Abstract: environmental pollutants, including endocrine disrupting chemicals (EDCs),

Abstract:

Bisphenol A enter in aquatic environments through discharged off effluents,
principally from industrial plants, commercial areas and have great influence
on variety of aquatic biota, including fish. Evidence for changes of physiology
in fish as a result of exposure of BPA is global, with some of the most widely
reported effects on sexual development and function. In recent years, research
has shown that BPA has great influence on fresh water fishes which result in behavioral
changes of individual level and ultimately population level. This review
presents a critical assessment on reported effects of bisphenol A on behavior in
fish, mainly disturbance in reproduction behavior. However, there are many
technical and interpretation challenges to predict the role of BPA in
endocrinal disruption and there is great criticism on how behaviors under
laboratory conditions

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Introduction:

Water is fundamental entity for all living
organisms to live. A satisfactory, safe, and good water supply should be
available for every individual and species. This is a duty of water suppliers
to provide good drinking quality of water to all living beings. However,
quality of drinking water is the affected by the presence of several environmental
pollutants, including endocrine disrupting chemicals (EDCs), pharmaceuticals
and personal care products (PPCPs), and other substances (Padhye et al., 2014).

 Bisphenol
A (BPA), one of the most studied EDCs, is an aromatic compound which used all
over the world as the precursor of plastics and chemical additives (Vandenberg et al., 2010). BPA is commonly used in
the production of polycarbonate plastics (very common for transparency, heat
resistance, and mechanical properties) and epoxy resins for coating of cans of
food and beverages.

In  aquatic 
environment,  BPA, Pharmaceuticals,  pesticides 
and  other  chemicals 
with  endocrine  disrupting chemicals enter through disposed
wastewater,  agricultural run-off,  and 
groundwater  discharge,  which may 
accumulate both  in  sediments and 
in biota  including  fish  (Hu  et  al., 2005). Fishes are most vulnerable
living organism when expose to pollutants like BPA because contaminated water
is directly in contact with fish organs like gills, skin can readily absorbed
BPA due to continuous exposure with BPA. BPA can also enter in fish body
through diet and drinking (gut). (Kwong et  al., 2008. In some cases, BPA also found
in developing eggs which ultimately has influence on embryo and can retard the
development of embryo  (Daley  et 
al., 2009). Exposure of pollutants 
like BPA and other EDCs can also cause variations in behavior of fishes
in which includes  reduction the  capability 
for  avoidance from predators,  reducing/eliminating  the 
ability  to  detect 
chemical  alarm  substances released by conspecifics,
affecting schooling behavior, influencing feeding behavior, and may change
social hierarchies within a group (Scott and 
Sloman,  2004). Many studies have
been conducted to study the effect of BPA on fish physiology, normally on
features which relates to growth, development and reproduction (Hutchinson et al., 2006).

 In this paper, I present a review of the existing
literature in order to easily identify the current scope of information
available regarding effects of Bisphenol A in endocrine disruption for fresh
water fish species. This review critically analyses the information which
determine the possible effects of EDCs, on behavioral changes in fish, mainly
on behaviors related to sex and reproduction. The goal of this review is to
provide the state of the science related to role of BPA in endocrinal
disruption of fishes live in freshwater and estuarine fish, in which short-term
(i.e., physiology and behavior) and long-term effects (trans generational) are
described.

Possible
Mechanisms of Action of BPA as an Endocrine Disrupting Chemical:

The general concept is that the estrogenic
activity of BPA is initiated when BPA is attach to estrogen receptors (ERs) in fisheries.
BPA has structural similarity to thyroid hormones (THs) bcause both have 2
benzoic rings. Due to structural similarity with thyroid hormone, BPA act as a
TH antagonist or agonist which result in disturbance of the thyroid system and
ultimately disturbance of whole body functions (Jung et al., 2007). For collection of data, models of fish metamorphosis
are mainly used. By using larval stages of fish, Iwamuro et al., (2006) found that in vivo, spontaneous and TH-induced
metamorphosis is blocked by BPA, as well as in vitro tail cell culture, tail
resorption is induced by throid hormones (THS). Corticotropin-releasing factor
(CRF) -inducible release of thyroid-stimulating hormone (TSH) and
thyrotropin-releasing hormone (TRH) -inducible release of both TSH and
prolactin from the pituitary gland are also inhibited by the compound. In fury,
the release of TSH and prolactin are not regulated by estradiol. This confirms
that ER binding is not related to the release of the pituitary hormones due to
BPA. In tail cell culture, the appearance of genes related to metamorphosis is
reduced by BPA, which reinforce the hypothesis that effects of BPA are induced
by directly binding to thyroid hormone receptors rather than estrogen receptors
(ERs)(Zoeller, 2005).

BPA as Endocrine disrupting chemicals and their biological effects:

In
an organism, BPA acts via mimicking or blocking natural hormone functions. An array
of hormonal systems including estrogen, androgen, progestagen, corticosteroid
and  thyroid  signaling 
systems are affected by BPA. Sex steroid action and sexual development and reproduction
are seriously affected by BPA. Almost all aspects of reproduction, including
mediating sexual differentiation, gonadal growth, and reproductive behaviors
are controlled by sex steroid hormone (Goodhead and  Tyler, 
2009).

Examinational
efforts show that at comparatively high concentrations (up to 21 µg l?1)
of BPA in streams and rivers cause serious biological effects in fisheries.
Results of experiments show that BPA is responsible to cause feminizing effects
in vivo and to induce zona radiata proteins (ZRPs) synthesis in a diverse range
of fish species. There are few examples of fisheries which are affected at
different concentration of BPA i.e. carp 100 µg l?1; fathead minnow
160 µg l?1,cod 50 µg l?1,medaka 1000 µg l?1;
rainbow trout 500 µg l?1 Lindholst et al. 2001).. In vivo studies
have shown that many other biological processes are influenced by BPA. Androgen
and estrogen synthesis and metabolism disorders are seriously affected by
exposure of BPA. Studies have been conducted  in carp and results showed that exposure of
low concentrations of BPA (1–10 µg l?1)  results in decrease the ratio of estrogen to
androgen in the plasma, while exposure to high concentrations (1000 µg l?1)
increases estrogen to androgen ratio (Mandich et al., 2007).

Changes
which are induces in the ratio between estrogens and androgens have biological
consequences which are diverse in nature which may comprise masculinization or
feminization of organisms, and/or alterations in other processes controlled by
these hormones (including growth, bone morphogenesis, insulin signaling, neural
development, cell division and apoptosis). Different studies provide evidence
that different species are sensitive at different concentration of BPA. For
example, when Atlantic cod (Gadus morhua)
and turbot (Scophthalmus maximus) both are exposed to 59 µg BPA l?1
via the water, then cod was more vulnerable than turbot because ZRP was more quickly
induced in the cod than in turbot which can interfere with fertility (Larsen et al., 2006). Rate of metabolic
transformation of BPA is possible reason for variation in sensitivity of
different species when exposed to BPA. Supporting this argument, removal and
metabolism of BPA occur more rapidly in zebra fish (D. rerio) than in the rainbow trout (Oncorhynchus mykiss)
(Lindholst et al., 2001).

Evidence for endocrine
disruption in wild fish

On
fish evidence for endocrine disruption in both undomesticated and wild
populations is broad. Cases  of  feminized 
responses  in  fish, 
include  production  of 
female proteins  in  males 
– vitellogenin  (VTG), and  amendments in 
germ cell  development –
production of  oocytes in  the testis 
(Lange  et al.,  2011) in 
fish exposed to BPA.

In  the 
USA  reported  androgenic 
reactions  include  masculinized 
secondary  sex characters  in 
female  mosquitofish (Gambusia 
holbrooki) exposed  to BPA
(Parks et 
al., 2001),  and  androgenic 
enhancement of  secondary  sex characters in male fathead minnows (Pimephales promelas) exposed to BPA(Ankley
et al., 2003). Effects of BPA on wild
fish populations have not yet been approached, although numerous modeling analyses
have tried to report this issue

Effects of BPA (estrogens)
in fish:

Estrogenic
properties of BPA were first reported in 1936. Wide  range of 
(anti-)estrogenic effects and influences have  been 
investigated  in  a  wide-ranging  series 
of  laboratory 

 

sudies.
Zebrafish  (Danio  rerio), medaka (Oryzias 
latipes),  fathead  minnow,  
and  three-spined  stickleback 
(Gasterosteus aculeatus) are
mostly used model species fisheries which are used to investigate the impacts
of BPA (Ankley and Johnson, 2004). Reproductive organs are mostly affected by
estrogens. Estrogens can skew the sex ratio towards females, reduce or prevent
spermatogenesis and delay   maturation of
the ovaries at higher concentration of BPA(Weber et al.,  2003).

Endocrinal
disruptor chemicals (BPA) can cause increasing masculinizing effect on  males, increasing  testis 
size  and speed up  spermatogenesis. Ovulation and manufacture of
VTG or yolk in females, skew sex ratio towards males and lessening ovary size
are adverse effects of BPA in females (Seki et  al., 2005). Some of the effects of BPA could
lessen the production of offspring which are documented through controlled
laboratory studies and therefore have a population significance. Effects on reproductive
development and fertility has been revealed due to exposure of environmental
estrogens

When
endocrine-disrupting chemicals such as BPA are introduce in fisheries habitat,
the possible adverse effects of these pollutants are not only passed on to
their offspring, but also onto their offspring’s offspring, and their offspring
too. Ramji et al., (2015) selected Medaka fish for this study due to their
shorter generations, which made it the perfect candidate for the research study
at hand. Results showed a 30% decrease in the fertilization rate of fish, two generations
after exposure and  20% reduction after
three generations. If those trends sustained, the potential for declines in
overall population numbers might be expected in generations.

In
the work of Nash et al. (2004) it was shown that exposure to BPA (5 and 0.5
ng/L) had no chief effects on reproductive production, growth, or fertilization
in the F0 generation of fishes. However, when the interaction was continued
into the F1, their breeding was intensely affected and the population failed
completely due to reduced sperm quality /infertility in the  males. 
Interestingly the sterile males still showed typical male spawning
behavior. These  consequences were
confirmed  on a  larger scale when  a lake in 
Canada dosed  with  4-6  ng/L  over 
a  period  of 
3  years  caused 
in the  failure of  the fathead 
minnow  population,  which 
then  consequently  recovered 
two  years  after cessation of dosing (Kidd et al., 2007). When  addressing 
population  level  effects 
of BPA,  however,
extrapolating  between  laboratory 
conclusions and  effects  in 
the  wild  is generally 
more difficult. Additionally, wild populations are normally exposed to BPA
with  diverse  means    

of
action,  rather  than  a  single chemical exposure, as  occurs in most laboratory  studies.

Reproductive and
developmental toxicity of BPA:

·        
Male
reproductive effects

There
is abundant qualitative evidence of BPA to cause toxic effects on reproductive
and developmental toxicity to aquatic organisms. Environmental toxicology of
Bisphenol A (BPA) was reviewed by Crain et
al. (2007), who conclude that BPA can cause disruption of endocrine system
of a diversity of species at environmentally relevant concentrations of 21 µg/L
or less.  Reported male reproductive
effects include:  apotosis of testicular
cells in swordtail freshwater fish, inhibition of gonadal growth and
spermatogenesis in fathead minnows (Sohoni et
al., 2001), reduced sperm density & motility in brown trout, decline of
testosterone and 11-ketotestosterone in turbot (Labadie and Budzinski, 2006),
and introduction of an intersex condition known as ?testis–ova? in medaka
(Metcalfe et al., 2001). Additionally, when BPA exposed to male medaka at
concentration and placed with fertile females, then as a result, reduced number
of eggs and hatchlings were observed; When BPA concentrations of 0.3, 1 and 3
µmol/L were introduce in fresh water fisheries habitat, then there was no
significant impacts were observed (Shioda and Wakabayashi, 2000).. 

·        
Female
reproductive effects:

 Different impacts of exposure of BPA on
different species of female fresh water fisheries were reported which
include:  reduction of gonadal growth and
egg production in fathead minnows (Sohoni et al., 2001), reduced hatchability
of in flathead minnow larvae, delay in, or complete stoppage of ovulation in
brown trout (Lahnsteiner et al.,
2005), less number of eggs and hatchlings in medaka (Shioda and Wakabayashi,
2000), introduction of Atlantic salmon eggshell zona radiata protein and
increased choriogenin mRNA expression in medaka (Tyl et al., 2002). When BPA expose for 3 weeks at concentration of 59
µg/L, it will result in promotion of estrone level in turbot (Labadie and
Budzinski, 2006).  Both morphological and
histological effects on salmon yolk-sac fry were observed at high concentration
of BPA. At three concentrations (10, 100 and 1000 µg/L) of BPA,variations were
observed in behaviour, morphology and histological structure which includes
fluid accumulation (oedema) in the yolk sac and haemorrhages in the front part
of the yolk sac and in the head around the gill arches at 1000 µg/L (Honkanen et al., 2004). In medeka, at 200 µg/L of
BPA, embryo lesions and deformities have been observed. BPA also have effects
on the offsprings which includes embryo lesions and deformities at 200 µg/L,
and yolk-sac hemorrhages and edema at 1000 µg/L (Honkanen et al., 2004).  

Dominance of Female
fisheries:

Comprehensive
information on some 25,000 fish from approximately 25 different populations was
gathered from Dutch database on freshwater bream populations. It was assumed
that the normal sex ratio should be equivalent, examination of these population
were conducted and results showed that 11 of them had considerably more females
than males. In most cases, between 60 and 65% of the fish were female, but in
one case, more than 70% of the fish were female. Significant majority of males
were not observed in any case. (Oehlmann et al,
2000).Sex
ratio data on fish populations can affect by many factors but introduction to
environmental BPA could be one interpretation of these data. Obviously, cause
and effect can never display by this type of investigation, but it does at
least increase the possibility of the influences of endocrine disruption at the
population level but the question of toxic impacts of estrogenic emissions on all
fish populations is one of the most important that still needs to be answered

Overview on the effect
of BPA on reproductive behaviors in fish         

On
fresh water fisheries, Many laboratory studies have been conducted which have
shown effects of BPA on reproductive behavior in individuals, with mainly focus
on males to show the impact of BPA. The adverse impacts of BPA on male fresh
water fisheries include disruption of nest building in adult male, delayed
onset of nest building or reduced care for the nest have all been reported. In
sand gobies exposure of adult fish to 4 ng /L 
was  shown  Reduction in  ability of 
males  to  gain 
and keep  a  nest 
and reduced their display of sexual behaviors was observed in sand
gobies when exposed at high concentration of BPA (Saaristo et al., 2009). Similarly, reduced care for the spawning site was
observed in adult male fathead minnows when exposed to higher concentration at
20 ng/L of BPA (Salierno and Kane, 2009). Similarly, diminished courting
response towards males and had lower reproductive success in females was
observed when exposed to BPA(at 9.86 ng/L) than unexposed females.

Critical
analysis:                                                  

Overall,
from available data in fresh water fisheries which have been collected from
experiments, there is agreement on the fact that BPA is a chemical which cause
toxic hazards for the ecosystem. In many cases, BPA cause such toxic effects when
its concentration exceed the optimum range in environment. The impacts of life-long
animal exposure to BPA cannot account in laboratory studies, since fish species
are continuously exposed of BPA and BPA continuously released in large amounts
in habitat of fresh water fisheries. Thus, an underestimation of the effects of
BPA in laboratory experiments is possible, additionally considering that
wildlife species may be exposed to higher BPA concentrations in matrices
(leachates, plants effluents, river, and marine sediments). Differences in
behavior, including boldness, shoaling, startling response, or anxiety, do
occur between different strains of laboratory zebrafish and zebrafish of
different origins and between different wild populations.                          

Some
of behavioral changes are not always easily measured, nor can then be
attributed to specific BPA or even modes of action. BPA. Not only sexual
behaviors are affected by BPA but non-sexual behaviors are also affected by BPA. When experiments are performed to understand
the effects of single concentration of BPA on behavior in wildfish, then wild
fish may experience multiple chemical exposure events at a same time which may
increase the complexity for interpreting behavior responses.

To
study the  effects  of  BPA  on 
fish behavior, one  of  the 
greatest  challenges is  translating 
them to  the  population 
level.  Much of this depends on
the significance of the behavior trait to successful reproduction. Clearly,male
female  interactions is prevented or
reduced due to exposure of BPA in 
the  spawning  process 
and  this occurs  for  the  whole population,  as a result, population  becomes 
extinct, even  if  the individuals are capable of producing
viable gametes.

Most
of the information fish has come from laboratory studies, on a very limited
number of fish species which describe the effects of BPA on sexual behavior in
fresh water fisheries. Furthermore, most of these studies have been done on laboratory
strains in which population maintained in captivity for many generations which
definitely are not true representatives of wild life fisheries sample. In general,
lower tolerance and phenotypic variability have been observed in both individuals
and populations with lower genetic diversity. 
.

Our
current understanding of the role of BPA in behavioral changes in reproduction
and population maintenance is still very limited and very little  work 
has  been conducted  which show the link  between genetic  diversity and responses  in  behavior  when there is exposed of BPA in  either 
laboratory  or  wild 
populations. So. Arguably a lot of fundamental research work is required
to obtain a more detailed understanding of fish sexual behaviors and
implications for alterations in these behaviors before they can be applied into
a risk assessment framework, or into predictive population modeling.

 

 

 

 

 

 

 

Conclusion:

In
conclusion, the collective findings in this review indicate that BPA can affect
sexual behaviors with reproductive consequences for fresh water fisheries and
potentially fish populations. The different studies which have been conducted on
very  limited  number 
of  species  of  fish
and results showed changes in  behavioral
phenotypes of fresh water fisheries  are  not
necessarily  specific to  BPA. Future efforts should done to increase an
understanding of role of BPA as endocrinal disruptor which threaten fresh water
fish population as well as species.

Recommendations:

Ø  Develop
a full toxicological assessment on BPA to determine an acceptable freshwater
exposure level.

Ø  Identify
which fresh water species are most at risk to environmental BPA levels.

Ø  Perform
more studies in the natural environment to evaluate real concentrations and
long-term exposures.

Ø  Investigate
the relative importance of different exposure pathway to BPA (digestive tract
and respiratory surfaces) for wildlife.

Ø  Evaluate
the bioaccumulation potential of BPA, especially in edible species.