Periphyton Changes Over 20 Years of Chemical Recovery of Lake Orta, Italy: Differential Response to Perturbation of Littoral and Pelagic Communities
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J. Limnol., 70(2): 177-185, 2011 DOI: 10.3274/JL11-70-2-03 Periphyton changes over 20 years of chemical recovery of Lake Orta, Italy: differential response to perturbation of littoral and pelagic communities Antonella CATTANEO*, Michèle DE SÈVE1), Giuseppe MORABITO2), Rosario MOSELLO2) and Gabriele TARTARI2) GRIL, Département de sciences biologiques, Université de Montréal, C.P. 6128, succ. Centre Ville, Montréal, QC, H3C 3J7, Canada 1)M.A. De Sève Consultants, 1232 Ducharme, app.1, Montréal, QC, H2V 1N4, Canada 2)C.N.R., Istituto Italiano per lo Studio degli Ecosistemi, L.go Tonolli 50, 28922 Pallanza, Italy *e-mail corresponding author: [email protected] ABSTRACT Lake Orta, a large Italian subalpine lake, has a long history of industrial pollution by acid, ammonia, and metals. A whole-lake liming treatment in 1989-1990 led to a gradual increase in pH (from 4.4 to 7) and a concomitant decline in ammonia (from 2.5 to 0.05 mg L-1) and metal concentrations (e.g., copper: from 35 to 3 µg L-1). In this study, we examine the response of the littoral zone, in terms of chemistry and periphyton assemblages, to contamination and recovery of Lake Orta. We compare these findings with a long-term data set of chemistry and phytoplankton collected in the pelagic zone. We sampled periphyton at two sites from the liming period (1989) through 2010 when the lake approached chemical equilibrium. Chemical variables collected in the littoral zone near the periphyton samples followed the same temporal trends observed in the pelagic zone. Chlorophytes, the dominant algae in the pre- liming period, progressively waned after the calcium carbonate addition. Diatom importance gradually increased to reach up to 80% of the total biovolume in the most recent years. There was a clear shift in the diatom taxonomic composition over the study period. Acidophilous Pinnularia subcapitata var. hilseana and metal-tolerant Achnanthes minutissima were dominant before liming. With the progressive increase in pH and decline in metal concentrations, there was successively the dominance of Fragilaria nanoides (formerly identified as Synedra tenera) and Cymbella microcephala in the transition period and of circumneutral Navicula cryptocephala, N. radiosa, and Synedra ulna in the most recent period. Pelagic diatoms were more affected than benthic diatoms by the industrial pollution and their recovery after the liming intervention was slower. Whereas present periphyton diatom assemblages are similar to those observed in nearby unpolluted Lake Mergozzo, pelagic assemblages are still in transition from severe disturbance towards characteristics reported before pollution. Our results suggest that the littoral zone may have acted as a refugium during contamination providing an inoculum for pelagic recolonization. Key words: metal contamination, liming, acidification, diatoms, phytoplankton fied Adirondack lakes (Charles 1985). In a lake affected 1. INTRODUCTION by watershed fires, benthic diatoms increased in periods Studies of anthropogenic stress in lakes are usually of perturbation (Philibert et al. 2003). The higher stress centered on the response of pelagic communities. tolerance of benthic taxa relative to the planktonic ones Monitoring of impact and recovery are mostly based on could be ascribed to a superior plasticity of littoral open water measurements of chemical and biological organisms, which are adapted to life in a highly variable characteristics. However, there are increasing evidences environment. This plasticity could lead to the replace- suggesting that the littoral zone may respond differently ment of planktonic taxa by usually benthic ones. from the open water because stress intensity could be Lake Orta, a large Italian subalpine lake, has a long different in the two habitats. The littoral zone is directly history of industrial pollution resulting in severe acidifi- affected by watershed inputs, which could either inten- cation and high metal concentrations (Bonacina et al. sify or lessen the contaminant concentrations. Further- 1986). A liming intervention in 1989-90 is leading to more, contaminant transfer may be slowed in thick progressive lake recovery (Calderoni & Tartari 2001). benthic biofilms because organisms are densely packed The objectives of this study were to examine the with abiotic material and metals may be bonded by response of the littoral zone, in terms of chemistry and polymers exuded by algae and bacteria (Ivorra et al. periphyton assemblages, to contamination and recovery 2000). of Lake Orta. We then compare these findings with a Planktonic diatoms were more affected than benthic long-term data set of chemistry and phytoplankton col- taxa in lakes heavily contaminated by metals in Abitibi, lected in the pelagic zone. We aim to test whether the Quebec (Cattaneo et al. 2008) and in Finland (Salonen response of the littoral zone to these anthropogenic dis- et al. 2006). A shift towards benthic diatoms has also turbances is different from that observed in the pelagic been documented under other stresses. Planktonic dia- water. In particular, we examined the possibility that the toms disappeared almost completely in severely acidi- littoral zone may provide a refugium in contaminated 178 A. Cattaneo et al. Fig.1. Map of Lake Orta with the two periphyton sampling stations. lakes in view of the different environmental conditions several plating factories started discharging directly into and the high plasticity of benthic communities. the lake large quantities of copper (Cu), nichel (Ni), zinc (Zn), and cromium (Cr). Furthermore, since the 2. LAKE ORTA l960s, in lake biochemical oxidation of ammonium acidified the lake water, which had naturally poor buff- Lake Orta (1.3 billion m3, max depth 143 m, surface -1 2 ering capacity (total alkalinity 0.3 0.4 meq L ) due to 18 km ) is an important subalpine Italian lake (Fig. 1). watershed geology. The lowest pH of 3.8 over the The lake basin was created by glacial erosion of a pre- whole water column was reached in 1985 (Vollenweider existing river valley. Gneiss, micaschists and granites 1963; Bonacina et al. 1986; Calderoni & Tartari 2001). prevail in the catchment basin so that the lake water is Despite actions in the 1980s to reduce ammonium naturally poorly buffered. Although mean annual pre- sulphate discharge, lake water pollution remained high, -1 cipitation rates are fairly high (1900 mm y ), the theo- due to the low pH (4.0-4.5) produced from the oxidation retical water residence time is quite long (8.5 y) of the ammonium still present in the water mass, which (Mosello et al. 1989). Only a few studies of the lake permitted high concentrations of trace metals (Fig. 2). A biota were made before the onset of the pollution in liming intervention was proposed by the Istituto Italiano 1926. Nevertheless, they demonstrate that the lake was di Idrobiologia (National Research Council) to acceler- oligotrophic, rich in high value fish species, and very ate lake's recovery from acidification. The liming was similar to the other oligotrophic subalpine lakes. In that done from May 1989 to June 1990 by spreading on the year, a rayon factory was built on the southern shore of lake surface a suspension of 14,800 t of finely powdered the lake, which directly discharged into the south basin natural limestone (Mosello et al. 1991; Calderoni et al. heavy loads of copper and ammonium sulphate (max 1992; Calderoni & Tartari 2001). -1 -1 loads 80 t Cu y and 3000 t N NH4 y ) (Bonacina 2001). The early effect was a dramatic disappearance 3. METHODS within two years of most biota, mainly due to copper toxicity. In the fifties, only a few phytoplankton species 3.1. Chemistry (Oscillatoria limnetica, Choricystis minor), one zoo- To monitor the chemical variables in the littoral, plankton (Cyclops strenuus), and few littoral fish were subsurface water samples were collected near the stones present; profundal benthos had disappeared. sampled for periphyton (see below). Pelagic samples In 1958, a treatment plant for copper recovery was were always collected in the zone of maximum depth of adopted by the rayon factory; however in the meantime, the lake. Analyses were performed on samples collected Periphyton changes throughout chemical recovery of Lake Orta 179 Fig. 2. Trends of concentrations of ammonium, nitrate, and pH (left panel) and of copper, zinc, and aluminum (right panel) measured in Lake Orta at spring circulation (whole lake volume weighted mean values). near the surface, in the epilimnion (0-25 m), and in the used for identification and nomenclature were those of hypolimnion (25-143 m). Whole lake concentrations Krammer and Lange-Bertalot (1986-1991). Cell vol- were calculated using volume weighted concentrations umes were calculated by approximation to solids of at the different depths. known volume. All chemical analyses were performed in the labo- ratory of the Institute of Ecosystem Studies using stan- 3.3. Phytoplankton dard analytical methods for natural water analyses. Water samples for phytoplankton analysis were col- Details are reported by Tartari & Mosello (1997). The lected monthly from January to December, at the station laboratory adopts strict QA/QC protocols and partici- corresponding to the deepest point of the lake. Only pates in national and international interlaboratory exer- mid-summer data are presented in this paper in order to cises (Uggerud & Hjellbrekke 2009a, b; Hovind 2010; compare with periphyton that was sampled only in that Marchetto et al. 2010). Special attention is given to season. Samples were taken with a Niskin bottle, col- avoid systematic errors due to changes of analytical lecting one sample every 2 m, in order to get an inte- methods, which may occur in long term studies, such as grated sample in the 0-20 m water layer. Phytoplankton the present one. determinations were carried out on sub-samples pre- served in acetic Lugol's solution. Algal cells (including 3.2. Periphyton ultraplankton cells of about 3-4 µm diameter) were Epilithon was sampled at two stations of Lake Orta counted on a Zeiss Axiovert 10 microscope, following (Valle and Crabbia; Fig.