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Article

Heavy Metal Exposures on Freshwater Snail Pomacea insularum: Understanding Its Biomonitoring Potentials

by
Chee Kong Yap
1,*,
Bin Huan Pang
1,
Wan Hee Cheng
2,
Krishnan Kumar
2,
Ram Avtar
3,
Hideo Okamura
4,
Yoshifumi Horie
4,
Moslem Sharifinia
5,
Mehrzad Keshavarzifard
5,
Meng Chuan Ong
6,7,
Abolfazl Naji
8,9,
Mohamad Saupi Ismail
10 and
Wen Siang Tan
11,12
1
Department of Biology, Faculty of Science, Universiti Putra Malaysia, 43400 UPM Serdang, Selangor, Malaysia
2
Faculty of Health and Life Sciences, INTI International University, Persiaran Perdana BBN, Nilai 71800, Negeri Sembilan, Malaysia
3
Graduate School of Environmental Science, Hokkaido University, Sapporo 060-0810, Japan
4
Graduate School of Maritime Sciences, Faculty of Maritime Sciences, Kobe University, Kobe 658-0022, Japan
5
Shrimp Research Center, Iranian Fisheries Science Research Institute, Agricultural Research, Education and Extension Organization (AREEO), Bushehr 7516989177, Iran
6
Faculty of Science and Marine Environment, Universiti Malaysia Terengganu, Kuala Nerus 21030, Terengganu, Malaysia
7
Ocean Pollution and Ecotoxicology (OPEC) Research Group, Universiti Malaysia Terengganu, Kuala Nerus 21030, Terengganu, Malaysia
8
Department of Fisheries, Faculty of Marine Science and Technology, University of Hormozgan, Bandar Abbas 7916193145, Iran
9
Leibniz Centre for Tropical Marine Research (ZMT), Wiener Str. 7, 28359 Bremen, Germany
10
Fisheries Research Institute, Batu Maung, Pulau Pinang 11960, Malaysia
11
Laboratory of Vaccines and Biomolecules, Institute of Bioscience, Universiti Putra Malaysia, 43400 UPM Serdang, Selangor, Malaysia
12
Department of Microbiology, Faculty of Biotechnology and Biomolecular Sciences, Universiti Putra Malaysia, 43400 UPM Serdang, Selangor, Malaysia
 
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*
Author to whom correspondence should be addressed.
Appl. Sci. 2023, 13(2), 1042; https://doi.org/10.3390/app13021042
Submission received: 13 October 2022 / Revised: 16 November 2022 / Accepted: 7 January 2023 / Published: 12 January 2023
(This article belongs to the Special Issue Advances in Heavy Metal Pollution in the Environment)
Versions Notes

Abstract

:
The present investigation focused on the toxicity test of cadmium (Cd), copper (Cu), nickel (Ni), lead (Pb) and zinc (Zn), utilizing two groups of juvenile and adult apple snail Pomacea insularum (Gastropod, Thiaridae) with mortality as the endpoint. For the adult snails, the median lethal concentrations (LC50) values based on 48 and 72 h decreased in the following order: Cu < Ni < Pb < Cd < Zn. For the juvenile snails, the LC50 values based on 48 and 72 h decreased in the following order: Cu < Cd < Ni < Pb < Zn. The mussel was more susceptible to Cu than the other four metal exposures, although the juveniles were more sensitive than the adults because the former had lower LC50 values than the latter. This study provided essential baseline information for the five metal toxicities using P. insularum as a test organism, allowing comparisons of the acute sensitivity in this species to the five metals. In conclusion, the present study demonstrated that P. insularum was a sensitive biomonitor and model organism to assess heavy metal risk factors for severe heavy metal toxicities. A comparison of the LC50 values of these metals for this species with those for other freshwater gastropods revealed that P. insularum was equally sensitive to metals. Therefore, P. insularum can be recommended as a good biomonitor for the five metals in freshwater ecosystems.

1. Introduction

Metals are generally thought to be pollutants, although it is crucial to note that they are naturally occurring compounds. Nevertheless, anthropogenic activities have resulted in higher quantities of heavy metals in environmental matrices and living resources, which surpass natural background values [1,2].
Metals are nonbiodegradable, unlike organic insecticides, they cannot be decomposed into less hazardous components. To effectively manage metal pollution, the concentration dependence of toxicity must be understood. Dose-response relationships serve as the foundation for assessing the dangers and risks associated with environmental contaminants. Toxicity testing is an indispensable method for analyzing the effect and fate of toxicants in aquatic environments, and it has been widely used to select acceptable organisms as bioindicators/biomonitors, and to develop water quality standards for chemicals. There are numerous methods for measuring toxicity, but mortality is the most common endpoint [3,4]. Consequently, it is essential to perform studies with local organisms that may be utilized to obtain data on metal toxicity, to assess the sensitivity of the organisms and to derive an acceptable level for Malaysian water that can protect the local aquatic populations.
Mollusks have been considered attractive bioindicator and biomonitoring subjects for quite some time. They are abundant in numerous terrestrial and marine environments, and are readily collected. They display a high buildup of contaminants, particularly heavy metals [5]. The snail Pomacea (family: Ampullaridae) was chosen for testing because of its vast distribution and abundance in aquatic environments, such as rivers, paddy fields, lakes and ponds. Melo et al. [6] suggested that the selection of a test species for toxicity testing is essential for a precise evaluation of environmental impact. The organism must: (a) belong to an important ecological group in terms of taxonomy, trophic level or niche; (b) be widely available in its environment, easily cultivated in the laboratory; (c) have a consistent and measurable response to the toxicant; and (d) be genetically stable. Finally, investigators must be familiar with the organism’s physiology, genetics, taxonomy, behavior, etc. Pomacea insularum appears to fulfil all of these conditions, with the exception of a database. In the scientific literature, little is known about the hazardous effects of metals on this snail. However, a large body of literature has been published on the toxicity testing of heavy metals employing freshwater snails; Abdel Gawad [7] on Theodoxus niloticus, Ab-del-Moati and Farag [8] on Lanistes bolteni, and Shuhaimi-Othman et al. [9] on Melanoides tuberculosus.
Cadmium (Cd) is a non-essential element which is toxic to organisms, even in trace amounts [10], and it could pose renal toxicity issues in humans in elevated accumulation [11]. Cd accumulates to high levels in various aquatic creatures due to its high solubility in water [10,12]. Copper (Cu), on the other hand, is a vital metal for many animals, including humans, but slightly above the threshold would result in extreme toxicity for aquatic organisms [13,14]. Nickel (Ni)’s biological functions in animals and humans are not well studied, but elevated quantities may have carcinogenic consequences [15,16,17,18]. For numerous species of microorganisms and plants, Ni is essential for growth and development [18,19,20]. Elevated lead (Pb) has been linked to a variety of malignancies, cardiovascular illness, central nervous system disorders, liver and kidney damage, hearing impairment in children and newborns [21,22,23] and inhibition of enzyme activities [24,25]. Iron (Fe) is a component of hemoglobin in red blood cells, while zinc (Zn) is an important nutrient for plant growth, serving as a cofactor for over 300 proteins [26].
Considering the abovementioned impacts of the five potentially toxic metals (Cd, Cu, Ni, Pb and Zn) to humans, animals, plants and the environment, the goal of this study was to examine the toxicity of exposures to these metals by the use of juvenile and adult P. insularum as test organisms.

2. Materials and Methods

2.1. Sample Preparations and Laboratory Experiments

The snails, P. insularum, were collected from Universiti Putra Malaysia’s Lake (N 02°59′58.84″, E 101°42′39.42″), on the 11 March 2007. The lake is considered unpolluted with low Cu concentration in the surface sediments (27.7 mg/kg dry weight) and with good surface water quality parameters; temperature (32.6 °C), conductivity (77.9 μS/cm), total dissolved solids (0.05 mg/L), dissolved oxygen (7.56 mg/L), pH (6.61) and turbidity (0.00 NTU) (unpublished data).
For acclimation, a maximum of 100 juveniles and 100 adult snails were kept per aquarium (30 cm length × 19 cm with × 18 cm height containing 6000 mL). During the acclimation period, the surface water quality parameters of the dechlorinated tap water in the plastic aquarium tanks ranged from 28.0 to 31.0 °C for temperature, 1.00–5.00 μS/cm for conductivity, 0.01–0.03 mg/L for total dissolved solids, 6.50–7.50 mg/L for dissolved oxygen, 6.70–7.10 for pH and 0.00 NTU for turbidity (unpublished data). Each aquarium was also regularly aerated to give a moderate airflow, in which the snails were acclimatized to laboratory settings for three days. To eliminate any potential bias in the experiments, the snails were divided into two groups, namely juvenile (shell lengths: 0.50 to 0.70 cm) and adult (shell lengths: 1.50 to 2.20 cm) snails for the experimental toxicity study.
Prior to static toxicity testing, range-finding-tests following the standard methods [27] were conducted to determine the critical range, which is defined as the interval between the lowest concentration of metals that kills very few or none of the experimental snails and the highest concentration that kills the majority or all of the experimental snails during the experimental period. The purpose of these tests was to determine the median lethal doses (LC50) of each metal in the snails exposed for 24, 48, 72 and 96 h (h).
Following the range-finding-tests, five nominal concentrations of Cu, Cd, Zn, Pb and Ni were chosen (Table S1). Metal solutions were prepared by diluting the metal stock solutions with dechlorinated tap water to respective nominal concentrations of the five metals. Dechlorinated tap water was used as the negative control. The control samples comprised snails which had not been exposed to any metal solutions and were treated with the identical experimental conditions as the experimental samples. The tests were carried out under static conditions, without renewal of the solution until the end of the experiment. The control and metal-treated groups each consisted of two replicates of 10 healthy snails in a plastic aquarium tank of 21 cm length × 13 cm with × 11.5 cm height, containing 1000 mL of the respective nominal concentrations of the five metals. During the experimental exposure period, the surface water quality parameters in the plastic aquarium tanks were 28.0–30.2 °C for temperature, 1.00–3.00 μS/cm for conductivity, 0.01–0.05 mg/L for total dissolved solids, 6.50–7.50 mg/L for dissolved oxygen, 6.50–7.05 for pH and 0.00 NTU for turbidity (unpublished data).
The standard stock solutions (100 mg/L) of Cd, Cu, Ni, Pb and Zn, were prepared from analytical grade metallic salts of CdCl2·2.5H2O, CuSO4·5H2O, NiSO4·6H2O, Pb(NO3)2 and ZnSO4·7H2O, respectively (Merck, Darmstadt, Germany), by diluting with deionized water in 1 L volumetric flasks. Acute Cu, Cd, Zn, Pb and Ni toxicity experiments were performed for a four-day (96-h) period using juvenile and adult snails, obtained from stocking tanks. The snail death rates were determined at 24-, 48-, 72- and 96-h periods. The deceased snails were removed from the experimental tanks at each period. The snails that did not recover after being placed in a tank with pure freshwater were considered dead.
No stress was observed for the snails in the solution, indicated by 100% survival for the snails in the control water until the end of the experiment. A total of 10 animals per treatment/concentration were used in the experiment, and a total of 300 healthy juveniles and 300 healthy adult snails were used in the present experimental toxicity study. All the procedures of toxicity testing were modified from Adam [4], Melo et al. [6], Abdel Gawad [7], Abdel-Moati and Farag [8] and Shuhaimi-Othman et al. [9]. Water samples for metal analysis were taken before and after the experimental study. The collected water samples were immediately acidified to 1% with ARISTAR nitric acid (65%) (BDH Inc., VWR International Ltd., Lutterworth, UK) before metal analysis by flame atomic absorption spectrophotometer (FAAS-Perkin Elmer model AAnalyst800, Waltham, MA, USA). The detection limits of the FAAS for Cd, Cu, Ni, Pb and Zn were 0.009, 0.010, 0.010, 0.009 and 0.007 mg/L, respectively.

2.2. Statistical Analysis

The mean values and standard deviations were calculated using Microsoft Excel 2003. The data and median lethal concentration (LC50) values for the toxicity test were examined utilizing Probit Analysis Biostat 2007 Professional Package 3.7 (Informer Technologies, Inc., Los Angeles, CA, USA).

3. Results

3.1. Toxicity Tests

Using mortality as an endpoint, studies on the toxicity and tolerance of heavy metals in P. insularum were conducted by short-term toxicity experiments. Table 1 provides a comparison of the LC50 values of five metals between juveniles and adults of P. insularum. For the adult snails, the 48-h LC50 concentrations (mg/L) of Cd, Cu, Ni, Pb and Zn were 24.73, 3.10, 10.73, 17.24 and 57.99, respectively, while the 72-h LC50 concentrations (mg/L) were 11.7, 1.84, 6.88, 11.45 and 26.97, respectively. For the juvenile snails, the 48-h LC50 concentrations (mg/L) of Cd, Cu, Ni, Pb and Zn were 3.67, 0.94, 4.77, 10.44 and 30.16, respectively, while the 72-h LC50 concentrations (mg/L) were 2.15, 0.50, 3.01, 8.35 and 11.36, respectively.
After 48-h exposure, the juvenile snail groups were most sensitive to Cu, followed by Cd > Ni > Pb > Zn, whereas the adult snail groups were most sensitive to Cu, followed by Ni > Pb > Cd > Zn. In addition, after 72-h exposure, the juvenile snails were most sensitive to Cu > Cd > Ni > Pb > Zn, while the adult snails were most sensitive to Cu, then Ni > Pb > Cd > Zn. According to Table 1, the juvenile snails were more sensitive and less tolerant to all metals (Cu, Ni, Pb, Zn and Cd) than adult snails.
The LC50 values based on 48 and 72 h declined in the following order for adult snails: Cu > Ni > Pb > Cd > Zn. The LC50 values based on 48 and 72 h declined in the following order for juvenile snails: Cu > Cd > Ni > Pb > Zn.

3.2. Changes in Observed Behavior and Morphology

During the experiment, the behavioral and morphological alterations in snails exposed to varying quantities of Cu, Zn, Cd, Pb and Ni were observed. When the snails were exposed to lower concentrations of these metals, they could move up and down, stretch their bodies from their shells, and attach themselves to the wall of the plastic container. The majority of the snails survived the experimental period, which corresponded well with the findings of Khangarot and Ray [28]. At moderate concentrations of these metals, the snails secreted mucus with a decreased movement rate. They were inert, incapable of attaching their feet or closing their operculum, and unable to retract their bodies into their shells. The bodies of the snails were mostly exposed in plastic containers. They produced a great deal of mucus, and their feet stretched from their shells but could not retract. Generally, they sunk to the bottom of the plastic containers and became immobile.
The crawling or movement of snails during the experimental periods in an attempt to escape the experimental aquaria was a major drawback of this static toxicity test. As a result, high metabolic rates may have resulted in a large uptake of toxicants at that time, or the snails’ activity in a starving condition may have decreased their resistance to toxicants. The size and age of the animals utilized in the toxicity test were additional variables that affected the LC50 values. It is well known that as an animal ages, its toxicity and tolerance to metals diminish. Cd and Cu concentrations in the soft tissues of freshwater clams have been found to similarly decrease with increasing age [29]. Young snails may be more sensitive to some metals due to their increased accumulation rates. Wier and Walter [30] revealed that juvenile Physa gyrina snails were three times as sensitive to Cd as their mature counterparts. Therefore, larger animals have greater resistance than smaller ones. The present study, using snails of two different sizes, confirmed the predicted result. On the other hand, these snails have an operculum to protect them when the water around them becomes toxic.
In the present experiment, P. insularum developed a white slime when they were exposed to high concentrations of Cd (19.98 mg/L) and Cu (4.08 mg/L). Based on the physiological reactions, Ravera [31] discovered that Biomphalaria glabrata was more resistant to heavy metals after 24 h of exposure. According to their observations, snails sank to the bottom with their operculum closed, expelled bubbles and slowed down their metabolic processes. When exposed to high levels of Cd and Cu, the snails could not adhere to the tank walls because the metals impede cell dynamics and injure the snails’ tissues and cells [32]. The metals eventually infiltrate the cells, resulting in cell necrosis and snail death [33]. Mule and Lomte [34] showed that exposing the freshwater snail Thiara tuberculosa to CuSO4 and HgCl2 decreased their oxygen consumption, and the heavy metal absorption from the medium dropped.

4. Discussion

4.1. Cu Is the Most Toxic Metal

The results showed that the mortality of the snails increased as they were exposed to increasing concentrations of metals or for longer durations. Cu was the most toxic metal. The snails were most susceptible to Cu with the lowest LC50 values compared to other metals. Comparing the LC50 values of Cd and Cu for P. insularum with those of other snail species (>10 species), including mussels, clams, sea anemones, cockles and shrimp, revealed that P. insularum was more sensitive to Cu than Cd, Ni, Pb and Zn. This is well indicated in the different species of bivalves and gastropods from the literature (Table 2, Table 3, Table 4, Table 5 and Table 6).
Even though juvenile snails were more sensitive to the five metals, Cu was shown to be the most toxic metal for both juvenile and adult snails, when compared to Ni, Pb, Cd and Zn. This is consistently correlative with research on the toxicity of heavy metals to freshwater organisms. For instance, the rank order of toxicity of some heavy metals to Daphnia magna was Cu > Zn > Cd > Pb > Ni (48 h) [35]; for rainbow trout (Salmo gairdneri) it was Cu > Zn > Cd > Pb > Ni (96 h) [35]; for amphibian tad-poles (Bufo melanostictus) it was Cu > Cd > Zn > Ni (96 h) [36]; and for Lymnaea luteola it was Cu > Cd > Ni > Zn (72 h) [28].
The findings of the present study showed that the LC50 values in the five metals significantly decreased (p < 0.05) from 48-h to 72-h periods in both juvenile and adult snails. This indicated that the longer period of toxicity testing resulted in the snails being more sensitive to the five metal toxicities. Taylor et al. [37] reported that the LC50 values of Cu in Gammarus pulex decreased from 0.047 to 0.037 after 48-h and 96-h periods, respectively. Similarly, they also found that the LC50 values of Cu in Chironomus riparius decreased from 1.20 to 0.70 after 48- and 96-h periods, respectively. Using P. canaliculata as the test organism, Dummee et al. [38] demonstrated that the LC50 values of Cu exposure periods of 4, 48, 72 and 96 h were 0.330, 0.223, 0.177 and 0.146 mg/L, respectively. This indicates a decreasing order of LC50 values with increasing Cu exposure period. All of these data demonstrated that the longer the duration of exposure, the more sensitive the invertebrates to pollutants.
Brix et al. [39] showed that the 96-h LC50 value of Cu in Lymnaea stagnalis was 31 g/L, indicating a moderate acute sensitivity to Cu. However, the projected EC20 value (the median effective concentration of a substance to 20% of test organisms) for Cu after a 30-day chronic exposure of juvenile L. stagnalis to Cu was 1.8 mg/L, making it the most sensitive organism to Cu investigated to date. In a different experiment with adult freshwater snails, Melanoides tuberculata, Shuhaimi-Othman et al. [9] observed an increase in the median lethal times (LT50) and concentrations (LC50) of eight metals after four days of laboratory exposure. Cu was the most hazardous metal to M. tuberculosis, followed by Cd, Zn, Pb, Ni, Fe, Mn and Al.
Several investigations suggested that Pomacea snails were efficient bioindicators for Cu and Cd. Pomacea canaliculata has the capacity to acquire Cu from a variety of metals (20, 30, 45, 67.5 and 101.3 mg/L), but demonstrated behavioral control at Cu concentrations of 67.5 and 101.3 mg/L, as determined by Pena and Pocsidio [40]. This provided evidence for using the golden apple snail (whole tissue analysis) as a sublethal Cu biomonitor (0–45 mg/L). Additionally, Manzla et al. [41] reported acute toxicity of Cu and Cd on the hepatopancreas cells of Helix pomatia (toxicity of Cu > Cd). Hoang and Rand [42] showed that CuCO3 was toxic to apple snails (Pomacea paludosa) due to the fact that Cu concentrations were higher in living snails than in dead snails. Their results indicated that apple snails could excrete deposited Cu [38]. They demonstrated that Pomacea was a suitable bioindicator and biomarker for Cu pollution biomonitoring in aquatic environments. Habib et al. [43] showed that B. alexandrina was a suitable organism for assessing Cd toxicity in freshwater environments based on short-term 96-h (LC50) and long-term exposure to Cd.
The outcomes of the present study indicated that both the smaller and bigger snail populations displayed the same decreasing order of metal toxicity: Cu > Cd. The order of toxicity of these metal ions correlates well with the metal toxicity levels of other freshwater organisms. For amphibian tadpoles [36], Daphnia magna [35] and pulmonate snails [44], Cu was more poisonous than Cd.
In understanding the toxicity of Cu, Hoang and Rand [42] indicated that the carbonate content of snails may explain the potential toxicity of Cu carbonate to snails. This is because snails need carbonate for shell growth; their carbonate need is greater than that of fish. Cu carbonate may enter snails as Cu, and dissociate after entering the snails by biological and chemical processes. Carbonate would be accessible for shell formation, while Cu would accumulate in soft tissue. Hoang et al. [45] also showed that the majority of deposited Cu in juvenile apple snails (Pomacea paludosa) was concentrated in soft tissue (about 60% in the viscera and 40% in the foot), and the shell contained less than 4% of the total accumulated Cu. Nevertheless, a comparison of the absorption rate in aquatic organisms revealed that, generally, the uptake rate constant is Zn > Cd > Cu [46]. This gap is likely related to the four-day metal exposure duration in this investigation. Other factors that may influence the bioaccumulation of heavy metals in aquatic organisms include feeding habits [47], growth rate and age of the organism [5], and the bioavailability of the metals, which is highly dependent on water hardness, pH and acid-volatile sulfide [48]. Hoang and Rand [42] demonstrated that apple snails (Pomacea paludosa) accumulated more Cu from soil-water treatments than water-only treatments, implying that apple snails accumulate Cu from environmental media (sediment or water). The rate of increase in the weight of a snail’s tissue and shell is typically greater than the rate of accumulation of metals in its body. Lau et al. [5] and Hoang et al. [45] showed that juvenile apple snails collected Cu during the exposure period and excreted Cu during the depuration phase. Metals accumulated in animals can be stored without excretion, leading to high body concentrations (accumulators), or the metal levels in the body can be maintained at a low constant concentration (regulators) by balancing the uptake with controlled excretion rates [49].

4.2. Juvenile Snails Are More Sensitive to Metal Toxicity

Smaller snails (0.50 to 0.70 cm) were shown to be more sensitive and less tolerant to all metals (Cd, Cu, Ni, Pb and Zn) than larger snails (1.50–2.20 cm). Previous research has demonstrated that younger organisms are more susceptible to toxicity [50,51]. In a study on mussels, Yap et al. [51] demonstrated that the species was most susceptible to Cu, followed by Cd; however, the small size group was more sensitive than the large size group, as the small group had lower LC50 values. In addition, it should be emphasized that other environmental variables, such as water quality, might influence the toxicity of a metal [52], and, therefore, can contribute to discrepancies in reported results. Although a standard test on a single species may provide information on the environmental risks of a toxicant, one should not establish safe environmental levels for toxicants based on a small number of test species. As the tolerance of Pomacea to metals was influenced by chemical type and test duration, it is imperative that the toxicity test encompasses a wider range of species and exposure times in future studies.
If other aspects of the snail’s life cycle had been researched, more information about its sensitivity to heavy metals would have been available. Wier and Walter [30] found that immature Physa gyrina snails were three times more vulnerable to heavy metals than their mature counterparts. Cheung and Lam [53] showed that the juvenile stage of Physa acuta freshwater snails was the most Cd-tolerant when compared to the embryo. Earlier life stages, such as embryos and larvae, were the most vulnerable to heavy metals, according to multiple investigations [54,55]. These results corroborated the present study’s conclusion that snails of a lower size range (0.50–0.70 cm) were more vulnerable to all metals than snails of a larger size range (1.50–2.20 cm) (Cu, Ni, Pb, Zn and Cd). The juvenile stage was found to be more vulnerable to heavy metals than the later stages.

4.3. Comparisons of LC50 Values with Those of Other Species of Molluscs

It is difficult to compare the LC50 values of metals in this species with those in other gastropod species due to the varying ability of closely related taxa or species belonging to the same genus that inhabit the same environments to accumulate metals in water with varying hardness. Using adult Theodoxus niloticus snails, Abdel Gawad [7] reported the 96-h LC50 values for Zn, Fe, and Pb to be 12.199, 8.6 and 18 mg/L, respectively. These values grew as the duration of exposure decreased. Fe was the most hazardous element to the snail, followed by Zn and Pb.
The findings of this investigation on the sensitivity of P. insularum to the toxicity of heavy metals supported the notion that the susceptibility of an animal to heavy metal toxicity differed among species [55,56,57,58]. This is demonstrated by comparing the LC50 values of P. insularum to those of other species. For example, Arthur and Leonard [59] reported that the 96-h LC50 of Cu in Physa integra was 0.039 mg/L, which is lower than the 96-h LC50 in P. insularum in the present study, which was 0.21 mg/L of Cu. The variation may be due to the various test animal species, techniques, and environmental conditions. Throp and Lake [60] reported that the 96-h LC50 values of Cd in the freshwater shrimp Paratya tasmaniensis were 0.06 mg/L. However, in the present investigation, the 96-h LC50 values of Cd in P. insularum were 2.55 mg/L. In addition, Lam [61] reported that the 96-h LC50 values of the tropical freshwater snail Radix plicatulus were 2.55 mg/L of Cd, which was comparable to the 72-h LC50 values of Cd in juvenile P. insularum (2.15 mg/L) in the present study. Consequently, based on the preceding examples, it can be concluded that the susceptibility of different species [62] and several factors such as experiment procedures, the physical and chemical characteristics of the experimental conditions such as temperature, DO, pH and water hardness [63], as well as the physiological, size, and age of the animals used, can influence the LC50 values in the toxicity study.
Multiple researchers have investigated the impact of environmental characteristics such as temperature, pH, and dissolved oxygen on the toxicity of heavy metals and published their findings in the scientific literature. In general, increasing respiration at higher temperatures directly increased toxicity. Moreover, high temperatures indirectly increase toxicity by reducing oxygen levels in water [64]. Temperature increases had a direct effect on the ramshorn snail, Helisoma campanulatum, and the pond snail, Viviparus benghalensis, according to Gupta et al. [65]. Eisler [58] also showed that at 20 °C, the mummichog was more vulnerable to Cd than at 5 °C. In contrast, it is well established that increased water hardness reduces the acute toxicity of metals [66]. However, as the temperature utilized in the present exposure investigation was constant, this abiotic parameter had no effect on the snails’ toxicity and tolerance to heavy metals.
Cu is more hazardous than Zn and Hg to the two intertidal snails Planaxis sulcatus and Trochus radiatus, according to an acute toxicity test performed by Kulkarni et al. [67] using static bioassay procedures. The availability of heavy metals due to different anthropogenic metal inputs could be attributed to their metal toxicities [68].
For all metals, Shuhaimi-Othman et al. [9] found that (LC50 increased with decreasing mean exposure concentrations and periods. Cu was discovered to be the most hazardous metal to M. tuberculosis, followed by Cd, Zn, Pb and Ni. Other studies demonstrated divergent patterns in the toxicity of certain snails. According to Luoma and Rainbow [40], the rank order of metal toxicity varies among organisms; Khangarot and Ray [28,29,30] demonstrated that the order of toxicity was Cd > Ni > Zn in Lymnaea luteola,; Gupta et al. [69] and Gadkari and Marathe [70] showed that the order of toxicity was Zn > Cd > Pb > Ni in Viviparus bengalensis.
According to Shuhaimi-Othman et al. [9], the LC50 values of Cu, Cd, Zn, Pb and Ni for 48 and 96 h were 0.39, 11.85, 13.15, 10.99 and 36.46 mg/L, and 0.14, 1.49, 3.90, 6.82 and 8.46 mg/L, respectively. Metals’ acute toxicity to M. tuberculosis was the subject of only a few studies. Nebeker et al. [71] showed that the 96-h LC50 value of Cu in Fluminicola virens was 0.08 mg/L, and that of Zn in Physa gyrina was 1.27 mg/L, which were lower than those reported by Shuhaimi-Othman et al. [9]. Bali et al. [72] and Mostafa et al. [73] reported 96-h LC50 values of Cu in M. tuberculosis were 0.2 and 3.6 mg/L, respectively, which were greater than those reported by Shuhaimi-Othman et al. [9].
Abdel Gawad [74] investigated the effect of different doses of Cd on the toxicity of Corbicula fluminalis. The 96-h LC50 and daily survival rates were evaluated to determine the acute toxicity. Their results indicated that the C. fluminalis mortality rate was proportional to the Cd concentration. After 96 h of exposure, the LC50 was 0.52 mg/L. After 96 h of exposure, the bioaccumulation value of the pollutant in the soft portions of the clam was greater than the comparable value in the shell.
Shuhaimi-Othman et al. [9] showed that the LC50 values in M. tuberculata were generally lower or comparable to those of other freshwater gastropods. It was difficult to make direct comparisons between the toxicity values found in this study and those in the literature due to changes in the test waters’ properties (mainly water hardness, pH, and temperature). Different species, ages, and sizes of the organisms as well as different test methods (water quality and water hardness) can influence toxicity [50,75,76,77,78]. In the present investigation, the water hardness was low (18.7 mg/L CaCO3), and the water was classified as soft (75 mg/L as CaCO3).
The snail M. tuberculata was found to be less sensitive to metals compared to other species [9]. Von Der Ohe and Liess [79] demonstrated that 13 Crustacea taxa were among the most sensitive to metal compounds, and they concluded that Crustacea taxa are comparable to one another and to Daphnia magna in terms of sensitivity to organics and metals, and that mollusks have an average sensitivity to metals. Mitchell et al. [80] observed that the snail has a tightly sealed operculum, which enables it to tolerate desiccation and, presumably, also boosts its chemical tolerance.
Table
Table 2. Comparison of LC50 values (mg/L) of Cd in Pomacea insularum with other mollusks reported in the literature.
Table 2. Comparison of LC50 values (mg/L) of Cd in Pomacea insularum with other mollusks reported in the literature.
MolluscsSpeciesWater Hardness (mg L−1)Live StageTest Duration LC50 (mg/L)References
BivalvesDonax faba29.9 pptAdult96-h EC500.99Din and Ong [81]
Anadara granosa29.5 pptAdult96-h EC500.94Din and Ong [81]
Perna viridisNANA24-h EC501.53Yap et al. [45]
Modiolus phillippinarumNANA96-h EC500.02Ramakristinan et al. [82]
GastropodsLymnaea luteola195Adult48-h EC502.10Khangarot and Ray [28]
Amnicola sp.50Adult96-h EC508.40Rehwoldt et al. [83]
Biomphalaria glabrata100NA96-h EC500.30Bellavere and Gorbi [84]
Viviparus bengalensis180NA96-h EC501.20Gupta et al. (1981a) [69]
Viviparus bengalensisNANANA2.54Gadkari and Marathe [70]
Aplexa hypnorum45Adult96-h EC500.09Holcombe et al. [85]
Physa fontinalisNANA96-h EC500.08Williams et al. [86]
Radix plicatulusNANA96-h EC502.50Lam [62]
Lymnaea luteola195Adult72-h EC501.60Khangarot and Ray [28]
Lymnaea luteola195Adult96-h EC501.52Khangarot and Ray [28]
Physa acutaNANA48-h EC501.05Cheung and Lam [48]
Potamopygus antipodarumNANA96-h EC500.72Hall and Golding [87]
Pomacea sp. NANA24-h EC502.25Piyatiratitivorakul et al. [88]
Pomacea sp. NANA48-h EC502.07Piyatiratitivorakul et al. [88]
Pomacea sp. NANA72-h EC500.68Piyatiratitivorakul et al. [88]
Pomacea sp. NANA96-h EC500.47Piyatiratitivorakul et al. [88]
Filopaludina martensi martensiNANA24-h EC5027.8Piyatiratitivorakul and Boonchamoi [54]
Filopaludina martensi martensiNANA48-h EC505.01Piyatiratitivorakul and Boonchamoi [54]
Filopaludina martensi martensiNANA72-h EC503.96Piyatiratitivorakul and Boonchamoi [54]
Filopaludina martensi martensiNANA96-h EC502.33Piyatiratitivorakul and Boonchamoi [54]
Melanoides tuberculata18.7Adult96-h EC501.49Shuhaimi-Othman et al. [9]
Cerithedia cingulataNANA96-h EC509.19Ramakristinan et al. [82]
Biomphalaria alexandrinaNANA96-h EC500.22Habib et al. [43]
Pomacea canaliculataNANA48-h EC504.26Huang et al. [89]
Pomacea canaliculataNANA72-h EC502.24Huang et al. [89]
Pomacea canaliculataNANA96-h EC501.98Huang et al. [89]
Pomacea insularum (small)65Juvenile48-h EC503.67This study
Pomacea insularum (small)65Juvenile72-h EC502.15This study
Pomacea insularum (large)65Adult48-h EC5024.73This study
Pomacea insularum (large)65Adult72-h EC5011.7This study
Note: NA = data not available.
Table
Table 3. Comparison of LC50 values (mg/L) of Cu in Pomacea insularum with other mollusks reported in the literature.
Table 3. Comparison of LC50 values (mg/L) of Cu in Pomacea insularum with other mollusks reported in the literature.
MolluscsSpeciesWater Hardness (mg/L)Live StageTest DurationLC50 (mg/L)References
BivalvesClam Donax fabaNANA96-h EC500.93Sommanee [90]
Donax faba29.9 pptAdult96-h EC500.20Din and Ong [81]
Anadara granosa29.5 pptAdult96-h EC500.23Din and Ong [81]
Perna viridisNANA24-h EC500.25Yap et al. [45]
Anadara granosaNANA48-h EC500.29Yap et al. [91]
Modiolus phillippinarumNANA96-h EC500.22Ramakristinan et al. [82]
GastropodsBiomphalaria glabrata100NA96-h EC500.04Bellavere and Gorbi [84]
Viviparus bengalensis (at 27.3 C)180NA48-h EC500.27Gupta et al. [66]
Viviparus bengalensis (at 27.3 C)NANA72-h EC500.12Gupta et al. [66]
Lymnaea luteolaNANA96-h EC500.172Mathur et al. [92]
Physastra gibbosaNANA96-h EC500.041Skidmore and Firth [93]
Melanoides tuberculataNAJuvenile24-h EC500.20Bali et al. [72]
Potamopyrgus jenkinsiNAAdult96-h EC500.08Watton and Hawkes [94]
Lithoglyphus virens21Adult96-h EC500.08Nebeker et al. [71]
Juga plicifera21Adult96-h EC500.015Nebeker et al. [71]
Lymnaea luteola195Adult48-h EC500.025Khangarot and Ray [28]
Lymnaea luteola195Adult72-h EC500.027Khangarot and Ray [28]
Lymnaea luteola195Adult96-h EC500.027Khangarot and Ray [28]
Biomphalaria glabrata44Adult48-h EC500.18De Oliveira-Filho et al. [95]
Melanoides tuberculataNANA48-h EC503.60Mostafa et al. [73]
Pomacea sp. NANA24-h EC504.84Piyatiratitivorakul et al. [88]
Pomacea sp. NANA48-h EC501.85Piyatiratitivorakul et al. [88]
Pomacea sp. NANA72-h EC500.92Piyatiratitivorakul et al. [88]
Pomacea sp. NANA96-h EC500.12Piyatiratitivorakul et al. [88]
Pomacea paludosa6860 d96-h EC500.14Rogevich et al. [96]
Melanoides tuberculata18.7Adult96-h EC500.14Shuhaimi-Othman et al. [9]
Cerithedia cingulataNANA96-h EC500.52Ramakristinan et al. [82]
Pomacea canaliculataNANA24-h EC500.33Dummee et al. [32]
Pomacea canaliculataNANA48-h EC500.22Dummee et al. [32]
Pomacea canaliculataNANA72-h EC500.18Dummee et al. [32]
Pomacea canaliculataNANA96-h EC500.15Dummee et al. [32]
Pomacea insularum (small)65Juvenile48-h EC500.94This study
Pomacea insularum (small)65Juvenile72-h EC500.50This study
Pomacea insularum (large)65Adult48-h EC503.10This study
Pomacea insularum (large)65Adult72-h EC501.84This study
Note: NA = data not available.
Table
Table 4. Comparison of LC50 values (mg/L) of Ni in Pomacea insularum with other mollusks reported in the literature.
Table 4. Comparison of LC50 values (mg/L) of Ni in Pomacea insularum with other mollusks reported in the literature.
MolluscsSpeciesWater Hardness (mg/L)Live StageTest DurationLC50 (mg/L)References
BivalvesUtterbackia imbecillis60Juveniles96-h EC500.19Keller and Lam [97]
Utterbackia imbecillis80Juveniles96-h EC500.252Keller and Lam [97]
Hamiota perovalis43Juveniles96-h EC500.313Gibson et al. [98]
Villosa nebulosa43Juveniles96-h EC500.51Gibson et al. [98]
GastropodsAmnicola sp.50Embryo96-h EC5011.4Rehwodlt et al. [83]
Amnicola sp.50Adult96-h EC5014.3Rehwodlt et al. [83]
Viviparus bengalensis180NA96-h EC509.92Gupta et al. [69]
L. acuminata375NA96-h EC502.78Khangarot et al. [99]
Lymnaea stagnalis100Juveniles96-h EC500.9Nebeker et al. [71]
Physa gyrina26NR96-h EC500.239Nebeker et al. [71]
L. luteola195Adult48-h EC501.7Khangarot and Ray [28]
L. luteola195Adult72-h EC501.7Khangarot and Ray [28]
L. luteola195Adult96-h EC501.43Khangarot and Ray [28]
Melanoides tuberculata18.7Adult96-h EC508.46Shuhaimi-Othman et al. [9]
Leptoxis ampla43Juveniles96-h EC500.033Gibson et al. [98]
Somatogyrus sp.43Adult96-h EC500.301Gibson et al. [98]
Pomacea insularum (small)65Juvenile 48-h EC504.77This study
Pomacea insularum (small)65Juvenile 72-h EC503.01This study
Pomacea insularum (large)65Adult48-h EC5010.73This study
Pomacea insularum (large)65Adult72-h EC506.88This study
Note: NA = data not available.
Table
Table 5. Comparison of LC50 values (mg/L) of Pb in Pomacea insularum with other mollusks reported in the literature.
Table 5. Comparison of LC50 values (mg/L) of Pb in Pomacea insularum with other mollusks reported in the literature.
MolluscsSpeciesWater Hardness (mg/L)Live StageTest DurationLC50 (mg/L)References
BivalveMussel Modiolus phillippinarumNANA96-h EC502.88Ramakristinan et al. [82]
GastropodsA. hypnorum60.9NA96-h EC501.34Call et al. [100]
Viviparus bengalensis165NA96-h EC502.54Gadkari and Marathe [70]
L. emarginata150NA96-h EC5014Cairns Jr et al. [101]
E. livescens150NA96-h EC5071Cairns Jr et al. [101]
Filopaludina sp.NAAdult24-h EC50319Jantataeme et al. [102]
Filopaludina sp.NAAdult48-h EC50271Jantataeme et al. [102]
Filopaludina sp.NAAdult72-h EC50235Jantataeme et al. [102]
Filopaludina sp.NAAdult96-h EC50192Jantataeme et al. [102]
Melanoides tuberculata18.7Adult96-h EC506.82Shuhaimi-Othman et al. [9]
Snail Cerithedia cingulataNANA96-h EC5015.5Ramakristinan et al. [82]
Freshwater snail Theodoxus niloticusNAAdult96-h EC5018Abdel Gawad et al. [7]
Archachatina papyraceaLand snailsAdults28-days EC501121Owojori et al. [103]
Pomacea insularum (small)65Juvenile 48-h EC5010.44This study
Pomacea insularum (small)65Juvenile 72-h EC508.35This study
Pomacea insularum (large)65Adult48-h EC5017.24This study
Pomacea insularum (large)65Adult72-h EC5011.45This study
Note: NA = data not available.
Table
Table 6. Comparison of LC50 values (mg/L) of Zn in Pomacea insularum with other mollusks reported in the literature.
Table 6. Comparison of LC50 values (mg/L) of Zn in Pomacea insularum with other mollusks reported in the literature.
MolluscsSpeciesWater Hardness (mg/L)Live StageTest DurationLC50 (mg/L)References
BivalvesCorbicula fluminea64NA96-h EC506.04Cherry et al. [104]
Actinonaias pectorosa170Glochidia96-h EC500.31Cherry et al. [104]
Medionidus conradicus170Glochidia96-h EC500.57Cherry et al. [104]
Phychobranchus fasciolaris170Juveniles96-h EC500.21Cherry et al. [104]
Utterbackia imbecillis60Juveniles96-h EC500.27Keller and Lam [97]
Utterbackia imbecillis80Juveniles96-h EC500.44Keller and Lam [97]
Utterbackia imbecillis60Juveniles96-h EC500.36Keller and Lam [97]
Utterbackia imbecillis80Juveniles96-h EC500.59Keller and Lam [97]
Villosa nebulosa170Glochidia96-h EC500.66Cherry et al. [104]
Actinonaias pectorosa40Juveniles96-h EC500.36–0.37McCann [105]
Actinonaias pectorosa160Juveniles96-h EC501.06–1.19McCann [105]
Villosa iris50Juveniles96-h EC500.34McCann [105]
Villosa iris160Juveniles96-h EC501.12McCann [105]
Villosa umbrans43Juveniles96-h EC501.30Gibson et al. [98]
Villosa nebulosa43Juveniles96-h EC500.44Gibson et al. [98]
Donax faba29.9 pptAdult96-h EC503.61Din and Ong [81]
Anadara granosa29.5 pptAdult96-h EC507.76Din and Ong [81]
Modiolus phillippinarumNANA96-h EC502.34Ramakristinan et al. [82]
GastropodsHelisoma campanulatum20Adult96-h EC500.87–1.27Wurtz [106]
Helisoma campanulatum100Adult96-h EC501.27–3.03Wurtz [106]
P. heterostropha20Adult96-h EC501.11Wurtz [106]
P. heterostropha100Adult96-h EC503.16Wurtz [106]
Physa heterostropha20Juveniles96-h EC500.30–1.39Wurtz [106]
Physa heterostropha100Juveniles96-h EC500.43–1.39Wurtz [106]
Amnicola sp.50Adult96-h EC5014.0Rehwodlt et al. [83]
Amnicola sp.50Embryo96-h EC5020.2Rehwodlt et al. [83]
Viviparus bengalensis180NA96-h EC500.64Gupta et al. [69]
Lymnaea luteolaNANA96-h EC506.13Mathur et al. [92]
L. acuminata375NA96-h EC5010.5Khangarot et al. [99]
Physa gyrina36Adult96-h EC501.27Nebeker et al. [71]
Lymnaea luteola195Adult96-h EC5011.0Khangarot and Ray [28]
Lymnaea luteola195Adult48-h EC503.80Khangarot and Ray [28]
Lymnaea luteola195Adult72-h EC503.80Khangarot and Ray [28]
Lymnaea luteola195Adult96-h EC501.68Khangarot and Ray [28]
Lanistes bolteniNANANA58.0Abdel-Moati and Farag [8]
Melanoides tuberculata18.7Adult96-h EC503.90Shuhaimi-Othman et al. [9]
Cerithedia cingulataNANA96-h EC508.99Ramakristinan et al. [82]
Leptoxis ampla43Adult96-h EC500.07Gibson et al. [98]
Somatogyrus sp.43Adult96-h EC500.33Gibson et al. [98]
Theodoxus niloticusNAAdult96-h EC5012.2Abdel Gawad et al. [7]
Pomacea insularum (small)65Juvenile 48-h EC5030.16This study
Pomacea insularum (small)65Juvenile 72-h EC5011.36This study
Pomacea insularum (large)65Adult48-h EC5057.99This study
Pomacea insularum (large)65Adult72-h EC5026.97This study
Note: NA = data not available.

4.4. Implications from Biomonitoring Perspective

The use of small prosobranch snails, such as P. insularum, as one of the biological indicators in toxicity testing, offers several benefits. First, because these snails are prevalent in still (ponds) and running (streams) waters, they can be utilized as ecologically significant target species in both lotic and lentic environments. Secondly, they are affordable, easily harvested and manageable. In addition, they are sensitive indicators of dangerous amounts of heavy metals such as Cu, Pb, Cd, Ni and Zn identified in this study, comparable to that reported by Ravera [52] and Lam [62]. They are possibly more susceptible to metals than larger snails, Brotia hainanensis, because they possess the same trait [107]. For a realistic approach to pollution consequences, additional research on the acute and chronic toxicity of various environmental contaminants under various environmental and biological circumstances is necessary. It is also necessary to assess the combined toxicity of substances. The mechanisms of contaminants at the cellular and molecular levels in these animals must also be comprehended.
Under controlled laboratory conditions, Pyatt et al. [108] evaluated the effects of Pb (5 or 10 mg/L) on the survival of the freshwater snail Lymnaea stagnalis (L.) collected from lead-contaminated or uncontaminated environments. Significantly more animals from the polluted environment survived subsequent acute (up to 24 days) Pb exposure than animals from the unpolluted environment. Acute exposure to Pb (72 h) hindered various behavioral activities, including movement, eating, tentacle elongation and emerging from the shell. Pb bioaccumulated in snail tissues, specifically the buccal mass and the stomach. The freshwater snail is an excellent system for researching the bioaccumulation and development of environmental Pb tolerance.
Nebeker et al. [71] observed that three snail species from western Oregon were exposed to metals: Juga plicifera and Lithoglyphus virens, which occupy temperate coastal streams, and Physa gyrina, which inhabits ponds in the Willamette Valley. J. plicifera was subjected to Cu and Ni in laboratory flow-through testing, while L. virens was exposed to Cu, and P. gyrina was exposed to Ni and Zn. J. plicifera had a 96-h LC50 Cu value of 0.015 mg/L, and a no observable effect level (NOEL) of 0.006 mg/L (at which mortality was not substantially different from that in control groups) (30-d survival). The 96-h LC50 and NOEL for Ni in J. plicifera were 0.23 mg/L and 0.124 mg/L, respectively. The 96-h LC50 and NOEL for Cu in L. virens were 0.008 mg/L and less than 0.008 mg/L, respectively. The 96-h LC50 for Ni in P. gyrina was 0.239 mg/L, the 96-h LC50 for Zn was 1.274 mg/L and the NOEL for Zn was 0.570 mg/L.
Piyatiratitivorakul et al. [88] investigated the acute toxicity of Cd and Cu to Pomacea sp collected from Thailand. The findings revealed the possibility of using the freshwater snail Pomacea sp. as a biomonitor for heavy metal levels in freshwater resources. Huang et al. [89] revealed the acute toxicity of Cd, in which the metal bioaccumulation in tissue was measured in P. canaliculata and its native competitor Sinotaia quadrata under experimental settings. The LC50 concentrations (mg/L) for the invasive species were 4.26, 2.08 and 1.98 after being exposed for 48, 72 and 96 h, respectively, which were approximately three times greater than those of the native species. The viscera gathered the highest concentration of Cd, followed by the foot and shell in both species. The metal concentrations in the aforementioned three tissues of P. canaliculata were significantly greater than those of S. quadrata, regardless of Cd dose and exposure time. They concluded that a high Cd tolerance, may partially explain P. canaliculata’s capacity to displace S. quadrata from Cd-contaminated habitats. Cd primarily accumulated in the hepatopancreas and kidneys of invading species, thus altering the activity of antioxidant enzymes and helping the animals to deal with the toxicity.

5. Conclusions

This investigation revealed that P. insularum exhibited the same metal sensitivity as other freshwater gastropods. Cu was the most harmful to P. insularum, followed by Cd, Zn, Pb and Ni. The acute toxicity tests revealed that P. insularum is more susceptible to Cu than Cd, Ni, Pb and Zn, which is consistent with the LC50 values reported in the literature for most invertebrate species. This study indicated that P. insularum may also be used as a biomonitor for acute and subacute Cd, Cu, Ni, Pb and Zn exposures. Since P. insularum is widely spread in urban and suburban regions, it is incredibly valuable for ecotoxicological research. This study demonstrated that P. insularum may be a biomonitor of potentially toxic metal contamination. Using P. insularum as a test organism, this study provided essential baseline data for PTM toxicity. Changes in the snail population due to PTM exposures may potentially influence the predation behavior of predators, which is an interesting area for future studies.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/app13021042/s1, Table S1: Nominal and measured concentrations (mg/L) of Cd, Cu, Ni, Pb and Zn in the toxicity test for the Pomacea insularum of two different sized groups (Shell lengths, small 0.50–0.70 cm; large: shell 1.50–2.20 cm); Table S2: Mortality of individuals (Pomacea insularum) for the small sized group (Shell length: 0.50–0.70 cm) collected after four different periods of exposure to a series of different concentrations of Pb, Ni, Cd, Zn and Cu; Table S3: Mortality of individuals (Pomacea insularum) for the large-sized group (Shell length: 1.50–2.20 cm) collected after four different periods of exposure to a series of different concentrations of Cd, Cu, Ni, Pb and Cu, Zn.

Author Contributions

Conceptualization, C.K.Y.; Formal analysis, B.H.P. and C.K.Y.; Funding acquisition, C.K.Y.; Investigation, B.H.P., C.K.Y. and W.H.C.; Methodology, B.H.P., C.K.Y., K.K. and M.C.O.; Project administration, C.K.Y. and W.H.C.; Resources, K.K., H.O., M.K., A.N., M.S.I. and W.S.T.; Supervision, C.K.Y.; Validation, K.K., R.A., H.O., Y.H., M.S., M.K., M.C.O. and A.N.; Visualization, R.A. and Y.H.; Writing—original draft, C.K.Y. and B.H.P.; Writing—review and editing, W.H.C., K.K., R.A., H.O., Y.H., M.S., M.K., M.C.O., A.N., M.S.I. and W.S.T. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

The authors would like to acknowledge the financial support provided through the Research University Grant Scheme (RUGS), [Vote no.: 9322400], by Universiti Putra Malaysia, and also Fundamental Research Grant Scheme (FRGS) Phase 1/2016 [Vote no. 5524953] by Ministry of Higher Education Malaysia.

Conflicts of Interest

The authors declare no conflict of interest.

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Table
Table 1. Comparisons of the LC50 values (mg/L) of Cd, Cu, Ni, Pb and Zn in both juveniles and adults Pomacea insularum, in 48 h and 72 h of exposure, with their standard errors (SE), upper confidential limits (UCL) and lower confidential limits (LCL) of the obtained LC50 values.
Table 1. Comparisons of the LC50 values (mg/L) of Cd, Cu, Ni, Pb and Zn in both juveniles and adults Pomacea insularum, in 48 h and 72 h of exposure, with their standard errors (SE), upper confidential limits (UCL) and lower confidential limits (LCL) of the obtained LC50 values.
SnailsJuvenileJuvenileAdultAdult
Periods48 h72 h48 h72 h
CdLC503.672.1524.7311.71
SE0.520.403.641.78
LCL2.631.3417.388.07
UCL4.712.9632.0915.35
CuLC500.940.503.101.84
SE0.210.280.560.58
LCL0.53−0.101.980.68
UCL1.361.094.223.00
NiLC504.773.0110.736.88
SE1.161.321.371.42
LCL2.420.327.953.90
UCL7.125.7013.509.85
ZnLC5030.1611.3657.9926.97
SE4.813.508.225.32
LCL20.434.1941.1815.84
UCL39.9018.5274.8038.10
PbLC5010.998.3517.2411.45
SE1.291.141.991.31
LCL8.396.0413.228.80
UCL13.5910.6621.2514.09
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Yap, C.K.; Pang, B.H.; Cheng, W.H.; Kumar, K.; Avtar, R.; Okamura, H.; Horie, Y.; Sharifinia, M.; Keshavarzifard, M.; Ong, M.C.; et al. Heavy Metal Exposures on Freshwater Snail Pomacea insularum: Understanding Its Biomonitoring Potentials. Appl. Sci. 2023, 13, 1042. https://doi.org/10.3390/app13021042

AMA Style

Yap CK, Pang BH, Cheng WH, Kumar K, Avtar R, Okamura H, Horie Y, Sharifinia M, Keshavarzifard M, Ong MC, et al. Heavy Metal Exposures on Freshwater Snail Pomacea insularum: Understanding Its Biomonitoring Potentials. Applied Sciences. 2023; 13(2):1042. https://doi.org/10.3390/app13021042

Chicago/Turabian Style

Yap, Chee Kong, Bin Huan Pang, Wan Hee Cheng, Krishnan Kumar, Ram Avtar, Hideo Okamura, Yoshifumi Horie, Moslem Sharifinia, Mehrzad Keshavarzifard, Meng Chuan Ong, and et al. 2023. "Heavy Metal Exposures on Freshwater Snail Pomacea insularum: Understanding Its Biomonitoring Potentials" Applied Sciences 13, no. 2: 1042. https://doi.org/10.3390/app13021042

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Yap, C. K., Pang, B. H., Cheng, W. H., Kumar, K., Avtar, R., Okamura, H., Horie, Y., Sharifinia, M., Keshavarzifard, M., Ong, M. C., Naji, A., Ismail, M. S., & Tan, W. S. (2023). Heavy Metal Exposures on Freshwater Snail Pomacea insularum: Understanding Its Biomonitoring Potentials. Applied Sciences, 13(2), 1042. https://doi.org/10.3390/app13021042

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