Benthic dynamics within a land-based semi-intensiveaquaculture fish farm: the importance of settlementponds

Susana Carvalho Æ Manuela Falcao Æ Joao Curdia Æ Ana Moura ÆDalila Serpa Æ Miguel B. Gaspar Æ Maria Teresa Dinis ÆPedro Pousao-Ferreira Æ Luıs Cancela da Fonseca

Received: 8 February 2008 / Accepted: 6 October 2008 / Published online: 31 October 2008� Springer Science+Business Media B.V. 2008

Abstract The present work aims to assess the importance of settlement ponds (SP) in

semi-intensive fish farms by studying benthic dynamics in an aquaculture fish farm, more

specifically in the water reservoir (WR) and SP and also in production (P) and nonpro-

duction (C) ponds during a 16-month period. In Portugal, a SP is only mandatory for

intensive fish farms, and another objective of the present study is to assess the importance

of these areas in semi-intensive fish farms. The WR was the area with highest diversity and

evenness, as well as the higher number of exclusive taxa and taxa sensitive to organic

enrichment. P and SP samples showed signs of higher disturbance levels, emphasized

namely by the association of the opportunistic annelids Capitella spp. and Tubificidae.

However, the benthic data from SP points to lower disturbance levels than P both due to an

increase in the percentage of sensitive taxa observed in June and October 2004 and by the

association of this latter sample with water reservoir samples as evidenced by canonical

correspondence analysis. Moreover, a higher and increasing number of taxa when com-

pared with the P area were also observed. Therefore, in semi-intensive fish farms, where

effluents from P ponds are directly discharged to the lagoon, the potential environmental

impacts would be more severe. In conclusion, the imposition of SP in semi-intensive fish

farms should be considered, especially because most fish farms are located within relevant

wetland areas.

S. Carvalho (&) � M. Falcao � J. Curdia � A. Moura � D. Serpa � M. B. Gaspar � P. Pousao-FerreiraInstituto Nacional de Recursos Biologicos (INRB, I.P.)/IPIMAR,Av. 5 de Outubro, 8700-305 Olhao, Portugale-mail: scarvalho@cripsul.ipimar.pt

M. T. DinisCCMAR-FCMA, Campus de Gambelas, 8005-139 Gambelas, Portugal

L. Cancela da FonsecaFCMA, Universidade do Algarve, Campus de Gambelas, 8005-139 Gambelas, Portugal

L. Cancela da FonsecaLaboratorio Marıtimo da Guia/Centro de Oceanografia (FCUL),Av. N. Sra. Do Cabo, 939, 2750-374 Cascais, Portugal

123

Aquacult Int (2009) 17:571–587DOI 10.1007/s10499-008-9227-1

Keywords Settlement ponds � Macrobenthic communities � Organic enrichment �Fish farming � Southern Portugal

Introduction

Currently, in Portugal most of land-based marine fish farming is undertaken within

earthen ponds under semi-intensive conditions. Nevertheless, as in other parts of the

world, little information is available regarding benthic processes (either biological or

geochemical) occurring in such production conditions (e.g. Hussenot and Martin 1995;

Riise and Roos 1997; Ganguly et al. 1999; Nunes and Parsons 2000; Tovar et al. 2000;

Mohanty 2001; Martınez-Cordova and Pena-Messina 2005; Heilskov et al. 2006; Carv-

alho et al. 2007). Most of these studies concern shrimp production and were not

undertaken in Europe. The impacts of fish farm production have mainly been focused on

offshore or floating cages in estuaries and bays (e.g. Hall et al. 1990; Findlay et al. 1995;

Troell and Berg 1997; Karakassis et al. 1999, 2000; Butler et al. 2001; Chamberlain

et al. 2001; Pohle et al. 2001; Katz et al. 2002; Vezzulli et al. 2002; Chou et al. 2004;

Pereira et al. 2004; Islam 2005; Tomassetti and Porrello 2005; Kalantzi and Karakassis

2006; Mente et al. 2006).

Fish production may have a strong negative effect on natural fish populations as a

consequence of the enormous needs of fish (from natural stocks) to be converted into

farmed fish feed (Naylor et al. 2000) and on the deterioration of coastal areas due to high

loads of organic matter and nutrients resulting from fish production (Hall et al. 1990,

1992; Holby and Hall 1991; Holmer and Kristensen 1992; Karakassis et al. 1998;

Christensen et al. 2000). The changes observed in sediment chemistry affect benthic

communities, usually by reducing species richness and biomass and increasing abun-

dance values (Weston 1990). This is a consequence of the enhancement of both aerobic

and anaerobic microbial activity in organically enriched sediments, resulting in dissolved

oxygen depletion and production of toxic products such as H2S (Holmer and Kristensen

1992). As a consequence, benthic fauna may completely disappear, creating an azoic

zone (Heilskov and Holmer 2001). This is of major concern as it is widely recognised

that benthic fauna plays an important role both in supplying and mineralising organic

matter (Heilskov and Holmer 2001), but can also act as food resource for the cultivated

fish (Gamito 1997). Therefore, the analysis of benthic communities in fish farm sedi-

ments may be valuable to assess the evolution of environmental quality within fish ponds

and settlement ponds as well as the importance of the latter. Moreover, fish production in

land-based fish farms involves large costs, namely in terms of water demand, oxygen

supply, food, antibiotics and electricity. They are also costly in terms of human

resources, as fish ponds require daily management due to the rapid growth of several

types of primary producers that must be removed to allow water circulation and avoid

oxygen depletion (Bartoli et al. 2005).

Environmental concern about the impacts resulting from fish farming has increased

during the last decades. For example, in 1993 decision makers from the Orbetello area

imposed the construction of phytotreatment ponds between fish farms and the lagoon in

order to decrease organic and nitrogen loadings (e.g. Porrello et al. 2003b). In these ponds,

high levels of nitrogen and phosphorous enhance rapid growth rates of algal macrovege-

tation, which remove N and P from the fish farm effluent (Porrello et al. 2003b). However,

as these ponds are not managed, this positive effect is lost in summer when vegetation dies

572 Aquacult Int (2009) 17:571–587

123

and its mineralization results in the release of N and P (Porrello et al. 2003b). These

authors found that the control of Ulva rigida standing stocks eliminating the excess bio-

mass may represent a successful approach to improve the reduction of N values (Porrello

et al. 2003a). Also, in shrimp farms in Thailand, the local department of fisheries are

encouraging shrimp farmers to use settlement ponds in order to improve the quality of

effluents (Ehler et al. 2007). These authors have shown that, with this strategy, nitrogen

concentrations in the water column will be reduced. Sediment must, however, be managed

to reduce remineralization during successive cropping cycles (Ehler et al. 2007). Man-

agement options proposed by these authors included periodical removal of settlement pond

sludge or drying ponds between crops. In the same study, it was also observed that adding

coconut fronds to the settlement ponds enhanced N removal. Like with the Ulva, vegetal

cover must be regularly removed to maintain efficiency. Experimental studies should be

undertaken in other systems in order to confirm these results. However, based on the

present and previous studies, it appears that the combination effect of settlement ponds and

a controlled used of macrovegetation within these areas, associated with a proper man-

agement scheme, would be encouraging in order to reduce the detrimental impacts

resulting from fish farming. Currently in Portugal settlement ponds are only mandatory for

intensive production. In semi-intensive fish farms effluents are directly discharged to the

adjacent lagoon channel. The purpose of the settlement ponds in a fish farm is to allow

organically rich particles in suspension to settle and avoid the discharge of water with high

organic loads into the main ecosystem. This is particularly important as the majority of fish

farms in Portugal (and probably worldwide) are located within important wetlands, some

of them protected by Portuguese law (protected areas) and/or European Directives. The

present work aims to assess the importance of settlement ponds in semi-intensive fish farms

by studying benthic dynamics in an aquaculture fish farm, more specifically in the water

reservoir and settlement pond, and also in production and nonproduction ponds (control)

during a 16-month period.

Materials and methods

Sampling strategy

The present study was undertaken within the Olhao Fish Culture Experimental Station,

located in the Ria Formosa Lagoon (southern Portugal, Fig. 1). Sampling was carried out

during a 16-month period (June 2003 to October 2004) at four different areas within an

aquaculture fish farm: the water reservoir (WR), the settlement pond (SP), a 400-m2 white

seabream [Diplodus sargus (Linnaeus, 1758)] semi-intensive production area (P) and a

similar area with no production, designated as control (C). In both ponds, the daily water

turnover rate varied between 20% and 40%, depending on water temperature and fish

biomass (in the case of the P area). Fish from the P area were fed with dry pellets every

hour for 15 min, between sunrise and sunset, using an automatic feeder. At the production

area the rearing of approximately 3,000 fish started on June 12, 2003. Both production and

control areas present similar conditions of water renewal and are filled with seawater

pumped from the WR. At the beginning of the experiment no animal life was present in P

and C ponds. The WR and SP, however, had already been filled for 6 months. Sampling

was undertaken in June, July, August and November 2003, and March, June and October

2004, following a D. sargus production cycle.

Aquacult Int (2009) 17:571–587 573

123

Macrobenthic communities

For each sampling period and area, three replicates were collected randomly using hand

corers (0.02 m2 total area per replicate). The macrofaunal samples were washed through a

0.5-mm square mesh sieve, and the retained material was preserved in 4% buffered

formaldehyde stained with Rose Bengal. In the laboratory, animals were hand-sorted into

major taxonomic groups, identified to the lowest practical taxonomic level and counted.

Environmental procedures

At each area, three sediment cores per replicate (PVC tubes of 15 cm length and 5 cm

diameter) and overlying water samples were collected by scuba divers. Sediment sampling

was carried out by carefully pushing the open-ended PVC tube into the sediment in order to

Fig. 1 A Ria Formosa Lagoon, southern coast of Portugal: location of the studied aquaculture fish farm.B Schematic layout of the aquaculture fish farm. WR water reservoir, SP settlement pond, P production area,C control area. PS pumping system, IFW inflowing water, OFW outflowing water

574 Aquacult Int (2009) 17:571–587

123

prevent any disturbance of sediment layers. Overlying water was collected 2 cm above the

sediment surface directed with precleaned syringes.

In laboratory, sediment cores were sliced in 2-cm layers, and samples were centrifuged

for 10 min at 3,000 rpm (1,600g) to separate pore-water from solid fraction. Prior to

analysis, pore-water and overlying water samples were filtered with 0.45-lm Macherey-

Nagel filters. Samples were analysed for ammonium (NH4?) and phosphate (HPO4

2-) using

a Skalar autoanalyser according to the Grasshoff (1983) methodology. Suspended partic-

ulate matter retained in glass-fibre filters was analysed for organic matter content, based on

weight loss after ignition at 450�C for 3 h. The upper sediment layer (0–2 cm) was dried to

80�C to constant weight and ground to a fine powder for determination of total organic

carbon (TOC) using a CNH analyser (NC 2500 CE instruments) with acetanilide as ref-

erence material (Byers et al. 1978). Chlorophyll a (chl a) and phaeopigments (Phaeop)

were extracted with acetone (90%) and determined by fluorimetry according to Parsons

et al. (1984). Sediment porosity was calculated from sediment weight loss at 105�C.

Data analysis

Faunal data were analysed for mean density, mean number of species (S), diversity

(Shannon–Wiener index H0, log2) and equitability (J0). These variables were calculated for

each sampling area and period. Multivariate analyses were performed using PRIMER v5.0

software (Clarke and Gorley 2001). Faunal data was analysed by ordination techniques

(nonmetric multidimensional scaling, MDS) based on Bray–Curtis similarity coefficient

after log(x ? 1) transformation. Each identified species was assigned to one of the five

ecological groups proposed by the marine biotic index AMBI based upon the list available

from the AMBI webpage (http://www.azti.es). The classification of species behaviour is

mainly related to their sensitivity to organic enrichment. Associations between assemblage

patterns and environmental parameters were analysed by canonical correspondence anal-

ysis (CCA), using the CANOCO v.4.5 program. A matrix of explanatory variables was

constructed to evaluate correlations between environmental parameters, species and vari-

ance in site patterns. This matrix comprised the following environmental variables:

suspended particles, chl a content, phaeo content, total organic carbon, sediment porosity,

NH4? concentration in pore-water, NH4

? concentration in overlying water, HPO42- con-

centration in pore-water and HPO42- concentration in overlying water. Monte Carlo

permutation tests were used to check the statistical validity of these associations. The

analyses were carried out using square-root-transformed abundances. The percentage

variability explained by the canonical correspondence analysis was determined by dividing

the sum of all canonical eigenvalues by the overall sum of eigenvalues from the corre-

spondence analysis (ter Braak and Verdonschot 1995).

Results

Water reservoir

In this area 101 taxa were identified, corresponding to a total of 5,948 individuals. Nev-

ertheless, 12 taxa were responsible for more than 90% of the total abundance, namely:

Microdeutopus gryllotalpa Da Costa, 1853, Pseudopolydora paucibranchiata (Okuda,

1937), Chironomidae, Capitella spp., Cerastoderma spp., Hydroides elegans (Haswell,

1883), Hydrobia ulvae (Pennant, 1777), Anthozoa, Bittium reticulatum (Da Costa, 1778),

Aquacult Int (2009) 17:571–587 575

123

Abra ovata (Philippi, 1836), Akera bullata O. F. Muller, 1776 and Gammarus insensibilisStock, 1966. The two first species were clearly dominant, presenting 1,476 and 1,361

individuals, respectively. However, their abundance decreased during the study period. M.gryllotalpa attained a peak of abundance in August 2003 (192.0 ± 209.6 ind. 9 0.02 m-2)

and P. paucibranchiata reached a maximum in July 2003 (141.7 ± 66.6 ind. 9 0.02 m-2)

(Table 1). The taxa Jujubinus striatus (Linnaeus, 1758), Ruditapes decussatus (Linnaeus,

1758), Heteromastus filiformis (Claparede, 1864), Spirorbidae, Gammarella fucicola(Leach, 1814), Lumbrineris gracilis (Ehlers, 1868) and Diopatra neapolitana Delle Chiaje,

1841 were also recorded among the most abundant species in some of the sampling periods

(Table 1). During the study period, the mean number of species did not present large

oscillations, varying from 14.0 ± 6.6 taxa 9 0.02 m-2 (June 2003) to 22.7 ± 2.9

taxa 9 0.02 m-2 (November 2003) (Fig. 2). In terms of abundance, an increase was

observed initially, reaching 457.0 ± 105.1 ind. 9 0.02 m-2 in July, but after November

2003 a generally decreasing trend was observed until the end of the study period (Fig. 2).

On the other hand, Shannon–Wiener diversity and Pielou’s equitability generally increased

from June 2003 until October 2004 (Fig. 2).

Settlement pond

The settlement pond was characterised by the taxa Capitella spp., M. gryllotalpa, Tubi-

ficidae, Neanthes caudata (Delle Chiaje, 1827), Desdemona ornata Banse, 1957 and

Chironomidae. Together, these six taxa (out of 43) accounted for more than 90% of the

total abundance (6,481 ind.). The polychaete Capitella spp. was clearly dominant, repre-

senting more than 50% of the total abundance (3,505 ind.), and did not show large

variability in abundance during the study period, except a slight decrease in October 2004

(Table 1). Concerning the biological variables analysed, the mean number of species

showed a general increasing trend. The exception was August 2003, when the minimum

value of 1.7 ± 0.6 taxa 9 0.02 m-2 was observed (Fig. 2). The diversity and evenness

indices presented a similar trend with extremely low values observed in August 2003

(Fig. 2). On the other hand, abundance showed some oscillations with a minimum in

November 2003 (118.3 ± 18.1 ind. 9 0.02 m-2) and maximum in March 2004

(491.3 ± 187.2 ind. 9 0.02 m-2) (Fig. 2).

Production area

A total of 4,951 individuals distributed in 29 taxa were collected within the production

area. The polychaetes Capitella spp. and P. paucibranchiata accounted for more than 90%

of total abundance. Capitella spp. was absent until August, reached a peak in November

(381.7 ± 117.4 ind. 9 0.02 m-2) and remained relatively high until the end of the study

period (Table 1). P. paucibranchiata showed higher abundance values in August 2003

(114.7 ± 38.4 ind. 9 0.02 m-2). The number of species was rather constant but also low,

never reaching more than 6.0 ± 1.7 taxa 9 0.02 m-2 (October 2004) (Fig. 2). Abundance

was very low in the two first sampling periods, increasing afterwards with some fluctua-

tions (Fig. 2). Diversity and evenness indices showed similar temporal patterns with a peak

in July 2003 (H0 = 1.71 ± 0.24; J0 = 0.85 ± 0.12) and a minimum in November 2003 for

diversity (0.37 ± 0.18) and June 2004 for evenness (0.16 ± 0.05), with values increasing

again in October 2004 (Fig. 2).

576 Aquacult Int (2009) 17:571–587

123

Ta

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Aquacult Int (2009) 17:571–587 577

123

Ta

ble

1co

nti

nu

ed

Mar

-04

Jun

-04

Oct

-04

Ta

xaN

Cu

m%

Ta

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Cu

m%

Ta

xaN

Cum

%

WR M

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ryll

ota

lpa

68

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9.6

M.

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llo

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0.0

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Cap

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Chir

on

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iro

no

mid

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9.0

78

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4.6

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itel

lasp

p.

14

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5.1

M.

gry

llo

talp

a2

1.0

90

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.g

ryll

ota

lpa

6.7

86

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B.

reti

cula

tum

8.0

10

0.0

WR

Wat

erre

serv

oir

;S

PS

ettl

emen

tpond;

PP

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ctio

nar

ea;

CC

on

tro

lar

ea

578 Aquacult Int (2009) 17:571–587

123

Control area

In this area 32 taxa were collected, totalling 2,941 individuals. Four taxa (Chironomidae,

Cerastoderma spp., Capitella spp. and M. gryllotalpa) were responsible for more than 90%

of total abundance. The insects and the bivalves were visibly dominant, presenting a total

abundance of 1,699 and 843 individuals, respectively. Regarding Cerastoderma spp., this

genus showed a clear drop from July 2003 (161.0 ± 116.1 ind. 9 0.02 m-2) to August

(1.0 ± 1.7 ind. 9 0.02 m-2), and subsequent recovery was not observed until the end of

the study period. Concerning the biological variables, the number of species was low and

more or less constant in this area (Fig. 2). On the other hand, abundance was initially high,

mainly due to chironomids and Cerastoderma spp., but decreasing after July, following the

abundance decrease of the bivalves (Fig. 2; Table 1) and remained relatively constant from

November 2003 to October 2004 (Fig. 2). A peak of diversity and evenness was observed

in March 2004 (H0 = 1.80 ± 0.48; J0 = 0.95 ± 0.04), while the minimum values were

recorded in August 2003 (H0 = 0.41 ± 0.33; J0 = 0.16 ± 0.09) (Fig. 2).

Community structure

The comparative analysis of the nonmetric MDS diagrams for each of the studied areas is

shown in Fig. 3. Two main groups could be distinguished in each area and the most

Fig. 2 Variation of the mean number of species (S, taxa 9 0.02 m-2), abundance (N, ind. 9 0.02 m-2),Shannon–Wiener diversity (H0) and Pielou’s equitability index (J0) during the sampling period. Vertical barsrepresent SD. WR water reservoir, SP settlement pond, P production area, C control area

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striking result was the separation between June and July 2003 samples from the others in

both SP and P areas (Fig. 3). Except for the October 2004 sampling period, the WR

showed less temporal variability when compared with the other areas. The C area samples

from 2003 appeared separated from those of 2004 (Fig. 3). The different patterns reflect

the dissimilarities in faunal composition and biological variables, as well as in the envi-

ronmental parameters. The CCA analysis of the species abundance data with stepwise

selection of environmental parameters retained three of these parameters: chl a, HPO42-

concentration in overlying water and porosity (Fig. 4). The first three axes of the CCA

diagram were statistically significant (axes 1 and 2, P \ 0.01; axis 3, P \ 0.05) and

presented the eigenvalues 0.276, 0.231 and 0.141, respectively, for a total inertia of 2.487,

therefore explaining 26.1% of the total variance of species data (Table 2). Cumulative

percentage of variance concerning species data was 26.1% (three first axes) and for spe-

cies-environment relation was 100% (Table 2).

The first ordination axis described a gradient from samples with high porosity and

HPO42- concentration in overlying water (negative end) to samples with high chl a. On the

other hand, the second ordination axis is mainly correlated to high concentrations of chl aand porosity. There was a clear pattern of species mainly associated to high chl a con-

centrations, such as the Tubificidae, D. ornata, G. insensibilis, N. caudata and Capitellaspp. (Fig. 4). Therefore, these species showed a high affinity to organically enriched

sediment with high microphytobenthos productivity. The species that are characteristic of

areas with less chl a values are mainly discriminated by porosity: the taxa Chironomidae,

Cerastoderma spp., P. paucibranchiata, Nemertini, H. elegans, B. reticulatum, Podarke sp.

Fig. 3 Cluster and MDS diagrams applying the Bray–Curtis similarity index after log(x ? 1) transforma-tion of the abundance data for each one of the analysed areas. WR water reservoir, SP settlement pond, Pproduction area, C control area

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and M. gryllotalpa were associated with samples of lower porosity, whereas A. bullata,

Corophium acherusicum (Costa, 1851), H. ulvae, Anthozoa and A. ovata were associated

with organically poor and coarser sediments (Fig. 4). The higher concentrations of HPO42-

were associated with samples from the WR and/or high-temperature sampling dates. This

association do not seem to have any relationship to fish production but with the increasing

availability of this parameter with increasing seawater temperature as observed by Serpa

et al. (2007a) for the Ria Formosa Lagoon. The WR is the area with more species, as the

majority of the represented species’ centroids are located more closely to the WR centroid

(Fig. 4). Both WR and C areas showed a lower temporal variability than that presented by

Fig. 4 Canonical correspondence analysis (CCA) ordination diagrams for macrobenthic species square-rootabundance data. For results of CCA see Table 2. Sample scores for each area and species scores along thefirst and second axes in relation to environmental parameters (Porosity, sediment porosity; chl a, chlorophylla concentration; HPO4

2- OW, HPO42- concentration in overlying water). h, water reservoir; j, settlement

pond; d, production area, s, control area. T1, T2, T3 and T4 represent June, July, August and November2003, respectively; T5, T6 and T7 represent March, June and October 2004, respectively. The vector linesreflect the relationship of significant environmental variables to the ordination axes, and their length isproportional to their relative significance. The orthogonal projection of a species point onto anenvironmental arrow represents the approximate centre of the species distribution along the particularenvironmental gradient. All species with more than eight individuals are presented

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the P and SP samples (Fig. 4). Two associations of samples should be mentioned: C and P

samples of June (first sampling period); and sample of October 2004 of the SP and sample

of June from the WR (Fig. 4).

Figure 5 shows the relative percentage of sensitive (I), indifferent (II), tolerant (III),

second-order opportunist (IV) and first-order opportunist (V) species per sampling period

and area. It is clear that the higher percentage of sensitive species was found in the WR,

which also presented the lowest percentage of first-order opportunists (Fig. 5). During

most of the sampling periods, SP was clearly dominated by first-order opportunists (mainly

Capitella spp.), but in June 2004 and in October 2004, a visible increase of sensitive

species was recorded (Fig. 5), indicating better quality of the benthic environment. The

production area was initially dominated by tolerant and second-order opportunists. How-

ever, after August 2003 and until the end of the study period first-order opportunists were

the main ecological group (Fig. 5). In the control area, only in November 2003 (22.7%)

and in March 2004 (31.4%) were first-order opportunists relatively well represented

(Fig. 5). Second-order opportunists were generally dominant, although after November

2003 a clear increase of sensitive species was observed (Fig. 5).

Discussion

Within land-based fish farms, the WR behave like small lagoons where there are one or

more openings to a tidal channel usually supporting macrofaunal communities that are

characteristic of estuarine-like systems (Gamito 1997, 2006). In fact the macrobenthic

communities of the WR analysed in the present study are common to those observed in Ria

Formosa Lagoon (Sprung 1994). When compared with the other areas analysed, the WR

presented a higher number of species, diversity and evenness, and exclusive species, as

well as a higher percentage of taxa sensitive to organic enrichment. The C area did not

present a disturbance due to organic enrichment but is conditioned by the water pump

system, justifying the reduced number of species observed when compared with the water

reservoir. The difference between the WR and the C area is also observed in the CCA,

which reflects the difference in species number and faunal composition between the two

areas. The two impacted areas (P and SP) exhibit a clear difference. While the SP has also

a direct connection with the lagoon to allow the discharges of effluents, the P area has a

Table 2 Results of canonical correspondence analysis (CCA) of macrobenthic species abundance data aftersquare-root transformation for the areas and periods studied

CCA Axis 1 Axis 2 Axis 3 Total inertia

Eigenvalue 0.276 0.231 0.141 2.487

F ratio 2.999 2.801 1.846

P value 0.002 0.002 0.034

Species-environment correlation 0.870 0.763 0.835

Cumulative % variance

Species data 11.1 20.4 26.1

Species-environment relationship 42.6 78.2 100

Correlations between the three first canonical axes and environmental parameters are presented as well asthe cumulative percentage of variance for the canonical axes for the species data and the species-envi-ronment relationship

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0

20

40

60

80

100

0

20

40

60

80

100

0

20

40

60

80

100

Jun-03 Jul Aug Nov Mar-04 Jun Oct

Sampling periods

I II III IV V

0

20

40

60

80

100

WR

SP

P

C

Fig. 5 Relative contribution of ecological groups during the study period for each analysed area. WR waterreservoir, SP settlement pond, P production area, C control area. Classification of species according tosensitivity to organic enrichment: I Sensitive species, II indifferent species, III tolerant species, IV second-order opportunistic species, V first-order opportunistic species

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more restricted water circulation. Therefore, it would be expected that the impact of

organic enrichment was most pronounced in this area. The higher disturbance levels

observed in these two areas were reflected in the increase of the dominance levels of

opportunistic annelids such as Capitella spp. and tubificids (Pearson and Rosenberg 1978).

This association was also evident in the CCA analysis as these species with Desdemonaornata, Gammarus insensibilis and Neanthes caudata were associated with the assem-

blages from the P and SP areas, as well as with high concentrations of chlorophyll a in the

sediment. Enhancement of microphytobenthos production is usually associated with

organically richer sediments, as in these sediments benthic remineralization is favored

(Brotas et al. 1990; Gutierrez et al. 2000). In fact, a significant relationship between

organic carbon and chlorophyll a in production ponds was already observed by Serpa et al.

(2007b) (TOC = -0.98 9 Chl a2 ? 60 9 Chl a ? 284). Therefore, these species not

only show a high affinity to high microphytobenthos productivity but also to organically

enriched sediments, which is in agreement with their association with SP and P areas. It is

worth noting that in terms of macrobenthic structure the SP present a better environmental

quality than the P area, emphasized by the higher number of sensitive taxa observed

particularly in June and October 2004, as well as by the association of this latter sample

and the June 2004 sample from the WR. Although the first sample collected within the P

area was closely related to the C samples, with the beginning of the production cycle

changes in benthic environment seem to begin promptly, as the samples from July and

August from both areas were clearly separated.

There is some evidence for Ria Formosa Lagoon that N and P entering the system are

promptly removed by primary producers (Falcao and Vale 2003). Serpa et al. (2007b)

found that, in white seabream fish earthen ponds, impacts on bottom sediment may be

observed when fish biomass and feeding rate exceed 500 g 9 m-3 and

150 kg 9 month-1, as then settled material, organic matter decomposition, nutrients in

pore-water and microphytobenthos production increase substantially. Nevertheless,

wastewater discharges with high nitrogen and phosphorous levels may lead to the dete-

rioration of water quality of coastal areas. The environmental impact depends strongly on

species, culture method, stocking density, food composition, feeding techniques and

hydrological regime of the site (Tovar et al. 2000). A recent study undertaken in the Ria

Formosa Lagoon showed that the effect of fish farming activity was more intense in

summer due to the higher loadings of dry feed added (Hubert et al. 2006). Moreover, the

organic matter decomposition rate is also higher during summer months, with a consequent

increase in oxygen consumption and potential sediment reduction (Bucci et al. 1992;

Millet and Guelorget 1994). Hubert et al. (2006) also found that the effects of effluents

from semi-intensive production were more harmful than those from intensive production.

The probable reason is the existence of a decantation process in the latter. Although the

effect may be insufficient in summer, this result supported the positive effect of settling

ponds in reducing organic matter and nutrients from effluent waters. In this way, the

discharges to adjacent lagoon systems may have a lower environmental impact, namely in

terms of eutrophication.

In Portugal and throughout Europe, the effects of discharges from land-based aqua-

culture fish farms on biodiversity are largely unknown. However, most fish farms are

located within protected coastal areas, most of which have high ecological and economical

value. Vizzini et al. (2005), using stable carbon and nitrogen isotopes to assess environ-

mental impact of aquaculture in the Mediterranean, showed that aquaculture wastes come

into the food web and change the natural isotopic composition of organisms. The authors

found that primary producers, benthic invertebrates and fish were affected. Primary

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producers take up inorganic aquaculture-derived nutrients, and consumers of higher trophic

levels are able to directly ingest particulates (Vizzini et al. 2005). High anthropogenic

nutrient loads have been associated with a decrease of phytoplankton diversity and the

growth of nuisance blooms (Smith et al. 1999; Alonso-Rodrıguez and Paez-Osuna 2003).

Therefore, the monitoring of several indicators at different distances from the facilities, of

both biological and environmental nature, should be undertaken and the results linked with

several factors (such as production system, produced species, season, amount of food) in

order to establish suitable management measures that will avoid severe impacts in the

future. Moreover, the results observed in the present study seem to indicate a positive

effect of SP even in fish farms using a semi-intensive regime. Although benthic assem-

blages from P and SP areas tend to be associated, macrobenthic structure in the latter

appears to be less disturbed, indicating better environmental quality. Therefore, if pro-

duction ponds were in direct connection with the lagoon, the potential environmental

impacts would probably be more severe. In conclusion, the implementation of settlement

ponds in semi-intensive fish farms should be hereafter considered.

Acknowledgments The authors would like to thank P. Pereira, F. Leitao, H. Saldanha, A. Silva, I.Ferreira, P. Vasconcelos and J. Guerra for technical support during sampling and laboratory work, as well asthe technicians from the fish farm for feeding and controlling fish production. We are also indebted to C.Martins and M. L. Inacio for their help in field and laboratory analyses. The present investigation wasfinancially supported by the projects ‘‘Tecnologias de Producao Aquıcola’’ MARE (22-05-01-FBR-00014-QCAIII) and PROMAR (INTERREG III A) ‘‘Cooperacao Algarve—Andaluzia para a promocao de Re-cursos Aquıcolas Marinhos no Litoral Atlantico Sul’’, as well as by a Ph.D. grant from Fundacao para aCiencia e a Tecnologia (SFRH/BD/8521/2002).

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