239
JournalofAquaticEcosystemHealth 5: 239-253, 1996. © 1996Kluwer Academic Publishers. Printed in the Netherlands.
Detection of environmental impacts by bottom trawling on Posidonia oceanica (L.) Delile meadows: sensitivity of fish and macroinvertebrate communities P. Sfinchez-Jerez & A. A. Ramos Esplfi Dept. Ciencias Ambientales y Recursos Naturales, Universidad de Alicante, Ap.C. 99, 03080 Alicante, Spain Email:
[email protected]
Received6 December1995;acceptedin finalform 11 July 1996 Key words: benthos, community structure, seagrass, habitat degradation, Mediterranean Sea
Abstract
Along the Mediterranean coast, Posidonia oceanica (L.) Delile meadows have a great ecological and economical importance. However, there is a general regression of these meadows due to human activities such as illegal bottom trawling, may be affecting to overall ecosystem health. We examined changes in the community structure of mobile fauna associated with P. oceanica meadows at different spatial scales and taxonomic levels. The aim of this paper was to identify the most efficient taxonomic level to use in environmental impact studies of bottom trawling. At the macroscale level (10 to 100 m), there were significant differences between sites in the densities of some fish species and also the total fish assemblage structure, at both family and species taxonomical levels. At the microscale (0.1 to 1 m), some species of amphipods and isopods showed significant differences in their population densities. In the overall analysis of community structure, the coarse taxonomical levels, such as phyla and class, did not show significant differences, however amphipods and isopods showed significant differences at family and species levels. From these results, both study scales are required to detect changes on Posidonia meadows' fauna. Monitoring of some fish species such as Diplodus annularis (Linnaeus, 1758) and the overall fish assemblage as well as the structure of the amphipod and isopod communities appears to be the most efficient tool in the assessment of environmental impacts by bottom trawling on P. oceanica meadows. 1. Introduction
Posidonia oceanica (L.) Delile is an endemic seagrass species on infralittoral bottoms of the Mediterranean Sea. It forms extensive meadows which support a large number of fishes and invertebrates by increasing habitat complexity and diversity in relation to surrounding unvegetated substrates (Bell & Harmelin-Vivien, 1982; Virnstein et al., 1983; Heck et al., 1989; GarcfaRaso, 1990; Gambi et al., 1992; Curras et al., 1993). Changes in the seagrass biomass (Ansari et al., 1991), foliar surface (Stoner, 1980, Lewis, 1984), density (Heck & Thoman, 1981; Bell & Westoby, 1986; Worthington et al., 1992), cover, physical structure, phenology (Hargeby, 1990) and detritus accumulated (Everret & Ruiz, 1993) all affect the quality of the
habitat for these fauna (Stoner, 1980) and predation rates (Heck & Thoman, 1981) within the community (Orth, 1992). Because of its ecology and economic importance, protection of P. oceanica meadows has been proposed (Boudouresque et al., 1991). It is already a protected species in France and in some regions of the Spanish Mediterranean coast. In spite of this, P. oceanica meadows in the Mediterranean have been decreasing steadily (Ptr~s, 1984). In addition to natural processes, anthropogenic actions are likely to have an influence on this decline (Ptr~s & Picard, 1975). The most important of these stems from the establishment of urban and industrial areas in the littoral zone (Bourcier, 1982), from construction of harbours and artificial beaches
240
tO.o Mediterranean Sea
10 2 0
ImpactSite/,
...,I,,, ""' ~,
l/f
40
5/
\ C:ntrolSit~?~"
\
Figure 1. Geographiclocalizationof sample sites.
(Ruiz et al., 1993), and from bottom trawling fisheries (Ardizzone & Pelusi, 1984). Effects of trawling on epibenthic habitats have received less attention than the other perturbations described above. Large numbers of trawlers usually work illegally over P. oceanica meadows in the southwest Mediterranean littoral zone, causing physical degradation with the trawling gear (S~chez Lizaso et al., 1990). One of the most important consequences of these activities maybe the long-term change in the benthic ecosystem (Jones, 1992). The effects of this perturbation on the P. oceanica seagrass meadow structure and their relationship with the faunaseagrass associated assemblage are currently poorly understoods and could have an important effect on ecosystem health. The aim of this paper was to identify the most efficient taxonomic level to use in environmental impact studies of bottom trawling. We explore methodology to identify the effects of bottom trawling on the P. oceanica ecosystem by examining perturbation effects
on the faunal assemblage at different spatial scales and taxonomic levels. Marine benthic organisms and communities have been used as a tool for monitoring environmental health, due to their relative lack of mobility and their trophic position (Smith et al., 1988). Moreover, in this kind of study, it is important to consider that the perception of "scale" is entrenched in our perception of the problems and the project's goals and we must also deal with the functional scales at which the organisms are likely to respond to their environment (Wiens, 1989; Andrew & Mapstone, 1987). We selected two spatial scales: macroscale - tens to hundreds of meters - and microscale - centimetres to meters - (Romero, 1985) in relationship to two different components of the meadow's biota, fish and mobile macroinvertebrates respectively. Selection of the taxonomic level to which individuals are identified could affect the results of a study (Sale & Guy, 1992; Warwick & Clarke, 1993). Moreover, it is only necessary to identify organisms to a
241 taxonomic level that is sufficient to meet the objectives of any study (Warwick, 1993). To detect changes, we examined populations and community structure at various taxonomic levels: phyla, classes, families and species. Also, some physical features of the meadow were examined to determine which were the most important changes wrought by bottom trawling in the study site. Within any ecosystem however, some organisms or communities may respond differently to perturbations, making them more or less appropriate for study. On a macroscale, we examined changes in fish community structure because many species exhibit site fidelity, their taxonomy is relatively straightforward (Warwick, 1993), quantitative evaluation of the population is possible (Shepherd, 1992) and a characteristic assemblage exists in these meadows (Bell & Harmelin Vivien, 1982). On a microscale, we examined changes in the invertebrate assemblage because they may be influenced by different features of the meadow and a change in this structure may result in a modification of the meadow's trophic levels organization (Mazella et al., 1992).
The two sites, about 2000 m 2 each, were located 6 km apart at the same depth (16 m). One site was affected by illegal trawling and the other was used as a control. The site selection was supported in the number of loose rhizomes on the bottom and the existence of gear erosion (long bands around 40 cm wide of dead meadow). Control site did not show any signs of erosion. We selected these places because they were environmentally alike (similar soft sediments, depth and oceanographic conditions), in an attempt to reduce sources of natural variation. It was impossible to find other close sites with similar natural conditions to use as control replicates because additional untrawled meadows could be found only on rocky or/and shallow bottoms. These factors could affect fauna assemblage and interfere with the interpretation of the results. No other environmental impacts were observed in either area. Since completion of this work, the meadow is now protected by an extensive antitrawling artificial reef (Ramos et al., 1993). Sampling was conducted during the summer of 1992 (July to September). The water temperature was constant during the period, with an average of 19.5°C in the surface and 17.31 °C at the bottom with a constant thermocline at 12 m depth.
2. Study site 3. Materials and methods This study was conducted on the P. oceanica meadow of El Campello (Alicante, SE Spain) (Figure 1), which has been modified by bottom trawling into a gradient of habitats ranging from relatively pristine, to completely degraded areas where the meadow is practically extinct. Seagrass in this meadow grows in almost all the infralittoral soft bottoms between 8 and 23 m in depth. Shoreward of the meadow, in shallow water, there are rocky reefs and patchy seagrass meadows of Cymodocea nodosa. In deep bottom areas detrital and Peysonnelia spp algal communities are found. It is estimated that 40 per cent of Posidonia meadows in E1 Campello are degraded by bottom trawling (S~lnchez Lizaso et al., 1990). Nearly 200 trawlers fish around the study site and it is a common practice to trawl in shallow bottoms, over seagrass meadow usually operating under cover of darkness, though it is illegal. It is very difficult to evaluate or predict this illegal activity because fishing depends on the weather, deep bottom species catch, market prices, etc. In the study area, fishing effort on Posidonia meadows could range between one cast (about three hours trawling) per day to one cast per month, making a spatial gradient of habitat degradation.
Table 1 shows a resume of the different scale and taxonomic levels considered in the study and the mathematical analyses that have been used. 3.1. Control of changes in the P. oceanica meadow's characteristics Shoot density (number of shoots per m 2 of meadow) was counted in eight quadrats of 0.125 m 2 each randomly selected. Meadow cover was estimated by measuring the quantity of substrate (meters) where the seagrass is growing along eight line transects of 100m (Ruiz et al., 1993; S ~ c h e z Lizaso, 1993). The meadow's overall density (number of shoots per m 2 of substrate) was calculated by using the data from density and cover (overal density = density/cover x 100; Romero, 1985). To measure the foliar biomass, foliar area and epiphytic biomass, 30 rhizomes were collected from each site by scuba diving (Giraud, 1977). Foliar and epiphytic biomass were measured after 48 h in a desiccator set at 70 °C (Francour, 1990). Vegetal detritus was taken from the invertebrate samples, by sorting fine (1 to 8 mm) and coarse (>
242 Table 1. Different scales and variables considered in this study P. oceanica
meadow features
Phyla, Classes and Population level
Community level
Macroscale
global density meadow
fish
fish
Microscale
density, detritus
macroinvertebrates (phyla, class, species)
Decapoda, Mysidacea Amphipoda, Isopoda
Analysis
univariate ANOVA
univariate ANOVA
ANOSIM, SIMPER species richness, diversity
8 mm) fractions and rhizomal fragments, drying in a desiccator for 24 h at 80°C (Romero et al., 1992) and weighing. The distance between the meristem and the sediment level was measured as an estimate of the rhizome growth rate (n ~ 50). 3.2. Fish community We chose a visual count technique for the evaluation of the fish assemblage by scuba diving (HarmelinVivien et al., 1985) because it is a non-destructive and more quantitative method than experimental beamtrawl (Ody, 1987) and is better for sampling sparids and labrids (Harmelin-Vivien & Francour, 1992), families very important in the P. oceanica meadow (Bell & Harmelin-Vivien, 1982). All observed fishes were recorded and their sizes estimated along eight transects of 150 m x 5 m (750 m 2 6000 m 2 in total), randomly located within each study site. Each transect was replicated two times to estimate the short term variation (2 x 750m2). Mean density of each fish species and family was calculated per 250 m 2. 3.3. Invertebrate community The samples were taken by an air suction pump (Kennelly & Underwood, 1985). A surface of 0.125 m 2 (using a box of 50 x 25 x 25 cm we attempted to preclude the escape of most mobile species) was suctioned continuously for five minutes, collecting the invertebrates among the leaves and rhizomes (Vadon, 1981; Francour, 1990), as well as the vegetal detritus, (5 cm depth in the bottom) accumulating the sample in a one millimetre mesh bag. This mesh size was chosen to retain animals within the definition of macrofauna expressed by Vitelo & Dinet (1979) and Rumorh (1990) i.e. the fauna bigger than 1 mm. The size of the bag was, big enough to contain the sample (60
x 20 cm), avoiding saturation. A total of 12 samples (1.5 m 2 in total) was collected randomly from each study site. The main taxa were sorted, counting all individual molluscs (Gastropoda and Bivalvia), annelids (Polychaeta), echinoderms (Holothuroidea, Echinoidea, Asteroidea and Ophiuroidea) and arthropods (Crustacea and Pycnogonida). Because crustaceans formed one of the most important groups, with a great number of species having different life history and ecological requirements, they were identified to species level and their density was calculated to individuals per m 2. The most important groups of crustaceans were Decapoda, Amphipoda, Isopoda and Mysidacea.
3.4. Mathematical analyses The general model attempted to assess that changes in P. oceanica meadow should induce differences in abundance of fishes and macroinvertebrates at different scales of study. We used a one-way ANOVA (a = 0.05) to test the null hypotheses that no differences existed in seagrass features, meadow characteristics and abundances of fish populations and invertebrate between the two study sites. We tested for homogeneity variances with a Cochran's test and used a logarithmic transformation of the data to obtain a normal distribution and better homogeneity of variance (Underwood, 1981). Species richness and diversity (Shannon-Weaver index) were calculated for the different groups of fishes and macroinvertebrates. Diversity values between sites were tested using a t-test (Magurran, 1991). An "analysis of similarities" test (ANOSIM) was used to find out differences between the study sites, taking into account the entire community structure, at the different spatial scales and levels of taxonomic study. This test is based on a non-parametric multivariate
243 Table 2. Mean(+ SD) of fish abundance (number ind. per 250 m2). Results of ANOVA between the study places: d.f. = 1-14, * =p < 0.05, ** =p < 0,01. Total sampling effort of 1200 m2 Species
Impact
Control
MS
ERROR
Sparidae Dentex dentex (Linnaeus, 1758) Diplodus annularis (Linnaeus, 1758) D. vulgaris (E. Geoffrey Saint-Hilaire, 1817)
0.02 4- 0.02 3.15 4- 0.37
0 1.61 4- 0.21
0.001 0,770**
0.001 0.074
Sarpa salpa (Linnaeus, 1758) spondylosoma cantharus (Linnaeus, 1758)
0.37 + 0.09 0.02 4- 0.02 0
0.26 + 0.14 0.10 ± 0.08 0.02 4- 0.02
0,039 0,016 0.001
0.057 0.018 0.001
Pagellus acarne (Risso, 1826)
5.52 4- 3.34
24.1 4- 6.26
10.755"
2.292
Maenidae Spicara maena (Linnaeus, 1758)
1.91 + 1.12
2.57 4- 1.18
0.179
0.796
1.07 4- 0.17
0.28 + 0.19
1.032"*
0.083
0.24 4- 0.07 0.26 q- 0.11
0,02 4- 0.02 0,37 4- 0.13
0.146"* 0.019
0.014 0.059
0
0,02 4- 0.02
0.001
0,001
0 0 5.19 4- 0.79 0.14 4- 0.03 0.02 -4- 0.02 0.2 4- 0.06 1.67 4- 0.61 0.12 4- 0.04 0.59 4- 0.12
0.02 4- 0.02 0.02 4- 0.02 3.27 4- 0.41 0.26 ± 0.05 0 0.31 -i- 0.09 0.47 4- 0.16 0.08 4- 0.04 0.72 ± 0.08
0.001 0.001 0.484 0.040 0.001 0.024 1.002" 0.006 0.033
0.001 0.001 0.110 0.011 0.001 0.030 0.183 0.011 0.038
0
0.04 4- 0.02
0.006
0.006
1.79 4- 1.36 22.3 4- 12.4 17 3.93
6.22 -4- 1.36 40.9 + 5.61 2O 2.14
6.557** 1.596"
1 0.547 0,221
Mullidae Mullus surmuletus (Linnaeus, 1758) Serranidae Serranus cabrilla (Linnaeus, 1758) S. scriba (Linnaeus, 1758) Haemulidae Pomadasys incisus (Bowdich, 1825) Labridae Labrus merula Linnaeus, 1758 L. viridis Linnaeus, 1758 Corisjulis (Linnaeus, 1758) Symphodus rostratus (Block, 1797) S. cinereus (Bonnaterre, 1788) S. melanocercus (Risso, 1810) S. ocellatus Forsskal, 1775 S. mediterraneus (Linnaeus, 1758) S. tinca (Linnaeus, 1758) Muraenidae Muraena helena Linnaeus, 1758 Pomaeentridae Chromis chromis (Linnaeus, 1758) Total density Species richness Diversity H rindex
technique, with the consequent lack of model assumptions. Triangular similarity matrices were calculated using Bray-Curtis similarity measures of fourth-root transformation abundance data. The data transformation was carried out to balance the contribution from the rarer species. An R statistic was then calculated and the associated significance level of sample statistic was derived by a permutation test (n = 5000). The taxa responsible for differences between groups and similarities within groups were recognised using the "analysis of similarity percentages" (SIMPER) showing only the taxa where the cumulative percentage of importance was bigger than 50% (Clarke, 1993).
*
4. Results 4.1. P. oceanica meadow The meadow's cover was significantly higher in the control (CO) (80 + 2%) than in trawled area (IM) (64 + 3%; ANOVA p < 0.01). The meadow's density was significantly higher in the control (209 + 12 sh.m -2) than in the trawled area (169 i 13 sh.m-2; ANOVA p < 0.05). Overall density was also significantly different between the two study sites (ANOVA p < 0.01; 184 4- 13 sh.m -2 in CO and 109 4- 9 sh.m -2 in IM) (Figure 2).
244
Overalldensity
Cover
Density I00
200
-tt
80
i
200
60 ~
40
,,~ 100
100
20 .i
0--
"~
0 Control Impact
0
Control Impact
Control
Impact
Figure 2. Some values of the density, cover, and overall density of P. oceanica meadow in the two study sites. Asterisks refer to result of
ANOVAbetween control and impact sites: * ~p < 0.05, ** ~p < 0.01.
100 o -8
~ F i n e detritus fraction
80
~
60 ~E
Coars¢ detritus fi-action
40
I "]Totaldelritus
20
~ R h i z o m e fragments
0 Control
Impact
Figure 3. Vegetal detritus (grams dry weight per m2) in the P. oceanica meadow. Asterisks refer to results of ANOVAbetween control and
impact sites: * ~p < 0.05, ** =p < 0.01.
The plant's features: foliar biomass, foliar area and epiphytic biomass, were not significantly different between the two study sites. The detritus, however, was significantly different in both the coarse and fine fractions, being more abundant in the trawled area. The fragments of rhizomes accumulated in the substrate did not show differences (Figure 3). In the trawled area, the rhizomes were almost underneath the sediment (39.1 + 27.7 mm), in contrast to the control, at which plants demonstrate substantial development (65.5 4- 27.2 mm; ANOVA p < 0.01) above the substrate.
4.2. Fish assemblages Twenty-six species of fishes were identified mainly in the families Labridae, Sparidae and Serranidae with an average number of species per census of 10. Species which were not commonly associated with P. oceanica meadows were not included in the analysis. Number of species was similar between the two sites with 17 species in the trawled area and 20 in the control area. The ecological diversity was significantly higher in the trawled area with a value of 3.93 (Ttest = p < 0.05). Abundances of fish families, were not significantly different (ANOVA p < 0.05). The most abundant family was Sparidae (55.8%) followed by Labridae (20.8%) and Pomacentridae (12.7%). Only six species were significantly different in abundance: MuUus sur-
245
Table3. Results of test ANOSIM,in the different level of environmental impactcarded out in this study. R-global is a comparative measureof the degree of separation of sampling sites, with values near to 1 meaning the biggest difference; p is the significantlevel of samplestatistic, and * shows the study levels at which the environmentalimpactcould be detected R global
p
Macroscale: Fish family species Microscale: Invertebrates Phyla Classe Decapoda family species Mysidacea family species lsopoda family species Amphipoda family species
0.520 0.430 0.004 -0.026 0.024 0.032 ~0.024 0.114 0.159 0.277 0.280
0.031 * 0.002* 0.359 0.725 0.304 0.261 0.516 0.051 0.021 * 0.0301" 0.0001 *
muletus Linnaeus, 1758, Chromis chromis (Linnaeus, 1758), Diplodus annularis (Linnaeus, 1758), Serranus cabrilla (Linnaeus, 1758), Symphodus ocelatus Forsskal, 1775 and Pagellus acarne (Risso, 1826) (Table 2). The structure of the total fish assemblage of the different samples obtained in the two study sites was significantly different, examined at both the species and family levels (Table 3). After the analysis of similarity percentages (SIMPER), the fish species which contributed most to the overall similarity among samples at the control site were C. chromis, Coris julis (Linnaeus, 1758), P. acarne and D. annularis. In the trawled site C. julis, D. annularis, M. surmuletus and S. ocellatus were most important. The species with a bigger weight in the dissimilarity analysis between the study sites were P. acarne, C. chromis, Spicara maena (Linnaeus, 1758), M. surmuletus, S. cabrilla, S. ocellatus and Diplodus vulgaris (Saint-Hilaile, 1817). The most important fish families for similarity among samples in both sites were Sparidae and Labridae. However, Pomacentridae, Centracantidae, Sparidae and Mullidae were the families which had more weight in the dissimilarity between sites.
4.3. Macroinvertebrates 4.3.1. High taxonomic level Macroinvertebrates, when examined at the phylum level were not, in general, significantly different between the two sites. Annelida (polychaetes) was the only group to display a difference (ANOVA p < 0.05) (Figure 4). The assemblages also did not differ between the study sites when examined at the Class level (Figure 5). The ANOSIM test on the community assemblage structure at a coarse taxonomic level did not show any significant differences (Table 4). 4.3.2. Low taxonomic level: Crustacea Decapods were among the best represented orders in the sample. A total of 34 species was found (Table 4), belonging to families which are usually associated with P. oceanica (e.g. Hippolytidae and Alpheidae). The community was dominated by Thoralus cranchii (Leach, 1817), Achaeus gracilis Costa, 1839 and Athanas nitescens (Leach, 1814). The species richness was slightly higher (T test, p < 0.05) in the control, with 29 species, as compared to 24 species in trawled area. The diversity index was, however, high in both sites, (close to 4 bits/ind.) and displayed no significant difference. No species were significantly more abundant in either site, except Pisidia longicornis, which was only present in the control site. Mysids were not abundant either in terms of species or individuals (Table 4). Siriella clausii Sars, 1877 was the dominant species at both sites and there were no significant differences between sites. Isopods were more important than mysids, however the number of species and diversity was still relatively low. The two dominant isopod species exhibited significant differences in abundances between sites: Synisoma carinata (Rathke, 1837) had a greater density in the trawled area (ANOVA, p < 0.05) and Cymodoce hanseni (Dumay, 1972) was most abundant in the control site (ANOVA, p < 0.05) (Table 4). The amphipods had a species richness and diversity similar to that of the decapods (around 4 bits/Ind.). They did not, however, show marked differences between sites. A few species showed significant variation in abundance between sites: Ampelisca spp. Kroyer, 1842, Dexamine spinosa (Montagu, 1813) and Maera knudseni Reid, 1951 were most abundant in the trawled area (ANOVA, p < 0.05) and Lysianassa longicornis Lucas, 1849 population was more abundant in the control (ANOVA, p < 0.01) (Table 4).
246 Table 4. Mean (4- SD) of crustacea species abundance (number ind. per 1 m2). Results of ANOVA between the study places: d.f. = 1-22, ms - mean square, ns - no significant difference, * =p < 0.05, ** =p < 0.01 Impact
Control
MS
ERROR
4.7 5:2.5 0 18.0 ± 7.3 0 15.3 q- 7.1 8.7 4- 4.2 2.0 5:1.4 0.6 -4- 0.6 0.6 4- 0.6 0 0.6 4- 0.6 3.3 -/- 1.2 1.3 5:0.9 0.6 5:0.6 2.0 ± 2.0 2.6 ± 1.1 0 0 0 0.6 ± 0.6 0 8.7 4- 2.3 3.3 4- 1.54 2.0 5:1.43 1.3 4- 0.9 2.6 ± 1.5 15.3 4- 4.6 2.0 ± 1.0 0.6 4- 0.6 3.3 4- 2.7 0 0 102.0 5:18.4 24 3.82
11.3 5:3.3 0.6 5:0.6 35.3 4- 9.9 0.6 5:0.6 10.0 4- 3.0 13.3 5:3.7 1.3 4- 0.9 0.6 4- 0.6 0.6 4- 0.6 2.0 4- 2.0 0 0.6 4- 0.6 1.3 5:0.9 0 0 4.0 5:2.3 3.3 5: 1.5 2.0 ± 1.4 0.6 5:0.6 2.0 4- 1.4 0.6 4- 0.6 8.0 4- 3.7 4.0 5:1.5 0.6 ± 0.6 1.3 ± 0.9 8.0 5:2.6 16.0 4- 3.3 0.6 ± 0.6 2.6 ± 2.6 2.6 4- 1.1
0.955 0.020 1.661 0.020 0.018 0.647 0.007 0.020 0.020 0.080 0.020 0.320 0.001 0.020 0.080 0.007 0.421" 0.134 0.020 0.050 0.020 0.134 0.020 0.05 0.000 0.721 0.148 0.080 0.035 0.009
0.362 0.020 0.825 0.020 0.489 0.417 0.101 0.020 0.020 0.080 0.020 0.084 0.073 0.020 0.080 0.184 0.082 0.065 0.020 0.085 0.020 0.339 0.168 0.085 0.073 0.225 0.391 0.069 0.128 0.178
1.3 4- 0.9 0.6 + 0.6 135 4- 27.1
0.080 0.020 0.180
0.036 0.020 0.176
29 4.01
ns
0.3 5: O.1 0.3 -4- 0.16 1.0 4- 0.21 I0 0.1 5:0.05 3.5 4- 1.0
0.2 -4- 0.1 0.2 + 0.1 0.6 5:0.2 0.2 5:0.1 0.1 ± 0.1 2.9 5:1.4
0.020 0.117 0.777 0.020 0.007 0.018
4 1.67
5 ns
Oecap~ta Hippolyte inermis (Leach, 1815) H. leptocerus (Heller, 1863) Thoralus cranchii (Leach, 1917) Alpheus macrocheles (Hailstone, 1835) Athanas nitescens (Leach, 1814) Processa modica Will. & Roch., 1979 Periclimenes scriptus (Risso, 1822) Cestopagurus. tubularis (Roux, 1830) C. timidus (Roux, 1830) Diogenes pugilator (Roux, 1829) Pagukristes eremita (Linnaeus, 1818) Pagurus cuanensis Bell, 1846 P. anachoretus Risso, 1827 P. chevreuxii (Bouvier, 1896) Anapagurus curvidactylus (Chev. & Bour. 1892) Galathea bolovari (Zariquiey-Alvarez, 1968) Pisidia longicornis (Linnaeus, 1767) P. longimana (Risso, 1816) Dromia personata (Linnaeus, 1759) Ethusa mascarone (Herbst, 1785) Ilia nucleus (Linnaeus, 1758) Ebalia edwards±Costa, 1838 Sirpus zariquieyi Gordon, 1953 Liocarcinus arcuatus (Leach, 1814) Eurynome aspera (Pennant, 1777) E. spinosa Hailstone, 1835 Achaeus gracilis Costa, 1839 Macropodia rostrata (Linnaeus, 1761) M. czeniavskii Forest & Zariquiey, 1964 Inachus phalagium Fabric±us, 1775 Pisa armata (Latreille, 1803) Maja crispata Risso, 1827 Total density decapods Species richness Diversity H rindex
Mysidacea Anchialina gracilis Sars, 1977 Gastrosaccus norman± (Van Benden, 1910) Sir±ella claus±Sars, 1977 Mysidacea spl Mysidacea sp2 Total density mysids Species richness Diversity Hqndex 1.35
0.201 0.216 0.594 0.020 0.070 0.167
247
Table 4. Continued Impact
Control
MS
ERROR
2.7 ± 1.5 0.7 4- 0.7
0.7 5:0.7 0
0.134 0.020
0.095 0.02
4.7 5:2.7 0 21.3 4- 7.3
1.3 5:0.9 2.0 5:1.0 2.7 5:1.5
0.180 0.180 3.486*
0.187 0.049 0.444
Total density isopods Species richness
0.7 4- 0.7 10.7 ± 2.3 1.3 -4- 0.9 0 42.0 5:9.6 7
3.3 5:1.8 22.7 ± 4.4 2.0 5:1.0 0.7 5:0.7 35.3 4- 5.5 8
0.201 1.276" 0.030 0.020 0.097
0.120 0.247 0.020 0.020 0.402
Diversity H pindex
1.95
1.48
ns
Isopoda Paranthura costana Bate & Westwood, 1868 Astacilla longicornis Cordiner, 1795 Cirolana cranchii (Hasen, 1905) Ghathia sp. Monod, 1910 Synisoma carinata (Rathke, 1837) Zenobiana prismatica (Risso, 1826) Cymodoce hanseni (Dumay, 1972) C. rubropunctata (Grube, 1908) Dynamene bidentata (Adams, 1800)
Amphipoda Iphimedia minuta Sars, 1882 Ampelisca spp. Kroyer, 1842 Amphitoe ramondi Audouin, 1826 Cymadusa crassicornis (Costa, 1857) Aora spinicornis Afonos, 1976 Leptocheirus guttatus (Grube, 1864) Apherusa chiereguinii Giordani-JSoika, 1950 A. vexatrix Krapp-Schickel, 1979 Corophium minimum Schiecke, 1979 Siphonocetes spp. Kroyer, 1845 Atylus guttatus (costa, 1851) A. vedlomensis (Bates & Westwood, 1862) Dexamine spiniventris (Costa, 1853) D. spinosa (Montagu, 1813) Eusiroides dellavalei Chevreux, 1899 Ceradocus semiserratus (Bate, 1862) Elasmopus rapax Costa, 1853 Gammarella fucicola Leach, 1814 Maera grossimana (Montagu, 1808) M knudseni Reid, 1951 Leucothoe spinicarpa (Abildgaard, 1789) Lepidepecreum longicorne (Bate & Westwood, 1861) Lysianassa longicornis Lucas, 1849 L. pilicornis Heller, 1866 Orchomenes humilis (Costa, 1853) Orchomenes humilis (Costa, 1853) Monoculodes carinatus (Bate, 1857) Pereinotus testudo (Montagu, 1808) Hyale stebbingi Chevreux, 1888 Caprella acanthiphera Leach, 1814 Phtisica marina Slabber, 1769 Pseudoprotella phasma (Montagu, 1804) Total density amphipods Species richness Diversity Hpindex
4.0 + 1,6 11.3 + 3.9 4.7 + 2.1 5.3 4- 3.3 12.0 5:4.1 1.3 5:0.9 0.7 5:0.7 1.3 5:0.9 0 5.3 4- 0.6 0 9.3 -4- 2.4 13.3 4- 3.9 8.0 + 2.4 0 0 0 0.7 5:0.7 1.3 5:0.9 12.7 ± 5.2 0.7 -4- 0.7 0 1.3 + 1.3 1.3 5:0.9 0.7 5:0.7 0.7 4- 0.7 0 0 0 2.7 -4- 1.1 1.3 4- 0.9 0.7 4- 0.7 114.0 5:12.3 22 3.74
2.7 5:2.0 2.7 5:2.0 1.3 5:1.3 2.0 5:1.4 5.3 5:4.2 0.7 ± 0.7 22.6 4- 5.8 5.3 ± 1.8 0.7 + 0.7 22.6 + 5.8 1.3 5:1.3 5.3 ± 2.0 4.7 ± 1.5 2.0 ± 1.4 4.0 4- 1.2 0.7± 0.7 0.7 5:0.7 1.3 + 0.9 2.0 -4- 1.4 20 ± 1.4 2.0 5:2.0 0.7 4- 0.7 12.0 -t- 3.3 0 2.0 4- 1.4 2.0 -+- 1.4 0.7 ± 0.7 0.7 -4- 0.7 2.0 4- 2.0 0.7 ± 0.7 2.0 4- 1.0 0 96.9 4- 19.8 29 4.08
0.134 1.613" 0.390 0.180 0.679 0.020 0.800 0.535 0.020 0.126 0.05 0.377 1.003 1.029" 0.721"* 0.020 0.020 0.020 0.007 1.905" 0.020 0.020 2.601"* 0,080 0.050 0.050 0,020 0.020 0.080 0.180 0.020 0.020 0.567 ns
0.178 0.288 0.159 0.219 0.365 0.056 0.193 0.140 0.020 0.576 0.050 0.246 0.305 0.209 0.066 0.020 0.020 0.056 0.101 0.291 0.100 0.020 0.242 0.036 0.085 0.085 0.020 0.020 0.080 0.078 0.086 0.086 0.274
248
1200 1000 ~
800
~e~
600
•~
Total
$_
400
o ~
. ~
200 0 Control
II
Echinoderms
I
Molluscs Arthropods
~'~
Annelids
Impact
Figure4. Abundanceof differentphylaof macroinvertebratesat the two study sites, expressedas numberof individualsper m2. Onlyannelids showed significantdifferences(* = p < 0.05) betweensites. From the results of ANOSIM (Table 3), the decapods and the mysids did not show any significant differences between sites. Family level of mysids was not used in this test because of all the species that we could identify belonged to the same family. However, the isopods showed significant differences at the species level. The most important species in the similarities in the stations was C. hanseni and at the dissimilarity between sites were S. carinata, C. hanseni and Cirolana cranchii (Hasen, 1905). Families and species of amphipods showed the most significant differences between the stations. After the results of SIMPER, Siphonoecetes spp Kroyer 1845, L. longicornis and Dexamine spiniventris (Costa, 1851) were the most important species in the similarities among the control samples. Siphonoecetes spp., M. knudseni, D. spiniventris and Atylus vedlomnesis (Bates & Westwood, 1862) were the most important in samples from the trawled area. The dissimilarities between places were mainly due to M. knudseni, L. Iongicornis, Ampelisca spp, Siphonoecetes spp, Aora spinicornis Afonso, 1976, D. spiniventris, D. spinosa and A. vedlomensis. The families Corophidae, Dexaminidae and Lysianassidae were the most important in the similarity in the control station and Dexaminidae,
Gammaridae and Corophidae in the trawled station. Gammaridae, Lysianassidae, Ampeliscidae, Dexaminidae, Amphithoidae and Corophidae were the principal families in the dissimilarity between sites.
5. Discussion The sustainable utilization of marine resources has become a high priority in marine ecosystem management and the effects of fisheries such as epibenthic trawling may be responsible for the continued decline of communities in such habitats (Sainsbury et al., 1993). The decline of P. oceanica meadows in the Mediterranean (P6r~s, 1984; S~achez Lizaso et al., 1990) underscores the importance of monitoring programs because of its direct and indirect effects on the survival of other species and its important role in the littoral ecosystem (Zieman & Wetzel, 1980; Stoner, 1980; Bell & Pollard, 1989; Virnstein, 1987; Orth, 1992). Changes to features of the meadows, such as density or cover, should affect the structure of the associated fauna assemblage (Connolly, 1995). These changes of the marine community structure could have an
249
Arthropods 200 !
T
150 t
~1 Amphipods
II tsopods
100
I'-'l Mysids
t
r~
[] Deeapods [ ] Pygnogonids
0 I
-H
Molluscs
O
80 T
A
*,gl
!
60 ra~
[:~l Bivalves [ ] Gastropods
40
.=.
Echinoderms
60 I
T
4° I 0
I Echinoids !---1 Holothuroids [~] Ophiuroids I~ Asteroids
t ~
Control
Impact
Figure 5. Abundanceof different groups (classes and orders) of macroinvertebrates at the two study sites, expressed as number of individuals
per m2. No significantdifferences were foundin the ANOVA.
important influence on processes such as primary and secondary production, affecting to overall ecosystem health. In this study, the most important differences between meadows were detected in overall density of meadow, with a reduction of about 40 percent
and an increase in accumulation of vegetal detritus in the impacted site, probably due to uptake of vegetal necromass from the sediment. The sedimentation ratio is modified by the bottom trawling (Jones, 1992) and this factor modifies the seagrass' development
250 (Boudouresque & Meinesz, 1982; Ruiz et al., 1993). In the study sites, the contrast in the mean distance between the meristeme and the sediment was important. That change may be important in the modification of available habitat, with a reduction of rhizome habitat like hard substrate. Most environmental impact studies focus on communities, because the structure at this level of investigation represents an integration of environmental conditions over a period of time (Warwick, 1993). However, there are situations where a single species must be studied because of the cause of an observed pattern of change or difference to a particular disturbance is very difficult to detect with multivariate analysis (Underwood, 1993). Monitoring of certain populations associated with P. oceanica could be useful, since some species of fishes and small mobile invertebrates in this study showed significant differences between the impact and control sites. For example, Diplodus annularis is a relatively abundant fish species and has an important relationship with the meadows (Bell & Harmelin-Vivien, 1982) which were more abundant in the trawled area maybe due to it is easier to obtain food in degradate meadows. Similarily, the different densities of the two more abundant species of isopods, Synisoma carinata and Cymodoce hanseni, and some amphipods such as Ampelisca spp or Maera knudseni could be used as indicators, concerning the autoecology of each species (Castello, 1986; Ruffo, 1982, 1989). In general, the environmental preference of the macroinvertebrates is not well known. However, as a cautionary note in the interpretation of the results it should be remembered that these results are preliminary because of the lack of spatial replication. The differences could be attributed to disturbance by trawling but experimental verification would be useful. The most simple measurements of community complexity, such as species richness and diversity, could be good descriptors of environmental impacts, but they do not adequately address the problem of changes in patterns of community complexity (Magurran, 1991). The number of species and diversity of the different taxa showed similar values, except the fish community diversity which was significantly higher in the disturbed habitat (Table 2). Monitoring the P. oceanica fish assemblage is very important since some species (mainly sparids and labrids) are of immediate commercial concern (Lleonart, 1990). Although identification to species is relatively easy, it may not be necessary because monitoring of a family may be sufficient to identify envi-
ronmental impacts by bottom trawling in meadows. In addition, it could prove of interest in the study of changes in a regional scale because most of the species change regionally but the families remain constant. Moreover, the structure of the total fish assemblage responds to changes in the meadow's cover and could be used to monitor other important impacts in the P. oceanica meadows, such as coastline construction, which also affect the overall density of surrounding meadows (Ruiz et al., 1993). Some authors have described community changes in the detection of environmental impacts of oil spills to phylum level (Warwick, 1988; Clarke & Ainsworth, 1993). This study, the coarse taxonomic levels did not reveal any significant difference, except in the abundance of polychaeta (Figure 4). This could be because impact by bottom trawling is only a mechanical modification of the habitat, as opposed to an oil spill which causes extreme changes to water chemistry and toxicity and in some cases physical degradation of the habitat. On a fine taxonomic level, e.g. family or species, the decapods showed no differences in community structure. Decapods cannot establish a local population, due to their great mobility and larval dispersion and hence are not useful as community descriptors (Amanieu et al., 1981). However, the peracarid crustaceans, without a planktonic larval stage, show great changes between study sites at the population and community levels, as has been shown by Virnstein (1987). In this study, abundances of seven peracarid species were significantly different. Mysids were exceptions, possibly due to the fact that they inhabit the water column for the most part and are less tied to the meadows than the other members of the peracarids. Thirty-three species of isopods have been recognised in the NW Mediterranean Sea (Castello, 1986) and about 18 of these are common in P. oceanica meadows (Gambi et al., 1992). Determination to species level is not extremely difficult (except with juveniles of some genera such as Cymodoce) and some (e.g. Synisoma spp. might be useful as bioindicators. The study of amphipods at the family level is likely to be the most effective method in terms of cost benefit. The main families are relatively easy to identify and more detailed identification requires involved procedures such as dissection of mouth parts. In general, the families most important in the similarity and dissimilarity among samples (e.g. Gammaridae, Lyssiamasidae and Dexaminidae) were composed of species with similar trophic and habitat requirements
251 (Scipione, 1989). Other authors have also indicated that the family-level identification appeared to be a good choice for assessing pollution impacts (Ferraro & Cole, 1990). The results of this study suggest that a m p h i p o d s and isopods are the most useful groups of crustaceans for m o n i t o r i n g e n v i r o n m e n t a l impact in P. oceanica meadows. Moreover, these groups have an important ecological function in the seagrass e c o s y s t e m and changes in their a b u n d a n c e s could be interpretate in relationship with the ecosystem health ( Z i m m e r m a n et al., 1979; Lorenti & Scipione, 1990; G a m b i et al., 1992).
Acknowledgements This study would not have b e e n possible without the assistance o f m a n y people. Colleagues at U n i v e r s i t y of Alicante and Institut d ' E c o l o g i a Litoral helped us in the s a m p l i n g and analysis o f material: J u a n Guill6n (decapods), D a v i d Grass (mysids), Sandra, Marco, Marcos, Ernesto, Juan Roberto and Maria Jesus. T h a n k s to B A I N C A I X A E U R O P A travel grants, we could visit the Laboratorio di Ecologia del B e n t h o s di Ischia (Napoli), where Dra. Maria Beatrice Scipione a n d M a u r i z i o Lorenti k i n d l y helped us with a m p h i p o d s and isopods taxonomy. T h a n k s to Dr. M. J. Kingsford for p r o v i d i n g the possibility to work in the Fish Ecology Laboratory at University of Sydney, where this m a n u s c r i p t was prepared. Special thanks to Eric Dorfm a n , G u i l l e r m o M o r e n o and Kirrily Moore for help with the English and Marti J. A n d e r s o n for help with P R I M E R statistical package. This work was financed through Ph.D. scholarship (FPI91 21478607) from the G o v e r n m e n t of Spain and through the lnstitut d 'Ecologia Litoral (El Campello, Spain).
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