Long-Term Recovery of Soft-Bottom Benthos Following Urban and Industrial Sewage Treatment in the Nervión Estuary (Southern Bay of Biscay)
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MARINE ECOLOGY PROGRESS SERIES Vol. 313: 43–55, 2006 Published May 11 Mar Ecol Prog Ser Long-term recovery of soft-bottom benthos following urban and industrial sewage treatment in the Nervión estuary (southern Bay of Biscay) Ángel Borja*, Iñigo Muxika, Javier Franco AZTI-Tecnalia Foundation, Marine Research Division, Portualdea, Herrera Kaia, s/n 20110 Pasaia, Spain ABSTRACT: The monitoring of marine benthic communities is based upon their ability to integrate long-term environmental conditions and it is considered an efficient, accurate and useful tool in the detection of pollution effects. However, long-term studies are scarce, and only few are devoted to recovery processes in estuaries following water treatment. In this contribution, the response of the Nervión estuary to sewerage processes is studied, using a long-term (1989 to 2003) data set of physico-chemical (dissolved oxygen, redox potential, organic matter, metals) and biological (density, richness and diversity in benthic communities) variables. The AMBI (AZTI’s Marine Biotic Index) was designed to investigate the response of soft-bottom communities to natural and human-induced changes in European coastal water quality and is evaluated here. The first factor controlling the Nervión’s benthic structure is found to be the bottom water oxygen saturation, hypoxia- and/or anoxia-produced azoic sediments. When water treatment commenced, benthic recolonisation was very rapid in terms of opportunistic species settlement. However, the community structure was highly disturbed, in terms of density, richness, diversity and AMBI values. AMBI and diversity values are highly correlated with oxygen saturation. When the water treatment continued, the high metal con- centrations in the sediments inhibited recovery in some areas; they were a secondary factor in deter- mining benthic structure. This contribution demonstrates that the AMBI is an efficient tool for detect- ing changes in benthic communities and in systems associated with sewerage schemes; it provides an indication of the proportions of opportunistic and sensitive species within a long-term series. KEY WORDS: Benthic recovery · Water treatment · AMBI · Dissolved oxygen · Metals · Estuary Resale or republication not permitted without written consent of the publisher INTRODUCTION of benthic communities is considered an efficient, accurate and useful tool in the detection of pollution Biological monitoring is a useful tool for the evalua- effects (Kröncke 1995, Brown & Shillabeer 1997, tion of recovery processes in estuarine and marine Currie & Parry 1999). However, long-term studies are environments and is a necessary part of environmental scarce, and only sometimes are they devoted to recov- management. The monitoring of marine benthic com- ery processes in estuaries (Shillabeer & Tapp 1989, munities is based conceptually upon their ability to Tapp et al. 1993, Dauer & Alden 1995, Attrill 1998, integrate long-term environmental conditions at a par- Wilson et al. 1998, Beukema et al. 1999, Hawkins et al. ticular site (Bilyard 1987, Warwick 1993). The use of 2002, Llansó et al. 2004). both the community (as an indicator of the level of bio- According to Spellerberg (1995), there is a clear and logical organisation) and the benthos (as an indicator urgent need for the development of rigorous biological of the biotic component) in monitoring programmes monitoring techniques, as well as some careful consider- has been justified largely for temperate coastal areas ation to the logistics of such monitoring programmes. (Clarke & Green 1988, Warwick 1993, Clarke & War- Therefore, the basic aspects to be considered in monitor- wick 1994, Eriksson et al. 2002). Long-term monitoring ing programmes are the requirements for studies previ- *Email: [email protected] © Inter-Research 2006 · www.int-res.com 44 Mar Ecol Prog Ser 313: 43–55, 2006 ous to the disturbance, i.e. before the commencement of and Brazil (Muniz et al. 2005, Muxika et al. 2005). The human activities (such as in the case of dumping, en- AMBI has been proposed also to be used, together with abling the application of corrective action), as well as the other structural parameters, for the assessment of the need to establish controls. When planning a monitoring ecological status of estuarine and coastal waters, accord- survey of the benthos, several decisions have first to be ing to the requirements of the European Water Frame- taken, such as the sampling methodology; the derived work Directive (Borja et al. 2004c,d). measurable attributes of the organisms and the criteria The Basque Country is located in the innermost part and levels of organism discrimination groupings for the of the Bay of Biscay in northern Spain (Fig. 1). This re- littoral zone under study (Warwick 1993). gion has a long history of industrialisation, especially in In this way, and in recent years, the interest in ben- the Nervión estuary, which encompasses the large thic indicators has increased dramatically, with a long commercial port of Bilbao (Fig. 1). The estuary is 22 km list of new indicators proposed (see Diaz et al. 2004 for long and is formed by the tidal part of the Nervión a review). One of these indicators, the AMBI (AZTI’s River. The natural features of the estuary have been Marine Biotic Index), was designed to establish the modified dramatically by urban, industrial and port set- ecological quality of European coasts, investigating the tlements, which have occupied practically the whole of response of soft-bottom communities to natural and the valley during the last 150 yr (Cearreta et al. 2004). human-induced changes in water quality (Borja et al. The original estuary has been reduced rapidly in size 2000, 2003, 2004a). Hence, the AMBI offers a ‘pollu- through land reclamation to form a tidal channel (aver- tion/disturbance classification’ of a particular site, rep- age dimensions: 100 m wide, <10m deep) completed in resenting the benthic community ‘health’ (sensu Grall 1885 (Junta de Obras del Puerto 1910). & Glémarec 1997). The AMBI is based upon well- Exploitation of abundant local iron ore led, in the known ecological models (Glémarec & Hily 1981, Hily mid-19th century, to the early industrial development 1984); its theoretical basis is that of the ecological of the area together with an increase in the density of adaptative strategies of r, k and T (McArthur & Wilson the population (around 2250 inhabitants km–2 and a 1967, Pianka 1970, Gray 1979) and ecological succes- total current population of 1 000 000) (Belzunce et al. sion in stressed environments (Bellan 1967, Pearson & 2004a). As a consequence, the estuary has received, Rosenberg 1978). over the last 150 yr, wastes from many sources (mineral The AMBI has been verified successfully in relation to sluicing, industrial wastes and urban effluents), which a very large set of environmental impact sources, includ- have significantly degraded its environmental quality ing drill cutting discharges, submarine outfalls, harbour (Belzunce et al. 2001, 2004a,b). Hence, the estuary and dyke construction, heavy-metal inputs, eutrophica- received (before treatment in 1984) some 250 000 m3 tion, engineering works, diffuse pollutant inputs, dredg- d–1 of urban wastewaters and 67 000 m3 d–1 of indus- ing processes, mud disposal, sand extraction, oil spills trial waters (produced mainly by the chemical, iron- and fish farming (Muxika et al. 2005). The geographical steel and paper sectors), highly charged with toxic areas where it has been applied extend to the Atlantic products (cyanide, heavy metals, fluorides and phe- Sea, Baltic Sea, Mediterranean Sea, North Sea and Nor- nols) (Azkona et al. 1984). This produced extremely wegian Sea, all in Europe; also in Hong Kong, Uruguay low concentrations of dissolved oxygen in the waters Fig. 1. Geographical location of Nervión estuary, within Bay of Biscay and northern Spain, showing sampling stations and main locations mentioned in text. STP = sewage treatment plant discharge at Galindo Borja et al.: Benthos recovery following sewage treatment 45 and a high content of organic matter and heavy metals (0.1 m2). The samples were sieved immediately follow- in the sediments (Belzunce et al. 2001, 2004b, Landajo ing collection using a sieve with a mesh size of 1 mm et al. 2004). and fixed in a solution of 4% formalin stained with rose These discharges led to a deterioration in the soft- Bengal (Holme & McIntyre 1971). and hard-bottom benthic communities (Gorostiaga et Sediment data. At each station, a third grab was al. 2004). The results obtained from an initial survey taken for sediment analysis (redox potential, organic (Rallo et al. 1988) revealed that the main feature matter content and metals). The redox potential was underlying the spatial distribution patterns of benthic measured, immediately after placing the sample on communities was a stress gradient from the open coast board the survey vessel, with an Orion 977800 plat- towards the pollution source (the Nervión River). inum electrode; this was connected to a Crison 501 pH- Consequently, in 1979, in order to reverse this situa- meter-millivoltmeter. The electrode was inserted some tion of poor environmental quality, a sewerage scheme 5 cm into the sediment directly without disturbing the for the area was approved by the Consorcio de Aguas sample within the grab. Bilbao-Bizkaia (henceforth Consorcio); this is the local A 200 g sediment sample was dried at 80°C for 24 h; authority responsible for water supply and wastewater it was then washed with freshwater on a sieve mesh of treatment. The diversion of outfalls began in the late 63 µm. The dried residue was sieved on a column of 8 1980s, and the ‘clean-up’ of water began in 1991 with sieves (4 mm to 31 µm). The percentages of gravel, physico-chemical treatment (Franco et al. 2004); in sand and mud were calculated as >2 mm fraction, 1995, the company causing most of the pollution in the 63 µm to 2 mm and <63 µm, respectively (Holme & estuary (the iron and steel company Altos Hornos de McIntyre 1971).