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metals by Pomacea canaliculata and a bivalve (possibly Corbicula fluminea) in the Naga City River, Philippines (Peña, unpublished).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. Both Pomacea and Ipomoea aquatica have more Mn in their tissues than in the sediment. Mn levels were positively correlated between sediment and snails (R = 0.959), sediment and plants (R = 0.891) and snails and plants (R = 0.793). Positive correlations were also found between Zn (R = 0.926) and Cu (R = 0.910) concentrations in snails and those in the sediment (Pearson correlation, P < 0.01 in all cases). At one station Mn and Zn concentrations were higher in the dry season while Cu concentration was higher in the wet season. Fe did not show significant seasonal variation. In a laboratory experiment in which three-month old snails were exposed to contaminated sediment for two months, Fe and Mn concentrations were significantly higher in the digestive gland (P < 0.05) than in other organs studied but there were no significant differences in Cu and Zn levels among organs (P > 0.05). Mn accumulation by Pomacea in the study of Dumee et al. (2012) is not in agreement with the result of Peña (2004) who found Mn levels in the snails to be lower than in the sediment. However, both studies showed that Cu accumulated more in digestive gland than in foot muscle and that there was no statistically significant difference in Cu concentrations among the organs studied. They also both showed that Fe concentration in snail tissue was lower than in the sediment and that Zn concentration in the snails was higher than the Cu concentration (in Peña’s 1996 study but not her 2004 study). Kruatrachue et al. (2011) investigated accumulation of heavy metals by a species of Pomacea they identified asP. canaliculata (this also could have been P. maculata) in the Mae Klong River (Samut Songkhram Province), which is one of the largest and most important rivers in Thailand. Sediments were taken from the river and its tributaries and analysed for Cd, Cr, Cu, Fe, Pb, Ni and Zn content using mass spectrometry. A laboratory experiment exposed the snails to these sediments for three months in water at

25 ± 2 °C, pH 6.8-7.3 and dissolved O2 7.5-7.8 mg/L. Heavy metals in digestive gland, digestive tract and gill were determined using a graphite atomic absorption spectrometer for Cd, Cr, Pb and Ni and a flame atomic absorption spectrophotometer for Cu, Fe and Zn. Concentrations in sediments were ranked as follows: Fe > Zn > Pb > Cr > Cu > Ni > Cd. The highest concentrations did not exceed the probable-effects levels of the US Environmental Protection Agency (1997). No snails died after three months exposure.

Accumulation Of Copper And Other Elements By The Apple Snail Pomacea Canaliculata 137 Tissue-specific analyses showed that Zn, Cr and Fe were stored mainly in the digestive gland. Levels of Cu did not differ significantly among organs (digestive tract, digestive gland, gill), as reported by Peña & Pocsidio (2008) and Dummee et al. (2012), although the gill showed the highest concentration, as also reported by Peña & Pocsidio (2008), and Fe levels being higher in the digestive gland agrees with the results of Dummee et al. (2012). Levels of some Cu and Zn were much greater in snails than in sediments (19 and 39 times respectively), as also found in Peña’s 2004 study, above, indicating that they were more available to snails than the other metals in these studies, and exceeded the standard limits for consumption (20 µg/g for Cu, 100 µg/g for Zn; Ministry of Public Health, Thailand) and may therefore be of concern. Sumritdee (2007) also studied metal accumulation by Pomacea in the Mae Klong River tributaries, providing data on levels in the sediment, snails from the tributaries and snails exposed experimentally to the sediment for 3 months (Table 2). Snails from the river exhibited the highest accumulation of Ni, Fe, Zn and Cd in the digestive gland, while kidney had the highest accumulation of Cu, Pb and Cr. Experimental snails had the highest levels of Cr, Zn and Fe in the digestive gland, the highest level of Ni in the gills, of Cu in the kidney and of Pb in the digestive tract. Cd was found in gill, digestive gland and digestive tract. That the highest level of Cu was found in the kidney, both in the wild and experimental snails, agrees with the result of Peña & Pocsidio (2008; Fig. 1). Kruatrachue et al. (2011) did not analyse kidney and found the Cu level to be highest in

Table 2. Heavy metal concentrations in sediment and apple snails from the Mae Klong River tributaries, Thailand (range of values), and apple snails exposed experimentally to the river sediment (mean values) (from Sumritdee, 2007).

Heavy metal concentration mg/kg

Sediment Snails from river Experimental snails

Digestive Digestive Digestive Kidney Gill Kidney Gill gland gland tract

Cadmium (Cd) 0.02-0.83 0.01-0.33 0.00-0.13 0.00-0.03 0.01 <0.005 0.01 0.01

Chromium (Cr) 2.90-14.3 0.02-0.80 0.00-6.25 0.00-0.05 1.15 <0.005 <0.005 <0.005

Copper (Cu) 1.72-57.5 6.00-176 0.00-781 35.3-224 44.87 70.93 96.49 94.27

Iron (Fe) 2,466-11,906 2,315-12,417 0.00-1,795 0.00-533 2,439 1,101 1,235 345

Lead (Pb) 3.53-18.9 0.05-3.86 0.00-55.8 0.00-36.2 0.09 0.15 <0.005 0.01

Nickel (Ni) 1.42-11.6 0.12-0.88 0.00-0.22 0.02-1.54 0.08 0.08 0.00 0.18

Zinc (Zn) 7.23-271 171-2,800 19.8-75.6 19.5-54.4 1657 1,657 10.57 <0.005

138 Biology and Management of Invasive Apple Snails the gill. Both Kruatrachue et al. (2011) and Sumritdee (2007), in the experimental snails, found higher concentrations of Fe, Zn and Cr in the digestive gland and Ni in the gills. However, the snails from the wild in the study of Sumritdee (2007) concentrated more Ni and Cd as well as Fe and Zn, but less Cr in the digestive gland. The highest level of Fe being in the digestive gland (Sumritdee 2007) agrees with the study of Dummee et al. (2012). A study in Argentina (Vega et al. 2012) on the differential ability of apple snail tissues, endosymbionts and eggs to bioaccumulate Zn, Cr, Fe, as well as antimony (Sb), arsenic (As), barium (Ba), bromine (Br), mercury (Hg), selenium (Se) and uranium (U) exposed Pomacea canaliculata from a cultured strain to drinking water and reconstituted water. The highest bioconcentration factors (BCF), in decreasing order, were: in the midgut gland, Ba, Zn, Se, As, U, Br and Hg; in the kidney, Ba, Br and Hg; and in the foot Ba, Hg, Br and Se, with the low levels of Fe and Zn in the foot agreeing with the results of Dummee et al. (2012). Calcified tissues (uterus containing eggs, shell) and eggs showed low BCFs except for Ba. Both C corpuscles (putative endosymbionts) and midgut gland tissue showed statistically higher BCFs than K corpuscles (the alternate form of the endosymbionts) for Ba, Fe, U, Br and Sb. The concentration of most of the elements was significantly lower in tissues and endosymbionts obtained from snails cultured in reconstituted water than in drinking water. Snails cultured in reconstituted water and then exposed to Hg, As and U (at the maximum contaminant level allowed by the US Environmental Protection Agency) also accumulated high levels in the midgut gland, endosymbionts and kidney. Vega et al. (2012) suggested that the midgut gland (and the symbionts therein), kidney and foot may be useful bioindicators of Hg, As and U pollution in freshwater bodies and that the unrestricted use of ampullariid snails as human and animal food must be considered with caution. Ruangareerat (2004) undertook experiments on juvenile Pomacea sp. in Thailand to assess the bioaccumulation of Hg, Cd and Cu and the possibility of using Pomacea sp. as a biomonitor for heavy metal contaminants in freshwater resources. Snails were exposed to a range of concentrations of each of Hg, Cd and Cu for 96 h. Uptake was measured in the whole soft body by spectrophotometry. Hg, Cd and Cu were not detected in the controls, in either the water or the snails. In all treatments, the concentration of Hg, Cd and Cu in the snail tissue differed significantly (P ≤ 0.05) from the control, and the concentration of the three metals in the snail tissue was higher than in the water to which they were exposed. The higher the metal concentration in the water, the higher it was in

Accumulation Of Copper And Other Elements By The Apple Snail Pomacea Canaliculata 139 the soft tissue. The bioconcentration factors were 7000-10,830 for Hg, 1000-1253 for Cd and 989-4543 for Cu. Pomacea sp. have also been used in a bioaccumulation study of radionuclides and heavy metals from lakes formed from abandoned mines in Kampung Gajah, Perak, Malaysia (Redwan, 2008). Element concentrations in snail muscle tissue were determined via short and long radiation at Nuclear Malaysia using the nuclear activation analysis method. The short radiation detected vanadium (V, 3.45 ppm), aluminium (Al, 127,367 ppm), manganese (Mn, 174.5 ppm), chlorine (Cl, 0.205 ppm), potassium (K, 5920 ppm) and sodium (Na, 2665 ppm); the long radiation, detected uranium (U, 1.73 ppm), bromine (Br, 0.616 ppm), arsenic (As, 31.23 ppm), ytterbium (Yb, 179.0 ppm), thorium (Th, 2351 ppm), cesium (Cs, 14.08 ppm), scandium (Sc, 1.28 ppm), iron (Fe, 2795 ppm) and samarium (Sm, 228.8 ppm). This study demonstrated the presence of these elements, including radioactive ones, in the snails, and therefore the possibility of their bioaccumulation by the snails. Another study, in the Niger Delta, Nigeria, on several freshwater snails identified as Pomacea canaliculata, Pomacea bridgesii and Lanistes libycus (the first two species are almost certainly incorrectly identified, as neither has been reported fromWest Africa previously; it is more likely that they were species of Pila; R.H. Cowie, pers. comm.) has been undertaken to investigate heavy metals in the edible portion of the snails (Adebayo- Tayo et al., 2011). Concentrations determined using atomic absorption spectrophotometry in the species identified asPomacea canaliculata were: Fe, 21.3-28.6 mg/kg; Zn, 83.2- 86.3 mg/kg; Cu, 12.6-15.7 mg/kg; Mg, 0.262-0.293 mg/kg; Mn, 58.6-71.8 mg/kg; Pb, 0.07-0.11 mg/kg; As, 0.04-0.15 mg/kg. Comparing the mean metal accumulation among the species, the species identified asP. canaliculata had the highest uptake of Fe, that identified asP. bridgesii the highest of Cu, Pb and As, and L. libycus the highest of Mg and Mn, although the values did not differ much among them. Concentrations were high except for Pb and As but the majority were within the standard limits prescribed by the Commission of the European Community and FAO. Adebayo-Tayo et al. (2011) suggested that these concentrations in the snails could be related to industrial and other human activities in the area, and that the presence of heavy metals, combined with the microbial status of the snails may mean that they are not totally safe for human consumption and may pose a serious health hazard to consumers. Another study in Thailand was undertaken in Beung Jode reservoir in Ban Gudnamsai, Nampong district, Khon Kaen province (Neeratanaphan & Phalaraksh, 2008). This reservoir receives a considerable amount of effluent from a paper mill factory

140 Biology and Management of Invasive Apple Snails before flowing into the Pong River. Nongbualamphu and Khon Kaen provinces use water in this river for daily use and agriculture. Concentrations of heavy metals in the water, sediments and snails were determined using an optical emission spectrometer in three consecutive seasons: rainy, cold-dry and hot-dry. The mean sediment concentrations were in the order Zn > Cu > Pb > Cd > Hg in the rainy season, while in cold and hot seasons they were in the order Zn > Pb > Cu >. Zn concentration was highest in the cold season, followed by the hot season and then by the rainy season. Mean concentration of Pb was highest in the hot season followed by the cold and rainy seasons. The concentrations of Cu were higher in the rainy season compared with the hot and cold seasons while Cd was only detected in the rainy season. Hg could not be detected in the sediment but was detected in the snails in the rainy season. Two snail species were analyzed: Filopaludina martensi (Viviparidae) and a species identified asPomacea canaliculata (which may be incorrect, see above). The concentrations of the metals in snails were in the order Zn > Cu > Pb in all three seasons. Heavy metal, especially Zn, concentrations in the snails were higher during the rainy season than in the dry seasons. In the rainy season, mean concentrations of Hg and Cd were 0.21 and 0.32 mg/kg respectively, while in the dry seasons neither could be detected. Zn concentration in Filopaludina martensi was higher than in Pomacea canaliculata but there were no differences between the species for the other metals. The concentrations of metals were higher in the snails than in the sediment, indicating that the snails, which were exposed to effluent from the paper mill, accumulate heavy metals in their tissues. Losussachan (2006), also in Thailand, used atomic absorption spectrophotometry to assess heavy metal contamination seasonally in the Phi Lok canal system, Phraek Nam Daeng district, Samut Songkhram province, assessing accumulation of Cd, Cu, Fe, Pb and Zn in the water, sediment, Pomacea sp. (identified asP. canaliculata) and fish. Heavy metal levels were in the order sediment > snail > fish > water and were highest near pig farms and lowest at fish and shrimp raising ponds, but varied according to the particular heavy metal, habitat, feeding behaviour and the animals’ desorption mechanism. In no case did heavy metals exceed values for human consumption designated by various health organizations. Seasonally, heavy metal concentrations in water were in the order cold > rainy > hot season, whereas those in sediment and snails were in the order rainy > cold > hot. This seasonality in the snails agrees with the findings of Neeratanaphan & Phalaraksh (2008) but is contrary to those of Peña (2004), who recorded higher Cu and Zn concentrations during the rainy season (September) than the hot season (May). Factors other than season may affect accumulation.

Accumulation Of Copper And Other Elements By The Apple Snail Pomacea Canaliculata 141 Finally, in southern China Deng et al. (2008) assessed Potamogeton crispus and a species of Pomacea (probably P. canaliculata) as potential biomonitors for metal contamination in the sediment. Samples (leaves of pondweed, snails and sediment) were collected in March 2004 from eight sites in Fankou Stream, which receives the wetland-treated effluent from Fankou Pb/Zn mine, and analyzed spectrometrically. There were statistically significant correlations between the concentrations of Pb and Zn in pondweed tissue and sediment. Cu concentration was highest at the site closest to the mine and lowest at the site farthest from the mine, but this trend for Cu was not as obvious as for the other metals, suggesting Cu accumulation by the pondweed was less dependent on Cu level in the sediment. Cd in the pondweed at the site farthest from the mine was much higher than in uncontaminated macrophytes. There was no significant correlation between metals in the snail tissue and those in the sediment, nor between the snails and the pondweed. Much higher levels of Cd, Cu, Pb and Zn were associated with the viscera than the head-foot. This suggests that P. crispus possesses several attributes of a biomonitor and its tissue concentrations of Cd, Pb and Zn may reflect the levels of sedimentary contamination by these metals, but that P. canaliculata, although it may accumulate metals to high levels, can only serve as an indicator of metal contamination and not of its level because tissue metal concentrations did not correlate with those of the sediment nor of the pondweed.

Conclusion

The studies summarised here show that species of Pomacea have potential as metal biomonitors over a wide geographical range. Pomacea bioaccumulates a wide range of elements: essential elements and heavy metals as well as radionuclide/radioactive elements. It is a strong (exceeded environmental concentrations) accumulator of Cu, Zn, Cd, Mn, Pb, Fe and Hg (this last at least in the rainy season). The snails accumulate Cu in proportion to the concentrations to which they are exposed, even for a short time (7 days) at sublethal concentrations. However, some results were inconsistent with this, reporting that although the snails accumulate metals to high levels and can serve as indicators of metal contamination, their tissue metal concentrations did not always correlate with those of the sediments or macrophytes. Thus, the pondweed Potamogeton crispus was considered better than P. canaliculata as a potential biomonitor because its metal concentrations correlated with those of the sediment (Deng et al., 2008). Another aquatic plant, Ipomea aquatica, exhibited similar

142 Biology and Management of Invasive Apple Snails bioconcentration regarding Mn (Dummee et al., 2012). Pomacea was a better metal accumulator than an unidentified bivalve (Peña, 2004) and fish (Losussachan, 2006). Bioaccumulation varied among species of ampullariid snails but the differences were not great (Adebayo-Tayo et al., 2011), and there was little difference between another snail, Filopaludina martensi, and Pomacea other than that the former exhibited higher Zn concentrations (Neeratanaphan & Phalaraksh, 2008). While some studies analysed the entire snail soft tissue, others used digestive gland, digestive tract, kidney, gill and foot, all of which exhibited bioaccumulation, but to varying degrees. Bioavailability of heavy metals depends on many factors but for a broad scale assessment Pomacea has potential as a biomonitor of heavy metal contamination in freshwater ecosystems.

Acknowledgments

Thank you to my family for being very supportive, especially to my youngest brother, Vice Governor Ato Peña, and his wife, Ses, who together with Javib and Calai, Pangpang and Donald encouraged me to write this contribution. My deepest thanks also go to my friend Dr. Rofeamor Obena for sending me some articles for this chapter.

References

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144 Biology and Management of Invasive Apple Snails