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Macrobenthic communities of saltpans from the Sado estuary (Portugal)
Acta Oecologica 20 (4) (1999) 327−332 / © 1999 E´ditions scientifiques et médicales Elsevier SAS. All rights reserved.
Macrobenthic communities of saltpans from the Sado estuary (Portugal) Maria José Amaral *, Maria Helena Costa Departamento de Ciências e Engenharia do Ambiente - Instituto do Mar (IMAR), Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa Quinta da Torre, 2825 Monte de Caparica, Portugal. * Corresponding author (fax: +351 1 2948554; e-mail: [email protected])
Received February 26, 1998; revised December 30, 1998; accepted February 26, 1999
Abstract — A 1-year study on the evolution of benthic communities of saltpans from the Sado estuary was carried out in order to evaluate its density, biomass and diversity, and to understand its trophic-dynamic structure under harsh environmental conditions. Physical and chemical parameters of the water column and sediments were also studied. Salinity and redox potential fluctuated sharply. Of eighteen taxa observed, a few occurred in significant numbers Chironomus salinarius (99 %) at crystallisation ponds where Artemia is present in the water column at salinities ranging from 23 to 249 g⋅L–1, Hydrobia (95 %) at evaporation pond (salinities between 29 and 112 g⋅L–1), while the reservoir, with salinities from 22 to 45 g⋅L–1, showed higher diversity nevertheless lower than in the estuary itself. It is colonised all year by Abra ovata, Cerastoderma glaucum, Hedistes diversicolor, Capitella sp., Microspio mecznikowianus, Mellina palmata, Polydora ciliata, Capitellidae and Microdeutopus gryllotalpa. The diversity of macrobenthic communities decreases with increasing salinity. Among trophic dynamic groups, surface detritivores burrowers, which are present at 85 % of the samples, are the dominant group at evaporation and crystallisation ponds and appears as an isolated group linked to organic matter of sediments and nutrients. © 1999 Éditions scientifiques et médicales Elsevier SAS Saltpans / macrobenthic communities / trophic-dynamic groups / bioturbation / Sado estuary
1. INTRODUCTION Portuguese saltpans or salinas are being progressively abandoned or converted into aquaculture facilities or rice production, due to economic constraints. Over 30 % of saltpans existing in the Sado estuary, in the fifties, were abandoned or even destroyed. Recognising the biological and cultural value of salinas, several institutions (universities, nature reserve board, owners associations) are now trying to promote their conservation [12, 14]. The production of salt in Sado saltpans, as in other Portuguese salinas, is seasonal, from spring (April/May) to autumn (September) in eighteen saltpan groups located in the saltmarshes of the Sado estuary. Sea water enters the feeder pond or reservoir every 15 d during spring tides and flows to evaporation and crystallisation ponds by gravity due to a slight gradient between ponds. Pisciculture facilities have been installed in reservoirs without previous knowledge on environmental impact of such activity. Brogueira and Cabeçadas [3] investigated several physical and chemical parameters in an extensive aquaculture located in the Sado estuary
and in the receiving water body, concluding that there was no significant difference between water quality inside and outside the aquaculture facility. The study of benthic communities structure is recommended to evaluate habitat modification, namely by organic enrichment. The investigation reported here, carried out in a more extensive work of environmental characterisation, deals mainly with trophic-dynamic structure of benthic communities related to environmental conditions. 2. MATERIALS AND METHODS Active saltpans of the Sado estuary (38°27’ N, 8°27’ W), on the west coast of Portugal, 45 km south of Lisbon, occupy an area of 385.83 ha [6]. Saltpans within an area of agricultural production and cattle raising in the Sado Estuary Nature Reserve were chosen for environmental characterisation studies and impact evaluation of extensive aquaculture facilities. The investigation reported here deals mainly with benthic communities of the Bandeira saltpans
328
Figure 1. Sado estuary, localisation of sampling stations and sampling sites at Bandeira saltpans (RA, RB, RC, EA, EB, CA, CB as in text).
(figure 1), the last one in activity at Vale de Judeus group (42.625 ha), with an area of 7.35 ha (17 % of total area). According to the variability of the system and water flow, seven sampling sites were chosen: three in the reservoir (RA, RB, RC), and two in both evaporation (EA, EB) and crystallisation ponds (CA, CB), and studied from February 1997 till January 1998. Parameters such as temperature (T, °C), pH, redox potential (Eh, mV), salinity (Sal, g⋅L–1) and dissolved oxygen (DO, mg⋅L–1) were measured in situ biweekly. Due to the shallowness of the ponds, water samples were collected at subsurface depth monthly, and analysed for nutrients (N-NO3–, N-NO2–, NH4+ and P-PO43–) according to Grasshoff et al. [8], total dissolved solids, total organic matter (TOM) and phytoplankton pigments (chlorophyll a, phaeopigments) as described by Strickland and Parsons [15] and pigments diversity index. Sediment cores were collected for granulometry (fine fraction, FF, obtained by hydraulic separation, after organic matter destruction and physical disaggregation of particles, under 63-µm mesh size), total organic matter (TOM) [5] and phytobenthos pigments analysis according to Lorenzen [10] modified by Plante-Cuny (described in [4]). Three replicates of macrozoobenthos were collected seasonally using corers of ∅ 11.7 cm (internal diameter) pushed to a penetration depth of 20 cm at all sampling sites as were those for granulometry. Samples of biota were preserved in 5 % formalin solution with Bengal Rose and sorted for species, abundance and biomass determinations. Species richness (S), abundance (A), biomass (B), Shannon-
M.J. Amaral, M.H. Costa
Figure 2. Annual parameter variation in reservoir (R), evaporation pond (E) and crystallisation pond (C). Mean (◆) minimum (}) and maximum (×) values.
Wiener diversity index (H’) and homogeneity index (J’) were computed for each sample. An hierarchical clustering analysis was performed in a matrix of normalised Euclidean distance on physical and chemical and biota data. Cluster dendrograms were produced, using the unweighed pair-group average linkage method, with the software Statistica 5.0 for PC. 3. RESULTS During the sampling period, apart from pH, physical and chemical parameters showed variation (figure 2) according either to the production cycle of salt or climatic conditions. Dissolved oxygen varied from 5.0 to 13.2 mg⋅L–1 in the reservoir, 5.8 to 14.2 mg⋅L–1 in the evaporation pond and 2.7 to 11.5 mg⋅L–1 in the crystallisation pond. Potential redox showed the largest variation both in the evaporation (–128 to 167 mV), crystallisation (46 to 186 mV) and reservoir (80 to 207 mV). Salinity varied from 22 and 45 g⋅L–1 in the reservoir, 29 and 112 g⋅L–1 in the evaporation and 23 to 249 g⋅L–1 in the crystallisation ponds. The concentration of nutrients and suspended solids and their organic fraction of the water column collected at the time of sediment samplings are given in table I. Nutrients were not detected in several samples of the water column. A great variation had been registered in each type of ponds. Among nitrogen compounds, there was a lack of ammonium in spring conditions and nitrite had the lowest concentrations. Chlorophyll a was detected in every reservoir water sample within the range 1.23 to 29.99 mg⋅m–3 and phaeopigments from 0.27 to 98.54 mg⋅m–3. The diverActa Oecologica
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Macrobenthic communities of saltpans
Table I. Concentration of nutrients, total suspended solids and total organic matter in the water column at the same sediment sampling time and sites (mean ± σE-03). RA, RB, RC, EA, EB, CA and CB as in text; *, not analysed; a) empty; b) salt. Sampling Site Parameter Winter N-NO2– (µmol⋅L–1) N–NO3– (µmol⋅L–1) N-NH4+ (µmol⋅L–1) P-PO43– (µmol⋅L–1) TSS (mg⋅L–1) TOM (mg⋅L–1) Spring N-NO2– (µmol⋅L–1) N-NO3– (µmol⋅L–1) N-NH4+ (µmol⋅L–1) P-PO43– (µmol⋅L–1) TSS (mg⋅L–1) TOM (mg⋅L–1) Summer N-NO2– (µmol⋅L–1) N-NO3– (µmol⋅L–1) N-NH4+ (µmol⋅L–1) P-PO43– (µmol⋅L–1) TSS (mg⋅L–1) TOM (mg⋅L–1) Autumn N-NO2– (µmol⋅L–1) N-NO3– (µmol⋅L–1) N-NH4+ (µmol⋅L–1) P-PO43– (µmol⋅L–1) TSS (mg⋅L–1) TOM (mg⋅L–1)
RA
RB
RC
EA
EB
CA
CB
0.00 0.97 ± 10.0 0.00 0.39 ± 2.8 13.80 *
0.12 ± 0.00 0.71 ± 11.5 0.13 ± 1.35 0.23 ± 2.1
0.00 0.45 ± 7.1 0.04 ± 9.78 0.25 ± 2.8
0.00 0.47 ± 1.7 0.08 ± 24.0 0.76 ± 2.1 94.00 *
0.00 0.69 ± 24.7 0.35 ± 51.5 0.61 ± 2.1
0.00 1.05 ± 39.8 0.15 ± 36.3 0.53 ± 5.7 45.50 *
0.00 0.50 ± 19.0 0.10 ± 3.8 0.24 ± 2.1
0.00 0.58 ± 2.5 0.00 0.00 42.2 *
0.00 0.52 ± 6.0 0.00 0.00
0.00 0.63 ± 8.5 0.00 0.00
0.00 0.27 ± 17.7 0.00 0.00 61.00 *
0.00 0.40 ± 17.6 0.00 0.00
0.00 1.46 ± 39.6 0.00 0.00 470.90 *
0.17 ± 4.9 5.17 ± 55.9 0.00 0.00
0.28 ± 1.4 0.30 ± 17.7 0.14 ± 25.8 0.00 33.30 6.70
0.28 ± 0.0 0.57 ± 13.3 0.06 ± 90.8 0.00
a) a) a) a)
0.24 ± 3.5 0.64 ± 12.7 0.08 ± 8.6 0.00 37.70 8.10
0.10 ± 0.0 1.20 ± 1.2 0.09 ± 16.3 0.00
0.22 ± 1.4 0.52 ± 0.52 0.02 ± 3.8 0.00 161.70 32.3
b) b) b) b)
1.24 1.74 ± 0.7 0.17 ± 6.6 0.00 14.4 4.40
1.26 2.24 ± 35.4 0.14 ± 1.9 0.08 ± 0.08
1.25 2.58 ± 21.2 0.20 ± 5.7 0.00
0.12 1.74 ± 9.2 0.39 ± 3.8 0.00 24.60 6.80
0.15 1.55 ± 2.1 0.35 ± 12.4 0.00
0.13 1.43 ± 8.5 0.38 ± 1 0.03 ± 0.8 21.30 11.30
0.13 1.27 ± 6.4 0.39 ± 18 0.01 ± 0.0
sity index given by the absorbance ratio between 430 and 630 nm varied from 2.28 to 5.00. The results of sediment analysis – chlorophyll a, phaeopigments concentration, total organic matter and sediment fine fraction – are given in figure 3. Phytobenthos, as well as chlorophyll a concentration, were always higher at water outflow in any type of pond. Sediments fine fraction was higher in water outflow of reservoir (91–97 %) and evaporation ponds (89–96 %). Macrozoobenthic communities were represented by eighteen taxa as shown in table II. Due to shallowness of the water column, some non-macrozoobenthic taxa occurred in the samples: Corixa Falleni, Artemia sp., Paleomnetes varians and non-identified crustacea and insecta larvae. Vol. 20 (4) 1999
The contribution of taxa to species richness was highest for Annelida (44.4 %), followed by Arthropoda (33.3 %), Mollusca (16.7 %) and Nematoda (5.6 %). The lowest density was recorded in spring at the crystallisation pond, 16 ind⋅m–2 Cerastoderma glaucum and the highest, in autumn, at the evaporation pond (96 127 ind⋅m–2 Hydrobia sp.). Biomass was always higher in the reservoir with an exception for the evaporation pond in autumn. Values for the Shannon-Wiener diversity index (H’) and homogeneity index (J’) are presented in table III. Primary biological variables S, A and B were related with physical and chemical parameters by clustering analysis (figure 4). Species richness is related to dissolved oxygen, while species diversity is related to TOM in association with nutrients and redox potential.
330
M.J. Amaral, M.H. Costa
Figure 5. Dendrogram resulting from cluster analysis of environmental parameters (DO, T, Sal, Eh, TOM, FF, NO3, NH4, PO4 as in text), chlorophyll of phytobenthos (Chlo) and relative abundance of trophic-dynamic groups of macrozoobenthos (ST, DT, OT, SE, H/SB, SB, DB and FB as in text) using the Euclidean distance and according to the rule unweighed pair-group average.
Figure 3. Seasonal variation of chlorophyll a and phaeopigments in µg⋅g–1 dry weight, total organic matter (%) and fine fraction of sediments (%).
Figure 4. Dendrogram resulting from cluster analysis of biological variables (S, B, A, H, J, Chlo as in the text) and environmental parameters (DO, T, Sal, Eh, TOM, FF, NO3, NH4, PO4 as in text) using the Euclidean distance and according to the rule unweighed pair-group average.
Organisms were also grouped according to their feeding and dynamic activity. The percentage of abundance for trophic groups was 33.3 % for surface detritivores, 16.7 % for subsurface detritivores, herbivores/detritivores, or animals with unknown feeding activity and 5.6 % for filter feeders, omnivores and carnivores. In communities found at the Bandeira saltpans, species are organised in eleven trophicdynamic groups: surface detritivores tube-builders (ST), subsurface detritivores tube-builders (DT) and omnivorous tube-builders (OT), surface detritivores epibenthic (SE), carnivores epibenthic (CE), herbivores or surface detritivores burrowers (H/SB), surface detritivores burrowers (SB), subsurface detritivores burrowers (DB) and filter feeders burrowers (FB), unknown feeding activity tube-builders and burrowers (?T; ?B). Surface detritivores burrowers were present in 85 % of the sampling sites and were dominant in the evaporation and crystallisation ponds. Epibenthic carnivores, surface detritivores and groups with unknown feeding activity were present only in less than 10 % of samples with a relative abundance lower than 7 %. Surface detritivores epibenthic were present only in 7 % of samples but they had a relative abundance of 94 %. For the analysis of dependence of trophicdynamic groups on environmental parameters, groups of unknown feeding activity and epibenthic carnivores were not considered in the hierarchical clustering analysis (figure 5). 4. DISCUSSION The annual fluctuation of dissolved oxygen was in agreement with that of temperature and salinity in the Acta Oecologica
331
Macrobenthic communities of saltpans
Table II. Seasonal variation on macrozoobenthic taxa present at sampling sites. R, Reservoir; E, evaporation pond; C, crystallisation pond; W, winter; Sp, spring; S, summer; A, autumn. Sampling sites Time
R W
TAXA (trophic/dynamic group) Nematoda (?B) Hydrobia sp. (H/SB) Abra ovata (SB) Cerastoderma glaucum (FB) Hedistes diversicolor (OT) Microspio mecznikowianus (ST) Polydora ciliata (ST) Capitellidae n.id. (DT) Capitella sp. (DT) Mellina palmata (ST) Polychaeta n.id. (?T) Oligochaeta n.id. (DB) Copepoda n.id. (?E) Gammarus sp. (H/SB) Microdeutopus gryllotalpa (H/SB) Chironomus salinarius (SB) Hydroporus lineatus (CE) Ochethebius sp. (SE)
+ + + + + + + + + +
S
A
+
+
+
+ + + + + + + +
+ + + + + + + +
+ +
+ + + +
+
+ +
+
E
Sp
+ + + + +
+ +
different ponds and according to seasonal pond activity [7, 11]. Annual data on nutrients did not evidence any typical variation pattern. Abnormal levels of precipitation occurred during the study period, and water retention at reservoir, due to maintenance opera-
Table III. Shannon-Wiener diversity index (H’) and homogeneity index (J≠). RA, RB, RC, EA, EB, CA, CB as in text; *, salt. Sampling site Index Winter H’ J’ Spring H’ J’ Summer H’ J’ Autumn H’ J’
RA
RB
RC
EA
EB
CA
CB
0.86 0.90
2.21 2.62
0.74 0.78
0.27 0.38
0.05 0.11
0.10 0.32
0.03 0.09
0.60 0.67
0.58 0.64
0.68 0.68
0.38 0.79
0.06 0.12
0.01 0.05
1.26 4.19
0.46 0.55
0.80 0.80
2.22 2.33
0.44 0.52
0.11 0.23
0.16 0.54
* *
0.18 0.18
0.68 0.97
0.50 0.59
0.07 0.25
0.16 0.54
0
* *
Vol. 20 (4) 1999
C
W
Sp
S
A
+
+
+
+
+
+
+
+
+
+
+
+
+ + +
W
Sp
+
+
+
+
S
A
+
+
+
+
+
tions, does not fully agree with periodicity of water intake. These conditions make difficult the establishment of any relation between phytoplankton, phytobentos and nutrients fluctuations. Relatively higher concentration of phytobenthos can be due to higher availability of nitrogen compounds and phosphates in sediments (FF was the closest environmental factor, as shown in figure 4). As pointed out by Valiela [16], nitrogen compounds, due to degradation of organic matter, low water percolation and presence of active exchange surfaces are much higher in the interstitial water of sediments. The redox state of a sediment determines the relative abundance of inorganic nitrogen compounds and, as benthic fauna is abundant near the surface of the sediments, their activity affects the physical and chemical processes within sediments through bioturbation (irrigation, excretion, burrow or tube building and feeding activity). Phosphate concentration in sediments is quite variable and its regeneration is temperature and salinity dependent. It is usually low in the water column due to phytoplankton uptake, adsorption to calcium carbonate, clay mineral particles and amorphous oxyhydroxides under aerobic conditions but it changes strongly under anaerobic environment.
332
Species richness was always higher at the feeder pond (five species in autumn to ten species in summer). Macrozoobenthos were absent at the crystallisation pond (CB) in the same seasons due to salt production. Taxa composition is different from that reported in the Aveiro salt ponds [17] where Mollusca are dominant while in Bandeira, the dominant group is Anellida. Values of density are lower in the Aveiro and Algarve saltpans [14] but agree with those recorded by Britton and Jonhson [2]. Higher density and biomass of Hydrobia sp. found in the present study can be due to spatial distribution pattern. Macrobenthic communities diversity decreases with increasing salinity (table II) although distribution of benthic macrofauna does not depend only on salinity [1]. The dendrogram presented in figure 4 shows that organic matter and redox potential are associated with water column nutrients and diversity evolution. Some trophic-dynamic groups, mainly surface detritivores burrowers (C. salinarius, A. ovata), herbivores/ surface detritivores burrowers (Hydrobia sp., Gammarus sp., M. gryllotalpa) and subsurface detritivores burrowers (Oligochaeta) are related to those environmental conditions (figure 5). Their bioturbating effect induces changes in geochemical characteristics of sediments. A similar result was found by Mucha [13] in the Sado estuary. Dissolved oxygen is associated to species richness influencing the abundance of surface detritivores (M. mecznikowianus, P. ciliata, M. palmata) and omnivorous tubicoles (H. diversicolor) in the reservoir, where they are dominant in winter and spring conditions (relative abundance of 49 and 84 %, respectively), decreasing in summer and autumn (3 and 5 % of total abundance, respectively). Surface detritivores epibenthic (Ochethebius sp.) are dominant in summer conditions at the evaporation pond – when salinity and temperature reach their maximum values. The main conclusion to be drawn from this study is that the dynamism of macrobenthic communities is dependent on environmental conditions but bioturbation is undoubtedly important in the release of dissolved substances, increasing the redox potential in water column and sediments and the depth of the oxidised layer through mixing and redistribution of particles. Acknowledgments This study was financed by ‘Fundação para a Ciência e Tecnologia’ – Praxis XXI – BD/5034/95.
M.J. Amaral, M.H. Costa
REFERENCES [1] Amaral M.J., Pimentel C., Costa M.H., Ecossistemas de salinas. Biodiversidade e problemática da conservação de sistemas únicos, Resumos, 1º Encontro Nacional de Ecologia, Portugal, 1996. [2] Britton R.H., Johnson A.R., An ecological account of a Mediterranean salina: The salin de Giraud, Camargue (S. France), Biol. Cons. 42 (1987) 185–230. [3] Brogueira M.J., Cabeçadas G., Aspectos do desenvolvimento da aquaculture em zonas costeiras, Relat. Tec. Cient. INIP, Lisboa (66), 1933, 10 p. [4] Brotas V., Avaliação dos Pigmentos Fotossintéticos das Microalgas Epibênticas do Estuário do Tejo, Provas de Aptidão Científica e Capacidade Pedagógica, Universidade de Lisboa, Portugal, 1987, 37 p. [5] Costa M.H., Macrofauna bêntica no infralitoral do estuário do Sado. Variabilidade e interacção, Ph.D. thesis, FCT-UNL Lisboa, 1989, 228 p. [6] Dias M.D.S., Contribuição para o conhecimento da Aquacultura no Estuário do Sado, in: Seminário sobre recursos hali uticos, ambiente, aquacultura e qualidade do pescado da península de Setúbal, Publicações Avulsas do IPIMAR n° 1, 1994, pp. 155-166. [7] Flindt M.R., Pardal M.A., Lillebø A.I., Martins I., Marques J.C., Nutrient cycling and plant dynamics in estuaries: A brief review, Acta Oecol. 20 (1999) 237–248. [8] Grasshoff K., Ehrhardt M., Kremling K. Methods of seawater analysis, (Eds.), Verlag Chemie, Germany, 1983, 419 p. [9] Lillebø A.I., Pardal M.A., Marques J.C., Population structure, dynamics and production of Hydrobia ulvae (Pennant) (Mollusca: Prosobranchia) along an eutrophication gradient in the Mondego estuary (Portugal), Acta Oecol. 20 (1999) 289–304. [10] Lorenzen C.J., Determination of chlorophyll and pheopigments: Spectrophotometric equations, Limnol. Oceanogr. 12 (1967) 343–346. [11] Martins I., Oliveira J.M., Flindt M.R., Marques J.C., The effect of salinity on the growth rate of the macroalgae Enteromorpha intestinalis (Chlorophyta) in the Mondego estuary (west Portugal), Acta Oecol. 20 (1999) 259–265. [12] Masero J.A., Pérez-González M., Basadre M., Otero-Saavedra M., Food supply for waders (Aves: Charadrii) in an estuarine area in the Bay of Cádiz (SW Iberian Peninsula), Acta Oecol. 20 (1999) 429–434. [13] Mucha A.P.C., Estudo das comunidades nacrozoobênticas em biótopos litorais de energia distinta. Sua relação com gradientes de carbono e nutrientes, Dissertação de Mestrado, Universidade Nova de Lisboa, 1997, 164 p. [14] Neves R., Rufino R., Importância ornitológica das Salinas: o caso particular do Estuário do Sado, Estudos de Biologia e Conservação da Natureza 15, Lisboa, 1995. [15] Strickland J.D.H., Parsons T.R., A Practical Handbook of Sea Water Analysis, 2nd ed., Bulletin of the Fisheries Research Board of Canada No. 167, 1972, pp. 1-130. [16] Valiela I., Marine Ecological Processes, 2nd ed., SpringerVerlag, Berlin, 1995, 689 p. [17] Vieira N., Amat F., The invertebrate benthic community of two solar salt ponds in Aveiro, Portugal, Int. J. Salt Lake Res. 5 (1997) 281–286.
Acta Oecologica
Macrobenthic communities of saltpans from the Sado estuary (Portugal) Maria José Amaral *, Maria Helena Costa Departamento de Ciências e Engenharia do Ambiente - Instituto do Mar (IMAR), Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa Quinta da Torre, 2825 Monte de Caparica, Portugal. * Corresponding author (fax: +351 1 2948554; e-mail: [email protected])
Received February 26, 1998; revised December 30, 1998; accepted February 26, 1999
Abstract — A 1-year study on the evolution of benthic communities of saltpans from the Sado estuary was carried out in order to evaluate its density, biomass and diversity, and to understand its trophic-dynamic structure under harsh environmental conditions. Physical and chemical parameters of the water column and sediments were also studied. Salinity and redox potential fluctuated sharply. Of eighteen taxa observed, a few occurred in significant numbers Chironomus salinarius (99 %) at crystallisation ponds where Artemia is present in the water column at salinities ranging from 23 to 249 g⋅L–1, Hydrobia (95 %) at evaporation pond (salinities between 29 and 112 g⋅L–1), while the reservoir, with salinities from 22 to 45 g⋅L–1, showed higher diversity nevertheless lower than in the estuary itself. It is colonised all year by Abra ovata, Cerastoderma glaucum, Hedistes diversicolor, Capitella sp., Microspio mecznikowianus, Mellina palmata, Polydora ciliata, Capitellidae and Microdeutopus gryllotalpa. The diversity of macrobenthic communities decreases with increasing salinity. Among trophic dynamic groups, surface detritivores burrowers, which are present at 85 % of the samples, are the dominant group at evaporation and crystallisation ponds and appears as an isolated group linked to organic matter of sediments and nutrients. © 1999 Éditions scientifiques et médicales Elsevier SAS Saltpans / macrobenthic communities / trophic-dynamic groups / bioturbation / Sado estuary
1. INTRODUCTION Portuguese saltpans or salinas are being progressively abandoned or converted into aquaculture facilities or rice production, due to economic constraints. Over 30 % of saltpans existing in the Sado estuary, in the fifties, were abandoned or even destroyed. Recognising the biological and cultural value of salinas, several institutions (universities, nature reserve board, owners associations) are now trying to promote their conservation [12, 14]. The production of salt in Sado saltpans, as in other Portuguese salinas, is seasonal, from spring (April/May) to autumn (September) in eighteen saltpan groups located in the saltmarshes of the Sado estuary. Sea water enters the feeder pond or reservoir every 15 d during spring tides and flows to evaporation and crystallisation ponds by gravity due to a slight gradient between ponds. Pisciculture facilities have been installed in reservoirs without previous knowledge on environmental impact of such activity. Brogueira and Cabeçadas [3] investigated several physical and chemical parameters in an extensive aquaculture located in the Sado estuary
and in the receiving water body, concluding that there was no significant difference between water quality inside and outside the aquaculture facility. The study of benthic communities structure is recommended to evaluate habitat modification, namely by organic enrichment. The investigation reported here, carried out in a more extensive work of environmental characterisation, deals mainly with trophic-dynamic structure of benthic communities related to environmental conditions. 2. MATERIALS AND METHODS Active saltpans of the Sado estuary (38°27’ N, 8°27’ W), on the west coast of Portugal, 45 km south of Lisbon, occupy an area of 385.83 ha [6]. Saltpans within an area of agricultural production and cattle raising in the Sado Estuary Nature Reserve were chosen for environmental characterisation studies and impact evaluation of extensive aquaculture facilities. The investigation reported here deals mainly with benthic communities of the Bandeira saltpans
328
Figure 1. Sado estuary, localisation of sampling stations and sampling sites at Bandeira saltpans (RA, RB, RC, EA, EB, CA, CB as in text).
(figure 1), the last one in activity at Vale de Judeus group (42.625 ha), with an area of 7.35 ha (17 % of total area). According to the variability of the system and water flow, seven sampling sites were chosen: three in the reservoir (RA, RB, RC), and two in both evaporation (EA, EB) and crystallisation ponds (CA, CB), and studied from February 1997 till January 1998. Parameters such as temperature (T, °C), pH, redox potential (Eh, mV), salinity (Sal, g⋅L–1) and dissolved oxygen (DO, mg⋅L–1) were measured in situ biweekly. Due to the shallowness of the ponds, water samples were collected at subsurface depth monthly, and analysed for nutrients (N-NO3–, N-NO2–, NH4+ and P-PO43–) according to Grasshoff et al. [8], total dissolved solids, total organic matter (TOM) and phytoplankton pigments (chlorophyll a, phaeopigments) as described by Strickland and Parsons [15] and pigments diversity index. Sediment cores were collected for granulometry (fine fraction, FF, obtained by hydraulic separation, after organic matter destruction and physical disaggregation of particles, under 63-µm mesh size), total organic matter (TOM) [5] and phytobenthos pigments analysis according to Lorenzen [10] modified by Plante-Cuny (described in [4]). Three replicates of macrozoobenthos were collected seasonally using corers of ∅ 11.7 cm (internal diameter) pushed to a penetration depth of 20 cm at all sampling sites as were those for granulometry. Samples of biota were preserved in 5 % formalin solution with Bengal Rose and sorted for species, abundance and biomass determinations. Species richness (S), abundance (A), biomass (B), Shannon-
M.J. Amaral, M.H. Costa
Figure 2. Annual parameter variation in reservoir (R), evaporation pond (E) and crystallisation pond (C). Mean (◆) minimum (}) and maximum (×) values.
Wiener diversity index (H’) and homogeneity index (J’) were computed for each sample. An hierarchical clustering analysis was performed in a matrix of normalised Euclidean distance on physical and chemical and biota data. Cluster dendrograms were produced, using the unweighed pair-group average linkage method, with the software Statistica 5.0 for PC. 3. RESULTS During the sampling period, apart from pH, physical and chemical parameters showed variation (figure 2) according either to the production cycle of salt or climatic conditions. Dissolved oxygen varied from 5.0 to 13.2 mg⋅L–1 in the reservoir, 5.8 to 14.2 mg⋅L–1 in the evaporation pond and 2.7 to 11.5 mg⋅L–1 in the crystallisation pond. Potential redox showed the largest variation both in the evaporation (–128 to 167 mV), crystallisation (46 to 186 mV) and reservoir (80 to 207 mV). Salinity varied from 22 and 45 g⋅L–1 in the reservoir, 29 and 112 g⋅L–1 in the evaporation and 23 to 249 g⋅L–1 in the crystallisation ponds. The concentration of nutrients and suspended solids and their organic fraction of the water column collected at the time of sediment samplings are given in table I. Nutrients were not detected in several samples of the water column. A great variation had been registered in each type of ponds. Among nitrogen compounds, there was a lack of ammonium in spring conditions and nitrite had the lowest concentrations. Chlorophyll a was detected in every reservoir water sample within the range 1.23 to 29.99 mg⋅m–3 and phaeopigments from 0.27 to 98.54 mg⋅m–3. The diverActa Oecologica
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Table I. Concentration of nutrients, total suspended solids and total organic matter in the water column at the same sediment sampling time and sites (mean ± σE-03). RA, RB, RC, EA, EB, CA and CB as in text; *, not analysed; a) empty; b) salt. Sampling Site Parameter Winter N-NO2– (µmol⋅L–1) N–NO3– (µmol⋅L–1) N-NH4+ (µmol⋅L–1) P-PO43– (µmol⋅L–1) TSS (mg⋅L–1) TOM (mg⋅L–1) Spring N-NO2– (µmol⋅L–1) N-NO3– (µmol⋅L–1) N-NH4+ (µmol⋅L–1) P-PO43– (µmol⋅L–1) TSS (mg⋅L–1) TOM (mg⋅L–1) Summer N-NO2– (µmol⋅L–1) N-NO3– (µmol⋅L–1) N-NH4+ (µmol⋅L–1) P-PO43– (µmol⋅L–1) TSS (mg⋅L–1) TOM (mg⋅L–1) Autumn N-NO2– (µmol⋅L–1) N-NO3– (µmol⋅L–1) N-NH4+ (µmol⋅L–1) P-PO43– (µmol⋅L–1) TSS (mg⋅L–1) TOM (mg⋅L–1)
RA
RB
RC
EA
EB
CA
CB
0.00 0.97 ± 10.0 0.00 0.39 ± 2.8 13.80 *
0.12 ± 0.00 0.71 ± 11.5 0.13 ± 1.35 0.23 ± 2.1
0.00 0.45 ± 7.1 0.04 ± 9.78 0.25 ± 2.8
0.00 0.47 ± 1.7 0.08 ± 24.0 0.76 ± 2.1 94.00 *
0.00 0.69 ± 24.7 0.35 ± 51.5 0.61 ± 2.1
0.00 1.05 ± 39.8 0.15 ± 36.3 0.53 ± 5.7 45.50 *
0.00 0.50 ± 19.0 0.10 ± 3.8 0.24 ± 2.1
0.00 0.58 ± 2.5 0.00 0.00 42.2 *
0.00 0.52 ± 6.0 0.00 0.00
0.00 0.63 ± 8.5 0.00 0.00
0.00 0.27 ± 17.7 0.00 0.00 61.00 *
0.00 0.40 ± 17.6 0.00 0.00
0.00 1.46 ± 39.6 0.00 0.00 470.90 *
0.17 ± 4.9 5.17 ± 55.9 0.00 0.00
0.28 ± 1.4 0.30 ± 17.7 0.14 ± 25.8 0.00 33.30 6.70
0.28 ± 0.0 0.57 ± 13.3 0.06 ± 90.8 0.00
a) a) a) a)
0.24 ± 3.5 0.64 ± 12.7 0.08 ± 8.6 0.00 37.70 8.10
0.10 ± 0.0 1.20 ± 1.2 0.09 ± 16.3 0.00
0.22 ± 1.4 0.52 ± 0.52 0.02 ± 3.8 0.00 161.70 32.3
b) b) b) b)
1.24 1.74 ± 0.7 0.17 ± 6.6 0.00 14.4 4.40
1.26 2.24 ± 35.4 0.14 ± 1.9 0.08 ± 0.08
1.25 2.58 ± 21.2 0.20 ± 5.7 0.00
0.12 1.74 ± 9.2 0.39 ± 3.8 0.00 24.60 6.80
0.15 1.55 ± 2.1 0.35 ± 12.4 0.00
0.13 1.43 ± 8.5 0.38 ± 1 0.03 ± 0.8 21.30 11.30
0.13 1.27 ± 6.4 0.39 ± 18 0.01 ± 0.0
sity index given by the absorbance ratio between 430 and 630 nm varied from 2.28 to 5.00. The results of sediment analysis – chlorophyll a, phaeopigments concentration, total organic matter and sediment fine fraction – are given in figure 3. Phytobenthos, as well as chlorophyll a concentration, were always higher at water outflow in any type of pond. Sediments fine fraction was higher in water outflow of reservoir (91–97 %) and evaporation ponds (89–96 %). Macrozoobenthic communities were represented by eighteen taxa as shown in table II. Due to shallowness of the water column, some non-macrozoobenthic taxa occurred in the samples: Corixa Falleni, Artemia sp., Paleomnetes varians and non-identified crustacea and insecta larvae. Vol. 20 (4) 1999
The contribution of taxa to species richness was highest for Annelida (44.4 %), followed by Arthropoda (33.3 %), Mollusca (16.7 %) and Nematoda (5.6 %). The lowest density was recorded in spring at the crystallisation pond, 16 ind⋅m–2 Cerastoderma glaucum and the highest, in autumn, at the evaporation pond (96 127 ind⋅m–2 Hydrobia sp.). Biomass was always higher in the reservoir with an exception for the evaporation pond in autumn. Values for the Shannon-Wiener diversity index (H’) and homogeneity index (J’) are presented in table III. Primary biological variables S, A and B were related with physical and chemical parameters by clustering analysis (figure 4). Species richness is related to dissolved oxygen, while species diversity is related to TOM in association with nutrients and redox potential.
330
M.J. Amaral, M.H. Costa
Figure 5. Dendrogram resulting from cluster analysis of environmental parameters (DO, T, Sal, Eh, TOM, FF, NO3, NH4, PO4 as in text), chlorophyll of phytobenthos (Chlo) and relative abundance of trophic-dynamic groups of macrozoobenthos (ST, DT, OT, SE, H/SB, SB, DB and FB as in text) using the Euclidean distance and according to the rule unweighed pair-group average.
Figure 3. Seasonal variation of chlorophyll a and phaeopigments in µg⋅g–1 dry weight, total organic matter (%) and fine fraction of sediments (%).
Figure 4. Dendrogram resulting from cluster analysis of biological variables (S, B, A, H, J, Chlo as in the text) and environmental parameters (DO, T, Sal, Eh, TOM, FF, NO3, NH4, PO4 as in text) using the Euclidean distance and according to the rule unweighed pair-group average.
Organisms were also grouped according to their feeding and dynamic activity. The percentage of abundance for trophic groups was 33.3 % for surface detritivores, 16.7 % for subsurface detritivores, herbivores/detritivores, or animals with unknown feeding activity and 5.6 % for filter feeders, omnivores and carnivores. In communities found at the Bandeira saltpans, species are organised in eleven trophicdynamic groups: surface detritivores tube-builders (ST), subsurface detritivores tube-builders (DT) and omnivorous tube-builders (OT), surface detritivores epibenthic (SE), carnivores epibenthic (CE), herbivores or surface detritivores burrowers (H/SB), surface detritivores burrowers (SB), subsurface detritivores burrowers (DB) and filter feeders burrowers (FB), unknown feeding activity tube-builders and burrowers (?T; ?B). Surface detritivores burrowers were present in 85 % of the sampling sites and were dominant in the evaporation and crystallisation ponds. Epibenthic carnivores, surface detritivores and groups with unknown feeding activity were present only in less than 10 % of samples with a relative abundance lower than 7 %. Surface detritivores epibenthic were present only in 7 % of samples but they had a relative abundance of 94 %. For the analysis of dependence of trophicdynamic groups on environmental parameters, groups of unknown feeding activity and epibenthic carnivores were not considered in the hierarchical clustering analysis (figure 5). 4. DISCUSSION The annual fluctuation of dissolved oxygen was in agreement with that of temperature and salinity in the Acta Oecologica
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Macrobenthic communities of saltpans
Table II. Seasonal variation on macrozoobenthic taxa present at sampling sites. R, Reservoir; E, evaporation pond; C, crystallisation pond; W, winter; Sp, spring; S, summer; A, autumn. Sampling sites Time
R W
TAXA (trophic/dynamic group) Nematoda (?B) Hydrobia sp. (H/SB) Abra ovata (SB) Cerastoderma glaucum (FB) Hedistes diversicolor (OT) Microspio mecznikowianus (ST) Polydora ciliata (ST) Capitellidae n.id. (DT) Capitella sp. (DT) Mellina palmata (ST) Polychaeta n.id. (?T) Oligochaeta n.id. (DB) Copepoda n.id. (?E) Gammarus sp. (H/SB) Microdeutopus gryllotalpa (H/SB) Chironomus salinarius (SB) Hydroporus lineatus (CE) Ochethebius sp. (SE)
+ + + + + + + + + +
S
A
+
+
+
+ + + + + + + +
+ + + + + + + +
+ +
+ + + +
+
+ +
+
E
Sp
+ + + + +
+ +
different ponds and according to seasonal pond activity [7, 11]. Annual data on nutrients did not evidence any typical variation pattern. Abnormal levels of precipitation occurred during the study period, and water retention at reservoir, due to maintenance opera-
Table III. Shannon-Wiener diversity index (H’) and homogeneity index (J≠). RA, RB, RC, EA, EB, CA, CB as in text; *, salt. Sampling site Index Winter H’ J’ Spring H’ J’ Summer H’ J’ Autumn H’ J’
RA
RB
RC
EA
EB
CA
CB
0.86 0.90
2.21 2.62
0.74 0.78
0.27 0.38
0.05 0.11
0.10 0.32
0.03 0.09
0.60 0.67
0.58 0.64
0.68 0.68
0.38 0.79
0.06 0.12
0.01 0.05
1.26 4.19
0.46 0.55
0.80 0.80
2.22 2.33
0.44 0.52
0.11 0.23
0.16 0.54
* *
0.18 0.18
0.68 0.97
0.50 0.59
0.07 0.25
0.16 0.54
0
* *
Vol. 20 (4) 1999
C
W
Sp
S
A
+
+
+
+
+
+
+
+
+
+
+
+
+ + +
W
Sp
+
+
+
+
S
A
+
+
+
+
+
tions, does not fully agree with periodicity of water intake. These conditions make difficult the establishment of any relation between phytoplankton, phytobentos and nutrients fluctuations. Relatively higher concentration of phytobenthos can be due to higher availability of nitrogen compounds and phosphates in sediments (FF was the closest environmental factor, as shown in figure 4). As pointed out by Valiela [16], nitrogen compounds, due to degradation of organic matter, low water percolation and presence of active exchange surfaces are much higher in the interstitial water of sediments. The redox state of a sediment determines the relative abundance of inorganic nitrogen compounds and, as benthic fauna is abundant near the surface of the sediments, their activity affects the physical and chemical processes within sediments through bioturbation (irrigation, excretion, burrow or tube building and feeding activity). Phosphate concentration in sediments is quite variable and its regeneration is temperature and salinity dependent. It is usually low in the water column due to phytoplankton uptake, adsorption to calcium carbonate, clay mineral particles and amorphous oxyhydroxides under aerobic conditions but it changes strongly under anaerobic environment.
332
Species richness was always higher at the feeder pond (five species in autumn to ten species in summer). Macrozoobenthos were absent at the crystallisation pond (CB) in the same seasons due to salt production. Taxa composition is different from that reported in the Aveiro salt ponds [17] where Mollusca are dominant while in Bandeira, the dominant group is Anellida. Values of density are lower in the Aveiro and Algarve saltpans [14] but agree with those recorded by Britton and Jonhson [2]. Higher density and biomass of Hydrobia sp. found in the present study can be due to spatial distribution pattern. Macrobenthic communities diversity decreases with increasing salinity (table II) although distribution of benthic macrofauna does not depend only on salinity [1]. The dendrogram presented in figure 4 shows that organic matter and redox potential are associated with water column nutrients and diversity evolution. Some trophic-dynamic groups, mainly surface detritivores burrowers (C. salinarius, A. ovata), herbivores/ surface detritivores burrowers (Hydrobia sp., Gammarus sp., M. gryllotalpa) and subsurface detritivores burrowers (Oligochaeta) are related to those environmental conditions (figure 5). Their bioturbating effect induces changes in geochemical characteristics of sediments. A similar result was found by Mucha [13] in the Sado estuary. Dissolved oxygen is associated to species richness influencing the abundance of surface detritivores (M. mecznikowianus, P. ciliata, M. palmata) and omnivorous tubicoles (H. diversicolor) in the reservoir, where they are dominant in winter and spring conditions (relative abundance of 49 and 84 %, respectively), decreasing in summer and autumn (3 and 5 % of total abundance, respectively). Surface detritivores epibenthic (Ochethebius sp.) are dominant in summer conditions at the evaporation pond – when salinity and temperature reach their maximum values. The main conclusion to be drawn from this study is that the dynamism of macrobenthic communities is dependent on environmental conditions but bioturbation is undoubtedly important in the release of dissolved substances, increasing the redox potential in water column and sediments and the depth of the oxidised layer through mixing and redistribution of particles. Acknowledgments This study was financed by ‘Fundação para a Ciência e Tecnologia’ – Praxis XXI – BD/5034/95.
M.J. Amaral, M.H. Costa
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