Seasonal, tidal and diurnal changes in fish assemblages in the Ria Formosa lagoon (Portugal)

Estuarine, Coastal and Shelf Science 67 (2006) 461e474 www.elsevier.com/locate/ecss

Seasonal, tidal and diurnal changes in fish assemblages in the Ria Formosa lagoon (Portugal) Joaquim Ribeiro*, Luis Bentes, Rui Coelho, Jorge M.S. Gonc¸alves, Pedro G. Lino, Pedro Monteiro, Karim Erzini Centro de Cieˆncias do Mar, Faculdade de Cieˆncias do Mar e do Ambiente, Universidade do Algarve, Campus de Gambelas, 8005-139 Faro, Portugal Received 17 June 2005; accepted 28 November 2005 Available online 24 February 2006

Abstract Fish fauna were collected in two different subtidal shallow sites, seagrass and sand, using a small beam trawl in the Ria Formosa lagoon (South Portugal). Samples were taken at low and high tides, during day and night, and in each season. Fish assemblages associated with each site were significantly different, with seagrass site supporting greater fish abundance and higher number of species than sand. These site-related differences in fish assemblages were stronger than any other factor studied. Both sites showed seasonal variations in their fish assemblages, mainly because of recruitment of marine juvenile migrants during spring and summer. No significant tidal or diel changes were observed in the fish assemblages of either site, but there was a significant siteetide interaction, with higher fish abundance in seagrass at low tide. In sand, tide effect was evident only for certain species, with resident species more abundant at high tide and marine species more abundant at low tide. Within the Ria Formosa coastal lagoon, ichthyofaunal composition and structure is mainly influenced by site followed by season. Ó 2005 Elsevier Ltd. All rights reserved. Keywords: fish fauna; coastal lagoon; seagrass; sand; temporal variations; Ria Formosa; South Portugal

1. Introduction Shallow areas of estuaries and coastal lagoons contain some of the most productive coastal habitats, such as tidal flats, seagrass beds, subtidal channels and salt marshes (Pihl and Rosenberg, 1982; Weinstein, 1982; Kneib, 1997). Many of these shallow habitats support diverse and abundant fish assemblages, and sustain significant populations of juveniles of many commercially important fish species (Bell and Pollard, 1989; Potter et al., 1990; Edgar and Shaw, 1995a; Lazzari and Tupper, 2002). However, the ichthyofauna is heterogeneously distributed among the different types of habitats, according to sediment type, vegetation preference and temporal scale (tidal, diel, lunar, seasonal). Several studies have * Corresponding author. E-mail address: [email protected] (J. Ribeiro). 0272-7714/$ - see front matter Ó 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecss.2005.11.036

compared seagrass beds with non-vegetated substrates, in particular sand, and have generally reported that the seagrass supports different and more abundant and diverse fish assemblages than non-vegetated habitats (e.g. Heck et al., 1989; Sogard and Able, 1991; Connolly, 1994a; Gray et al., 1996; Jenkins et al., 1997; Guidetti, 2000; Travers and Potter, 2002). Besides the differences in fish assemblages associated with the various habitat types, ichthyofaunal compositions and structure can also undergo consistent cyclical and temporal changes within habitats. Seasonal shifts in fish communities are common, as a result of sequential immigration and emigration of certain fish species (Hyndes et al., 1999; Thiel and Potter, 2001). Tidal and diel shifts in fish assemblages have also been reported by several authors (e.g. Sogard et al., 1989; Rountree and Able, 1993; Gray et al., 1998; Griffiths, 2001; Methven et al., 2001; Morrison et al., 2002; Guest et al., 2003). The aim of this study was to examine

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the effect of season, tide and diel variations in fish assemblages associated with two subtidal sites, seagrass and sand, present in the Ria Formosa coastal lagoon (Algarve, South Portugal). 2. Materials and methods 2.1. Study area This study was carried out in the western part of the Ria Formosa (Ria Faro-Olh~ao). The Ria Formosa is a large tidal lagoon extending for about 55 km along the south coast of Portugal, with a maximal width of 6 km (Fig. 1). A seaward belt of dunes protects a system of salt marshes, subtidal channels and tidal flats, with a total surface area of approximately 170 km2. The tidal elevations are 1.30 and 2.80 m at mean neap tide and spring tide, respectively, and the minimum and maximum areas covered by water during spring tides are
14.1 and 63.1 km2 (Aguas, 1986). A strongly branched system of creeks and channels is connected with the ocean by six outlets. The average depth is less than 3 m, with 14% of the lagoon surface permanently submersed (subtidal channels) and the intertidal area covers approximately 1/3 of the total area of the lagoon. The system has semi-diurnal tides, with 50e
75% of the water volume exchanged during each tide (Aguas, 1986). The lagoon does not receive any permanent freshwater input: salinity is 35.5e36.9 all year, except for surface waters for brief periods after winter heavy rainfalls (Falc~ao et al., 1992). Water temperature varies from 12 to 28
C (Sprung, 1994). 2.2. Sampling design Fish fauna were collected from two different subtidal shallow sites, separated by 1.5 km (Fig. 1). One site represented the seagrass habitat and was located in a medium size subtidal channel (37
000 N, 07
570 W), with around 50 m width and an average depth of 1.5 m at low tide. The tidal current velocity is relatively low compared to that observed in the vicinity of

the inlets (Lima and Vale, 1977), and the bottom consists of muddy sandy sediments (sand e 35.7%; silt e 31.7%; clay e 32.6%), covered with several extensive patches of seagrass, Cymodocea nodosa. The second site represented the sand habitat and was located in a subtidal channel that gives access to an inlet, artificially opened in 1997 (36
590 N, 07
570 W). The tidal current velocity is much stronger than in the seagrass site, and the sediments were dominated by well calibrated mediumcoarse sand (sand e 99.4%; silt e 0.3%; clay e 0.3%). This channel was 30 m wide with an average depth of 1.9 m at low tide and no vegetation was present during the sampling period. Both sites were sampled on a seasonal basis over a one-year period, with samples taken in May 2001 (spring), August 2001 (summer), November 2001 (autumn) and February 2002 (winter). In each season the sampling took place in one single day, and the two sites were visited at the beginning of the ebb tide (high tide sampling) and at the beginning of the flood tide (low tide sampling), both during the day and night. At each visit, three replicate tows of 200 m each were made, using a beam trawl (2.6 m wide and 0.45 m high at the mouth) with a stretched mesh size of 9 mm in the cod end. Since this sampling gear is not effective for catching pelagic species (e.g. Atherina spp., Liza spp. and Sardina pilchardus), this study focuses on benthic and epibenthic fish communities, present in each sampled site. All samples were taken during neap tide, near the last quarter moon. In the laboratory, all fish were identified to species and counted. 2.3. Data analysis The independent variables were site (seagrass and sand), season (spring, summer, autumn and winter), tide stage (high/ebb tide and low/flood tide) and diel period (day and night). A four-way factorial analysis of variance (ANOVA) was used to test for differences in the number of species and individuals, with all factors considered fixed (SAS Institute, 1988). Number of species was square-root transformed and number of individuals was ln transformed. When significant main effects were detected in the multifactor ANOVAs,

Fig. 1. Western part of the Ria Formosa lagoon (Ria Faro-Olh~ao) showing the location of the two sampling sites: (1) seagrass and (2) sand.

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Tukey’s Honestly Significant Difference (HSD) test was used to find which means differed. Analysis was performed on the transformed data but the level of significance set to P  0.01 to minimize the chances of Type I errors occurring (Underwood, 1981). Significant interactions between factors were examined graphically. To test for differences in number of individuals between season, tide and diel period, three-way factorial analysis of variance (ANOVA) were performed for the 10 most abundant species in each site. Data from seagrass site were square-root transformed and Tukey’s HSD test was used when significant differences were detected (P  0.05). Spatial and temporal variations in the structure of the fish assemblages were assessed by non-metric multi-dimensional scaling (nMDS) and analysis of similarities (ANOSIM) (Field et al., 1982; Clarke, 1993) using the statistical software PRIMER 5.0 (Clarke and Warwick, 2001). Both presence/ absence and abundance data were used. For the abundance data square-root transformed values were used so that each species contributed fairly evenly to each analysis (Clarke and Green, 1988), except in the seasonal analysis for the sand site because species abundances were very low. Sample similarity matrices based on the BrayeCurtis similarity coefficient were generated, after which non-metric multi-dimensional scaling (nMDS) was used to create two-dimensional ordination plots, and one-way analysis of similarities (ANOSIM) was used to determine which assemblages differed (Clarke, 1993). Pairwise ANOSIM comparisons were made between all groups, using 10 000 simulations in each case. To compare the fish assemblage functional structure in relation to each independent variable, species were classified according to their ecological guild adapted from Elliott and Dewailly (1995): (D) diadromus migrant species, (MA) marine adventitious visitors, (MJ) marine juvenile migrants and (R) resident species. The vertical distribution guild adapted from the same authors was used to compare the fish assemblages present in the two sites: (B) benthic and (EB) epibenthic species.

3. Results A total of 17 232 fish were caught, representing 63 species and 21 families. Seagrass supplied 15 796 fish (44 species) and sand 1435 fish (44 species) (Table 1). Twenty-six species (41.3%) were common to both sites, 19 species (30.2%) occurred only in the seagrass, and 18 species (28.6%) occurred only in sand (Table 1). In sand, seven species were present only during the low tide, 10 were caught exclusively at high tide, and 30 were present during both tidal stages. In seagrass, 12 species were found only during the low tide, seven were caught exclusively at high tide and 29 were common to both tidal stages. Species present in both tidal stages represented more than 97% of the total catch in each tidal stage in both sites. Again in sand, eight species were present only during the day, 10 were caught exclusively at night and 29 were present during both day and night. In seagrass, nine species were

463

found only during the day, 10 were caught exclusively at night and 29 were common to both periods. In each site, the species present during both day and night, represented more than 99% of the total catch in each period, indicating that species that occur only at night or daytime were poorly associated with the site assemblages. 3.1. Number of species and individuals Overall number of species was similar for both sites (Table 1), but mean number of species was significantly higher in seagrass (Table 2). Season effect was also responsible for significant differences in number of species, but siteeseason interaction was also significant and therefore trends within site should be investigated (Table 2). In seagrass, the Tukey HSD test revealed that mean number of species differed significantly between all seasons except for spring and summer, which had significantly higher numbers than autumn and winter (Fig. 2). In sand, mean number of species did not differ between spring and summer, and between autumn and winter, with the first two seasons having significantly higher numbers than the later. This interaction also indicated that number of species was significantly higher in seagrass than sand, across all seasons. All other main effects and interactions were not significant. The overall fish abundance was 10 times higher in seagrass than sand, with a significant difference in mean number of fish between sites (Tables 1 and 2). There was also a significant seasonal variation in mean number of fish. Site  season interaction was significant, with seagrass presenting significantly higher mean numbers of fish in spring and summer compared to autumn, which had significantly higher abundance than winter (Fig. 3). In sand, only spring differed significantly from other seasons, with higher mean fish abundance. There was no significant effect of tide and diel period on mean fish abundance, but there was significant siteetide, seasonediel and siteeseasone tideediel interactions. Siteetide interaction indicated that mean number of fish was significantly higher at low tide in the seagrass site, while in sand there was no significant difference between tidal stages (Fig. 4). For seagrass, mean fish abundance was never significantly higher during high tide, while it was significantly higher during low tide for at least one sampling visit in each season (Fig. 5). With respect to seasonediel and siteeseasonetideediel interactions, although significant differences in mean fish abundance were identified, no clear pattern of mean fish abundance was identified, with F-values lower than other significant effects (Table 2). 3.2. Species composition The species common to both sites Gobius niger, Diplodus vulgaris and Symphodus bailloni had a similar rank order in abundance in each site, but were much more abundant in the seagrass (Table 1). Gobius paganellus, Spondyliosoma cantharus and Symphodus cinereus showed a much greater abundance and a higher rank order of abundance in this site (Table 1). The syngnathidae species, Hippocampus guttulatus, Syngnathus

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Table 1 List of fish families and species caught over seagrass and over sand, total abundance (n), relative abundance (n%), and ecological and vertical distribution classification Family

Species

Sand

Anguillidae

Anguilla anguilla

1

Batrachoididae

Halobatrachus didactylus

0

e

Blenniidae

Salaria pavo Parablennius gattorugine Parablennius pilicornis

0 4 6

Bothidae

Arnoglossus laterna Arnoglossus thori Bothus podas

Callionymidae

Callionymus maculatus Callionymus risso

Congridae

Conger conger

Gobiidae

Gobius couchi Gobius cruentatus Gobius niger Gobius paganellus Pomatoschistus microps Pomatoschistus minutus Pomatoschistus pictus

Gobiesocidae

Diplecogaster bimaculata

Labridae

Ctenolabrus rupestris Labrus bergylta Labrus merula Symphodus bailloni Symphodus cinereus Symphodus melops Symphodus ocellatus Symphodus roissali Symphodus rostratus

0 0 0 44 14 1 0 1 0

Mullidae

Mullus surmuletus

Rajidae

n

Seagrass n(%)

n

Guilds n(%)

Ecological

Vertical

64

0.41

D

B

621

3.93

MJ

B

e 0.28 0.42

3 15 0

0.02 0.09 e

R R R

B B B

1 19 30

0.07 1.32 2.09

0 0 0

e e e

MA R MA

B B B

37 1

2.58 0.07

0 0

e e

MA MA

B B

1

0.07

5

0.03

MA

B

2 1 145 25 53 798 16

0.14 0.07 10.10 1.74 3.69 55.57 1.11

284 3 5080 2851 28 0 2

1.80 0.02 32.16 18.05 0.18 e 0.01

R MA R R R R MA

B B B B B B B

22

0.14

R

B

e e e 3.06 0.97 0.07 e 0.07 e

1 1 1 302 3151 0 2 4 1

0.01 0.01 0.01 1.91 19.95 e 0.01 0.03 0.01

MA MA MA R R MA MA MA MA

EB EB EB EB EB EB EB EB EB

12

0.84

0

e

MJ

B

Raja undulata

7

0.49

0

e

MA

B

Scophthalmidae

Scophthalmus maximus Scophthalmus rhombus

1 4

0.07 0.28

0 0

e e

MA MA

B B

Scorpaenidae

Scorpaena notata Scorpaena porcus

9 9

0.63 0.63

1 57

0.01 0.36

MA MJ

B B

Serranidae

Serranus cabrilla Serranus hepatus

0 1

e 0.07

1 2

0.01 0.01

MA MA

EB EB

Soleidae

Microchirus azevia Microchirus boscanion Monochirus hispidus Solea lascaris Solea senegalensis Synaptura lusitanica

3 0 4 22 0 2

0.21 e 0.28 1.53 e 0.14

4 3 0 0 1 0

0.03 0.02 e e 0.01 e

MJ MA R MJ MJ MA

B B B B B B

Sparidae

Dentex marrocanus Diplodus annularis Diplodus bellottii Diplodus cervinus Diplodus puntazzo Diplodus sargus Diplodus vulgaris Lithognathus mormyrus Sarpa salpa Spondyliosoma cantharus

0 0 0 1 0 2 47 1 3 15

e e e 0.07 e 0.14 3.27 0.07 0.21 1.04

1 650 105 0 7 48 873 0 50 1057

0.01 4.11 0.66 e 0.04 0.30 5.53 e 0.32 6.69

MA MJ MJ MA MJ MJ MJ MJ MJ MJ

EB EB EB EB EB EB EB EB EB EB

0

0.07

e

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Table 1 (continued) Family

Species

Sand

Seagrass

n Hippocampus guttulatus Hippocamus hippocampus Nerophis lumbriciformes Nerophis ophidion Syngnathus abaster Syngnathus acus Syngnathus typhle

Syngnathidae

Torpedinidae

Torpedo marmorata

Trachinidae

Echiichthys vipera Trachinus draco

Triglidae

Trigla lucerna

n(%) 15 6 0 0 1 5 2

1.04 0.42 e e 0.07 0.35 0.14

0

n(%) 223 10 1 4 12 133 110 1

e

59 5

Guilds

n

4.11 0.35

0 0

Ecological

Vertical

1.41 0.06 0.01 0.03 0.08 0.84 0.70

R R MA R R R R

EB EB EB EB EB EB EB

0.01

MA

B

MA MA

B B

MA

B

e e

0

e

1

Total no. of individuals Total no. of species

1436 44

e e

15 796 44

e e

Resident Marine juvenile migrants Marine adventitous

1143 114 178

79.6 8 12.4

12 228 3473 31

77.4 22 0.2

Table 2 F-values and significance levels for four-way ANOVAs of mean number of species and fish, testing for differences between sites (H), season (S), tide (T) and diel (D) Effects

df

No. of species

No. of fish

F

P

F

P

Site (H) Season (S) Tide (T) Diel (D) HS HT HD ST SD TD HST HSD HTD STD HSTD

1 3 1 1 3 1 1 3 3 1 3 3 1 3 3

202.71 30.51 1.39 0.55 4.98 0.04 3.52 0.26 1.59 0.14 0.42 0.40 0.23 0.50 2.59

<0.001 <0.001 0.234 0.462 0.004 0.848 0.065 0.856 0.201 0.711 0.740 0.757 0.634 0.682 0.060

1117.38 29.21 3.69 3.76 12.19 13.03 1.81 0.47 6.32 0.46 3.76 0.51 1.86 0.21 8.30

<0.001 <0.001 0.059 0.057 <0.001 <0.001 0.183 0.704 <0.001 0.498 0.015 0.677 0.178 0.887 <0.001

paganellus and Symphodus cinereus clearly dominated the fish assemblages in the seagrass throughout the year, with some seasonal variation. Gobius niger abundance was highest in the spring, with lowest values in the summer (Table 4). In contrast, the abundance of G. paganellus was lowest in the spring and highest in the summer. Symphodus cinereus abundance was maximal in autumn and minimal in the spring. The juvenile migrant species Diplodus vulgaris, Diplodus annularis, Halobatrachus didactylus and Spondyliosoma cantharus were absent or almost absent in the autumn and winter, but were both abundant and frequent in the spring and/or summer. In seagrass, the three-way ANOVA also detected a significant tide effect on number of fish for all species, except for Hippocampus guttulatus (Table 3). Tukey HSD test revealed that those species were significantly more abundant at low tide. Diel effect on fish abundance was present in only one species, H. didactylus, which was significantly more abundant at night. Interaction terms were significant in very few cases, and no three factor interactions were found. F-values of interactions were almost always less than main effects, in particular

20

Mean number of species

acus and Syngnathus typhle, although less abundant than the previous three species, were much more abundant in the seagrass than in sand. On the other hand, although the overall abundance of Pomatoschistus microps, Pomatoschistus pictus and Scorpaena porcus was low, these species were more abundant in the sand site. Of the species present only in the seagrass, Diplodus annularis and Halobatrachus didactylus were numerically the most important. Of the species present only in sand, the most important were Arnoglossus thori, Bothus podas, Callionymus maculatus, Echiichthys vipera, Mullus surmuletus, Solea lascaris and, in particular, Pomatoschistus minutus (55.6% of the total fish abundance in sand). The 10 most numerically important species in the seagrass all revealed significant differences in abundance with season (Table 3). The resident species Gobius niger, Gobius

0.01

Sand

Seagrass

16 C 12

C D

8

E A

A

4 B 0

B

Sprin Summer Autum Winte

Sprin Summer Autum Winter

Fig. 2. Mean number of species over seagrass and sand across all seasons. Error bars represent þ1 SE and unlike letters denote seasons that differed statistically from each other in Tukey HSD test.

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Mean number of fish

500 Sand

Seagrass

400 300

C

C

200 100

D B

0

D

A B

B

Spring Summer Autum Winter Spring Summer Autum Winter

Fig. 3. Mean number of fish over seagrass and sand across all seasons. Error bars represent þ1 SE and unlike letters denote seasons that differed statistically from each other in Tukey HSD test.

for season and tide, indicating that these factors made a greater contribution to the source of variance. In sand, a significant seasonal effect on number of fish was found for all 10 most important species, except for Callionymus maculatus for which no factors or interactions were significant (Table 5). Pomatoschistus minutus clearly dominated the fish assemblage in sand throughout the year, with greatest abundance in spring and lowest in summer (Table 6). In the summer Bothus podas, Gobius paganellus and Symphodus bailloni were relatively abundant, while they were absent or almost absent in the rest of year. Diplodus vulgaris and Solea lascaris were relatively abundant in spring and summer, but they were absent or almost absent in the rest of year. Gobius niger and Pomatoschistus microps were abundant only in spring. Tide effect was responsible for differences in fish abundance in half of the species tested for sand (Table 5). The Tukey HSD test revealed that the abundance of marine adventitious species, B. podas and Echiichthys vipera, and marine juvenile migrant species, D. vulgaris, were significantly higher at high tide, while those of resident species G. niger and P. microps, were significantly higher at low tide. Diel period has a significant effect on the abundance of three species, E. vipera, P. microps and S. bailloni. 3.3. Functional guilds In terms of ecological guilds, both sites were clearly dominated by resident species, but marine juvenile migrant species were more important in seagrass, and marine adventitious visitors were more important in sand (Table 1). In both sites, the relative importance of each ecological guild follows a clear

Mean nubmer of fish

500 Sand

Seagrass

400 B

300 200 100 0

C A

A

Low tide

High tide

seasonal pattern, with marine juvenile migrant species being more abundant in spring and summer, and absent or almost absent in the autumn and winter, while the resident species dominated the assemblage year round (Tables 4 and 6). In seagrass, the relative importance of each ecological guild was similar for both tide stages, while in sand, marine adventitious and migrant species (Bothus podas, Callionymus maculatus, Echiichthys vipera and Diplodus vulgaris) were more important at low tide, and the resident species (e.g. Pomatoschistus minutus, Pomatoschistus microps, Gobius niger and Gobius paganellus) were more important at high tide (Table 6). The relative importance of the ecological groups was similar during day and night in both sites. Relative fish abundance in the vertical distribution guilds for each site shows that sand was clearly dominated by benthic species, while both benthic species and epibenthic species populated seagrass (Fig. 6a). In terms of ecological guilds both habitats were clearly dominated by resident species, while the marine juvenile migrant species were more important in the seagrass than in the bare sand and marine adventitious visitors were more important in the bare sand than in the seagrass (Fig. 6b). 3.4. Fish assemblage structure The nMDS ordination plot based on presence/absence data clearly shows a separation of samples from sand and seagrass (Fig. 7a). The seagrass samples are tightly grouped, indicating high similarities, while the sand samples constitute a more dispersed group, with a lower similarity between samples. A similar pattern was evident using abundance data (Fig. 7b), indicating that it was the presence/absence of species, rather than their abundance, that separated these two groups. ANOSIM indicated that the fish assemblages associated with the two sites differed significantly (R-statistic ¼ 0.985, P < 0.001). The nMDS ordination showed a clear separation by season of seagrass samples, both for presence/absence and abundance data (Fig. 8a,c), while sand samples showed some seasonal overlap, especially for presence/absence data (Fig. 8b,d). ANOSIM revealed an overall significant seasonal effect on the fish assemblage structure for both sites, with significant differences between all pairwise seasonal comparisons, except for autumn and winter in the sand (Table 7). ANOSIM revealed no significant differences in fish assemblage structure associated with tidal effect for seagrass (R-statistic ¼ 0.053, P ¼ 0.069) or sand (R-statistic ¼ 0.005, P ¼ 0.337), and no significant differences in fish assemblage structure associated with diel effect for seagrass (R-statistic ¼ 0.023, P ¼ 0.184) or sand (R-statistic ¼ 0.029, P ¼ 0.112). 4. Discussion 4.1. Site differences

Low tide

High tide

Fig. 4. Mean number of fish over seagrass and sand across at high and low tide. Error bars represent þ1 SE and unlike letters denote seasons that differed statistically from each other in Tukey HSD test.

The fish fauna of Ria Formosa was more diverse and considerably more abundant over seagrass than over sand, as generally reported in many studies elsewhere (e.g. Heck

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(a) 900 Winter

Spring

Summer

Autumn

Mean number of fish

800 700 600 500 400 300 200 100 0

Low tide

High tide

Low tide

High tide

Low tide

High tide

Low tide

High tide

(b) 90 Winter

Spring

Summer

Autumn

Mean number of fish

80 70 60 50 40 30 20 10 0

Low tide

High tide

Low tide

High tide

Low tide

High tide

Low tide

High tide

Fig. 5. Mean number of fish over seagrass (a) and sand (b) across season, tide stage and diel period. Error bars represent þ1 SE. White bars e day samples and dark bars e night samples.

et al., 1989; Sogard and Able, 1991; Connolly, 1994a; Gray et al., 1996; Guidetti, 2000; Travers and Potter, 2002). Previously, Monteiro et al. (1990) found that the fish assemblages associated with seagrass were more diverse and abundant than other habitat types inside the Ria Formosa. These differences in fish diversity and abundance are likely due to higher structural complexity and higher productivity of the seagrass beds compared to unvegetated areas, providing protection and shelter from predators (Stoner, 1983; Orth et al., 1984; Pollard, 1984; Bell and Pollard, 1989; Connolly, 1994a) and offering higher food availability and diversity (Burchmore et al., 1984; Connolly, 1994b). In the Ria Formosa, Calva´rio (unpublished data) found that invertebrate communities of

subtidal seagrass habitats were more diverse and abundant than those of subtidal sand, in part due to an important presence of detritivorous and herbivorous fauna associated with structural elements of the macrophytes (e.g. leaves and rhizomes). In the Ria Formosa, fish assemblage structures associated with seagrass also differed from those found over sand, like in other parts of the world (e.g. Gray et al., 1996; Jenkins et al., 1997; Gray et al., 1998). The multivariate analyses showed that site-related differences were greater than any seasonal, tidal or diel variation, with several species occurring consistently in only one site, or predominantly caught in one site, indicating that different types of fish species were

Table 3 F-values and significance levels for three-way ANOVAs of mean number of fish of 10 most numerically abundant species in seagrass, testing for differences between season (S), tide (T) and diel (D). *P < 0.05; **P < 0.01; ***P < 0.001; (ns) not significant Species

Season (S)

Tide (T)

Diel (D)

ST

SD

TD

STD

D. annularis D. vulgaris G. couchi G. niger G. paganellus H. didactylus H. guttulatus S. cantharus S. bailloni S. cinereus

19.905*** 465.828*** 36.492*** 9.257*** 20.581*** 45.788*** 8.970*** 11.151*** 61.273*** 8.308***

4.186* 10.557** 8.736** 31.126*** 7.547** 17.902*** 0.045 (ns) 4.602* 5.102* 5.062*

1.744 (ns) 0.645 (ns) 0.785 (ns) 0.311 (ns) 1.042 (ns) 6.404** 1.463 (ns) 2.003 (ns) 0.689 (ns) 2.737 (ns)

1.150 (ns) 8.065*** 3.103* 0.792 (ns) 1.900 (ns) 1.986 (ns) 0.783 (ns) 1.558 (ns) 1.961 (ns) 0.518 (ns)

6.662*** 3.851* 0.382 (ns) 1.946 (ns) 2.335 (ns) 4.720** 1.115 (ns) 1.738 (ns) 2.559 (ns) 0.900 (ns)

7.053* 0.594 (ns) 1.046 (ns) 1.470 (ns) 0.189 (ns) 0.057 (ns) 2.107 (ns) 0.012 (ns) 1.551 (ns) 0.003 (ns)

3.561 2.924 2.466 3.361 3.247 2.648 0.553 0.303 1.090 0.332

(ns) (ns) (ns) (ns) (ns) (ns) (ns) (ns) (ns) (ns)

468

Table 4 List of the most abundant species caught in the seagrass site, by season, tidal stage and diel period, presenting their absolute (n) and relative (n%) abundance, and frequency of occurrence ( f %) Species

Season

Tide

Spring n

f(%)

n

Autumn n(%)

f(%)

n

Winter n(%)

f(%)

n

13 16

0.30 0.36

50.0 50.0

51 1

1.03 0.02

91.7 8.3

0 5

e 0.15

0.0 25.0

0 0

188

4.27

91.7

391

7.87

91.7

51

1.51

75.0

20

0.0

98

1.97

91.7

7

0.21

41.7

0

0

e

High n(%)

f(%)

Low n(%)

n

Day n(%)

n

Night n(%)

n

n(%)

0.0 0.0

38 8

0.63 0.13

26 14

0.27 0.14

32 20

0.39 0.25

32 2

0.42 0.03

58.3

228

3.80

422

4.31

327

4.02

323

4.21

0.0

44

0.73

61

0.62

60

0.74

45

0.59

e e 0.66

n

e

11 822 220 1847 218

0.25 18.66 5.00 41.94 4.95

66.7 100.0 91.7 100.0 100.0

15 50 10 652 1503

0.30 1.01 0.20 13.12 30.24

50.0 91.7 58.3 100.0 100.0

20 1 11 1161 731

0.59 0.03 0.33 34.4 21.66

66.7 8.3 33.3 100.0 100.0

2 0 43 1420 399

0.07 e 1.41 46.6 13.09

16.7 0.0 91.7 100.0 100.0

12 327 93 1639 1085

0.20 5.44 1.55 27.28 18.06

36 546 191 3441 1766

0.37 5.58 1.95 35.15 18.04

26 385 139 2443 1368

0.32 4.73 1.71 30.04 16.82

22 488 145 2637 1483

0.29 6.37 1.89 34.41 19.35

50

1.14

83.3

405

8.15

100.0

126

3.73

100.0

40

1.31

83.3

202

3.36

419

4.28

292

3.59

329

4.29

86

1.95

100.0

44

0.89

75.0

19

0.56

83.3

74

2.43

100.0

105

1.75

118

1.21

123

1.51

100

1.30

26

0.59

58.3

2

0.04

8.3

0

0.0

0

0.0

18

0.30

10

0.10

22

0.27

6

0.08

41 9

0.93 0.20

66.7 33.3

0 23

e 0.46

0.0 58.3

0 24

e 0.71

0.0 83.3

9 1

0.30 0.03

16.7 8.3

22 31

0.37 0.52

28 26

0.29 0.27

8 24

0.10 0.30

42 33

0.55 0.43

473

10.74

100.0

504

10.14

100.0

74

2.19

100.0

6

0.20

25.0

460

7.66

597

6.10

639

7.86

418

5.45

19

0.43

66.7

242

4.87

100.0

38

1.13

100.0

3

0.01

16.7

125

2.08

177

1.81

181

2.23

121

1.58

312

7.08

880

17.71

100.0

1017

30.13

100.0

942

30.92

100.0

1407

23.42

1744

17.82

1861

22.88

1290

16.83

15

0.34

75.0

39

0.78

100.0

36

1.07

83.3

43

1.41

100.0

64

1.07

69

0.70

82

1.01

51

0.67

15

0.34

75.0

21

0.42

50.0

34

1.01

91.7

40

1.31

91.7

55

0.92

55

0.56

58

0.71

52

0.68

100

e

e

Total no. of individuals Total no. of species

4404

e

e

4970

e

e

3375

e

e

3047

e

e

6235

e

9561

e

8132

e

7664

e

29

e

e

32

e

e

23

e

e

18

e

e

35

e

37

e

37

e

35

e

Resident Marine juvenile migrants Marine adventitious

2786 1600

63.3 36.3

e e

3413 1491

68.7 30.0

e e

3065 303

90.8 8.0

e e

2964 79

97.3 2.6

e e

4844 1340

77.7 21.5

7384 2133

77.2 22.3

6319 1762

77.7 21.7

5909 1711

77.1 22.3

5

0.1

e

15

0.3

e

7

0.2

e

4

0.1

e

13

0.2

18

0.2

19

0.2

12

0.2

J. Ribeiro et al. / Estuarine, Coastal and Shelf Science 67 (2006) 461e474

Anguilla anguilla Diplecogaster bimaculata Diplodus annularis Diplodus bellottii Diplodus sargus Diplodus vulgaris Gobius couchi Gobius niger Gobius paganellus Halobatrachus didactylus Hippocampus guttulatus Pomatoschistus microps Sarpa salpa Scorpaena porcus Spondyliosoma cantharus Symphodus bailloni Symphodus cinereus Syngnathus acus Syngnathus typhle

Summer n(%)

Diel

J. Ribeiro et al. / Estuarine, Coastal and Shelf Science 67 (2006) 461e474

469

Table 5 F-values and significance levels for three-way ANOVAs of mean number of fish of 10 most numerically abundant species in sand, testing for differences between season (S), tide (T) and diel (D). *P < 0.05; **P < 0.01; ***P < 0.001; (ns) not significant Species

Season (S)

Tide (T)

Diel (D)

ST

SD

TD

STD

B. podas C. maculatus D. vulgaris E. vipera G. niger G. papganellus P. microps P. minutus S. lascaris S. bailloni

11.971*** 0.447 (ns) 8.782*** 16.87*** 11.095*** 4.231* 29.344*** 96.590*** 3.455* 3.237*

4.261* 2.750 (ns) 7.750** 23.439*** 4.538* 0.338 (ns) 15.044*** 3.490 (ns) 0.727 (ns) 1.306 (ns)

0.087 (ns) 2.750 (ns) 2.331 (ns) 37.098*** 2.579 (ns) 0.043 (ns) 3.967 (ns) 10.990** 2.909 (ns) 5.226*

2.232 (ns) 2.750 (ns) 6.503*** 11.732*** 3.424* 0.396 (ns) 13.989*** 5.880** 0.121 (ns) 2.758 (ns)

0.841 (ns) 0.568 (ns) 0.825 (ns) 19.667*** 3.659* 0.303 (ns) 4.553* 22.600*** 1.576 (ns) 3.366*

2.174 (ns) 3.841 (ns) 2.331 (ns) 12.902*** 0.671 (ns) 0.051 (ns) 10.560** 0.130 (ns) 0.182 (ns) 1.306 (ns)

1.768 (ns) 1.538 (ns) 1.212 (ns) 11.211*** 1.195 (ns) 0.300 (ns) 11.498*** 2.720 (ns) 0.303 (ns) 2.242 (ns)

associated with these two sites. The dominance of benthic species like Arnoglossus thori, Bothus podas, Callionymus maculatus, Echiichthys vipera, Mullus surmuletus, Solea lascaris and Pomatoschistus minutus, observed only in sand show a clear adaptation of the fish assemblage to exposed hydrodynamic conditions, associated with this site. These conditions favour the settlement of benthic species that avoid strong tidal currents by close association with the sandy bottom. In contrast, the seagrass site located over muddy sediment is associated with weaker current velocities, allowing the settlement of epibenthic fish along with benthic fish species. These conditions explain the important presence of species with poor mobility, like syngnathids and young-of-the-year (YOY) of marine migrant species. The higher structural complexity also enhances settlement capabilities, working like a trap for YOY (Bell et al., 1987) and allowing the attachment of syngnathids to the leaves and rhizomes (Howard and Koehn, 1985). The benthic fish assemblage also differs from sand, with larger gobids like Gobius niger and Gobius paganellus, dominating this part of the assemblage. The high abundance of YOY in the seagrass, almost 20 times higher than in the sand, is clear evidence that seagrass is an important habitat for juvenile fish, in particular commercially important species like sparids. Structural complexity may aid the settlement of YOY by providing protection against predation, food and enhancing early growth and survival. The sand site, in spite of the low abundance of YOY, is nevertheless an important habitat for juvenile fish from a different suite of species including Callionymus maculatus, Echiichthys vipera, Mullus surmuletus and Solea lascaris. 4.2. Seasonal changes The seasonal patterns in fish assemblage structure, with increased number of species and fish in the spring and summer, were consistent with the findings of other studies in the Ria Formosa (Monteiro et al., 1987), and elsewhere in estuaries and other temperate shallow habitats (e.g. Nash and Gibson, 1982; Potter et al., 1986; Guidetti and Bessotti, 2000). The recruitment of marine juvenile migrant species during the spring and summer is consistent with the late winter and spring spawning season of most of these species (Gonc¸alves and

Erzini, 2000a,b). The decline in numbers of these fish species in autumn and winter suggests they may migrate to the adjacent coastal areas within their first year. The seasonal fluctuations in the abundance of the dominant resident species could also be attributed to their life cycle, since the majority of these species breed during the warmer seasons precisely when changes in their abundance occurs. Seasonal changes in fish assemblage structure in both sites is a consequence of the seasonal shifts in species abundance and species composition, reflecting both spawning events within the lagoon and seasonal movements to and from the adjacent marine environment (Livingston et al., 1976; Yoklavich et al., 1991; Potter et al., 1997; Jackson and Jones, 1999). 4.3. Tidal changes In the seagrass site, the tides affect the different species in a similar way, with the most important species having higher abundances at low tide than at high tide. Tidal changes in fish abundance could be due to the movement of fish from subtidal channels throughout the inundated intertidal areas with the flooding tide. This pattern in fish abundance along the tidal cycle has been reported for tidal flats and marshes located in estuarine areas, coastal lagoons and other shallow coastal areas (Kneib and Wagner, 1994; Rozas, 1995; Morrison et al., 2002; Greenwood and Hill, 2003). Other studies also reported that intertidal habitats are temporarily used by fish and other nekton during the period of submersion (e.g. Rey et al., 1990; Minello and Zimmerman, 1992; Rountree and Able, 1992; Rozas and Reed, 1993; Thomas and Connolly, 2001). The transversal movements to the intertidal habitats during the flood tide are generally explained by the fact that they allow fish to access the productive intertidal foraging grounds, only available during the periods of tidal inundation (Weisberg and Lotrich, 1982; Boesch and Turner, 1984; Rozas and Odum, 1988; Cattrijsse et al., 1994; Edgar and Shaw, 1995b). Several studies show that some fish species forage during their stay in intertidal areas (Kelley, 1988; Raffaelli et al., 1990; Laffaille et al., 1999), supporting the hypothesis that intertidal areas function as foraging grounds for fish. Calva´rio (unpublished data) found that number of species, density and biomass of benthic macroinvertebrate in the intertidal areas of the Ria Formosa were higher than in subtidal areas,

470

Table 6 List of the most abundant species caught in the sand site, by season, tidal stage and diel period, presenting their absolute (n) and relative (n%) abundance, and frequency of occurrence ( f %) Species

Season

Tide

Spring n

f(%)

n

Autumn n(%)

f(%)

n

Winter n(%)

f(%)

n

High n(%)

f(%)

n

Low n(%)

n

Day n(%)

n

Night n(%)

n

n(%)

11 2 10

1.51 0.28 1.38

58.3 8.3 50.0

6 25 12

2.11 8.80 4.23

25.0 66.7 50.0

2 3 8

1.05 1.57 4.19

8.3 25.0 41.7

0 0 7

e e 3.00

0.0 0.0 33.3

13 8 13

1.69 1.04 1.69

6 22 24

0.90 3.30 3.60

16 16 24

1.97 1.97 2.96

3 14 13

0.48 2.24 2.08

35 14 112 2 4

4.81 1.93 15.41 0.28 0.55

58.3 58.3 100.0 8.3 16.7

12 10 15 22 8

4.23 3.52 5.28 7.75 2.82

50.0 41.7 50.0 58.3 50.0

0 2 3 1 1

e 1.05 1.57 0.52 0.52

0.0 16.7 16.7 8.3 8.3

0 33 15 0 2

e 14.16 6.44 e 0.86

0 58.3 83.3 0.0 16.7

8 14 105 20 7

1.04 1.82 13.65 2.60 0.91

39 45 40 5 8

5.86 6.76 6.01 0.75 1.20

15 49 48 17 7

1.85 6.04 5.92 2.10 0.86

32 10 97 8 8

5.13 1.60 15.54 1.28 1.28

0 52

e 7.15

0.0 75.0

11 0

3.87 e

41.7 0.0

0 1

e 0.52

0.0 8.3

0 0

0.0 0.0

2 45

0.26 5.85

9 8

1.35 1.20

2 17

0.12 2.10

10 36

1.60 5.77

440

60.52

100.0

67

23.59

100.0

143

74.87

100.0

148

63.52

100.0

426

372

55.86

477

58.82

321

51.44

5

0.69

16.7

0

0.0

0

0.0

11

4.72

41.7

8

1.04

8

1.20

7

0.86

9

1.44

9 1

1.24 0.14

58.3 8.3

9 11

3.17 3.87

58.3 41.7

4 2

2.09 1.05

25.0 16.7

0 1

e 0.43

0.0 8.3

13 6

1.69 0.78

9 9

1.35 1.35

15 6

1.85 0.74

7 9

1.12 1.44

3

0.41

25.0

32

11.27

50.0

7

3.66

33.3

2

0.86

16.7

31

4.03

13

1.95

40

4.93

4

0.64

4

0.55

25.0

3

1.06

16.7

5

2.62

25.0

2

0.86

16.7

9

1.17

5

0.75

10

1.23

4

0.64

e

e

e e

55.4

Total no. of individuals Total no. of species

727

e

e

285

e

e

190

e

e

233

e

e

769

e

666

e

812

e

623

e

28

e

e

31

e

e

20

e

e

18

e

e

33

e

38

e

35

e

35

e

Resident Marine juvenile migrants Marine adventitious

634 46

87.2 6.3

e e

172 56

60.4 19.6

e e

164 9

86.3 4.7

e e

173 3

74.3 1.2

e e

673 36

87.5 4.7

470 78

70.6 11.7

652 49

80.3 6.0

491 65

78.8 10.4

47

6.5

e

57

20.0

e

17

9.0

e

57

24.5

e

60

7.8

118

17.7

111

13.7

67

10.8

J. Ribeiro et al. / Estuarine, Coastal and Shelf Science 67 (2006) 461e474

Arnoglossus thori Bothus podas Callionymus maculatus Diplodus vulgaris Echiichthys vipera Gobius niger Gobius paganellus Hippocampus guttulatus Mullus surmuletus Pomatoschistus microps Pomatoschistus minutus Pomatoschistus pictus Solea lascaris Spondyliosoma cantharus Symphodus bailloni Symphodus cinereus

Summer n(%)

Diel

J. Ribeiro et al. / Estuarine, Coastal and Shelf Science 67 (2006) 461e474

(a) Percentage of fish number

100 Vertical distribution guilds

80

EB

60 40 B

20 0 Sand

Seagrass

Percentage of fish number

(b) 100 Ecological guilds

80

R

60

MA

40 MJM

20 0 Sand

471

to the immersed intertidal areas. The habitat and benthic macroinvertebrate homogeneity of sand subtidal habitat and the surrounding intertidal areas (Calva´rio, unpublished data), along with the low fish density, seems not to offer any additional advantage in terms of dispersal foraging and predation avoidance. However, the fish functional organization suffers some tidal changes, with a higher proportion of marine species (marine adventitious and marine juvenile migrants) observed at low tide, and a higher proportion of resident species at high tide. Since the high tide sampling took place at the beginning of ebb tide, and the low tide sampling was at the beginning of the flood tide, it seems plausible that the direction of a relatively intense tidal current, due to the close presence of an inlet, was the main factor explaining the observed tidal changes in sand fish community organization. The longitudinal movement of the water from the coastal areas into the lagoon during the flood tide facilitates the immigration of fish from the surrounding coastal areas, followed by their emigration on the ebb tide (Greenwood and Hill, 2003). On the other hand, the flood tide tends to push the resident species towards the interior of the lagoon, while the ebb tends to drag them to more peripherical areas.

Seagrass

Fig. 6. Percentage of fish number in each guild, over sand and seagrass sites: (a) vertical distribution guilds (B e benthic; EB e epibenthic); and (b) ecological guilds (R e resident; MA e marine adventitious; MJM e marine juvenile migrant).

suggesting that fish feeding activities may play an important role in recycling the intertidal productivity within the coastal lagoon. These foraging activities allow energy transfer between intertidal benthic invertebrate assemblages and fish consumers (Kneib, 1997). Protection from predation is also an argument used to explain these tidal-related movements (Minello and Zimmerman, 1983; Boesch and Turner, 1984; Kneib, 1987; Rozas and Odum, 1988). Although the immersed area of the Ria Formosa coastal lagoon increases by up to 5
times during the high tide (Aguas, 1986), the fish abundance in the subtidal channel only declines by 1.5e2 times, suggesting that most of the fish species probably only use the adjacent intertidal areas close to the edge of the subtidal channels (Kneib and Wagner, 1994). In contrast, on sand there was no evidence of tidal changes in fish assemblage structure, number of species or in general fish abundance that supports the possibility of dispersal movements

4.4. Diel changes The number of species and fish abundance, as well as the fish assemblage structure associated with both sites did not differ substantially between day and night. These results are consistent with those found by several authors in estuarine vegetated habitats in Australia (Gray et al., 1996; Gray et al., 1998). However, others studies reported diel changes in certain species abundance, and/or greater overall fish abundances and number of species at night in seagrass (e.g. Adams, 1976; Horn, 1979; Robblee and Zieman, 1984; Mattila et al., 1999; Guest et al., 2003), and over sand in various shallow marine and estuarine environments (Gray et al., 1998; Methven et al., 2001; Travers and Potter, 2002; Guest et al., 2003; Pessanha and Arau´jo, 2003; Pessanha et al., 2003). The absence of significant diel changes in the fish assemblage and the observation of fish movements associated with tidal rhythm, suggest that the tide pulse is the major effect responsible for daily fluctuations in the fish community of the Ria Formosa coastal lagoon. This is an expected result since this ecosystem is affected by a semi-diurnal mesotidal regime, where approximately 70e80% of its surface represents a very

Fig. 7. Non-metric multi-dimensional scaling ordination plots of the presence/absence data (a) and abundance data (b). Stress values are given in the top right corner of each plot. (:) e Sand samples and (P) e seagrass samples.

J. Ribeiro et al. / Estuarine, Coastal and Shelf Science 67 (2006) 461e474

472

Fig. 8. Non-metric multi-dimensional scaling ordination plots of the presence/absence data for seagrass (a) and sand (b); and of the abundance data for seagrass (c) and sand samples (d), both classified by season. Stress values are given in the top right corner of each plot. (-) spring; ( ) summer; (P) autumn; (:) winter.

productive intertidal area that functions as an important feeding ground. The imposition of a diel rhythm over a tidal one would mean that many foraging opportunities would be lost. In the summer, when the days are longer, this would be particularly critical for species that only used the intertidal areas during the night. 5. Conclusions The fish assemblages associated with seagrass and sand sites were substantially different, both in terms of species composition and their relative abundance. Structurally more complex, the seagrass supports a much more abundant and diverse fish community, and was an important juvenile fish habitat for more species than sand. These site-related differences were greater than any seasonal, tidal or diel variations in fish assemblages, suggesting that the habitat type (e.g. degree of structural complexity, sediment type, topography) might have had an important role in the definition of the fish Table 7 Results of ANOSIM tests, with overall and the pairwise for differences amongst the seasonal combinations in both sites Seasons comparisons

Sand R-statistic

P-value

Seagrass R-statistic

P-value

Overall

0.531

P < 0.001

0.831

P < 0.001

Winteresummer Winterespring Wintereautumn Autumnesummer Autumnespring Summerespring

0.637 0.756 0.209 0.492 0.747 0.953

P < 0.001 P < 0.001 P ¼ 0.090 P < 0.001 P < 0.001 P < 0.001

0.953 0.923 0.440 0.615 0.940 0.957

P < 0.001 P < 0.001 P < 0.001 P < 0.001 P < 0.001 P < 0.001

assemblage structure in the Ria Formosa coastal lagoon. In spite of these differences, both sites showed similar seasonal changes in the fish assemblage structure. These seasonal patterns in the fish assemblages were related to ontogenic shifts in the presence and abundance of marine juvenile migrant species, mainly due to reproduction timing and large-scale movements, to and from the adjacent marine environment. On the other hand, small-scale temporal changes in fish assemblages appear related to tidal and diel cycles, which may be related to small-scale movements associated with feeding, shelter usage and predator avoidance. In the Ria Formosa these smallscale movements are mainly associated with tidal rhythm rather than diel rhythm. Acknowledgements This research was funded in part by the European Commission (EC-DG XIV/C1; Study project no. 99/061) and was also sponsored by the Fundac¸~ao para Cieˆncia e Tecnologia through a PhD grant awarded to the first author (grant reference: SFRH/BD/6812/2001, Portuguese Ministry of Science and Technology). The authors would like to thank to all the colleagues and volunteers who assisted with the field sampling and laboratory work and also to the fishing boat skipper Isidoro Costa. References Adams, S.M., 1976. The ecology of eelgrass, Zostera marina (L.), fish communities, I. Structural analysis. Journal of Experimental Marine Biology and Ecology 22, 269e291.
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