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Environ Monit Assess (2015) 187:768

DOI 10.1007/s10661-015-4937-0

Bioaccumulation of heavy metals in Mbaa River


and the impact on aquatic ecosystem
M. N. O. Ajima & P. C. Nnodi & O. A. Ogo &
G. S. Adaka & D. I. Osuigwe & D. C. Njoku

Received: 4 May 2015 / Accepted: 20 October 2015


# Springer International Publishing Switzerland 2015

Abstract The bioaccumulation and toxic effects of consumption. The study also reveals the use of fish as
heavy metals have caused ecological damage to aquatic bioindicator of aquatic environment.
ecosystem. In this study, concentration of heavy metals
including zinc, lead, cadmium, iron, and copper were Keywords Accumulation . Fish . Heavy metals . Mbaa
determined in the sediment and water as well as in the River . Pollution
muscle, gill, and intestine of two fish species
(Pelmatochromis guentheri and Pelmatochromis
pulcher) of Mbaa River in Southeastern Nigeria. Sam-
Introduction
ples were collected at three different spots from the river,
and the level of heavy metals specified above were
Contamination of aquatic environment by heavy metals
determined by atomic absorption spectroscopy (AAS)
poses a risk to aquatic lives and is of great concern to
after a modified wet digestion process. The results indi-
many researchers, hence the need for considerable at-
cated that sediment had the highest concentration of the
tention and concerted efforts at both local and interna-
heavy metals investigated while water had the lowest
tional levels. The term Bheavy metal^ refers to any
concentration. Fish tissues showed appreciable bioaccu-
metallic element which is relatively of high density
mulation of these metals as evidenced by a higher con-
and toxic or poisonous even at low concentration
centration profile when compared with that of water.
(Lenntech 2004).The consequence of heavy metal pol-
Furthermore, the concentration of these heavy metals
lution is not only a threat to fish and other aquatic lives
in water and their bioconcentration factor in the fish
but also of significant health risks to consumers
were above the recommended limit by WHO and FEPA,
(Alhashemi et al. 2012; Yi et al. 2011). Heavy metals
indicating that Mbaa River along Inyishi may not be
when ingested in excess amounts or allowed to accu-
suitable for drinking nor the fish safe for human
mulate above tolerable limits can lead to random bind-
ing with cellular biomolecules such as enzymes and
other proteins to form complexes which may compro-
M. N. O. Ajima (*) : P. C. Nnodi : G. S. Adaka :
mise their structure and/or function (Duruibe et al.
D. I. Osuigwe : D. C. Njoku 2007). Aquatic environment may be contaminated with
Department of Fisheries and Aquaculture Technology, Federal many heavy metals from different natural and anthropo-
University of Technology, Owerri, Nigeria genic sources, including industrial or domestic waste
e-mail: malajimo@gmail.com water, application of pesticides and inorganic fertilizers,
O. A. Ogo storm runoff, leaching from landfills, shipping and har-
Department of Biochemistry, College of Health Sciences, Benue bor activities, as well as geological weathering of the
State University, Makurdi, Nigeria earth crust and atmospheric deposition. Studies have
768 Page 2 of 9 Environ Monit Assess (2015) 187:768

shown that some of these metals accumulate in tissues of potential public health risks that may be associated with
aquatic animals at concentrations that can be considered consuming fishes obtained from Mbaa River.
as indicators of public health concern both to animals
directly and humans upon consumption of aquatic foods
(Ashraf 2005; Yilmaz 2009; Montalvo et al. 2014;
Materials and methods
Farombi et al. 2007; Abdel-Baki et al. 2011).
Fish is one of the reliable indicative factors in fresh-
Study area
water systems and accumulation levels in fish can be
used for the estimation of trace metal pollution
Mbaa River has its source at Ugiri community in Isiala
(Kalyoncu et al. 2012). Reports on the effects of distri-
Mbaino Local Government Area of Imo State from
bution and accumulation of heavy metals at high levels
where it flows into Oramiriukwa River and to Inyishi
in various organs of fish and water bodies are well
(the study area is shown Fig. 1). Inyishi lies between
documented (Yıldırım et al. 2009; Benzer et al. 2013;
longitudes 7° 11′ E and 7° 12′ E of Greenwich and
Stancheva et al. 2013; Javed and Usmani 2014; Pulatsü
between latitudes 5° 34′ N and 5° 38′ N of the equator.
and Topçu 2015).
The vegetation is rain forest and farming is the predom-
In Nigeria, toxicity of heavy metals to fish that em-
inant occupation of inhabitant of this area, supplement-
anates from industrial discharges of untreated wastes has
ed by fishing. The area serves as a depository site for
been reported. Alinor and Obiji (2010) noted the con-
effluents and other pollutants from domestic and indus-
tamination of Nworie River with heavy metals such as
trial sources such as aluminum extrusion industries lo-
Pb, Fe, Cd, Mn, Hg, Cu, and Zn and suggested that this
cated few meters away from Mbaa River. Fishing is
could be transferred to man upon consumption. Farombi
carried out at different sites in the river, while the water
et al. (2007) reported accumulation of heavy metals in
is used for drinking and other domestic purposes by the
some vital organs of Clarias gariepinus as well as
adjoining communities.
aquatic environmental stress using antioxidant enzyme
system and malondialdehyde formation as surrogate
biomarkers of aquatic pollution in African catfish of Collection of samples
Ogun River in Nigeria.
Mbaa River, located in Imo State, Southeastern Ni- Water sample was obtained below the water surface of
geria, is extensively contaminated with untreated efflu- the river by using 1-l acid-leached polythene bottles at
ents from aluminum extrusion industries located at close three different points in each of the sampling stations.
proximity to the river. This problem is compounded by The rate of 0.5 l of the water samples were collected at
the fact that many other surrounding rivers which have each sampling station. The samples were acidified with
been reportedly contaminated flow into Mbaa River, 10 % HNO3, placed in an ice bath, and taken to the
thus increasing the risk of drinking water or consuming laboratory. The samples were then filtered through a
fish from this source. There have been growing interests 0.45-μm micropore membrane filter and kept at 4 °C
in assessing levels of heavy metals in aquatic environ- for analysis.
ments in general and of fishes in particular. Such inter- Sediment samples were collected at three different
ests are aimed at ensuring the safety of food supply and points in each of the three sampling stations using Van
to minimize the potential hazardous effect to human Veen Grab Sampler. These were then dried, ground to
health exposed to such contaminated fish and drinking fine powder, and stored at −20 °C in labeled polythene
polluted water. bags until required for analysis.
Pelmatochromis guentheri and Pelmatochromis A total of 18 fish specimens of P. guentheri and P.
pulcher are freshwater fishes of the Cichlid family that pulcher (mean weight 35 ± 0.05 g) were caught from the
are of great commercial importance not only because of three sampling stations of the river through the services
their nutritive value but also their use as aquarium fish of a hired fisherman. The fish specimens were put into
species. The present study was therefore designed to an ice box and transported to the laboratory. The fish
determine the accumulation of zinc, lead, cadmium, samples were washed with distilled water, sealed in
iron, and copper in water, sediment, and in the muscle, polyethylene bags, and kept in a freezer until use for
gill and intestine of the fish species and to assess the analysis.
Environ Monit Assess (2015) 187:768 Page 3 of 9 768

Fig. 1 Map showing Mbaa River (source: Google)

Determination of heavy metals in the samples cupboard to cool for 20 h, followed by total dis-
lodgement of the metals from the samples and,
Heavy metals (Pb, Zn, Cu, Fe, and Cd) were determined thereafter, filtered through Whatman filter paper.
in the water samples using atomic absorption spectro- The digested portion was diluted to a final volume
photometer (AAS) (Unicam 919, Analytical Technolo- of 50 ml with de-ionized water. Determination of the
gy Inc., Cambridge, UK). Sediment samples were elements in the fish parts was carried out using
weighed and placed into the digestion bombs with AAS. The results were expressed as micrograms
10 ml of HNO3/HCl (1:3 v/v) and digested in a micro- per gram wet weight.
wave digestion system. Bioconcentration factor (BCF) was determined ac-
Prior to determination of metal content in the fish cording to the methods of Lau et al. (1998) using the
gills, muscle, and intestine, the samples were homog- following formula:
enized and digested with 0.1 N HCl following the
methods of Manutsewee et al. (2007). In the proce-
dure, wet digestion process with different concentra-
BCFfish ¼ C fish =C water
tions and volumes of acids were used. One gram of
each homogenate (gill, muscle, and intestine) was
taken and placed into a digestion mixture containing
high purity HNO3, HCl (10 M) and H2O2 (35 %) in where Cfish is the metal concentration in fish in milli-
the ratio of 3:1:2. The samples were heated at grams per kilogram, Cwater is the metal concentration in
130 °C until a clear solution indicating complete water in milligrams per liter, and BCF fish is the
dissolution was obtained. This was left in the fume bioconcentration factor for the organism (fish).
768 Page 4 of 9 Environ Monit Assess (2015) 187:768

Statistical analysis source of solubilization into water depending on the


physicochemical parameters and the uptake by benthic
Data obtained were analyzed using SPSS statistical organisms (Ogoyi et al. 2011). Sediments are important
software version 20.0 (SPSS Inc. Chicago, IL, USA). reservoir for various pollutants such as pesticides and
Differences in test concentrations and control were sub- heavy metals and also play a significant role in the
jected to one-way analysis of variance (ANOVA) remobilization of contaminants in aquatic environment
followed by Duncan’s multiple range tests to determine under favorable conditions (Rashed 2001). Similarly,
level of significance at 5 % probability level. The results sediments have been reported as a major depository of
were expressed as mean ± standard error. heavy metals holding more than 99 % of the total
amount of metal present in the aquatic system (Ozturk
et al. 2009). The observation presented in this study that
sediments accumulated more heavy metals than the
Results and discussion water and fish samples is in consonance with other
documented studies (Adejare et al. 2011; Ambedkar
Heavy metal concentration in sediment and water and Muniyan 2012; Edward et al. 2013).
The concentration of Fe, Cu, Cd, and Pb in water as
The results of heavy metal concentration in the sediment indicated in our study is higher than those reported by
and water samples are presented in Table 1. It was Mohamed and Osman (2014) in White Nile Sudan and
observed that sediment contained the highest concentra- Dusukcan et al. (2014) in Karakaya Dam Lake in Tur-
tion of Fe (56.14 ± 1.23 mg/kg) followed by water key but lower than the report of (Odoemelam et al.
(5.68 ± 0.23 mg/l). The mean concentration of Pb in 2014) in both water and sediment from Cross River at
the sediment was 8.23 ± 0.23 mg/kg while that in the Afikpo, Nigeria. Comparatively, the concentration of
water samples was 2.08 ± 0.02 mg/kg. Zinc had mean heavy metals found in water and sediment samples in
concentration of 3.18 ± 0.12 mg/kg in the sediment and this study was higher than the recommended
0.65 ± 0.01 mg/l in the water sample. The mean con- permissible levels prescribed by regulatory bodies
centrations of Cd and Cu in the sediment and water such as WHO (2003) and FEPA (2003), thus predispos-
samples were 1.09 ± 0.90 and 5.64 ± 0.04 mg/kg and ing aquatic lives of Mbaa River to toxicity.
0.44 ± 0.02 and 1.06 ± mg/l, respectively. Although the The result of assessment of heavy metal content of
concentration of all metals analyzed was found to be P. guentheri and P. pulcher as presented in (Table 1)
higher in sediment compared with water, Cd was re- showed that the concentrations of Fe
corded as having the lowest mean concentration in both (17.19 ± 1.01 mg/kg) and Pb (5.40 ± 0.21 mg/kg) were
sediment and water samples. The order of heavy metal higher in P. pulcher while Cd had the lowest concentra-
concentration in sediment and water sample followed tion of 0.59 ± 0.02 mg/kg. A similar pattern was ob-
the same pattern as Fe > Pb > Cu > Zn > Cd. served in P. guentheri. However, the mean concentra-
The amount of metal present in sediments is indica- tions of Pb and Fe were higher in P. pulcher compared
tive of the degree of pollution and could serve as a with P. guentheri, while there were higher concentra-
tions of Zn and Cu in P. guentheri. Statistical analysis
showed that there was no significant difference
Table 1 Concentration of heavy metals in sediment, water, and
fish (P. guentheri and P. pulcher) samples of Mbaa River (p > 0.05) in mean concentration of the various heavy
metals in the fish species studied. The heavy metal
Heavy Sediment Water (mg/ P. pulcher P. guentheri concentration in the study area vary according to the
metal (mg/kg) l) (mg/kg) (mg/kg)
rank profile of sediment > fish > water. The concentra-
Pb 8.23 ± 0.23 2.08 ± 0.02 5.40 ± 0.21 3.57 ± 0.24
tion of metals in the fish species studied may be attrib-
uted to the feeding habit of the species, which are
Zn 3.18 ± 0.12 0.65 ± 0.01 2.21 ± 0.34 2.24 ± 0.08
regarded as bottom feeders, thus are exposed to more
Cd 1.09 ± 0.09 0.44 ± 0.02 0.59 ± 0.02 0.30 ± 0.01
of these elements. It is possible that the fishes consumed
Cu 5.64 ± 0.04 1.06 ± 0.04 2.61 ± 0.23 3.65 ± 0.15
food which was mixed with the metals in the bottom
Fe 56.14 ± 1.23 5.68 ± 0.23 17.19 ± 1.01 14.68 ± 1.03
sediment, thereby increasing the concentration of the
Data are presented as mean ± SE metals in their body. The higher concentration of metals
Environ Monit Assess (2015) 187:768 Page 5 of 9 768

in P. pulcher may be attributed to the fact that P. pulcher 2005).The differences in the level of accumulation of
consumed more of the sediment in the process of feed- metals in the different organs studied may not be un-
ing than the P. guentheri. This assertion is supported by connected with the differences in the physiological roles
the observation that the concentrations of metal in fish of each organ as alluded to by (Karuppasamy 2004).
tissues is dependent on feeding behavior and may be Our findings are consistent with those of Edward et al.
derived from metal content in benthic organisms living (2013) and Nwani et al. (2010) who reported the highest
in the polluted sediment (Ben Salem et al. 2014). accumulation of heavy metals in gill of the fish species
at Afikpo and Odo-Ayo Rivers both in Nigeria, respec-
Heavy metal concentration in fish tissues tively. Also, Stancheva et al. (2013) and Ben Salem et al.
(2014) reported similar findings in Bulgaria Black Sea
The two fish species studied were found to have accumu- Coast and in draining system pond in France. In
lated heavy metals at varying degrees in their organs addition, Mohamed and Osman (2014) documented
(muscle, gill, and intestine). It is known that essential higher concentration of heavy metal in White Nile.
metals such as Fe, Cu, and Zn and non-essential metals However, these findings appear to differ from the re-
including Cd and Pb are toxic even in trace amounts and ports of Olaifa et al. (2004) who documented lower
have been reported to be bioaccumulated in both fish concentration of heavy metals in the gills and bones
species (Fernandes et al. 2008). The results of the levels compared to muscles and intestines of C. gariepinus in
of concentration of heavy metals in the muscle, gill, and lake and fish farm in Ibadan, Nigeria.
intestine of P. guentheri and P. pulcher as presented in Iron, an important element in human diet, is involved
(Table 2) showed that Fe was found to have the highest in the biosynthesis of hemoglobin in the red blood
concentration of the heavy metals in the tissues of both corpuscles and as it plays a significant role in metabolic
fish species studied. The highest concentration of the processes being a component of many enzymes (Ed-
heavy metals was recorded in the gill while the least was ward et al. 2013). High intake of Fe, however, can cause
recorded in the muscle. The gill tissues play an important excess Fe to be stored in the organs, which may result in
role in metal ion regulation and nitrogenous wastes excre- iron overload (Stancheva et al. 2014). Although the
tion which signifies a key role for these tissues at the concentration of Fe found in Mbaa River is lower than
interface with the environment (Karthikeyan et al. 2007). that of Cross River at Afikpo, Nigeria (Odoemelam et al.
The higher accumulation of the heavy metal in the gill 2014), the mean value in the fish parts far exceeded the
may be attributed to the fact that gills are in direct contact WHO (2003) and FEPA (2003) recommended limits of
with the contaminated water allowing easy penetration of 0.5 mg/kg in fish foods (Table 3).
these metals through its thin epithelium. This position is The concentration of Pb recorded in this research is
supported by previous studies that identified gill as also higher in the gill of the fish species compared to
possessing the thinnest epithelium, which facilitates its other tissues. Statistical analysis showed that there was
respiratory and filtration functions (Bebianno et al. 2004; no significant difference (p > 0.05) in the mean values of
Oluyemi et al. 2008). Accumulation of metals in different Pb and Cd in the tissues. However, there was a signif-
fish species depends on the bioavailable metal concentra- icant difference (p < 0.05) between the mean concentra-
tion in the abiotic components of their habitats, their tion of Zn in the muscle and gill; Cu in the muscle, gill,
feeding habits, ecological needs, metabolism, age, and and intestine; and Fe between the muscle and intestine.
size of the fish (Marcovecchio 2004). The relatively lower The order of the concentration of heavy metals in the
concentration of heavy metals recorded in the muscle tissues was gill > intestine > muscle.
compared to the gills and gut might suggest the transfer Lead is one of the most ubiquitous and useful metal
of these metals from the gill to gut, liver, and kidneys known to humans and it is detectable in all phases of the
during metabolic processes. Madhusadan et al. (2003) inert environment and in biological systems (Castro-
noted that under metal-induced stress, the metal burden González and Méndez-Armenta 2008). Moreover,
is shifted to these organs where they could easily be lead-induced changes in the histological structure of
sequestered or excreted. gills and kidneys (Palaniappan et al. 2008) have been
Muscles are not active tissue regarding bioaccumu- reported to cause neuropsychological and functional
lation when compared to the gills and liver (Visnjic- decline in humans (Mason et al. 2014). The concentra-
Jeftic et al. 2010; Shukla et al. 2007; Bajc et al. tion of lead recorded in the fish species in this study
768 Page 6 of 9 Environ Monit Assess (2015) 187:768

Table 2 Concentration (μg/g wet wt.) of heavy metals in the muscle, gill, and intestine of fish species of Mbaa River

Fish Tissue Pb Zn Cd Cu Fe

P. guentheri Muscle 1.02 ± 0.09a 0.28 ± 0.08ab 0.05 ± 0.01c 0.30 ± 0.10ab 4.56 ± 1.16b
b b a c
Gill 1.45 ± 0.13 1.0.29 ± 0.38 0.16 ± 0.01 2.07 ± 0.28 5.10 ± 0.38d
b c a b
Intestine 1.10 ± 0.33 0.67 ± 0.11 0.09 ± 0.01 1.28 ± 0.65 5.02 ± 0.81d
a b b b
P. pulcher Muscle 1.48 ± 0.53 0.49 ± 0.14 0.28 ± 0.19 0.34 ± 0.14 4.41 ± 0.20c
Gill 2.08 ± 0.27c 0.99 ± 0.17b 0.18 ± 0.01a 1.50 ± 0.44c 6.06 ± 0.42d
c b a b
Intestine 1.84 ± 0.33 0.73 ± 0.08 0.13 ± 0.02 0.76 ± 0.12 6.72 ± 0.44d

Data (n = 36) are presented as mean ± SE. Values with different superscript across the rows differ significantly (p < 0.05) at 5 % probability
level

exceeded WHO (2003) and FEPA (2003) recom- whereas the highest mean values were found in gills.
mended limits of 2.0 mg/kg indicating that the fish Cadmium is a non-essential metal that is potentially
are unsafe for human consumption. However, our toxic to most freshwater organisms including fish as
result is higher than the reports of Dusukcan et al. well as wildlife. Studies have shown that cadmium
(2014) in Karakaya Dam Lake of Turkey but low- poses a serious ecological threat and contributes greatly
er than the report of Khan et al. (2014) in fish to toxicity response rate, being more toxic than arsenic
species of river Buriganga in Bangladesh. and lead (Min et al. 2013).The concentration of Cd in
Although Cu is an essential element that is carefully this study is, however, lower than the maximum permis-
regulated by physiological mechanisms in most organ- sible value recommended by WHO (2003).
isms (Erdoĝrul and Ates 2006), when accumulated to Zinc is involved in many cellular processes either as
higher amounts could pose health hazards to both structural component of regulatory proteins or catalytic
animals and humans (Bashir et al. 2013).The maximum part of enzymes. However, when accumulated in high
average concentration of Cu in the present study is lower amounts can be deleterious to all living organisms in-
than that recorded in gills of Channa punctatus from the cluding fish. For instance, Zn can be toxic above the
canal water at Kasimpur, India, as reported by Javed limit of 50 μg/g in the muscle (Ardakani and Jafari
et al. (2015) and the maximum acceptable limit 2014). The maximum mean concentration of Zn in the
recommended by WHO (2003) and FEPA (2003), fish species in this study was below that reported in
which is 3.0 mg/kg. This result implies that consump- Arius thalassinus and Johnius belangeri species from
tion of the fish with Cu bioaccumulation from the study the coastal waters of Kapa and Mersing, Malaysia, by
area may not pose any health hazards to consumers. Bashir et al. (2013). The concentration of zinc here also
The occupational levels of Cd exposure prove to be a falls below the maximum acceptable limit in fish rec-
risk factor for chronic lung disease and testicular degen- ommended by FAO (1983) indicating that consumption
eration (Stancheva et al. 2013). In the present study, the of fish from Mbaa River may not predispose consumers
lowest concentration of Cd was recorded in the muscle, to zinc toxicity.

Table 3 Recommended levels


for heavy metals in water, sedi- Heavy metals Water Sediment Fish
ment, and fish Maximum permissible Maximum permissible Maximum permissible
limit WHO/FEPA limit WHO/FEPA limit WHO/FEPA
(mg/l) (mg/kg) (mg/kg)

Fe 0.300 0.030 0.5


Zn 3.00 0.0123 30 (FAO 1983)
Pb 0.010 0.040 2.0
Cu 1.000 0.025 3.0
Cd 0.003 0.006 0.5
Source: Edward et al. (2013)
Environ Monit Assess (2015) 187:768 Page 7 of 9 768

Table 4 Bioconcentration factor (BCF) of heavy metals in the muscle, gill, and intestine of fish species of Mbaa River

Fish Tissue Pb Zn Cd Cu Fe

P. guentheri Muscle 0.49 ± 0.01a 0.43 ± 0.05a 0.11 ± 0.03b 0.28 ± 0.01b 0.80 ± 0.06c
a b c b
Gill 0.70 ± 0.02 1.98 ± 0.09 0.36 ± 0.01 1.95 ± 0.07 0.89 ± 0.02a
a b c b
Intestine 0.52 ± 0.02 1.03 ± 0.04 0.20 ± 0.01 1.21 ± 0.06 0.88 ± 0.06d
a a a b
P. pulcher Muscle 0.71 ± 0.06 0.75 ± 0.03 0.64 ± 0.03 0.32 ± 0.01 0.78 ± 0.03a
Gill 1.00 ± 0.03a 1.52 ± 0.08b 0.41 ± 0.04c 1.42 ± 0.08b 1.07 ± 0.05a
a b c a
Intestine 0.84 ± 0.04 1.12 ± 0.04 0.30 ± 0.04 0.72 ± 0.05 1.18 ± 0.09b

Data are presented as mean ± SE. Values with different superscript across the rows differ significantly (p < 0.05) at 5 % probability level

Bioconcentration factor of metals in fish tissues heavy metal content in the water, sediments, and fish
from Mbaa River. It was observed that the concentrations
The bioconcentration (BCF) in the gill, muscle, and intes- of some of the heavy metals recorded in the water and
tine of the fish species studied (Table 4.) showed that there fish samples are higher than the recommended standards.
is appreciable accumulation of the different heavy metals Consequently, the use of the water therein or consump-
in different tissues, which may be indicative of the regula- tion of fish from this source may not be without adverse
tory and physiological potentials of each organ of the fish. effects to users. In addition, the data could be used to
However, there were higher BCF of the heavy metals in assess and monitor health risk associated with the con-
the gills compared to muscles and intestine. The BCF is in sumption of the fish and water from the river.
the order gill > intestine > muscle. The high concentration
of the metals in the gills could be attributed to element Acknowledgments The authors are grateful to the staff of the
complexion with the mucus coverings in the gills which Department of Physical and Chemical Oceanography, Nigerian
cannot be completely eliminated from the gill lamellae Institute for Oceanography and Marine Research, Victoria Island,
Lagos, Nigeria, for their technical assistance in the course of the
before analysis (Khalil and Faragallah 2008). The BCF
study.
of Zn was the highest while the lowest was recorded for Cd
in both fish species. The BCF followed the ranking order
of gill > intestine > muscle. The rank profile of the metals
in the tissue were (Zn > Cu > Fe > Pb > Cd) in the gill and References
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