The European Zoological Journal
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Comparative study of haematology of two teleost
fish (Mugil cephalus and Carassius auratus) from
different environments and feeding habits
V. Parrino, T. Cappello, G. Costa, C. Cannavà, M. Sanfilippo, F. Fazio & S.
Fasulo
To cite this article: V. Parrino, T. Cappello, G. Costa, C. Cannavà, M. Sanfilippo, F. Fazio & S.
Fasulo (2018) Comparative study of haematology of two teleost fish (Mugil�cephalus and Carassius
auratus) from different environments and feeding habits, The European Zoological Journal, 85:1,
193-199, DOI: 10.1080/24750263.2018.1460694
To link to this article: https://doi.org/10.1080/24750263.2018.1460694
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The European Zoological Journal, 2018, 193–199
Vol. 85, No. 1, https://doi.org/10.1080/24750263.2018.1460694
Comparative study of haematology of two teleost fish (Mugil cephalus
and Carassius auratus) from different environments and feeding habits
V. PARRINO1#*, T. CAPPELLO1#*, G. COSTA2, C. CANNAVÀ2, M. SANFILIPPO1,3,
F. FAZIO3, & S. FASULO1
1
Department of Chemical, Biological, Pharmaceutical and Environmental Sciences, University of Messina, Messina, Italy,
Department of Human Pathology in Adult and Developmental Age, University of Messina, Messina, Italy, and 3Department
of Veterinary Sciences, University of Messina, Messina, Italy
2
(Received 2 November 2017; accepted 29 March 2018)
Abstract
Haematological parameters are valuable indicators of fish health status. This study is aimed to provide baseline data of the
blood profile of two teleost fish species living in different environments and with divergent feeding behaviour, namely the
flathead grey mullet Mugil cephalus Linnaeus, 1758, a marine herbivorous fish, and the goldfish Carassius auratus (Linnaeus,
1758), a freshwater omnivorous fish. Using an automated system coupled with flow cytometry and light microscopy,
significant variations were found between M. cephalus and C. auratus blood parameters, except for haemoglobin
concentration (Hgb). A significant increase in red blood cell count (RBC) and haematocrit (Hct) levels, associated with
reduced mean corpuscular volume (MCV), was revealed in mullets in respect to goldfish. These data may be attributable to
differences in fish species, or to their divergent physiological activeness as high RBC values are associated with fast
movement and high activity with streamlined bodies, or to environmental factors such as water salinity, an increase in
which may lead to erythropoiesis as an adaptive process in seawater fish. Additionally, lower values of white blood cell
count (WBC) and thrombocyte count (TC) were recorded in mullets with respect to goldfish, and these changes may be due
to divergent feeding habits of the two fish species, or to their different environments since increased salinity may inversely
affect WBC. Overall, findings from this study provide a better understanding of the influences of divergent environmental
conditions and feeding habits on fish blood parameters. The combined use of an automatic haematological count with flow
cytometry was demonstrated to be effective for an early assessment of blood parameters in different fish species.
Keywords: Blood parameters, mullet (Mugil cephalus), goldfish (Carassius auratus), flow cytometry, light microscopy
Introduction
Haematological parameters are commonly used as
valuable indicators for the assessment of fish health
status (Gabriel et al. 2004). Variations in blood parameters depend upon the fish species, aquatic biotope,
health and nutritional status, age and sexual maturity
(Blaxhall 1972; Chaudhuri et al. 1986; Wilhem et al.
1992; Hrubec et al. 2001; Fazio et al. 2016).
Moreover, blood parameters of fish are highly sensitive
to environmental changes. Quality of water, oxygen,
temperature and salinity are directly reflected in blood
parameters (LeaMaster et al. 1990; Luskovav 1997;
Sheikh & Ahmed 2016), as well as basic ecological
factors such as feeding regime and stocking density
(Což-Rakovac et al. 2005; Ferri et al. 2011). A correct
interpretation of fish haematology depends on the
availability of reference values, helpful in understanding the relationship of blood characteristics to the
phylogeny, activity, habitat and adaptability of the
species to the environment (Blaxhall 1972; Wilhem
et al. 1992). This study is therefore aimed at providing
baseline data of the haematological profile of two teleost fish species living in different aquatic environments, namely the flathead grey mullet Mugil
*Correspondence: T. Cappello, Department of Chemical, Biological, Pharmaceutical and Environmental Sciences, University of Messina, Viale F. Stagno
d’Alcontres 31, 98166 Messina, Italy. Tel: +39 090 391435. Fax: +39 090 6765556. Email: tcappello@unime.it; V. Parrino, Department of Chemical,
Biological, Pharmaceutical and Environmental Sciences, University of Messina, Viale F. Stagno d’Alcontres 31, 98166 Messina, Italy. Tel: +39 090 391435.
Fax: +39 090 6765556. Email: vparrino@unime.it
#
These authors contributed equally to this work.
© 2018 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group.
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which
permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
194
V. Parrino et al.
cephalus Linnaeus, 1758, a marine herbivorous fish,
and the goldfish Carassius auratus (Linnaeus, 1758),
a freshwater omnivorous fish.
Grey mullets (Osteichthyes: Mugilidae) have a
worldwide distribution, commonly inhabiting tropical
and warm-temperate estuaries. Even if spawning
occurs in the sea, grey mullets are highly euryhaline
as they are capable of living in a wide range of salinities, from marine to estuarine and freshwater environments (Cardona 2006; Brandão et al. 2015;
Cappello et al. 2016a,b). Although M. cephalus larvae
are planktivorous, juveniles and adults undergo a
change in diet and feed mainly on detritus and benthic
microalgae, especially diatoms (Whitfield et al. 2012).
Mugil cephalus is also a species of considerable commercial value as it is widely exploited worldwide, being
an important fishing resource as well as aquaculture
species (Cardona 2006; Whitfield et al. 2012).
Goldfish (Cypriniformes: Cyprinidae) primarily
inhabit freshwater environments and are distributed
widely in and around the Eurasian continent
(Takada et al. 2010). Goldfish are ominvorous, and
their diet includes planktonic crustaceans, phytoplankton, insect larvae, fish eggs and fry, benthic vegetation and detritus (Specziár et al. 1998). Goldfish can
tolerate low oxygen levels, temperature fluctuations
and high levels of anthropogenic pollution, and for
these reasons they are frequently used as sentinel species in various laboratory studies (Fan et al. 2013;
Maisano et al. 2013; Zhelev et al. 2016). Also, C.
auratus is a domesticated ornamental fish of economic
relevance in the freshwater aquarium fish industry.
The haematological profiles of the grey mullet M.
cephalus and the goldfish C. auratus were herein
determined by the use of an automated system,
coupled with flow cytometry and light microscopy.
Material and methods
Fish collection and acclimation
Twenty flathead grey mullets M. cephalus were
caught from Faro Lake, a coastal brackish system
located in north-eastern Sicily, Italy (Fazio et al.
2013; D’Agata et al. 2014; Maisano et al. 2016b).
All fishes (fork length: 21.25 ± 2.72 cm; weight:
75.40 ± 12.35 g) were considered healthy on the
basis of an external examination for any signs of
abnormalities or infestation. After collection, all animals were transported to the laboratory to be acclimated for 3 weeks in 400-L tanks each containing
pond water (physico-chemical characteristics are
reported in Table I), equipped with filter and oxygenation systems. According to a previous study conducted in the laboratory with mullets (Faggio et al.
2013), for the first 3 days of the acclimatisation
period, fish were fasted and then fed twice per day
with commercial floating pelleted feed (0.45 cm diameter), the proximate composition of which was, on
a wet basis, 8.9% moisture, 51.1% protein, 8.0%
lipid and 11% ash.
Additionally, 20 goldfish C. auratus (fork length:
18.13 ± 1.45 cm; weight: 70.50 ± 7.20 g) were
purchased from a commercial supplier. Upon arrival, fish were transferred to circular tanks supplied
with aerated and dechloraminated water, the physico-chemical features of which are reported in
Table I. The fish were held in aquaria for acclimation for 3 weeks, and fed with commercial pellets
(0.3 cm size) 2 times a day.
For the entire acclimation period, both the mullet
tanks and goldfish tanks were maintained under a
12:12-h light:dark photoperiod. Water temperature,
pH, salinity, dissolved oxygen (DO2) and ammonia
(NH3/NH4) levels, as reported in Table I, were
checked daily in each tank using a multi-parametric
probe C 203 (Hanna-Instruments, United Kingdom).
No mortality was recorded during the entire acclimation period.
Fish blood collection
For both mullets and goldfish, feeding was stopped
24 h prior to blood sampling. The fish were anaesthetised using tricaine methane sulfonate (MS-222;
0.3 g/L) immediately before blood collection. Blood
samples were drawn from the caudal vein using a
sterile plastic syringe (2.5 mL), and transferred into
microtubes (Miniplast 0.6 mL, LP Italiana Spa,
Milano) containing ethylenediamine tetraacetic acid
(EDTA, 1.26 mg/0.6 mL) as the anticoagulant
agent. Animal maintenance and experimental procedures were in accordance with the ethical guidelines
Table I. Water physico-chemical characteristics for acclimation of Mugil cephalus and Carassius auratus.
Fish species
Temperature
pH
Conductivity
Dissolved oxygen (DO2)
Salinity
(NH3/NH4)
M. cephalus
C. auratus
18.2°C
18.1°C
8.23
8.01
47.6 mS/cm
342.1 μS/cm
5.7 mg/L
5.3 mg/L
38°/oo
0.03°/oo
0.20 mg/L
0.23 mg/L
Blood parameters of mullets and goldfish
of the European Union Council (Guide for Care and
Use of Laboratory Animals, Directive 2010/63/EU).
Automatic haematological analysis
The haematological profile was determined immediately after collection of mullet and goldfish wholeblood samples using an automated haematology analyser (HeCo Vet C; SEAC, Florence, Italy). This
apparatus uses an impedance analysis system that
was already used and validated by comparative manual tests in the veterinary field to investigate haematological profiles in various fish species (Faggio et al.
2013; Fazio et al. 2013, 2016). Evaluation of the
haemogram involved the determination of the red
blood cell count (RBC), haematocrit (Hct), haemoglobin concentration (Hgb), white blood cell count
(WBC), thrombocyte count (TC), mean corpuscular
volume (MCV), mean corpuscular haemoglobin
(MCH) and mean corpuscular haemoglobin concentration (MCHC). All fish blood samples were analysed in duplicate by the same operator.
195
Morphological analysis
Morphological analysis of the grey mullet M. cephalus and goldfish C. auratus erythrocytes was carried
out by smearing heparinised whole blood on a glass
slide. The slides were air-dried overnight and then
fixed in absolute methanol for 20 min before staining
with 10% Giemsa solution for 15 min. Blood smears
were observed using a 63 × oil-immersion objective
with a motorised Zeiss Axio Imager Z1 microscope
(Carl Zeiss AG, Werk Göttingen, Germany)
equipped with an AxioCam digital camera (Zeiss,
Jena, Germany).
Statistical analysis
Data obtained for haematological parameters were
tested for normality using Kolmogorov–Smirnov
test, using P < 0.05 as the threshold for significance.
Unpaired t-tests were used to determine statistical
differences between the two fish species in all parameters measured. Data were considered statistically
significant at P < 0.05. All calculations were carried
out using the statistical software Prism v. 5.00
(Graph Pad software Ldt., USA, 2003).
Flow cytometric analysis
Flow cytometric analysis was performed within 5 h
of drawing mullet and goldfish whole-blood samples,
using ImageStreamX (Amnis, Seattle, WA), a multispectral flow cytometer combining standard microscopy with flow cytometry. It can acquire up to 100
cells/s, with simultaneous acquisition of six images of
each cell, including bright field, scatter and multiple
fluorescent images. For the present study, the integrated software INSPIRE, running on the
ImageStreamX Mark II, was applied. Samples were
always left on ice before being injected into the flow
cell. Then, the cells were allowed to form a single
core stream before acquisition. Images were analysed
using IDEAS image-analysis software (Amnis).
Results
Automatic haematology
The haematological parameters of the two teleost
fish species, M. cephalus and C. auratus, are reported
as mean values ± standard error of the mean (SEM)
in Table II. In detail, a statistically significant
increase in the levels of RBC and Hct was recorded
in grey mullets with respect to goldfish. In contrast,
the values of MCV, MCH, MCHC, WBC and TC
were statistically significantly lower in mullets than
goldfish. Additionally, no statistical differences
between the two teleost fish were found in the level
of Hgb.
Table II. Mean values ± standard error of the mean (SEM) of haematological parameters
recorded in the two teleost species Mugil cephalus and Carassius auratus (*P < 0.05).
Haematological parameters
Mugil cephalus
(n = 20)
Carassius auratus
(n = 20)
RBC (×106/μL)
Hct (%)
Hgb (g/dL)
MCV (fL)
MCH (pg)
MCHC (g/dL)
WBC (× 103/μL)
TC (× 103/μL)
2.08
19.55
4.45
92.11
21.58
23.63
30.08
27.96
0.50
7.56
4.18
1152.80
84.54
55.93
66.35
83.75
±
±
±
±
±
±
±
±
0.16*
1.86*
0.33
2.10*
0.36*
0.61*
2.28*
3.58*
±
±
±
±
±
±
±
±
0.01
0.12
0.18
3.70
3.79
2.72
2.46
4.19
RBC, red blood cell count; Hct, haematocrit; Hgb, haemoglobin concentration; MCV, mean
corpuscular volume; MCH, mean corpuscular haemoglobin; MCHC, mean corpuscular haemoglobin concentration; WBC, white blood cell count; TC, thrombocyte count.
196
V. Parrino et al.
Figure 1. Flow cytometry performed on blood samples of (a) the grey mullet Mugil cephalus and (b) the goldfish Carassius auratus. The score
plots show a clear grouping of red blood cells (RBC; in orange), white blood cells (WBC; in blue), thrombocytes (TC; in green) and debris
(in yellow).
Flow cytometry
The results obtained by the flow cytometric analysis
performed on the blood samples of the two teleost
fish are shown in Figure 1. A clear grouping of the
three main blood cell populations, namely RBC,
WBC and TC, is depicted in the score plots, as
well as appreciable variations between the two fish
species, with higher RBC and lower WBC and TC in
the grey mullet M. cephalus (Figure 1(a)) than in
goldfish C. auratus (Figure 1(b)).
Red blood cell morphology
Microscopic examination of fish blood samples
revealed the presence of a high number of erythrocytes of reduced size in the grey mullet M. cephalus
(Figure 2(a)). Conversely, the red blood cells of the
goldfish C. auratus appeared lower in number but
much greater in size in comparison with those
observed in mullets (Figure 2(b)).
Discussion
Fish are known to live in a very intimate contact with
their environment, and therefore they are extremely
dependent upon it (Guerriero et al. 2003; Acharya &
Mohanty 2014; Giannetto et al. 2014; Maisano et al.
2016a). It is well documented that ambient changes
influence blood cell number, morphology and distribution (Srivastava & Choudhary 2010). Haematological
parameters are therefore widely used as an early signal of
changes in fish health status, and have proven to be a
valuable approach also for monitoring the effects of
Figure 2. Erythrocytes from (a) the grey mullet Mugil cephalus and (b) the goldfish Carassius auratus. Scale bars: 20 μm.
Blood parameters of mullets and goldfish
habitat changes on fish biology (Gabriel et al. 2004;
Fazio et al. 2012a, 2012b, 2012c, 2013; Sheikh &
Ahmed 2016).
In order to use blood parameters as biomarkers, it
is necessary to know their standard values and reference interval for a given fish species. However, the
ranges of normal values of the key haematological
parameters are still undefined for some fish species
living in different habitats. The evaluation of the
haematological parameters of mullets and goldfish
was herein conducted using an automated system,
together with flow cytometry and light microscopy,
which provided comparable results.
Except for the Hgb value that proved to be nearly
the same in the two fish species, a significant increase
in RBC and Hct levels, coupled with reduced MCV
(and therefore directly linked also to decreased
MCH and MCHC), were revealed and microscopically observed in M. cephalus with respect to C.
auratus. It is known that the RBC of an organism
determines the carrying capacity of dissolved oxygen
(Al 2000). Therefore, the differences herein
observed may be attributable to the divergent physiological activeness of the examined fish species. As
previously reported by Svobodova and collaborators
(Svobodova et al. 2008), active species present
higher values of haematological parameters compared to less active forms. Indeed, high RBC values
are usually associated with fast movement and high
activity with streamlined bodies, as already documented in various studies conducted on wild and
farmed species, including grey mullets (Fazio et al.
2012a, 2012b, 2013, 2016). Additionally, environmental factors such as water salinity have a direct
effect on various blood parameters such as RBC and
Hct through their effect on the haemoglobin oxygenbinding properties and thus on oxygen transport
(Witeska 2013). The increased number of erythrocytes and concomitant reduction in their volume
recorded herein in mullets is due to an adaptive
process to salinity of seawater habitat. Oxygen transportation in salt water moves faster than in fresh
water, and this implies a degeneration of part of the
red cells resulting in an increased erythropoiesis.
This leads to an augmented production of new erythrocytes with a decreased volume unit. Similar data
were provided by Izergina et al. (2007), after investigating the influence of water salinity on the physiological status of juvenile chum salmon.
Interestingly, lower values of WBC and TC were
herein recorded in mullets with respect to goldfish.
It is known that WBC play a major role in the
immune defensive system of fish, whereas TC are
blood cells that serve mainly to form protective
197
barriers (Magnadottir 2006). The numbers of
WBC and TC may change in relation to various
environmental parameters or stimuli such as infection, as well as multiple other factors, from the age
of fish to species characteristics or nutritional differences (Romano et al. 2017), which may explain
the variations in WBC and TC values observed
herein in mullets compared to goldfish, probably
reflecting the different feeding habits of the two
fish species under study. Notably, in a previous
study it was reported that M. cephalus showed the
lowest WBC and TC values with respect to two
other seawater carnivores species, namely Sparus
aurata and Dicentrarcus labrax (Fazio et al. 2016).
Also, increased salinity may inversely affect the
values of WBC as documented for M. cephalus
collected from two habitats with different physicochemical features (Fazio et al. 2012c).
The results of this preliminary study provide
basic knowledge of the blood profile of M. cephalus
and C. auratus, two teleost species of ecological
and economic importance, allowing better comprehension of the influences of divergent environmental conditions and feeding habits on fish blood
parameters. Additionally, findings from this study
demonstrate the effectiveness of coupling an automatic haematological count with flow cytometry as
diagnostic tools for an early understanding of the
variability of blood cells in different fish species.
Disclosure statement
No potential conflict of interest was reported by the
authors.
Ethical approval
All sampling, animal maintenance and experimental
procedures of this study involving fishes were performed in accordance with the ethical guidelines of
the European Union Council, namely the Guide for
the Care and Use of Laboratory Animals, Directive
2010/63/EU.
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