SE

RA

0.1

0.1

0.1

0.8

1.1

SE

0.8

0.04

0.04

0.1

0.1

1.3 1.4

1.3 1.4

CCHR

0.02

0.02

LMER LVIR SROI STIN SCIN

0.02 0.02 0.04 0.2

0.02 0.02 0.04 0.2

SAUR DVUL LMOR OMEL SSAL

GNIG GATE GBUC GCOB GPAG PMAR MMAC

1.8 0.1 0.1

1.8 0.1 0.1

3.6 0.2 0.2

0.2

0.1

0.5

0.4

0.3

0.9

20.9 2.0

10.0 2.0

42.9 4.1

0.01 3.9 22.4 6.2

ASPH LCAN LDAL LPAV PSAN CARG

0.1 1.1 13.3

0.1 0.6 12.3

0.2 2.3 27.2

0.02 0.1 0.3 81.8 2.3

SE

RA

Mean

0.4

2.0 0.2

0.7 0.2

12.8 1.3

1.2

1.2

0.2

0.2

0.05

0.3

0.7

0.3

4.4

0.2 1.4

0.2 0.9

0.4

0.4

0.8

2.2

0.2

0.1

1.0

0.2

0.2

7.5 0.1

5.9 0.1

48.5 0.6

3.8

1.0

7.5

0.01 0.1 4.0 0.02

0.01 0.1 4.0 0.02

0.1 0.8 26.2 0.1

44.4

21.5

93.9

0.01

0.01

0.1

0.01

0.02 0.1 0.2 23.2 1.0

28.8

4.6

82.8

0.2

0.1

0.6

0.2

0.1

0.5

0.5

0.4

3.2

0.03

0.02

0.2

0.2

SE

Mean

Before

Mean

2.3 7.0 2.9

CPUS CRET CRIS

Dredging areas After SE

Mean

After SE

Mean

SE

7.6

7.4

6.9

4.1

3.9

67.0

60.2

69.8

48.7

28.3

305.6

162.5

0.1

0.1

A. Pe´rez-Ruzafa et al. / Marine Pollution Bulletin 53 (2006) 107–120

Anguillidae Anguilla anguilla Syngnathidae Syngnathus abaster Syngnathus typhle Nerophis ophidion Hippocampus ramulosus Serranidae Serranus scriba Sparidae Sparus aurata Diplodus vulgaris Lithognathus mormyrus Oblada melanura Sarpa salpa Pomacentridae Chromis chromis Labridae Labrus merula Labrus viridis Symphodus (Crenilabrus) roissali Symphodus (Crenilabrus) tinca Symphodus (Crenilabrus) cinereus Gobiidae Gobius niger Gobius ater Gobius bucchichi Gobius cobitis Gobius paganellus Pomatoschistus marmoratus Millerigobius macrocephalus Callionymidae Callionymus pusillus Callionymus reticulatus Callionymus risso Blenniidae Aidablennius sphynx Lipophrys canevai Lipophrys dalmatinus Lipophrys pavo Parablennius sanguinolentus Clinidae Clinitrachus argentatus

Sandy bottoms Artificial

0.2

113

(continued on next page)

0.2 0.00 1.0 0.00 4.0 1.0 0.2 0.2 1.4 0.4

63.7 70.2 101.9 21.7 51.4

4.1 1.1

6.9 130.4

0.7 0.2 3.5 0.4 1.7 0.3 Richness Diversity (bits individual1)

Bold figures indicate the dominant species at each community.

0.7 0.2 4.2 1.4

438 Total abundance (individual 100 m )

SVUL

Tripterygiidae Tripterygion melanurus Tripterygion tripteronotus Mugilidae Mugilidae spp. Atherinidae Atherina (Hepsetia) boyeri Scorpaenidae Scorpaena porcus Soleidae Solea vulgaris

Table 3 (continued)

2

SPOR

5.0 ABOY

5.0

22.6

10.2

5.4 1.4

19.6

32.2

0.2 0.3

4.9

0.9

15.3

0.9 0.3

0.1 0.02 0.02

0.4 0.03 0.1 6.3 1.2 2.2

6.0 1.4 2.1 0.1 0.1 0.5 0.2 MSPP

0.2

0.9 3.5 0.9 8.2 2.3 1.6 1.1 0.8 TMEL TTRY

0.8 0.5

0.5 0.2

372.6 36.3

3.1 3.1

SE Mean SE Mean RA SE Mean RA SE

RA

SE

Mean

SE Mean Mean

3.3. Effect of pumping and dredging on fish assemblage

3.0 0.8

148.0

SE Mean Mean

SE

After Before

Dredging areas

After Pumping areas

Before Controls Natural

Caulerpa meadows Sandy bottoms

Controls Artificial

Rocky bottoms

ramulosus, Symphodus cinereus, Lipophrys pavo and Atherina boyeri were also considered to be frequent species.

1.2 0.00

A. Pe´rez-Ruzafa et al. / Marine Pollution Bulletin 53 (2006) 107–120

114

In general, total abundance and abundance of the most frequent species were higher in dredging areas, and, to lesser extent, in pumping areas, compared with the controls (Fig. 6), but these differences were not statistically significant. Species richness (Fig. 6) and diversity decreased after the works in all sampling areas, including the control sites. Only 4 out of 14 fish species (those with a frequency of occurrence higher than 15%) have been tested for differences in abundance (Fig. 6). Among these, S. abaster showed much higher abundance in the situation ‘‘before’’; in fact it did not appear in the situation ‘‘after’’ neither in pumping or in control areas, despite showing the higher values in the dredging before works commenced. In the case of H. ramulosus, its abundance decreased in the pumping area after works occurred, while increasing in the controls (it did not appear at the dredging sites). G. niger increased in abundance after operations in dredging areas, although it appeared not to be statistically significant owing to the high variability of the data. Finally, no significant effects were detected for the abundance of P. marmoratus, although it shows higher abundance in the dredging than in pumping or control areas (in both before and after situations) but decreasing after works. The analysis of the dredging zone data comparing the inside of the holes with the surrounding areas and separating the controls as sandy assemblages and Caulerpa prolifera meadows shows clearer results (Fig. 7). Both the inside of holes and surrounding affected areas shows significant higher total abundance than controls after works were carried out. Conversely, species richness and diversity reached comparable and higher values, respectively, in the outer areas of the dredging zone after works than in controls, whereas much lower values were encountered inside the holes. The temporal assessment of assemblage variables of originally sandy bottoms in pumping and dredging zones, (Fig. 8), shows that abundance increased just after perturbation and then progressively recovered to the prior values with time. Species richness decreased in the first moments, but recovered after several months. Diversity showed a more complex behaviour, with an initial decrease followed by an increase and then decrease. 3.4. Changes in fish inhabiting hard substrata A comparison of artificial rocky bottoms of breakwaters with natural ones in the lagoon shows significant differences in total abundance (p < 0.01), this variable reaching 130 individuals 100 m2 at breakwaters against 40 individuals 100 m2 at natural rocky bottoms (Fig. 9). This increase is mainly due to the blenniid Lipophrys pavo which

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115

Fig. 5. Ordination of samples (A) and species (B) in the biplot representations of the first axes of the Correspondence Analyses performed on fish abundance in visual censuses. Key of abbreviations for samples and species are showed in Tables 1 and 3, respectively.

reached densities of 82 individuals 100 m2 in the breakwaters. Some other species as Gobius buchichi and Parablennius sanguinolentus were only present at breakwaters near the El Estacio Channel (T9 and T10), probably as a consequence of the stronger Mediterranean influence in this area, as they were absent in the rest of the lagoon. Other species as Tripterygion tripteronotus or Gobius paganellus

showed also higher abundance at breakwaters, but this difference is only marginally statistically significant. Gobius cobitis, the dominant species in natural rocky bottoms, maintained the same densities (22.4 vs. 20.9) on breakwaters and natural substrata. No significant differences are detected for species richness or diversity among artificial and natural rocky bottoms.

A. Pe´rez-Ruzafa et al. / Marine Pollution Bulletin 53 (2006) 107–120

116

6 4 2

400 300 200 100

0

Abundance

2

1

0

Number of species

0

H. ramulosus

Species richness 4 3 2 1 0

Pumping

160

Abundance

Total abundance

500

S. abaster

Abundance

Abundance

8

Dredging Control

G. niger 120 80 40

Abundance

0

400

P. marmoratus

300 200 100 0

Pumping Dredging

Control

Fig. 6. ANOVA results for fish assemblages considering factors time (before/after: white/black columns, respectively) and pumping/dredging/control. Error bars correspond to mean standard error.

Colonization of breakwaters takes place in the first months after the installation of artificial substrata (Fig. 10). Abundance remains constant through time, but species richness and diversity tend to increase with years, exponentially in the first case, and showing a logarithmic trend, i.e. tending to an asymptote, in the case of diversity. 4. Discussion At present 73 species of fishes have been reported for the Mar Menor (Lozano, 1969; Ramos and Pe´rez-Ruzafa, 1985; Pe´rez-Ruzafa, 1989; Barcala, 1999), from which 38 (54%) species have been taken in the present study. Moreover six species of Mugillids have been previously reported in the lagoon but here have been grouped because the difficulty to be identified by visual surveys. Most of the species previously observed but not found in this study correspond to pelagic species (Sardina pilchardus, Engraulis encrasicholus, Belone belone), marine straggler species (Conger conger, Epinephelus guaza, Lichia amia, Seriola dumerilii, Argyrosomus regius, Trigla lucerna, Aspitrigla cuculus, etc.), or

marine migrants (Dicentrarchus labrax, Mullus barbatus), or they are species being occasionally reported close to the channels of communication with the Mediterranean (as is the case for Gobius cruentatus). The fish fauna of the Mar Menor corresponds to other Mediterranean coastal lagoons at the specific level (e.g. Casabianca and Kiener, 1969; Paris and Quignard, 1971; Herve´ and Brusle, 1980, 1981; Mariani, 2001) and with lagoons from other latitudes at generic or family level, as Gobiidae, Blenniidae, Mugillidae or Sparidae are the main families constituting the fish assemblages. However, the Mar Menor tends to show higher species richness. Several factors are likely to determine this high biodiversity, such as its size, substratum diversity, environmental heterogeneity, and its degree of communication with the open sea. At present, after the enlargement of El Estacio channel in the early 1970s, the Mar Menor is under a process of slow but continuous colonization by marine species (Pe´rez-Ruzafa, 1989; Pe´rezRuzafa et al., 1991). This effect is greater at the mouth, as well as in areas situated close to the communication channels, in agreement with the confinement theory of

A. Pe´rez-Ruzafa et al. / Marine Pollution Bulletin 53 (2006) 107–120

Abundance (indiv. * 100 m-2)

Abundance

600

400

200

0 CM CS

DI

117

y = 1.1x3 -17.1x 2 + 18.8x + 318 2 R = 0.3

1200 1000 800 600 400 200

DO

0 -5

0

6

5

10

15

Time (months)

4

y = 0.02x2 - 0.3x + 2.1

6

2

3

R = 0.4

2 1 0

CM

CS

DI

DO

1.2

Richness (# species)

Richness

5

5 4 3 2 1

1.0 -5

0

5

10

15

Time (months)

0.6 0.4 0.2

1.8

0.0

1.6

CM

CS

DI

DO

Fig. 7. Total abundance, species richness and diversity of fish assemblages in control areas in Caulerpa meadows (CM) and sandy bottoms (CS) and in dredging areas inside holes (DI) and surrounding areas (DO), after the engineering works.

Gue´lorget and Perthuisot (1983) as stated by Pe´rez-Ruzafa and Marcos (1992, 1993), and as used by Mariani (2001) to explain spatial distribution of fishes in two Mediterranean coastal lagoons. Despite the above conclusions, the results here show that lagoon benthic fish assemblages are not homogenous. Therefore, they do not constitute a unique community characterized by the ‘‘paralic’’ domain sensu Gue´lorget and Perthuisot (1983) and Mariani (2001). Lagoon or paralic species organize themselves into distinct lagoon communities depending on the nature of the substratum and vegetation cover, as with the marine environment. The confinement would have an additional effect on the fish assemblage, superimposed on that of habitat characteristics, rather than determining it as a unique factor. ANOVA did not detect statistical significant effects of dredging and pumping operations compared to control

Diversity (bits* indiv.-1)

Diversity

0

0.8

y = -0.002x3 + 0.03x2 - 0.1x + 0.3 2

R = 0.3

1.4 1.2 1.0 0.8 0.6 0.4 0.2 0.0 -0.2 -5

0

5

10

15

Time (months)

Fig. 8. Temporal succession of abundance, species richness and diversity of previously sandy bottoms in areas affected by pumping or dredging of sand at the Mar Menor lagoon.

zones. This lack of discrimination is likely to be due to the fact that in the initial sampling design no distinction was made among sandy bottoms and Caulerpa prolifera communities. Hence the effect of a progressive transformation of sandy bottoms to muddy bottoms with higher contents of organic matter and covered by Caulerpa meadows is disguised by the inclusion of Caulerpa beds in the control areas. The increase in abundance of Gobius niger (the

118

A. Pe´rez-Ruzafa et al. / Marine Pollution Bulletin 53 (2006) 107–120

Fig. 9. Total abundance and abundance of significant species in rocky fish assemblages comparing natural bottoms and breakwaters (**p < 0.05; *p < 0.16).

dominant species in Caulerpa meadows) and the decrease of Pomatoschistus marmoratus (the dominant species in sandy bottoms) observed in dredging areas after the works can be interpreted in this sense of responses to complex changes in vegetation cover and sediment characteristics. In effect, increasing stress caused by sediment re-suspension in dredging and pumping areas can boost the primary production in microphytobenthos (Pe´rez-Ruzafa et al., 1991). This effect, added to a decrease in hydrodynamism and, in the case of dredging holes, the increase in depth, favours the accumulation of organic matter and fine particles and the colonization of the opportunistic algal species Caulerpa prolifera. The stress caused by dredging and pumping leads to similar consequences on substratum characteristics and fish assemblages in areas affected by both activities. These responses can be interpreted against a framework of a general response to perturbations. Stress may increase fish abundance, in a first step, by increasing productivity or the availability of food in the sediment and/or substituting K-strategist species by opportunistic ones. Species richness and diversity decrease strongly in greatly affected areas (inside the holes) but tend to increase under moderate perturbations (probably the situation in pumping areas and surrounding spaces of dredging zone) after the first impact, according to the intermediate disturbance hypothesis (Connell, 1978). Finally, the colonization by Caulerpa prolifera meadows leads to a large change in the fish assemblage by substituting the characteristic community of sandy bottoms, dominated by Pomatoschistus marmoratus by a community dominated by Gobius niger. It appears evident that a confounding effect of a purely spatial factor derives from the sampling design (‘‘peudo-replication’’ sensu Hurlbert, 1984), as we have only one dredging and one pumping

zone: no replication of the factor ‘‘type of action’’ is possible. Therefore, environmental factors other than the effects of pumping and/or dredging could be acting to determine the observed differences between areas. The introduction of artificial rocky substrata leads to a process of colonization similar to that observed on artificial reefs (e.g. Bayle et al., 1994). The community at breakwaters is similar to those living on natural rocky bottoms in the lagoon, both in terms of species composition and assemblage structure. The observed increase in abundance, although in most cases not significant, occurs in nearly all the species and can be attributed to the higher availability of holes and crevices offered by artificial structures compared to natural rocky bottoms. Breakwaters at the Mar Menor are built with rocky blocks of about 1–2 m of diameter and this size class have been found to be the most relevant to explain abundance of fishes in the Mediterranean (Garcı´a-Charton and Pe´rez-Ruzafa, 1999, 2001). The fact that Gobius cobitis maintained its densities can be explained by its territorial behaviour which can be a limiting factor of its population density. The present study shows that colonization takes place in a few months after the installation of artificial substrata, although the arrival of new species and the process of assemblage structuring can continue throughout the years. Abundance remains constant through time, whereas species richness and diversity tend to increase with years, exponentially in the first case and logarithmic, tending to an asymptote, in the case of diversity as shown by the data here. This can be explained because, as stated before, since the opening of El Estacio channel in the early 1970s the lagoon is under a process of continuous colonization by new species (Pe´rez-Ruzafa, 1989; Pe´rez-Ruzafa et al., 1991).

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Abundance (indiv. 100 m-2)

300 250 200 150 100 50 0 0

5

10

15

20

119

could be considered, by itself, a way to increase the environmental diversity in coastal lagoons. However, sandy bottoms tend to be substituted by muddy ones as a consequence of processes of sedimentation caused by the presence of jetties, dykes, breakwaters and other defence works. Hence, the suitability of installing breakwaters or other artificial rocky substrata, their effect on hydrodynamics and, as a result, on sedimentation rates and bottom characteristics in their area of influence should be taken into account during the planning stage or the environmental impact assessment.

Time (years) 20 Richness (# species)

18

References

0.11x

y = 2.01e R2 = 0.73

16 14 12 10 8 6 4 2 0 0

5

10

15

20

15

20

Time (years)

Diversity (bits indiv.-1)

3

y = 0.50Ln(x) + 0.86 2 R = 0.81

2.5 2 1.5 1 0.5 0 0

5

10 Time (years)

Fig. 10. Temporal succession of abundance, species richness and diversity of fish assemblage at artificial rocky substrata used for stabilization of beaches and the construction of sportive harbours at the Mar Menor lagoon.

In summary, in terms of ecosystem damage, pumping and dredging of sands cause a real stress leading to the substitution of typical sandy bottoms communities by Caulerpa prolifera communities. Therefore, pumping and dredging works accelerate the process of sandy-bottom destruction; with the subsequent loss of environmental diversity. For its part, artificial hard substrates could be considered, under certain conditions, as positive, because they add species richness and biological diversity to the original fish assemblage, as in coastal lagoons rocky bottoms are very scarce, even nonexistent in most of the lagoons. In this sense, the moderate introduction of rocky bottoms

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