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GASTROPODS AND
BIVALVES:
BIOMONITORS FOR
METAL CONTAMINATION
IN THE ENVIRONMENT
BY
OLADIMEJI AKINSILE
DEPARTMENT OF GEOSCIENCES
RWTH ARCHEN UNIVERSITY
TABLE OF CONTENTS
Title Page
Abstract
Certification
Dedication
Acknowledgements
Table of Contents
List of Tables
List of Figures
CHAPTER ONE: GENERAL INTRODUCTION
1.1 Background of Study
1.2 Aim and Objectives of Study
1.3 Statement of Problem
1.4 Research Questions
1.5 Significance of Study

CHAPTER TWO: LITERATURE REVIEW
2.1 Sources of Heavy Metals
2.2 Permissible Limits of Heavy Metals for organisms and in the Environment
2.3 Adverse Effects of Heavy Metal Contamination
2.4 Major Outbreaks of Toxic Poisoning Due to Heavy Metals
2.5 Previous Attempts to Monitor Heavy Metals in Environments
2.6 Common Tools for Environmental monitoring of Heavy Metals
2.7 Application of Gastropods and Bivalves as environmental Biomonitors
2.8 Mechanism of Element incorporation and Heavy Metal Uptake in soft tissue and shells of
Gastropods and Bivalves
CHAPTER THREE: MATERIALS AND METHOD OF STUDY
3.1 Collation of Datasets on Heavy Metal incorporation in gastropods and bivalves from
published studies
3.2 Description Statistics of Datasets
3.3 Statistical Data Treatment

CHAPTER FOUR: RESULTS AND INTERPRETATION
4.1 Results and discussion
4.2 Variability of Metal Concentrations and Metal Relationships in Shells and Soft Tissues
across taxonomic units
4.3 Soft tissues and shells of gastropod and bivalves species for bio-monitoring and as
environmental archives of heavy metals, using BCF, BMF and TSR as tools.
CHAPTER FIVE: SUMMARY, CONCLUSION AND
RECOMMENDATION
5.1 Summary and Conclusion
5.2 Recommendation
REFERENCES
CHAPTER ONE: INTRODUCTION

1.1 Background of Study
Heavy metals are naturally occurring elements (metals and metalloids) which have a high atomic
weight, density at least five (5) times greater than that of water (Fergusson, 1990; Duffus, 2002).
Heavy metals are broadly grouped into essential and non-essential elements based on their
usefulness or requirement by living organisms for biological processes and survival, as in the
case of gastropods and bivalves (mollusks). The essential heavy metals and semi-metals include
iron (Fe), zinc (Zn), copper (Cu), manganese (Mn), cobalt (Co), nickel (Ni), molybdenum (Mo)
and selenium (Se). This group is termed essential because of the dependence of mollusks on
them, albeit in minute or trace quantities, for basic metabolic activities. Inadequate supply of
these micro-nutrients results in a variety of deficiency diseases or syndromes (WHO/FAO/IAEA,
1996). When above tolerable levels, the presence of these essential metals in mollusks results in
harmful physiological effects. The non-essential heavy metals however, have no known benefits
to the living systems as several of them are toxic, not only to mollusks but their habitats as well,
even at low-level concentrations. Non-essential heavy metals include lead (Pb), mercury (Hg),
arsenic (As), tin (Sn), aluminium (Al), cadmium (Cd), silver (Ag), strontium (Sr), gold (Au),
antimony (Sb), tellurium (Te), bismuth (Bi), palladium (Pd), platinum (Pt), vanadium (V),
titanium (Ti), Uranium (U), and chromium (Cr), particularly the hexavalent form (Cr VI)
(Tchounwou et al., 2012). That some heavy metals are termed as non-essential does not negate
the fact that the society depends on them for advancements in technology and industrial
manufacturing processes. On the surface of the earth, heavy metals are mainly found chemically
bound in carbonates, sulfates, oxides, silicate rocks or they may occur in their metallic, elemental
forms. In nature, the agents of denudation such as weathering and erosion usually result in the
leaching and migration of heavy metals into soils, rivers, oceans and groundwater from the Earth
crust (Koller and Saleh, 2018). The combined effect of increased devastating geogenic
occurrences, that is, natural occurrences such as volcanic eruptions; and anthropogenic
processes, which are human activities; such as oil refining, mining, printing, production of
alloys, steel fabrication, textiles, coal combustion, paint production, pesticides, paper making,
production of fertilizers, discharge of industrial effluents, sewage, etc., negatively impacts the
environments of both humans and organic-life such as various species of mollusks. Also, their
contamination of drinking water sources cannot be underestimated both in developed and
underdeveloped regions (Ali and Khan, 2018; Ali et al., 2019; Idowu, 2022). Renewed concerns
about heavy metals and their impact on organisms and the environment arise from the fact that
they often find their ways into the food chain, either through bioaccumulation in plants or in
animal species, most especially in mollusks (gastropods and bivalves) which get ingested by
humans. Heavy metals get incorporated in the soft tissues and shells of gastropods and bivalves.
This metal uptake can lead to bioaccumulation in these mollusks, that is, once heavy metals get
absorbed or ingested by mollusks, they do not degrade out of their systems; rather they get stored
up within them. Due to some unique characteristics such as, the high degree of adaptability of
mollusks for survival, their resistance to harsh environmental conditions, mobility, lifespan, shell
secretion and growth patterns, the ability of their shells to be preserved in the geological record,
their abundant occurrence over a wide range of freshwater and marine environments, gastropods
and bivalves are favorable tools to exploit for environmental bio-monitoring; which is hereby
simply defined as the observation of the input or availability of heavy metals in the environment
(Yap et al., 2021; Krupnova et al., 2018; Fang et al., 2001). The shells of gastropods and bivalves
are quite essential in the fossil record as they can incorporate heavy metals during their growth
phases thereby recording prevailing environmental conditions throughout their lifetimes. These
shells are well preserved even after death; hence they can be used as environmental archives
(Gibson et al., 2001; Schone et al., 2007).
1.2 AIM AND OBJECTIVES OF STUDY
The aim and objectives of this work is to determine the level of metal uptake in the tissues and
shells of various species of gastropods and bivalves in freshwater and marine environments
across the world using collated data; to evaluate the usage and effectiveness of gastropods and
bivalves as environmental bio-monitoring tools for heavy metal contamination; and the usage of
their shells as environmental archives.
1.3 STATEMENT OF PROBLEM
Several authors have both criticized and condemned the usage of gastropods and bivalves as
heavy metal bio-monitors in the environment (Yap et al., 2021; Zuykov et al. 2013). This
research will help reinforce the effectiveness of the soft tissues and shells of gastropods and
bivalves as bio-monitoring tools, as well as reveal patterns of heavy metal uptake and their
controlling parameters by means of data interpretation. Also, numerous individual studies exist
on metal uptake in molluscs for specific cases and for some specific species, but there is no
general overview or consideration which gathers all these specific studies.
1.4 RESEARCH QUESTION
The research answers the following question:
i. Can the soft tissues and shells of gastropods and bivalves be used as heavy metal bio-
monitors in the environment?

ii. What are the controlling parameters that influence the input of heavy metals in the
soft tissues and shells of gastropods and bivalves?
iii. Does the type of organisms and taxonomic units determine the rate of heavy metal
uptake in gastropods ad bivalves?
iv. Is the enrichment of heavy metal in the soft tissues of gastropods and bivalves
relatively greater those of shells and vice versa for specific organisms?
v. Are specific elements preferentially incorporated in the soft tissues and shells of
gastropods and bivalves?
vi. Does heavy metal concentration in water and sediments lead to enhanced heavy metal
concentration in the shells and soft tissues of gastropods and bivalves?
vii. Does temperature have an impact on heavy metal uptake in either soft tissues or shells
of gastropods and bivalves?
viii. Can the shells of gastropods and bivalves be used as environmental archives?
1.5 SIGNIFICANCE OF STUDY
This research and the proper understanding of the trend of data relationships and interpretations
will give more insight on heavy metal contamination; assist researchers to appropriately tailor
their future researches for better scientific impact and societal relevance. Also, this will help
policy makers in mitigating avoidable health risks, devising means for environmental protection
and by extension, safeguarding public health using measurable levels of heavy metals within the
soft tissues of gastropods and bivalves in consonance with other valuable information embedded
and archived in their shells
CHAPTER TWO: LITERATURE REVIEW

2.1 SOURCES OF HEAVY METALS
Sources of heavy metals are largely grouped into two (2), they are geogenic sources and
anthropogenic sources.
2.1.1 Geogenic Sources
Heavy metals are embedded within the earth’s crust. Naturally occurring disasters or activities
such as volcanic eruptions, uplift, weathering, soil erosion of metal ions and leaching, easily
introduce these metals into the environment, that is, the air, land, rivers and oceans which serves
as habitats for various species of living organisms. In some cases, the consumption of
contaminated living organism such as fishes, mollusks and plants by humans also serve
secondary geogenic sources (Jyorti, 2020).
2.1.2 Anthropogenic Sources
Anthropogenic sources of heavy metals are directly or indirectly linked to Human activities.
They cover a wide range of activities such as industrial, agricultural, pharmaceutical, domestic
and atmospheric (He and Stoffella, 2005). These include oil refining, gold ore processing, usage
of leaded fuels, plumbing, brass manufacturing, copper polishing, plating, printing, hip alloy
replacement case, medications, steel fabrication, electroplating, textile, production of batteries,
coal combustion, paint industry, mining activities, usage of pesticides, paper industry, production
of plastics and fertilizers, the open dumpsites, sewage, weapon manufacturing, radioactive
wastes, etc. (Jyorti, 2020).
2.2 PERMISSIBLE LIMITS OF HEAVY METALS FOR ORGANISMS AND IN THE
ENVIRONMENT
The permissible limits of lead, cadmium, arsenic, mercury and other heavy metals in different
environmental matrices such as air, drinking water, natural water, soil are presented in Table 2.1
and Table 2.2; Table 2.3 however presents the daily human consumption limits for heavy metals
as suggested by various international agencies and authorities such as USEPA (Environmental
Protection Agency), WHO (World Health Organization), and OSHA (Occupational Safety and
Health Administration).
Table 2.1. Permissible limits of different toxic elements in the human blood and environmental
matrices such as air, drinking water and soil (Jyorti, 2020).
Heavy USEPA WHO OSHA

Metal
Ambient Air Drinking Soil Ambient Drinking Soil Air at Blood
3
(μg/m ) Water (ppm) Air Water Workplace (μg/dL)
(mg/L) (mg/L) (μg/m3)
Pb 0.15 15000 400 (in play - 0.015 - 30 40
areas); 1200
(in non-play
areas)
Cd .0065–0.13 0.005 85 - 0.003 - 5 -
As 50 0.01 - - 0.01 - 10 -
Hg 500 0.002 4–16 - 0.001 - - -
Table 2.2. Critical concentrations (that is, toxic or dangerous levels) of some heavy metals
in natural waters according to EPA (After Odobašić et al., 2019)
Heavy Metal Maximum Allowable Concentration (μg/mL)

Mercury 0.002
Arsenic 0.5
Lead 0.5
Copper 0.6
Cadmium 0.04
Zinc 5
Table 2.3. Daily human consumption limits for the five heavy metals (μg/day) a (After Balali-
Mood et al., 2021)

DATA Hg Pb Cr Cd As
SOURCE
A - 0.5 8.2 4.1 -
B 20 20 - 6 10
C 21 (inorganic) - 210 70 21 (inorganic)
D 50 250 120 56 150
E 16 250 - 70 150
F 2 10 - 4.1 10
G 16 (methyl) - 63 (hexavalent) 25 210
A- The California Safe Drinking Water and Toxic Enforcement Act (California Proposition 65)
maximum allowable dose levels for chemicals causing reproductive toxicity, μg/day;
B- American National Standards Institute (ANSI)/International Dietary Supplement Standard
173 = ANSI 173 Guidelines to the Dietary Supplement;
C- United States Environmental Protection Agency (EPA) daily reference doses, μg/day;
D-The Food and Agricultural Organization/World Health Organization Joint Expert Committee
on Food Additives Acceptable Daily Intakes;
E- Europe/WHO;
F- American Herbal Products Association (AHPA);
G- The European Food Safety Authority (EFSA).
*
For cases where few regulations presented limits as tolerable weekly intake. Such thresholds
were considered and shown as the maximum daily exposure.
2.3 ADVERSE EFFECTS OF HEAVY METAL CONTAMINATION

The toxicity of Heavy metals depend on certain factors which includes, but are not limited to
their dosage, exposure route, chemical species, age and gender of exposed individuals or
organisms, also, the genetics, and nutritional status of exposed individuals. Arsenic, cadmium,
chromium, lead, and mercury rank among the priority metals that are of public health
significance due to their high toxicity. They are considered systemic toxicants well known to
induce multiple organ damage, even at lower levels of exposure, and according to the United
States Environmental Protection Agency (USEPA), and the International Agency for Research
on Cancer (IARC), they have been classified as human carcinogens (Tchounwou et al., 2012).
Other adverse effects include cardiovascular diseases, developmental abnormalities, neurologic
and neurobehavioral disorders, diabetes, hearing loss, hematologic and immunologic disorders.
The main pathways of exposure include ingestion, inhalation, and dermal contact. The severity
of adverse health effects have been positively correlated to the types of heavy metal, their
chemical form, period of exposure, dosage, etc. they cause long-term health problems in human
populations (Abdullah et al., 1990; Lopez et al., 2004; Tchounwou et al., 2012). Bakulski et al.,
(2020) reported that the presence of lead and cadmium in the human body have the ability to
reach the brain and result in Alzheimer’s disease. Cadmium for instance, shows its toxic effects
on the gastric system and leads to gastric cancer, breast cancer, lung cancer, and it also affects
the excretory system and leads to renal cancer (Jyorti, 2020).
2.4 MAJOR OUTBREAKS OF TOXIC POISONING DUE TO HEAVY METALS
There have been numerous reports of heavy metal contamination since the earliest twentieth
century. Some of which includes the following:
2.4.1 Minamata Syndrome:

As far back as 1932 in Minamata Bay, Japan, there have been several devastating reports of
heavy metal contamination. Sewage containing methyl mercury was reported to have been
released by Chisso's chemicals works into Minamata Bay in Japan. The mercury accumulated in
sea creatures, leading eventually to mercury poisoning in the population. By 1952, the first
incident of mercury poisoning appeared in the population of Minamata Bay, which resulted from
the consumption of fish already contaminated with mercury, leading to over 500 fatalities. Since
then, Japan has had the strictest environmental laws in the industrialised world. Minamata Bay
had to be restored by removing more than 1.5 million cubic meters of contaminated sediments
over ten years at a cost of 48 billion yen (WEPA, 2022).
2.4.2 Hinckley Water Contamination
Between 1952 and 1966, Pacific Gas and Electric used hexavalent chromium to prevent
corrosion in a cooling tower system. The water from the system was eventually discharged into
unlined ponds, ultimately contaminating the groundwater and affecting 5.12 square kilometres
zone around the plant. On entry of the contaminated water into the drinking water supply, scores
of residents in the area became sick and it also increased the instances of breast cancer,
Hodgkin’s disease, miscarriages, kidney and ovarian tumours, as well as lungs, brain and
gastrointestinal cancer (Alpha Environmental, 2016). As at 2013, the ongoing groundwater
remediation had cost over $750 million.
2.4.3 Pollution of the Rhine at Basel, Sandoz
On the first of November 1986 in Sandoz, after a major fire outbreak, the wter used by fire-
fighters to extinguish the fire carried fungicides which contained mercury into the Upper Rhine.
This resulted in the near annihilation of Fish in the region, killing different species of fishes over
a stretch of 100 km. The shock served as momentum to drive several Environmental Assessment
projects.
2.4.4 Contamination of the Coto de Donana Spanish Nature Reserve
In April 1998, the Spanish nature reserve was contaminated with heavy metals after an
environmental disaster. A rupture in a dam which belonged to a mine released toxic chemicals
which were transported into the Coto de Donana nature reserve in southern Spain. About 5
million cubic metres of mud containing sulphur, lead, copper, zinc and cadmium flowed down
the Rio Guadimar. Experts concluded that the damage caused by the pollution on Europe's
largest bird sanctuary, as well as Spain's agriculture and fisheries, is permanent.
2.4.5 Mariana Dam Collapse, Brazil
The Mariana dam collapse at a mine on 15 th November, 2015 was the worst environmental
disaster in Brazilian history and one of the biggest worldwide (Queiroz et al., 2018; Zebral et al.,
2022). It resulted in the release of a heavy metal contaminated mud tsunami that adversely
affected both aquatic and terrestrial biota. The water supply of about 250,000 people in the area
was interrupted as a result of the contamination. High levels of mercury, arsenic, chromium and
manganese were discovered to have contaminated the sources of drinking water. It released
heavy metals into the Doce River and even reached the coast of the State of Espirito Santo,
thereby affecting the marine ecosystem.
2.5 PREVIOUS ATTEMPTS TO MONITOR HEAVY METALS IN
ENVIRONMENTS
There have been several attempts made by scientists, corporate bodies and governments to
monitor heavy metal contamination in the environment, their impact on human public health and
Remediation action plans. Some of the previous works done in this field of research includes:
2.5.1 Mussel Watch Program
The mussel watch program which was pioneered by The United States of America’s National
Oceanic and Atmospheric Administration (NOAA) is the most comprehensive scientific attempt
ever made to monitor heavy metal contamination of the coastal and marine environment, on the
largest scale, till date. The NOAA’s Mussel Watch Program (MWP) monitors the status and
trends of chemical contamination of U.S. coastal waters. The program began in 1986 and is one
of the longest running, continuous coastal monitoring programs that is national in scope. The
program is based on annual collection and analysis of oysters and mussels (Johnson et al., 2012).
Since bivalves are sessile organisms which filters particles from water; thus, measuring
contaminant levels in their tissue is a good indicator of local contamination. Mussel Watch data
are useful for characterizing the environmental impact of new and emerging contaminants,
extreme events (hurricanes and oil spills), and for assessing the effectiveness of legislation,
management decisions, and remediation of coastal contamination levels. As a result of
monitoring all major estuaries for chemical contamination, Mussel Watch results can be used to
identify geographic areas of concern and potential human exposures to elevated levels in
seafood. In 1986, the inaugural year of the Mussel Watch Program, 145 sites were sampled.
Today, Mussel Watch is comprised of nearly 300 monitoring sites, where more than 140
chemical contaminants, chosen through consultation with experts and scientists from academia
and government, are measured. Many of these contaminants are listed as Environmental
Protection Agency (EPA) Priority Pollutants (Keith and Teillard, 1979). Legislation has been
passed to regulate most of the organic contaminants analyzed by the Mussel Watch Program
(http://NSandT.noaa.gov). The majority is toxic to aquatic organisms, and some are taken up and
stored in animal tissues with the potential to be transferred through food chains to humans. Part
of the objectives of the Mussel Watch Program is to assess chemical and microbial
contamination in both the tissue and sediment matrices of bivalves. To collect mussels, and
sediment from sample sites and conduct analyses for chemical and microbial contamination;
sediment toxicity, and benthic infaunal organism species characterization (Johnson et al., 2012)
2.5.2 Other independent or organization-funded researchers and their findings
Samsi et al., 2017 reviewed the usage of Gastropods as bio-indicators and bio-monitors of heavy
metal pollutions. The terms bio-monitor and bio-indicator have been used in varying ways to
describe different approaches and techniques for studying biological responses to pollution.
However, bio-monitoring can be seen as both a qualitative (bio-indicator) and quantitative (bio-
monitor) approach to pollution control (APIS, 2016). Bio-monitors hold quantitative information
on the health of an ecosystem. The terms are sometimes used interchangeably as a bio-monitor is
also a bio-indicator, except that it quantifies the impact of pollutants or eventual outcome on an
organism ecosystem. In comparison, bio-indicators provide a pollutant measurement which can
be compared with an instrument measurement. They provide information on the quality of the
environment and the actual condition of an organism or ecosystem (APIS, 2016). According to
(Markert et al., 1999), for ideal bio-monitors, there is a linear relationship between the
concentration in the environment and that in the organism, as only such a linear relationship
allows organisms to supply unequivocal statements about their environment.

In their research, Samsi et al. (2017) concluded that gastropods can be used as bio-indicators and
bio-monitor heavy metal pollution and that the response of these organisms to pollutants is
indicated by the decrease in their abundance, size changes and community structure. They noted
that heavy metals are capable of affecting the hardness, thickness, volume and color of gastropod
shells. The review identified various gastropod species which are useful to bio-moitor heavy
metals. These includes: Littoraria scabra in mangrove ecosystems (Wolf et al., 2001; Wolf and
Rashid, 2008); Terebralia palustris; Nucella lapillus and Nassarius reticulatus to determine the
pattern of bioaccumulation butylin (Ruiz et al., 2008; Ruiz et al., 2010). El-Sorogy et al. (2013)
used the shells Nerita albicilla and Canarium (Gibberellus) gibbosus as indicators of pollution in
the Red Sea, Egypt. Yap and Noorhaidah (2012) used Telescopium telescopium gastropod
species to biomonitor Cd, Cu, Pb, Fe, Ni, and Zn in Sungai Sepang Besar, Malaysia.
Abdel Gawad (2018) investigated the Concentrations of heavy metals in water, sediment and
mollusk gastropod, Lanistes carinatus from Lake Manzala, Egypt. In his research, he focused on
estimating the concentration of eight heavy metals (Mn, Fe, Co, Ni, Cu, Zn, Cd and Pb) in
gastropod L. carinatus as well as in water and sediment from Lake Manzala, the most heavily
polluted lake in Egypt. He concluded that The mean heavy metal concentrations in soft tissue
were in the following order Fe > Mn > Zn > Ni > Co > Cu > Pb > Cd. Also, that Bio-water
accumulation factor of soft tissue and shell of L. carinatus were much higher than bio-sediment
accumulation factors, thereby suggesting that L. carinatus could be used as a bio indicator for
some heavy metals in water. Partitioning factor values, also called the Tissue-Shell ratio (TSR),
which is the ratio of the mean metal concentrations in the soft tissue and the shell from each site
(Cravo et al. 2004) indicate that these metals have a much greater chance to be accumulated into
soft tissue than in shell. On the other hand, Co and Ni have a greater chance to be accumulated
into the shell than in soft tissue. Furthermore, high precision (lowest percentage Coefficient of
Variance) of Cd and Pb concentrations in gastropod L. carinatus support soft tissue and shell of
this gastropod as a suitable bio indicator for these heavy metals in Lake Manzala.
Amin et al. (2006) carried out a comparative study of heavy metal concentrations in Nerita
lineata from the intertidal zone between Dumai Indonesia and Johor Malaysia. In their study,
they concluded that the preponderance of industrial and anthropogenic activities in Johor
Malaysia as compared to Dumai Indonesia was reflected in higher concentrations of metals
accumulated in the N. lineata collected from Johor. They noticed that metal concentrations
recorded in N. lineata collected from the stations close to industries and anthropogenic activities
in both Dumai and Johor areas were higher. The abundance of N. lineata in the intertidal area of
both Malaysia and Indonesia, favors their consideration as potential biomonitors of heavy metal
pollution. Hence, they proposed that the operculum and shell of N. lineata could be potential bio-
monitoring materials for heavy metals, especially for Cd, Pb and Ni, whilst the soft tissue could
be good bio-monitoring organ for Cu, Zn and Fe.
Amin et al. (2008) also studied gastropod assemblages as indicators of sediment metal
contamination in Mangroves of Dumai, Sumatra, Indonesia. In their study, the impacts of heavy
metal concentrations in sediments on the gastropod community structure were assessed in the
coastal waters of Dumai, Sumatra, Indonesia. This was done by relating the levels of heavy metal
pollution with the changes of gastropod community structure in the study area. The
concentrations of Cd, Cu, Pb, Zn, Ni, and Fe in surface sediments analyzed were correlated with
the abundance, species richness, and diversity of gastropod populations. It was discovered that
sediments at stations with relatively more anthropogenic activities accumulated higher
concentrations of heavy metals and consequently, lower abundances, species richness and
diversity of gastropods; while stations with lower heavy metal concentrations in sediments
showed the opposite pattern in gastropod community metrics. Among the metals analyzed, Cu
and Zn had strongest negative correlations with the gastropod diversity which suggests that these
metals were the most detrimental to gastropod populations in the mangrove area of Dumai
coastal waters.
Yap et al. (2021) gave a commentary on the use of bivalve mollusks in monitoring metal
pollution levels. In their work, they critiqued the work of Zuykov et al. (2013). Zuykov et al.
(2013) made some controversial assertions. Some of which includes the following: Firstly, that
the uses of bivalves as bio-monitors of metal pollution are primitive methods; secondly, that the
use of shells to construct pollution history blueprint is futile; and thirdly, that there has not been
any documented evidence of severe health effects of bivalves due to metal accumulation.
In light of these, Yap et al. (2021) reviewed the use of bivalves’ soft tissues for metal pollution
studies from some of the available literature. At least, ninety-two (92) of such literatures from
world renowned researchers were put under consideration. The literatures reviewed covered
more than five hundred and sixty-eight (568) sites across several countries and continents using
at least thirty-six (36) different bivalve species such as: Mytilus galloprovincialis, Perna viridis,
Perna canaliculus, Mytilus edulis, Ameghinomya antiqua, Aulacomya atra Mytilus chilensis,
Anodonta cygnea, Mytilus edulis chilensis, Gafrarium tumidum, Isognomon isognomon, Mytilus
trossulus, Saccostrea cucullata, Crassostrea madrasensis, Anomalocardia brasiliana,
Brachidontes exustus, Crassostrea rhizophorae, Mytella guyanensis, Perna perna, Donax
trunculus, Modiolus Capax, Perumytilus purpuratus, Semelle solida, Tagelus dombeii, Mytella
strigata, Crassostrea gigas, Meretrix lusoria, Anodonta anatina, Unio pictorum, Unio tumidus,
Mytilus edulis trossulus, Crenomytilus grayanus, Pletholophus swinhoei, Crassostrea gasar,

Pinctada radiate, Paphia textile, Brachidontes rodriguezii, Choromytilus meridionalis, Unio
crassus, Mytilus unguiculatus, Mytilus edulis L., Xenostrobus secures, Mytilus edulis platensis,
Chamelea gallina and Unio elongatulus eucirrus; to bio-monitor heavy metal contamination in
the environments. Yap et al. (2021)’s commentary condemned Zuykov et al. (2013)’s position
that the use of shells to construct pollution history blueprint is futile. Since this is one of the main
objectives of this particular research, hence the findings of Yap et al. (2021) in contrast to the
position of Zuykov et al (2013) is very crucial and critical to this study.
Yap et al. (2021) believed that the original idea of using the shell as a reliable bio-monitoring
material for the reconstruction of pollution history is acceptable, workable and reliable when
compared to the use of soft tissues. This is one of the reasons why so many researchers
conducted such related studies using molluscs’ shells for the bio-monitoring of metal pollution,
to compare the current with the past history of metal bioaccumulation in bivalve shells. To
counter Zuykov et al. (2013)’s position, Yap et al. (2021) reviewed the research work of thirty-
six (36) different researchers who made use of the bivalve shells in metal pollution studies and
thirty-seven (37) researchers who used bivalves’ biomarkers in metal pollution studies on
bivalves. Their conclusions were that, with all the reported studies using bivalves as bio-
monitors of heavy metal pollution, the effectiveness of using Mussel Watch is beyond reasonable
doubts. However, they encouraged the development of more accurate methodology of heavy
metal data interpretation and the precision of the bio-monitoring studies using bivalves as bio-
monitors both in coastal and freshwater ecosystems.
2.6 COMMON TOOLS FOR ENVIRONMENTAL MONITORING OF HEAVY
METALS
There are several tools which are used for monitoring the presence of heavy metals in an
environment, either as a contaminant, pollutant or harmful constituent of the environment.
2.6.1 Molecular Biomarkers
Kadim and Risjani (2022) reviewed the usage of Biomarker for monitoring heavy metal
pollution in aquatic environments, focusing on the molecular perspectives. Biomarkers are
measurable organic compounds or molecules which are formed by organisms in response to
heavy metals. Biomarkers are biochemical, cellular, physiological or behavioral variations in the
tissue, body fluids or whole body of an organism that provide evidence of exposure to chemical
pollutants and may also indicate toxic effects (APIS, 2016; Puntmann, 2009; Parente and
Hauser-Davis, 2013). Molecular biomarkers are one of the essential tools used for monitoring
heavy metal contaminations in the environment using aquatic organisms. For instance, Risjani et
al. (2022) studied the changes or imbalance of ‘17 beta estradiol hormone’ as a biomarker in the
green mussels, Perna viridis species from Java Sea in Indonesia.
2.6.2 Soil Enzyme Activities
Soil enzyme activity have been suggested as suitable indicators for the evaluation of metal
contamination because they are susceptible to microbial changes caused by heavy metal stress
and are strictly related to soil nutrient cycles. Cui et al. (2020) evaluated heavy metal pollution in
soils based on enzyme activities. The most common methods of heavy metal pollution evaluation
based on enzyme activities, includes single enzyme index, combined enzyme index, enzyme-
based functional diversity index, microbiological stress index, and ecoenzymatic stoichiometry
models.
2.6.3 Common Plants:

Malizia et al. (2012) stated that common herbaceous and leguminous plants could be used as
alternative and simple analytical tools for monitoring environmental pollution most importantly,
soil pollution by heavy metals. The Heavy metal patterns found in roots and leaves of Plantago
major L., Taraxacum officinale L. and Urtica dioica L. and pretense L., led to the conclusion that
the heavy metals content in plant roots is higher than in leaves and that accumulation process of
herbaceous plants does not significantly differ from leguminous plants, that is, the higher the
heavy metal concentration in the soil, the higher the concentration in roots and consequently in
leaves of common plants. Some green algae or phytoplankton such as Scenedesmus subspicatus,
Chlorella vulgaris and Pseudokirchneriella subcapitata are standard biomonitors (Ratte et al.
2003). Algal mats of the green algae genera Klebsormidium are good indicators of high Fe
concentration in water, while the presence of Fucus vesiculosus suggests heavy metal pollution
in marine environments (Das et al. 2009). Different plant organs (leaves, flowers, needles, bark
and roots) of trees such as spruce, birch, pine, oak, olive, poplar, ash tree can be used for heavy
metal bio-monitoring in various ecosystems (Serbula et al. 2012; Filipovic-Trajkovic et al.
2012). Mosses and lichens are used as bio-monitors of aerial heavy metals contamination
because of their bio-accumulative properties (Blagnyte and Paliulis, 2010; Mojtaba et al., 2020).
Analysis of indigenous mosses is currently used in international and national monitoring
programmers, particularly in Europe (Harmens et al., 2008; Blagnytė and Paliulis, 2010; Zhou et al.,
2017; Zechmeister et al., 2020). Mosses have been applied to measure heavy metal levels and
trends within and around urban and industrial areas (Suchara et al. 2011). The use of fungi in the
monitoring of heavy metal pollution is limited but some fungal groups are better bio-
accumulators than others (Joksimovic and Stankovic 2012). Other plants which have been
employed for biomonitoring heavy metal include: Mexican sunflower (Bello et al., 2020) , Acer
negundo, Aesculus hippocastanum, Tilia platyphyllos, Prunus ceracifera, Ailanthus altissima,
etc. (Bayraktar et al., 2022).
2.6.4 Small Mammals:
The distributions of heavy metals in polluted areas can reflect in the body of small mammals.
Small mammals like rodents have interesting features which makes them acceptable as a bio-
indicator species in different studies. They are suggested to apply in monitoring of heavy metals
due to their large population, wide distribution, and similarity to human in terms of habitat and
internal organs, short life spans, and many other characteristics. (Zamani, 2020). Shrews, moles,
voles and mice) fulfill the basic requirements for use in bio-monitoring and eco-toxicological
studies (Sánchez-Chardi and Nadal 2007; Adham et al. 2011; Okati and Rezaee 2013). They also
have widespread occurrence, a limited home range, generalized food habits, short life span, and
high reproductive rates and are easily collected. They are more exposed to environmental
contaminants than large mammals due to their small body size and high metabolic rate
(Levengood and Heske 2008). Martiniaková et al. (2011) investigated the usage of the bones of
bank and voles to monitor heavy metal contamination. Also, the internal organs of organisms
such as Microtus agrestis, Sorex araneus and Talpa europaea have been used by Andrews et al.
(1984) and Pankakoski et al. (2019) to monitor heavy metal contamination in various
environments.
2.6.5 Technological Tools: Biosensors
Numerous technologies have been developed to monitor heavy metal concentration in the
environment, be it water, plants, air or soils. One of such technological tools is the use of
Biosensors (Odobašić et al., 2019). Biosensors are analytical sensory devices that combine
physical and chemical sensing techniques (Najeeb et al., 2017; Bhalla et al., 2016). Biosensors
allow estimation of biological effects, e.g., toxicity of specific chemicals, by detecting their
bioavailable concentrations in the environment (Damborsky et al., 2016). There are various
categories of biosensors such as: Electrochemical, Optical, Piezoelectric, Thermal, Affinity and
Catalytic biosensors. Asides environmental monitoring, other applications of biosensors include:
food safety, detection of various diseases, artificial implantable devices such as pacemakers, etc.
(Odobašić et al., 2019). Some of the other technologies employed to monitor heavy metals in the
environment include: Usage of ion-exchange resin sachets and micro-XRF core-scanning, With
the use of technology, Proteomics, genomics and bioinformatics, certain procedures such as
DNA and RNA sequencing, as well as mass spectrometry based proteomics can be used to
monitor heavy metal contaminations (Kadim and Risjani, 2022).
2.6.6 Avian Blood and Feathers
Zebral and Bianchini (2022) used avian blood and feathers as biological tools to track the
impacts from heavy and trace metals bioaccumulation from the Mariana environmental disaster in
Brazil. They discovered that Levels of Pb, Hg, As and Cd found in birds were frequently above proposed
threshold levels, indicating possible health impacts and that birds from areas impacted by Mariana's
disaster still presents elevated contamination even after 5years following the event.
Other not so common tools for bio-monitoring heavy metal contamination in the environment as
well as exposure to organisms, especially humans include urine (Al-Saleh, 2020;
Saravanabhavan et al., 2017; Wilhelm et al., 2004), placenta (Al-Saleh et al., 2011), and breast
milk (Al-Saleh, 2021) .

2.7 APPLICATION OF GASTROPODS AND BIVALVES AS ENVIRONMENTAL
BIOMONITORS
Much attention has been paid to the capability of marine organisms, especially mollusks to
accumulate metallic toxicants from the marine environment where it lives. As far back as early
20th century, Goldberg (1978) used bivalves as a surveillance tool of coastal pollution. Shell-
bearing bivalves (mussels, clams) and gastropods are relevant biological models to study the
degree of contamination of environments by heavy metals. There are several advantages
gastropods and bivalves have over other organisms as bio-monitors. Compared to other
invertebrate groups like arthropods and vertebrates, mollusks, particularly gastropods and
bivalves exhibit a limited ability to excrete pollutants directly using their kidneys, tissues and
other excretory organs. They are also limited in metabolizing organic chemicals and to
physiologically detoxify their systems of heavy metals through the formation or binding to
metallothioneins (Largierse et al., 1998). In consequence, they achieve higher bioaccumulation
factors for many toxicants than other organism groups. Bio-monitoring of heavy metal
contamination and bioavailabilities using the total soft tissues of gastropods and bivalves nearly
eliminates the avoidable risk of lack of precisions in defining the heavy metal contamination
levels in an environment (Yap et al., 2006). Terrestrial and marine gastropods directly consume
plants known to heavily bio-accumulate heavy metals (Johnson et al., 2009; Kennedy et al.,
2012). They have multiple compartments for bioaccumulation (e.g., liver, mantle, foot, digestive
gland-gonad complex, shell etc.) and are a food source for higher level organisms (e.g., birds)
that could further mobilize heavy metals from the initial site of contamination through trophic
transfer (Allison et al., 2015). Their skeletal parts also record the changes in their tissue
structures due to the environmental conditions in which they lived. Shells can provide a more
accurate indication of environmental change and pollution because they exhibit less variability
than the living organism’s tissue, and they provide a historical record of metal content
throughout the organism’s lifetime. This record remains preserved after death (Carriker et al.,
1982, Thorn et al., 1995; Huanxin et al., 2000; Yasoshima and Takano, 2001). Some species,
such as Margaritifera margaritifera can live more than 100 years and can provide a valuable
record of environmental changes over a significant period of time (Carell et al., 1987) and
Velesunio ambiguus has been known to live up to 30 years (Walker, 1992; Dar et al., 2018;
Kesavan et al., 2013). Gastropods and bivalves are ideal monitors.
2.8 MECHANISM OF ELEMENT INCORPORATION AND HEAVY METAL
UPTAKE IN SOFT TISSUE AND SHELLS OF GASTROPODS AND BIVALVES
As filter-feeders and detritus feeders, the uptake of heavy metals in these organisms is not only
from food and water but also from ingestion of inorganic particulate materials and sediments
(Fang et al., 2003; El-Silkaly et al., 2004, Sidoumou et al., 2006; Kupekar et al., 2012). They
feed on plant detritus and algae and were found to take up metals from water and suspended
particulate matter. Their gills were found subjected to maximum filtration of water than other
body parts and thus found to uptake high concentration of metals (Rajendran et al., 1988; Bu-
Olayan and Thomas, 2001)
The mechanism of heavy metal uptake comprises of at least two processes:
i. Bioavailability of heavy metals from source or environment
ii. Bioaccumulation or incorporation of heavy metals into soft tissues and shells of
gastropods and bivalves through feeding habits, absorption, diffusion and secretion
According to Worms et al. (2006), there are three exposure scenarios for heavy metal uptake as
shown in Figure1. These include the free metal ions, the metal complexes and the particle-bound
metals. Toxicity or bioaccumulation occurs when the levels of metal absorption from all sources
of contamination exceed the combined level of detoxification and excretion of the heavy metals.
Bio-accumulators are organisms that accumulate pollutants within their tissues. They may be less
sensitive to, or indeed unaffected by pollution but are nevertheless good indicators of the
exposure of the ecosystem to pollutants
Figure 2.1. Mechanism of heavy metal uptake in the biological membranes of Gastropods and
Bivalves (After Worms et al., 2006 and Samsi et al., 2017). Note: M-C Metal complexes; M-I
Metal Ion; MLB Metal particles labile bond; M-T Metal target sites; M-L Metal bound with a
biological ligand.
In aquatic environments, heavy metals can exist in either dissolved or particulate phases.
Gastropods and bivalves take up these metals from surrounding environments directly through
their exposed tissues and through feeding (Chapman et al., 1998). These metals can then
accumulate in their body tissues, thereby causing lethal or sub-lethal effects (Bryan and
Langston, 1992, Bat and Raffaelli, 1998). The uptake of dissolved heavy metals may be
facilitated by diffusion via the permeable surfaces of the organisms, such as the gut and
respiratory surfaces (Depledge and Rainbow, 1990, Wang, 2001). The efficiency with which
dissolved heavy metals is absorbed happens to be an important factor when assessing the toxicity
of heavy metals to particular gastropods and bivalves in aquatic environments (Wang et al.,
1996). Heavy metal uptake in form of particulates usually occurs through feeding. It is affected
by the assimilation efficiency of the metals and the ingestion rates of the organisms (Wang et al.,
1996).
Within gastropod and bivalve species, the ability to take up cations varies from one element to
another and with their morphology; this is also dependent on their environment (Fukunuga and
Anderson, 2011). It has been discovered that heavy metal contaminants are preferentially
concentrated in the gonadal and non-gonadal tissues of bivalves and gastropods (Ellis et al.,
1993; Lee, 1993; Abbe et al., 1994; Cunningham and Tripp 1975; Mo and Neilson, 1993; Kim et
al., 2006). Gastropods and bivalve species which grow in environments which are not polluted
by heavy metals, still have a basic content of the essential heavy metals in minute quantities.
These content levels have to be taken into account while evaluating element concentrations.
There are several factors which affect heavy metal uptake by gastropods and bivalves. If high
concentrations of certain cations are present in the sediment depositions or environment, they
inhibit the uptake of other cations. In areas with a marine influence, for example, the high
concentration of sodium and magnesium reduces the uptake of zinc and cadmium (Gjengedal
and Steiness, 1990). Also, there are some evidences which suggest that the presence of Lead
could increase the bioaccumulation of Zinc (Fukunuga and Anderson, 2011).

CHAPTER THREE: MATERIALS AND METHOD OF STUDY
3.1 Collation of datasets on heavy metal incorporation in gastropods and bivalves from
published studies
Datasets on the use of gastropods and bivalves for heavy metal bio-monitoring from research
publications by various researchers and organizations were used for this study. Data was
retrieved from academic and scientific websites; open access and subscribed journals while few
were personally requested from some of the authors.
3.2 Description Statistics of Datasets
The dataset gathered for this research comprises some or all of the following statistical elements:
i. Scientific classification of gastropods or bivalves used for the study
ii. Location of study.
iii. Climatic condition during the course of investigation
iv. Environmental habitat
v. Time of research publication
vi. Salinity
vii. Temperature
viii. Number of samples per location
ix. Measured heavy metal concentration values in shell elements
x. Measured heavy metal concentration values in tissue elements
xi. Measured heavy metal concentration values in sediments
xii. Measured heavy metal concentration values in water

3.3 Statistical Data Treatment
The metal concentrations and metal relationships in shells and soft tissues of gastropods and
bivalves were subjected to statistical data treatment to determine possible variations within
individual species, organism body parts and taxonomic units for application across various
environments. Statistical elements considered include:
3.3.1 Bio-concentration Factor (BCF)
The bio-concentration factor was used to estimate the accumulation of heavy metals in the
mollusks (Gobas and Morrison, 2000; Ibrahim and El-Regal et al., 2014).
BCF = Concentration Biota

Concentration Water
3.3.2 Bio-mineralization Factor (BMFM)
The bio-mineralization factor was used to evaluate the differential abilities of the studied
mollusk species to bio-mineralize heavy metals within their shells, the bio-mineralization factor
(BMFM) was modulated from the equation of the bioaccumulation factor (BAF) estimated by
Gobas and Morrison, (2000) as also used by Dar et al. (2018).
BMF = Metal concentration in shell

Metal concentration in sediment
3.3.3 Tissue-Shell Relationship
The tissue-shell relationship was determined by calculating the ratio of the heavy metals
concentrations in the tissues and shells of each gastropod and bivalve species (Walsh et al., 1995;
Szefer and Szefer, 1990).

TSR = Metal concentration in tissues
Metal concentration in shells
3.3.4. Environment-Tissue Relationship
The environment-tissue relationship was determined by comparing the fractions of heavy metals
incorporated within the tissues of gastropod and bivalve species with those present in the water
and sediments and drawing inferences from observations.
CHAPTER FOUR: RESULTS AND INTERPRETATION
4.1 Results and discussion

The tissue, shell, water and sediment concentrations of metals such as Cd, Pb, Cu, Zn, Cr, Ni,
Co, Mn, Fe and Hg in sixty-eight different species of gastropods and bivalves across different
countries and continents of the world are presented in Tables 4.1 and 4.2 (THAT IS, SHEET 1
AND 2 OF THE EXCEL FILE), respectively. The mean concentrations of all the metals studied
in soft tissue, shells, environments, as well as their ratios are presented in Charts 3 to 66. It
includes the variation in elemental compositions across the tissue, shell and environment of
individual species studied, simple statistical plots of individual species against heavy metal
concentrations in their tissues, shells and environments. Also, plots of individual species against
bio-concentration factors, bio-mineralization factors and tissue-shell indices. Mytilus
galloprovincialis recorded the lowest and highest Arsenic concentration values of 0.22 and 29.44
from the Taranto gulf of southern Italy and the Asturias Coastline of Northern Spain
respectively.
4.2 Variability of Metal Concentrations and Metal Relationships in Shells and Soft
Tissues across taxonomic units
4.2.1 Cerithium scabridum

Figure 4.1 Curve showing the mean tissue concentration, mean water concentration and mean
sediment concentration of heavy metals for Cerithium scabridum
Figure 4.2 Curve showing the bio-concentration factor for heavy metal in Cerithium scabridum
There is a random variation in the heavy metal concentration and distribution in the soft tissues
of Cerithium scabridum. Cr concentration has a range of 0.9 to 1.72, Cu 1.32 to 4.96, Ni 2.25 to
5.22, Pb 2.29 to 15.4, V 2.36 to 6.88and Zn 0.32 to 0.37 as shown in Table 4.3. The mean
sediment and water concentrations of chromium, 104.13 and 48.13 (ug/g) exceeds that of Cu, Ni,
Pb and V as shown in Figure 4.1. This suggest that the environment is relatively polluted with
chromium, but its low incorporation in the soft tissues of this species (1.39 ug/g) in comparison
with other metals show that Cerithium scabridum preferentially bio-accumulates Pb, V, Ni, and
Cu in its soft tissues, that is, in decreasing order of preference. This is further confirmed by the
BCF curve which peaks at 12.74 for Pb as shown in Figure 4.2.
4.2.2 Perna viridis

Figure 4.3 Curve showing the mean tissue concentration of heavy metals for Perna viridis
The heavy metal concentration and distribution in the soft tissues of Perna viridis varies. Cd
concentration has a range of 0.02 to 19.10, Cr 0.50 to 6.00, Cu 1.50 to 11.30, Ni 3.40 to 8.10, Pb
0.35 to 2.14, Zn 12.60 to 79.00 and Mn 30.20 to 108.60 as shown in Table 4.4. The mean tissue
concentration of manganese and zinc, 51.04 and 35.95(ug/g) significantly exceeds other metals
as shown in Figure 4.3.
4.2.3 Hemifusus pugilinus

Figure 4.4 Curve showing the mean tissue concentration, mean shell concentration and mean
sediment concentration of heavy metals for Hemifusus pugilinus
Figure 4.5 Curve showing the mean bio-concentration factor and tissue-shell ratios for heavy
metals in Hemifusus pugilinus

The heavy metal distribution patterns for the mean tissue, shell and sediment concentrations in
Hemifusus pugilinus have clearly similar curves as shown in Figure 4.4. Although the
concentration of all heavy metals in the species and its environment are quite low as almost all
values are below 0.5ug/g, except for the mean tissue concentration of manganese and the mean
shell concentrations of manganese, iron and copper which are approximately 0.5ug/g. The curve
shows that the rate of secretion or incorporation of Mn, Fe and Cu by the shells of slightly
exceeds the heavy metal concentration of the soft tissues and sediments. Also, the mean BMF
and TSR curves seem laterally symmetrical as shown in Figure 4.5. The mean BMF factors for
all metals are >1.00 while the TSR for all metals are <1. This indicates that the shells of
Hemifusus pugilinus have better potentials of usage in monitoring the history of heavy metal
pollution in the environment compared to soft tissues.
4.2.4 Bursa spinosa
sediment concentration of heavy metals for Bursa spinosa

Figure 4.7 Curve showing the mean bio-mineralization factor and tissue-shell ratios for heavy
metals in Bursa spinosa
The heavy metal distribution patterns for the mean shell and sediment concentrations in Bursa
spinosa have similar patterns as shown in Figure 4.6. The concentration of all heavy metals in
the species and its environment are quite low but peaks at its Cu and Fe values which ranges
between 0.40 and 0.61ug/g .The curve shows that the degree of incorporation of Cu and Fe into
the soft tissues of Bursa spinosa exceeds other measured metals, as well as the mean shell and
sediments concentrations. The mean BMF and TSR curves seem laterally symmetrical and also
intersects on the Fe concentration values as shown in Figure 4.7. This indicates that both the soft
tissues and the shells of Bursa spinosa incorporate Fe at quite a similar, if not the same rate.
Meanwhile, generally speaking, higher BMF values show that the shells secrete heavy metals
from the sediments better than soft tissues does from water.
4.2.5 Nerita oryzarum

Figure 4.8 Curve showing the mean tissue concentration of heavy metals for Nerita oryzarum
The heavy metal distribution patterns for the mean shell and sediment concentrations in Bursa
spinosa have similar patterns as shown in Figure 4.6. The concentration of all heavy metals in
the species and its environment are quite low but peaks at its Cu and Fe values which ranges
between 0.40 and 0.61ug/g .The curve shows that the degree of incorporation of Cu and Fe into
the soft tissues of Bursa spinosa exceeds other measured metals, as well as the mean shell and
sediments concentrations. The mean BMF and TSR curves seem laterally symmetrical and also
intersects on the Fe concentration values as shown in Figure 4.7. This indicates that both the soft
tissues and the shells of Bursa spinosa incorporate Fe at quite a similar, if not the same rate.
Meanwhile, generally speaking, higher BMF values show that the shells secrete heavy metals
from the sediments better than soft tissues does from water.
4.2.6 Cipangopaludina chinensis malleata
sediment concentration of heavy metals for Cipangopaludina chinensis malleata
Figure 4.10 Curve showing the mean bio-mineralization factor and tissue-shell ratios for heavy
metals in Cipangopaludina chinensis malleata

The heavy metal concentration and distribution in the soft tissues of Cipangopaludina chinensis
malleata varies. The mean tissue and sediment concentrations are highest for Zn at 199.33 and
124ug/g respectively as shown in Table 4.8 and Figure 4.9. For this study, despite the relatively
high values of heavy metals in the sediments, the BMF curve is almost flat, therefore, the usage
of the shells Cipangopaludina chinensis malleata as a biomonitor or environmental archive is
not recommended. Conversely, the soft tissues are useful for bio-monitoring purposes, especially
for metals such as Cu and Zn as evident in the TSR curve shown in Figure 4.10.
4.2.7 Austrocochlea constricta
Figure 4.11 Curve showing the mean tissue concentration and mean shell concentration of heavy
metals for Austrocochlea constricta

Figure 4.12 Curve showing the mean tissue-shell ratios for heavy metals in Austrocochlea
constricta
The heavy metal concentration and distribution in the soft tissues of Austrocochlea constricta
varies from one metal to the other. The mean tissue and mean shell concentrations both have
similarly shaped curves with peak recordings for Zn at 8.46 and 5.66ug/g respectively, followed
by Cu as shown in Table 4.9 and Figure 4.11. For this species, Cu has the highest TSR value as
shown in Figure 4.12, thereby indicating the preference of its soft tissues for bio-monitoring Cu
in water bodies. Conversely, the low TSR value of Zn indicates the usefulness of the shells of
Austrocochlea constricta as an environmental archive compared to its soft tissues.
Figure 4.13 Curve showing the mean tissue concentration of heavy metals for Archachatina
marginata
The heavy metal concentration and distribution in the soft tissues of Archachatina marginata
varies from one metal to the other. The mean tissue concentrations are highest in Fe, followed by
Zn and Mn respectively as shown in Figure 4.13. This indicates that the soft tissues of these
species are useful for bio-monitoring Fe, Zn and Mn pollution in water bodies.
Figure 4.14 Curve showing the mean tissue concentration of heavy metals for Nacella
magellanica
The heavy metal concentration and distribution in the soft tissues of Nacella magellanica varies
from one metal to the other. The mean tissue concentrations are highest in Zn and Cu
respectively as shown in Figure 4.14 and Table 4.11. This indicates that the soft tissues of these
species are useful for bio-monitoring Zn and Cu contamination in water bodies.

Figure 4.15 Curve showing the mean tissue concentration of heavy metals for P. caerulea
The heavy metal concentration and distribution in the soft tissues of P. caerulea varies. The
mean tissue concentrations are highest in Zn, 210.56ug/g, followed by Pb and Cu respectively as
shown in Figure 4.15 and Table 4.12. This indicates that the soft tissues of these species are
useful for bio-monitoring Zn, Pb and Cu contamination in water bodies.
Figure 4.16 Curve showing the mean tissue concentration of heavy metals for N. concinna
The heavy metal concentration and distribution in the soft tissues of N. concinna varies. The
mean tissue concentrations are highest in Zn and Cu with values of 69.9 and 27.6ug/g
respectively as shown in Figure 4.16 and Table 4.13. This indicates that the soft tissues of these
species are useful for bio-monitoring Zn and Cu contamination in water bodies
Figure 4.17 Curve showing the mean tissue concentration of heavy metals for Patinigera sp.
The heavy metal concentration and distribution in the soft tissues of Patinigera sp varies. The
respectively as shown in Figure 4.17 and Table 4.14. This indicates that among other things, the
soft tissues of these species have useful potentials for the bio-monitoring of Zn and Cu
contamination in water bodies
Figure 4.18 Curve showing the mean tissue concentration of heavy metals for P. aspera.
The heavy metal concentration and distribution in the soft tissues of P. aspera varies. The mean
tissue concentrations are highest in Zn and Cu with values of 98.93 and 8.03ug/g respectively as
shown in Figure 4.18 and Table 4.15. This indicates that among other things, the soft tissues of
these species have useful potentials for the bio-monitoring of Zn and Cu contamination in water
bodies
Figure 4.19 Curve showing the mean tissue concentration of heavy metals for Mytilus edulis
chilensis
The heavy metal concentration and distribution in the soft tissues of Mytilus edulis chilensis
varies. The mean tissue concentrations are highest in Zn and Cu with values of 124.56 and
5.14ug/g respectively as shown in Figure 4.19 and Table 4.16. This indicates that among other
things, the soft tissues of these species have useful potentials for the bio-monitoring of Zn and
Cu contamination in water bodies
Figure 4.20 Curve showing the mean tissue concentration of heavy metals for B. barbatus.
The heavy metal concentration and distribution in the soft tissues of B. barbatus varies. The
mean tissue concentrations are highest in Zn, Pb and Cu with values of 388.25, 91.9 and
10.44ug/g respectively as shown in Figure 4.20 and Table 4.17. This indicates that among other
things, the soft tissues of these species have useful potentials for the bio-monitoring of Zn, Pb
and Cu contamination in water bodies.
Figure 4.21 Curve showing the mean tissue concentration of heavy metals for N.
galloprovincialis.
The heavy metal concentration and distribution in the soft tissues of B. barbatus varies. The
respectively as shown in Figure 4.21 and Table 4.18. This indicates that among other things, the
soft tissues of these species have useful potentials for the bio-monitoring of Zn and Cu
contamination in water bodies.
sediment concentration of heavy metals for Patinigera sp.















Mya arenatia (Szefer and Szefer, 1990)





















4.3 Soft tissues and shells of gastropod and bivalves species for bio-monitoring and as
environmental archives of heavy metals, using BCF, BMF and TSR as tools.
Although, quite a number of authors have carried out scientific investigations and made attempts
to interpret measured and collated data on the heavy metal concentration in gastropods and
bivalves. However, in this study, it is suggested that the direct usage of the measured heavy
metal concentration values from several body parts of gastropods and bivalves, such as soft
tissues and shells, as reported by various authors, for the interpretation of their suitability for bio-
monitoring heavy metals and environmental archiving purposes is not enough, as it might not be
able to paint the precise and accurate picture required as compared to the usage of indices such
as the bio-concentration factors (BCF), bio-mineralization factors (BMF) and tissue-shell ratios
(TSR). In light of this, attempts were made to interpret the suitability of various species of
gastropods and bivalves from different continents and environments to bio-monitor each heavy
metal based on their calculated BCF, BMF and TSR values, as compared to the popular usage of
tissue, shell, water and sediment concentration values for interpretation. This method of
interpretation will eliminate errors or inconsistencies which might have been caused by uniform
analytical procedures. Also, it takes into consideration and assumption that these simple ratios
are not seriously affected by the environmental conditions across various localities of sampling
in comparison with the direct usage of tissue, shell, water and sediment concentration
measurements, which are greatly affected. This method makes the interpretation and implication
of heavy metal variation in gastropods and bivalves easy. Also, it indicates clearly, preferential
heavy metal incorporation across gastropod and bivalves species and within their body parts
using BCF, BMF and TSR

CHROMIUM
The mean BCF values for Cerithium scabridum is quite low (0.03) while that of Gibbula sp. is
above unity (1.48). This indicates the usefulness of the soft tissues of Gibbula sp. as
environmental biomonitor for chromium. The mean BMF values for Cipangopaludina chinensis
malleata and Mytilus galloprovincialis are 0.05 and 0.19 respectively, indicating low ability of
these species to secrete chromium from sediments into their shells. However, the mean TSR
values of 9.14 and 1.34 respectively for both species show that their tissues relatively absorb
more chromium in comparison to shells.

CADMIUM
The mean BCF values of Lanistes carinatus, Gibulla sp. and Mytilus edulis of 9.7, 1.63 and 0.21
respectively, indicates that the soft tissues of Lanistes carinatus and Gibulla sp. are potentially
useful as cadmium biomonitors in the environment. Hemifusus pugilinus, Bursa spinosa and
Lanistes carinatus have mean BMF values of 1.4, 1.37 and 0.68 respectively, thereby indicating
that the shells of Hemifusus pugilinus and Bursa spinosa will serve as good environmental
archives for cadmium contamination in the aquatic environment. Hemifusus pugilinus, Bursa
spinosa, Austrocochlea constricta, Lanistes carinatus, Nerita lineata, Neritina violacea and
Astarte borealis have mean TSR values of 0.57, 1.01, 1.22, 3.3, 0.22, 0.72, 82.4 respectively,
thereby indicating that the soft tissues of Astarte borealis are excellent biomonitors for cadmium,
followed by Lanistes carinatus, Austrocochlea constricta and Bursa spinosa respectively.

COPPER
The mean BCF values of Cerithium scabridum, Lanistes carinatus and Gibulla sp. of 0.08,
202.02, and 1.24 respectively, indicates that the soft tissues of Lanistes carinatus, in particular
makes an excellent biomonitor for copper in contaminated waters in comparison to Gibulla sp.
and Cerithium scabridum. Hemifusus pugilinus, Bursa spinosa, Cipangopaludina chinensis
malleata, Mytilus galloprovincialis and Lanistes carinatus have mean BMF values of 1.15, 1.19,
0.03 and 0.04 respectively, thereby indicating that Bursa spinosa and Hemifusus pugilinus can
incorporate copper into their shell better than the water column, thereby useful as an
environmental archive for copper in waters. Hemifusus pugilinus, Bursa spinosa,
Cipangopaludina chinensis malleata, Austrocochlea constricta, Mytilus galloprovincialis,
Lanistes carinatus, Nerita lineata, Neritina violacea, Mytilus edulis, Macoma balthica, Mya
arenatia, Cardium glaucum and Astarte borealis have mean TSR values of 0.9. 0.86, 39.13,
8.89, 10.29, 3.18, 2.98, 9.38, 4.48, 3.76, 16.97, 8.67, 11.69 respectively, thereby indicating that
of all species considered in this study, the soft tissues of Cipangopaludina chinensis malleata
have the highest effectiveness for use as copper biomonitors, followed by Mya arenatia, Astarte
borealis, Mytilus galloprovincialis, Neritina violacea, Austrocochlea constricta, Cardium
glaucum, Mytilus edulis, Macoma balthica, Lanistes carinatus, Nerita lineata, Hemifusus
pugilinus and Bursa spinosa in order of their ability to accumulate copper in their soft tissues.
NICKEL
NICKEL
The mean BCF values of Cerithium scabridum and Lanistes carinatus are 1.85 and 65.46
respectively. This indicates that the soft tissue of Lanistes carinatus is a good bioaccumulator for
nickel and can serve as a biomonitor. Cipangopaludina chinensis malleata, Mytilus
galloprovincialis and Lanistes carinatus have mean BMF values of 0.68, 0.71 and 0.39
respectively, thereby indicating that the shells of the three species are not suitable to biomonitor
nickel in water and sediments. Conversely, Cipangopaludina chinensis malleata, Mytilus
galloprovincialis, Lanistes carinatus, Nerita lineata, Neritina violacea, Mya arenatia and Astarte
borealis have mean TSR values of 0.15, 0.43, 0.37, 0.26, 0.5, 0.26 and 1.71, thereby indicating
that the soft tissue of Astarte borealis will make a good biomonitor for nickel in water and
sediments.
LEAD
The mean BCF values of Cerithium scabridum, Lanistes carinatus and Gibulla sp. are 12.74, 7.7
and 1.85 respectively. This indicates that their soft tissues could be used to biomonitor lead
contamination in the environment and that they are more effective in the same order. Hemifusus
pugilinus, Bursa spinosa, Cipangopaludina chinensis malleata, Mytilus galloprovincialis,
Lanistes carinatus and Mytilus edulis however, have mean BMF values of 1.24, 1.2, 0.01, 0.01,
0.93 and 0.00. This indicates that of these species, the shells of Hemifusus pugilinus and Bursa
spinosa are better environmental archives which can indicate lead concentration in water bodies
compared to others. For mean TSR values, Hemifusus pugilinus, Bursa spinosa,
Cipangopaludina chinensis malleata, Austrocochlea constricta, Mytilus galloprovincialis,
arenatia, Cardium glaucum and Astarte borealis have values of 0.7, 0.69, 3.07, 1.82, 9.12, 1.94,
0.26, 0.03, 2.13, 3.03, 2.79, 6.24 and 0.00 respectively. Hence, the soft tissues of Mytilus
galloprovincialis, Cardium glaucum, Cipangopaludina chinensis malleata, Macoma balthica,
Mya arenatia, Mytilus edulis, Lanistes carinatus and Austrocochlea constricta could serve as
good biomonitors for lead contamination in water bodies due to their ability to accumulate it in
their tissues.
ZINC
Lanistes carinatus, Gibulla sp. and Mytilus edulis have mean BCF values of 445.84, 1.94 and
0.00. Hence, this indicates that the soft tissues of Lanistes carinatus and Gibulla sp., especially
the former, can serve as zinc biomonitors. Hemifusus pugilinus, Bursa spinosa, Cipangopaludina
chinensis malleata, Mytilus galloprovincialis and Lanistes carinatus have mean BMF values of
1.08, 1.13, 0.04, 0.05 and 0.15 respectively. This indicates that the shells of Hemifusus pugilinus
and Bursa spinosa could serve as zinc environmental archives. For mean TSR values, Hemifusus
pugilinus, Bursa spinosa, Cipangopaludina chinensis malleata, Austrocochlea constricta,
Mytilus galloprovincialis, Lanistes carinatus, Nerita lineata, Neritina violacea, Mytilus edulis,
Macoma balthica, Mya arenatia, Cardium glaucum and Astarte borealis have values of 0.94,
0.92, 41.5, 2.26, 62.73, 3.81, 23.1, 1.91, 13.48, 29.65, 16.1, 11.08 and 1.45. As such, the soft
tissues Hemifusus pugilinus and Bursa spinosa are not suggested as favorites for zinc
biomonitoring purposes.
IRON
Lanistes carinatus have a mean BCF value of 1216.5. This indicates that the soft tissues of
Lanistes carinatus can be used as an iron biomonitor in water bodies. Hemifusus pugilinus,
Bursa spinosa and Lanistes carinatus have mean BMF values of 1.15, 0.98 and 0.04,
respectively. This indicates that the shells of Hemifusus pugilinus could serve as an
environmental archive for iron. For mean TSR values, Hemifusus pugilinus, Bursa spinosa,
arenatia, Cardium glaucum and Astarte borealis have values of 0.9, 0.97, 1.33, 0.06, 2.87, 8.56,
4.09, 6.7, 2.62 and 0.49. As such, the soft tissues Hemifusus pugilinus, Nerita lineate, Astarte
borealis and Bursa spinosa are not suggested as favorites for iron biomonitoring purposes.
MANGANESE
Lanistes carinatus have a mean BCF value of 615.22. This indicates that the soft tissues of
Lanistes carinatus can be used for biomonitoring the manganese content in water bodies.
Hemifusus pugilinus, Bursa spinosa and Lanistes carinatus have mean BMF values of 1.17, 0.98
and 0.15, respectively. This indicates that the shells of Hemifusus pugilinus could serve as an
environmental archive for manganese. For mean TSR values, Hemifusus pugilinus, Bursa
spinosa, Lanistes carinatus, Neritina violacea, Mytilus edulis, Macoma balthica, Mya arenatia,
Cardium glaucum and Astarte borealis have values of 0.96, 0.87, 3.49, 5.59, 0.78, 2.27, 5.2, 1.91
and 0.52. As such, the soft tissues Lanistes carinatus, Neritina violacea, Macoma balthica, Mya
arenatia and Cardium glaucum are suggested as favorites for manganese biomonitoring
purposes.
VANADIUM
A mean BCF value of 1.9 for Cerithium scabridum indicates that its soft tissues can be used as a
potential biomonitor for vanadium water bodies.
COBALT
The mean BCF value of 119 for Lanistes carinatus, indicates that the soft tissues of these species
are great bioaccumulators for cobalt, and as such could be used to biomonitor cobalt
contamination in water bodies. Mytilus galloprovincialis and Lanistes carinatus have mean BMF
values of 1.16 and 0.82, which indicates that the shells of Mytilus galloprovincialis are better
biomonitors and environmental archives for cobalt as compared with Lanistes carinatus. For this
study, Astarte borealis have the highest mean TSR value of 1.46, followed by Neritina violacea,
Lanistes carinatus, and Mytilus galloprovincialis with values of 1.13, 0.93 and 0.3, respectively.
This indicates that the soft tissues of Astarte borealis and Neritina violacea could be used for the
biomonitoring of cobalt in water bodies.

CHAPTER FIVE: SUMMARY, CONCLUSION AND RECOMMENDATION
Summary and Conclusion
This research work titled “Gastropods and bivalves: bio-monitors for metal contamination in the
environment” has been carried out to investigate the usefulness of the soft tissues of gastropods
and bivalves species as bio-monitors for heavy metal contamination and the usage of their shells
as environmental archives. Data were collated from various researchers who had attempted the
usage of the tissues and shells of gastropods and bivalves as heavy metal bio-monitors from
diverse environments and continents across the world. These data were subjected to certain
statistical treatment to determine the bio-mineralization factors, bio-concentration factors and
tissue-shell ratios of various species, especially where acquired data were sufficient for this
analysis, with the intent to test their effectiveness as bio-monitors by carefully examining the rate
of heavy metal uptake and juxtaposing the metal content in the various parts of these relative to
their habitat. From the BCF, BMF and TSR values of various gastropod and bivalve species, it
has been discovered through this research that the soft tissues and shells of gastropods and
bivalves are very useful and effective for the monitoring of heavy metal contamination in the
environment. As such, on the usefulness of soft tissues of gastropods and bivalves species as bio-
monitors for heavy metal contamination in the environment, this study concluded the following,
Gibbula sp, Cipangopaludina chinensis malleata and Mytilus galloprovincialis are useful for
bio-monitoring chromium in the environment. Also, Lanistes carinatus, Astarte borealis,
Austrocochlea constricta, Bursa spinosa and Gibulla sp. are useful as cadmium bio-monitors in
the environment. This study affirms that Lanistes carinatus, Cipangopaludina chinensis
malleata, Mya arenatia, Astarte borealis, Mytilus galloprovincialis, Neritina violacea,
Austrocochlea constricta, Cardium glaucum, Mytilus edulis, Macoma balthica, Lanistes

carinatus, Nerita lineata, Hemifusus pugilinus and Bursa spinosa are excellent bio-monitors for
copper in contaminated waters while the soft tissues of Lanistes carinatus and Astarte borealis
serve as good bio-monitors for nickel in water and sediments. Likewise, Cerithium scabridum,
Lanistes carinatus, Mytilus galloprovincialis, Cardium glaucum, Cipangopaludina chinensis
malleata, Macoma balthica, Mya arenatia, Mytilus edulis, Gibulla sp. and Austrocochlea
constricta could serve as good bio-monitors for lead contamination in water bodies.
This study shows that the shells of Hemifusus pugilinus and Bursa spinosa will also serve as
good environmental archives for cadmium contamination in the environment. Bursa spinosa and
Hemifusus pugilinus can incorporate copper into their shell better than the water column, thereby
useful as an environmental archive for copper in waters. In the same vein, Lanistes carinatus,
Hemifusus pugilinus, Bursa spinosa and Gibulla sp., can serve as zinc bio-monitors, while the
soft tissues of Lanistes carinatus, Hemifusus pugilinus, Nerita lineate, Astarte borealis and
Bursa spinosa are useful as an iron bio-monitor in water bodies. The result of this research
suggests that the soft tissues Lanistes carinatus, Neritina violacea, Macoma balthica, Mya
arenatia and Cardium glaucum are favorites for manganese bio-monitoring purposes, while
Cerithium scabridum can be used as a potential bio-monitor for vanadium water bodies and the
soft tissues of Lanistes carinatus, Astarte borealis, Mytilus galloprovincialis and Neritina
violacea could also be used to bio-monitor cobalt contamination in water bodies.
On the potential usage of the shells of gastropods and bivalves as environmental archives of
heavy metal contamination in the environments, this study shows that the shells of Hemifusus
pugilinus and Bursa spinosa can indicate the history of lead contamination in water bodies. Also,
the shells of Hemifusus pugilinus and Bursa spinosa could serve as zinc environmental archives.
Likewise, the shells of Hemifusus pugilinus could serve as an environmental archive for iron and
manganese, while the shells of Mytilus galloprovincialis serve as good archive for cobalt
contamination in the environment.
In conclusion, although the level of metal uptake in the tissues and shells of different species of
gastropods and bivalves in freshwater and marine environments varies across the world, and the
pattern of heavy metal uptake in the soft tissues and shells of gastropods and bivalves is not
uniform as a result of wide variations in the physico-chemical controlling parameters such as
organism type, taxonomic units, disparity in the rate of heavy metal uptake between tissues and
shells, variance in the degree of bio-accumulation of certain species, preferential incorporation of
certain elements, temperature and other environmental factors, yet the soft tissues and shells of
gastropods and bivalves are useful as bio-monitors for heavy metal contamination and as
environmental archives.
Recommendation
The usage of the soft tissues and shells of gastropods and bivalves for bio-monitoring heavy
metal contamination of the environments has the potential for further development.
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GASTROPODS AND

CHAPTER ONE: GENERAL INTRODUCTION

1.1 Background of Study

1.2 Aim and Objectives of Study

1.3 Statement of Problem

1.4 Research Questions

1.5 Significance of Study

2.1 Sources of Heavy Metals

2.3 Adverse Effects of Heavy Metal Contamination

2.4 Major Outbreaks of Toxic Poisoning Due to Heavy Metals

2.5 Previous Attempts to Monitor Heavy Metals in Environments

2.6 Common Tools for Environmental monitoring of Heavy Metals

2.7 Application of Gastropods and Bivalves as environmental Biomonitors

Gastropods and Bivalves

CHAPTER THREE: MATERIALS AND METHOD OF STUDY

3.2 Description Statistics of Datasets

3.3 Statistical Data Treatment

4.1 Results and discussion

across taxonomic units

CHAPTER FIVE: SUMMARY, CONCLUSION AND

5.1 Summary and Conclusion

CHAPTER ONE: INTRODUCTION

these micro-nutrients results in a variety of deficiency diseases or syndromes (WHO/FAO/IAEA,

contamination of drinking water sources cannot be underestimated both in developed and

(Gibson et al., 2001; Schone et al., 2007).

1.2 AIM AND OBJECTIVES OF STUDY

their shells as environmental archives.

1.3 STATEMENT OF PROBLEM

general overview or consideration which gathers all these specific studies.

1.4 RESEARCH QUESTION

The research answers the following question:

monitors in the environment?

soft tissues and shells of gastropods and bivalves?

uptake in gastropods ad bivalves?

gastropods and bivalves?

concentration in the shells and soft tissues of gastropods and bivalves?

of gastropods and bivalves?

1.5 SIGNIFICANCE OF STUDY

and archived in their shells

CHAPTER TWO: LITERATURE REVIEW

2.1.1 Geogenic Sources

secondary geogenic sources (Jyorti, 2020).

2.1.2 Anthropogenic Sources

replacement case, medications, steel fabrication, electroplating, textile, production of batteries,

wastes, etc. (Jyorti, 2020).

2.2 PERMISSIBLE LIMITS OF HEAVY METALS FOR ORGANISMS AND IN THE

as suggested by various international agencies and authorities such as USEPA (Environmental

matrices such as air, drinking water and soil (Jyorti, 2020).

Heavy USEPA WHO OSHA

in natural waters according to EPA (After Odobašić et al., 2019)

Heavy Metal Maximum Allowable Concentration (μg/mL)

Mood et al., 2021)

A - 0.5 8.2 4.1 -

C 21 (inorganic) - 210 70 21 (inorganic)

D 50 250 120 56 150

G 16 (methyl) - 63 (hexavalent) 25 210

2.3 ADVERSE EFFECTS OF HEAVY METAL CONTAMINATION

Other adverse effects include cardiovascular diseases, developmental abnormalities, neurologic

the excretory system and leads to renal cancer (Jyorti, 2020).

2.4 MAJOR OUTBREAKS OF TOXIC POISONING DUE TO HEAVY METALS

century. Some of which includes the following:

2.4.1 Minamata Syndrome:

over ten years at a cost of 48 billion yen (WEPA, 2022).

2.4.2 Hinckley Water Contamination