Accumulation of Copper and Other Elements by the Apple Snail Pomacea Canaliculata
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Accumulation of copper and other elements by the apple snail Pomacea canaliculata Silvia C. Peña Naga City Employees Housing Project, San Felipe, Naga City, Philippines. Email: [email protected], [email protected] Abstract Heavy metal pollution is now prevalent in almost all aquatic ecosystems and will eventually affect human health. There is, then, a need to monitor the presence of these heavy metals. Studies have shown that Pomacea canaliculata is a potential biomonitor of heavy metals in freshwater ecosystems because of its ability to bioaccumulate a wide array of elements and because it is a better accumulator than some of the other organisms considered. Studies of bioaccumulation by P. canaliculata are reviewed. Additional keywords: Ampullariidae, Filopaludina martensi, fresh water, heavy metals, Ipomoea aquatica, Mollusca, Potamogeton crispus, sediment Introduction The increasing accumulation of heavy metals in the environment, especially in aquatic ecosystems, needs monitoring and this calls for a monitoring tool. Several studies have been done to assess the apple snail Pomacea canaliculata as a metal biomonitor in freshwater ecosystems. Pomacea canaliculata is an agricultural pest that has continued to spread despite numerous attempts to eliminate it or prevent its spread. Since it cannot be eliminated, is found in almost any freshwater ecosystem in many countries, is big enough to provide sufficient material (soft tissue) for analyses and because it is easy to handle, easy to collect, easy to culture, long lived, numerous, sedentary and can survive for a long time without food, it has the potential to be used widely as a heavy metal biomonitor. This contribution reviews studies of Pomacea canaliculata that have been done to assess its bioaccumulation of heavy metals. 133 Review of studies of bioaccumulation by Pomacea A preliminary study was undertaken on the accumulation of heavy metals by Pomacea canaliculata and a bivalve (possibly Corbicula fluminea) in the Naga City River, Philippines (Peña, unpublished). Sediment, bivalve and apple snail samples were taken from the most contaminated part of the river. The river bed is a recipient of road run off, domestic sewage and effluents from markets and other commercial and industrial establishments of the city. The first samples were taken in May 1996 and analysed for heavy metal content using flame atomic absorption spectrophotometry (Table 1). Cadmium (Cd) in the sediment was below the detection limit of the instrument but accumulated by the snail and the bivalve from the sediment. Chromium (Cr) was not detected in snail and bivalve samples and lead (Pb) was not detected in the bivalve. Snail soft tissue contained much higher values of copper (Cu) and zinc (Zn) than the sediment. The concentrations of cobalt (Co), iron (Fe), manganese (Mn), nickel (Ni) and Pb in the snail samples were much lower than in the sediment. The metal concentrations in the bivalve were much lower than in the sediment except for Cu and Cd, and all metal concentrations were much lower than those in the snail. Thus, Cd, Cu and Zn are Table 1. Heavy metal concentrations in sediment, water, apple snails and bivalves in the Naga City River, Philippines, 1996 and 2004. Heavy metal concentration mg/kg Sediment Water Snail Bivalve 1996 2004 2004 1996 2004 1996 Cadmium (Cd) * * * 0.798 * 0.304 Cobalt (Co) 47.7 – – 14.5 – 1.83 Chromium (Cr) 60.8 – – * – * Copper (Cu) 33.2 141 * 373 1050 40.0 Iron (Fe) 114,000 – – 9460 – 1080 Lead (Pb) 54.7 – – 7.04 * Manganese (Mn) 1360 – – 520 – 85.7 Nickel (Ni) 29.2 – – 9.48 – 5.67 Zinc (Zn) 55.6 250 0.028 1450 580 0.669 134 BIOLOGY AND MANAGEMENT OF INVASIVE APPLE SNAILS accumulated by the snail from the river sediment better than the other metals, and the snail is a better accumulator of heavy metals than the bivalve. As a follow up, samples of water, sediment and apple snails were taken from the same river and the same site in September 2004. They were analysed for the presence of Cd, Cu and Zn, the metals better accumulated by the snails in the 1996 samples (Table 1). The concentrations of Cu and Cd in the water were below the detection limit of the instrument. Cd was also not detected in the sediment and snails. The concentration of Zn in the water was far below that in the sediment but the concentration in the snail tissue was more than twice that in the sediment. Cu concentration in the snails was seven times higher than that in the sediment. The concentrations of Cu and Zn were much higher in 2004 than 1996 in the sediment and snails but the proportional difference between the levels in the snails and the sediment for these elements was higher in 1996 (Table 1). These results confirm that the metal concentration in sediment is much higher than that in the water and that Cu and Zn are bioaccumulated by the snails. The results also show that there is a continued supply of Cu and Zn into the river but that the accumulation pattern of the snails differed between 1996 and 2004. There could be changes in the conditions of the river that caused the lower uptake of the metal by the snails but the level in the snails is still higher than that in the sediment. These preliminary results indicated that Pomacea canaliculata could be used as a biomonitor especially for Cd, Cu and Zn. Although other metals were detected in the snails, it is a particularly strong net accumulator of Cd, Cu and Zn. Following the preliminary study a further study was undertaken focussing on accumulation of Cu by Pomacea canaliculata (Peña & Pocsidio, 2008). Cu and Zn are essential elements, micronutrients, but become toxic above certain threshold levels; Fig. 1. Rate of copper accumulation above basal level from food (previously soaked in 67.5 μg/L Cu solution), sediment (from the Naga City River) and from water (Merck titrisol Cu (1000 mg/L) added to a final concentration of 67.5 μg/L) by the different organs of Pomacea canaliculata (from Peña & Pocsidio, 2008). ACCUMULATION OF COPPER AND OTHER ELEMENTS BY THE APPLE SNAIL POMACEA CANALICULATA 135 however, Cu is much more toxic than Zn. Three-month old apple snails were exposed for seven days to five Cu concentrations: 20, 30, 45, 67.5 and 101.25 µg/L.The experiment was done under natural photoperiod (13:11 h light:dark) at pH 6.0-6.5, 7-8 ppm dissolved oxygen and temperature of 28-32o C. Behavioural responses (closing of operculum, respiratory pumping, mucus secretion) were only seen at 67.5 and 101.25 µg Cu/L. Cu was accumulated by the snails at all concentrations, with the control having the lowest levels (15.47 ± 3.29 µg/g dry weight) and those exposed to 45 µg/L having the highest levels (90.98 ± 15.21). Levels in the 45 and 67.5 µg/L treatments were significantly greater than in the control at the 5% significance level (ANOVA followed by Tukey’s multiple comparison test). The reduction of net accumulation at high copper concentrations could be explained by behavioural responses of the snails. At 67.5 µg/L, if they could still remain upright, they still opened the operculum but showed increased respiratory pumping and produced more mucus, which might reduce net copper accumulation. At 101.25 µg/L the snails never opened the operculum until they became flaccid, signalling the lethality of the solution, although copper was still accumulated in their tissues despite the closed operculum. When exposed to sediment from the Naga City River (Table 1), the snails had an accumulation rate of 8.97 µg Cu/g/day and an assimilation efficiency of 89%, indicating a high capacity to accumulate and assimilate copper from food and the surrounding environment in just a seven-day exposure. Whole soft tissue copper accumulation from dissolved Cu, sediment and food differed significantly from those of the controls. Cu uptake from the sediment and dissolved Cu do not differ significantly but they are significantly higher (p < 0.05) than that from the food (Fig. 1). There were no significant differences (p > 0.05) in total Cu accumulation (from dissolved Cu, sediment and food) among the snails’ organs (kidney, digestive system, foot, gills), though the highest value of accumulated Cu was in the gill (Fig. 1). Gills absorbed by far the most dissolved Cu from the water (Fig. 1). The gill is the route of exposure for dissolved Cu. Pomacea canaliculata is thus a good Cu accumulator at sublethal concentrations and could be used as a biomarker at high concentrations. Dummee et al. (2012) studied accumulation of heavy metals by a species of Pomacea in Thailand (although identified as Pomacea canaliculata, it could have been P. maculata, as both are present in Thailand and many authors have not distinguished them). They studied seasonal changes in the concentrations of Cu, Mn, Fe, Zn, Pb and Cd in water, sediment, Pomacea and the aquatic plant Ipomoea aquatica in three tributaries of Beung Boraphet reservoir, Nakhon Sawan province, central Thailand. Fe, Cu, Mn and Zn were detected in all sediment samples (both in wet and dry seasons) using a flame 136 BIOLOGY AND MANAGEMENT OF INVASIVE APPLE SNAILS atomic absorption spectrophotometer. Cd and Pb were below detection limits. Metal concentrations in sediment were in the order Fe > Mn > Cu > Zn. Fe, Mn, Cu and Zn were found in Pomacea tissues and the Mn concentration was higher than that in the sediment, especially in the wet season (33 times higher). The bioconcentration factors (BCF) in snails were in the order Mn > Zn > Cu > Fe and in the plant were Mn > Zn > Fe > Cu.