Received: 25 May 2016
|
Revised: 27 March 2017
|
Accepted: 28 March 2017
DOI: 10.1111/are.13374
ORIGINAL ARTICLE
A comparative histological study on early thyroid gland development in Acipenser stellatus and A. gueldenstaedtii larvae in hatchery Tulay Akayli1
| Devrim Memisß2 | Erol Rustu Bozkurt3
1 Department of Fish Diseases, Faculty of Fisheries, Istanbul University, Laleli-Istanbul, Turkey
Abstract The thyroid is an endocrine gland, with an important role in fish growth, develop-
2
Department of Aquaculture, Faculty of Fisheries, Istanbul University, Laleli-Istanbul, Turkey 3
Department of Pathology, Istanbul Education and Research Hospital, SamatyaIstanbul, Turkey
ment and adaptation of larvae. The aim of this study was to describe the development of the thyroid gland and to determine the initial functional activity of thyroid gland and hormones in Acipenser gueldenstaedtii and A. stellatus larvae using immunohistochemistry. For this aim, fertilized eggs of two species were reared in a hatchery and larval samples were collected daily for 20 days post hatching (dph).
Correspondence Tulay Akayli, Department of Fish Diseases, Faculty of Fisheries, Istanbul University, Laleli-Istanbul, Turkey. Email:
[email protected]
For immunostaining, rabbit polyclonal primary antibodies for thyroglobulin and mouse monoclonal antibodies for thyroid transcription factor-1 (TTF-1) were used. In histological analyses, it was observed that the first development of the thyroid gland in stellate sturgeon larvae occurs on the 3–4 dph and on the 4–5 dph in Rus-
Funding information Food and Agriculture Organization, Grant/ Award Number: FAO:TCP/TUR/3202(D)
sian sturgeon larvae in the ventral pharyngeal region of the fish. In the immunostaining analyses of 12-day-old stellate larvae and 19-day-old Russian sturgeon larvae, the thyroid follicles showed dispersion in great numbers around the aorta, and also it was observed that they were stained positively with antithyroglobulin staining, but the same sections gave negative results with TTF-1 staining. Also melanomacrophage centres, which are generally found in the haemopoietic tissues in some cases, were first observed around the thyroid follicles of sturgeon larvae. The results of this study revealed a similarity in the early thyroid gland development between two sturgeon species but using immunostaining methods, it was described that A. stellatus shows a faster functional development and earlier hormone production than A. gueldenstaedtii. KEYWORDS
A. gueldenstaedtii, A. stellatus, immunohistochemistry, sturgeon, thyroid
1 | INTRODUCTION
but today are on the verge of extinction. The population of sturgeon has decreased over the past century because of overfishing and lack
Russian sturgeon, Acipenser gueldenstaedtii (Brandt & Ratzeburg,
of management control (Chebanov & Galich, 2013; Dettlaff et al.,
1833), and stellate sturgeon, Acipenser stellatus (Pallas, 1771), are
1993; Gessner & Arndt, 2006). Russia, Italy, Iran (Chebanov & Galich,
endemic species in Turkey (Memis, 2014; Memis, Ercan, Celikkale,
2013; Chebanov et al., 2011) and Turkey (Memis, 2014; Memis
Timur & Zarkua, 2009), occurring in the southern basin of the Black
et al., 2009) tried to adapt the aforementioned species for aquacul-
Sea (Chebanov & Galich, 2013; Dettlaff, Ginsburg & Schmalhausen,
ture and achieved various degrees of success in both research and
1993). Both species played an important role in commercial fishing
commercial scales (Chebanov & Galich, 2013).
Aquaculture Research. 2017;48:5533–5540.
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© 2017 John Wiley & Sons Ltd
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As an adaptation to environmental factors at particular crucial
AKAYLI
ET AL.
and Genetics for Aquaculture, Krasnodar, Russia, in May 2010 and
stages of development in many species of animals, as well as fish,
were brought to Yedikır Fish Culture and Research Station, Gen-
changes in hormones can be seen (Tanaka et al., 1995; Power et al.,
eral Directorate of State Hydraulic Works (Amasya, Turkey). In the
2001; Boiko & Grigoryan, 2002; Blanton & Specker, 2007). In this con-
hatchery, standard feeding regime was utilized for both sturgeon
nection, the examination of the functional and structural development
species and active feeding of the larvae was started with Artemia
of endocrine system at early stages of ontogeny in fish plays an impor-
salina on the 7 dph (days post hatching), and during the whole
tant role (Gorbman, 1969; Hibiya, 1982; Power et al., 2001). The thy-
larval phase, water temperature was kept at 16–21.5°C. Two larval
roid gland secrets thyroxine (T4) and triiodothyronine (T3), hormones
samples were collected daily from hatching (0 dph) until 20 dph.
that control various metabolic processes such as growth, differentia-
In total, 40 samples were collected from each species. Prior to
tion, metamorphosis, reproduction, respiration, migratory behaviour,
the histological processing, total length of the larvae was mea-
central nervous system activity and seasonal adaptation in fish (Blan-
sured.
ton & Specker, 2007; Power et al., 2001). In contrast to mammals, a calorigenic response is not produced by thyroid hormones in fish. However, there is an influence of these hormones on carbohydrate
2.2 | Histology
metabolism and also the mobilization of lipid reserves (Roberts & Ellis,
Larval samples were immediately fixed in phosphate-buffered forma-
2012). There is a close link of these reactions in fish to thyroid hor-
lin solution, which contains 4% formaldehyde, for 48 hr. The fixed
mones on factors such as ambient temperature, nutritional conditions,
samples were processed using routine laboratory methods. Samples
photoperiod and salinity (Gorbman, 1969; Power et al., 2001).
were washed in running water, dehydrated in ascended ethanol ser-
Tanaka et al. (1995) have reported the histological ontogeny of
ies (70%, 90% and absolute ethanol) and clarified with xylene. Later,
the thyroid follicles in various marine fish larvae such as Pacific her-
they were embedded in paraffin blocks. Histological slides of 5-lm
ring, yellowfin tuna and Japanese flounder. Also, Yakovleva (1964)
sections were prepared in rotary microtome and stained with haema-
carried out a histological study on the early development of the thy-
toxylin–eosin (H&E).
roid gland in sturgeons. In other studies, histophysiological methods (such as radioimmunoassay) were used to detect the thyroid hormones activity in sturgeons (Gorbman, 1969; Boiko et al. 2002;
2.3 | Immunostaining
Plohman, Dick & Eales, 2002), but immunostaining, a reliable and rel-
All thyroid tissue went through immunohistochemical staining with
atively easier method, was used to detect thyroxine activity in some
thyroglobulin and TTF-1. Primary antibodies for thyroglobulin
freshwater fish species such as rainbow trout, carp and tilapia
(N1565, rabbit poly-clonal, DAKO Corporation) and mouse MoAb for
(Geven, Boogaart, Spanings, Flik & Klaren, 2007; Raine & Leather-
thyroid transcription factor-1 (TTF-1) (8G7G3/1, Cell Maraque Cor-
land, 2000; Santos et al., 2015).
poration) were used as per producer-proposed procedures (Ramos-
The synthesis of thyroxine (T3) and triiodothyronine (T4) is
Vara et al., 2002).
observed at certain tyrosine residues on thyroglobulin and these hor-
After the completion of the tissue blocks, 4-lm sections were
mones are closely related to fish development (Ortiz Delgado, Ruane,
cut and they were air-dried overnight. Afterwards, the slides were
Pous~ ao-Ferreira, Dinis & Sarasquete, 2006; Plohman et al., 2002;
put into an oven, melted for 30 min at the temperature of 60°C and
Yamano, Nomura & Tanaka, 2007). The transcriptional activity of
went through deparaffinization in three changes of xylene and rehy-
thyroid-specific genes is regulated by TTF-1 and thyroglobulin, which
dration in graded alcohols (100%, 95% and 70%). Deionized water
is a large glycosylated protein that plays an important role in cell
was used to rinse the slides. The application of antibodies to the tis-
growth, development and differentiation. Immunostaining of thy-
sue was performed in accordance with the protocols for each anti-
roglobulin and TTF-1 is used to investigate the normal and patholog-
body. The performance of all steps on the immunostainer was
ical conditions of the thyroid gland in many organisms including
carried out at the temperature of 40°C.
humans (Katoh et al., 2000; Ramos-Vara, Miller, Johnson & Pace, 2002), but the effects of this factor were not investigated in fish.
For thyroglobulin, slides with ready-to-use proteinase K were incubated for 10 min at room temperature. After comparing results
The aim of this study was to describe the thyroid gland develop-
with proteinase K and steam heat on citrate buffer, pH 6.0, at differ-
ment and to determine the initial functional activity of this gland and
ent incubation times, steam heat on ethylenediametetra acetic acid
its hormones in cultured larvae of A. gueldenstaedtii and A. stellatus
buffer, pH 8.0, 40 min at 90–95°C, was the antigen retrieval
using immunostaining of thyroglobulin and TTF-1 hormones.
method, which was chosen for TTF-1. Slides being cooled for 20 min after steam heat were put directly in Tris buffer after pro-
2 | MATERIALS AND METHODS 2.1 | Larval sampling
teinase K treatment. The incubations which remained were performed at room temperature. The incubation of the primary antibodies to thyroglobulin was performed for 30 min; incubation with MoAb to TTF-1 was performed for 60 min. While a labelled
Samples of fertilized eggs (newly hatched larvae) of two Acipenser
streptavidin–biotin–peroxidase detection method was used for thy-
species used in this study were obtained from Center of Selection
roglobulin, Horseradish–peroxidase system was used for TTF-1.
AKAYLI
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3 | RESULTS
of the developing thyroid follicles increased and the insides of
3.1 | Ontogenic development of the thyroid gland
material (Figure 2f).
The first development of the thyroid gland in stellate sturgeon lar-
7 days after hatching and later, the first exogenous feeding activities
vae was observed at 3–4 days post hatch (dph). It was determined
begin. On this period, the Russian sturgeon samples showed a faster
that the thyroid follicles observed on this date showed dispersion
growth and reached from 1.1 to 1.7 cm on the 7th dph. In this spe-
in the ventral part of the head, in a very small number, around
cies, thyroid follicles were first observed on the 4th dph with a
the ventral aorta in the connective tissue and the follicles did not
diameter of 25–105 lm but remain in the same size on the next
develop completely (Figure 1a, b). On 6 dph, the formation of one
3 days. With the initiation of exogenous feeding, larvae size reached
follicle was observed in the area between two branches of aorta
to 4.5 cm on the 19th dph but their thyroid gland did not developed
these structures were filled with a stained acidophilic homogeneous Russian sturgeon larvae also fed through the yolk sac on the first
(Figure 1c, d). On the 8th dph, the development of two follicles
so rapidly. On the 12th dph, they had follicles of 30–130 lm, but
with these structures being filled with a weakly stained acidophilic
later, on the 19th dph, it was observed that their lumen is filled with
homogeneous material (Figure 1e, f). It was observed that the thy-
thyroglobulin and the follicle size reached to 50–300 lm (Table 1).
rocytes surrounding the follicle are with large nuclei and with narrow cytoplasm, besides the intracytoplasmic vacuoles found in these cells push the nucleus aside and contribute to the follicle
3.2 | Immunohistochemical results
formation inside follicles of the early period. In the histological
The thyroid tissues of the larvae samples analysed in this study were
sections of the larvae in this group, melanin granules containing
stained immunohistochemically with antithyroglobulin (TG) and TTF-
brown small circular pigments which are compact and which are
1. In the immunostaining analyses of 12-day-old stellate larvae and
single were observed around aorta branches and on the thyrocytes
19-day-old Russian sturgeon larvae, the thyroid follicles showed dis-
(Figure 1f). On the 12th dph, it was observed that the follicles
persion in great numbers around the aorta, and also it was observed
developed, their insides were filled with a dark-coloured acidophilic
that they were stained positively with antithyroglobulin staining (Fig-
liquid and two branches of the aorta merged and became united
ure 3a). Mass immune staining of the thyroglobulin hormone is a
(Figure 1g).
proof of functional development in the thyroid gland and production
After hatching, stellate larvae are fed through the yolk sac during
of this hormone. In this study, thyroglobulin production in two stur-
the first 7 days where the first exogenous feeding activities begin.
geon species could be detected using antithyroglobulin staining
Hence, stellate larvae that were sampled on the first 7 days showed
method, but negative results were achieved in the sections prepared
a relatively slow development in size and they reached from 0.9 cm
from the 20-day sampling study stained with TTF-1 stain
to 1.2 cm. Thyroid follicles were first observed on 3 dph with a
(Figure 3b).
diameter between 10 and 40 lm. With the initiation of exogenous
With immunostaining of the tissues, the first thyroglobulin pro-
feeding, the larvae showed a faster growth rate and reached to size
duction was determined on the 12th dph. At this point, the minimum
of 3.6 cm on 19 dph. A similar fast development was also observed
thyroid cell follicle size was measured as 30 lm where the maximum
in the follicle diameter and follicular cell size on the 12th and 19th
measured size was 130 lm in stellate larvae when they reached a
dph. The follicle sizes of the stellate and Russian sturgeon larvae
size of 1.7 cm. On the contrary, this thyroglobulin production was
reached to a range between 30–150 and 40–190 lm, respectively
determined on the 19th dph in Russian sturgeon when the larvae
(Table 1). Besides, beginning from the 12th day, it was observed that
reached to a size of 4.5 cm. In this species, at the same point, the
their lumen is filled with a dark-coloured acidophilic liquid which is
minimum thyroid cell follicle size was measured as 50 lm where the
regarded as thyroglobulin.
maximum measured size was 300 lm (Table 1).
The thyroid follicles started forming for the first time in the larvae of Russian sturgeon on the 4–5 dph in the same manner in the ventral pharyngeal region of the fish, inside the branches of the
4 | DISCUSSION
ventral aorta as two pieces and outside as one pieces (Figure 2a, b). On the 7th dph, it was observed that some thyroid tissue con-
Functional and structural development of endocrine system at early
taining follicle space shows diffuse development between the
stages of ontogeny in fish plays an important role (Gorbman, 1969;
branches of the aorta and some of a close packed structure started
Hibiya, 1982; Power et al., 2001). The thyroid gland secrets hor-
to develop (Figure 2c). In different sections of the larvae in this
mones that control various metabolic processes such as growth, dif-
period, some follicles again developed as protuberate to the inside
ferentiation, metamorphosis and central nervous system activity and
of the vein, and the colloid number in the follicle lumen was very
seasonal adaptation in fish (Blanton & Specker, 2007; Power et al.,
small and contained melanin granules in small numbers (Figure 2d).
2001). Both A. stellatus and A. gueldenstaedtii larvae samples used in
On the 15th dph, an increase in the number of the follicles located
this study showed a normal pattern for organ and tissue develop-
between two branches of the ventral aorta was detected (Fig-
ment in the first month of larval life when compared to the previous
ure 2e). Since the 19 dph, the colloid number found in the lumen
€e,1995). In this study, studies (Gawlicka, Teh, Hung, Hinton & Nou
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ET AL.
F I G U R E 1 Photomicrographs of the thyroid gland of the stellate sturgeon larvae during early development stage. (a, b) Early appearance of thyroid follicles (3–4 days old); (c, d) developing thyroid follicles (6 days old); (e, f) an increase in the number of follicles (8 days old); (g) activated thyroid follicles and the appearance of the aorta in a single piece (12 days old); (va) ventral aorta; (m) mouth opening; (tf) thyroid follicle; (c) colloid; (bc) blood cell; (vl) vacuol; (m) melanin granules; (g) gill filament [Colour figure can be viewed at wileyonlinelibrary.com]
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ET AL.
T A B L E 1 Changes in the follicle size and mean total length of the larvae samples during the study
5537
In contrast to the previous reports in which the thyroid gland development and thyroid hormone activity in sturgeons were
Follicle size (lm) (length–height)
Mean total length of the larvae (cm)
detected using histophysiological and radioiodine methods (Gorbman,
Stellate sturgeon (min–max)
Russian sturgeon (min–max)
Stellate sturgeon (n = 40)
Russian sturgeon (n = 40)
nier, 2014); an immunostaining method, which includes anti-human
0
–
–
0.9
1.1
gland activity in sturgeons.
2
–
–
0.9
1.1
As well as being mainly used for the diagnosis of viral and bacte-
3
10–40
–
1
1.2
rial infections of fish (Adams & Marin de Mateo, 1994), immunos-
4
10–40
25–105
1
1.2
taining has been used in a variety of fish species and especially in
5
15–110
25–120
1.1
1.3
sturgeons for various aims such as determination of structural anat-
6
20–130
30–120
1.1
1.5
~uela & Northcutt, 2007) and omy (Domeneghini et al., 2002; Pin
Sampling point (dph)
1969; Boiko et al. 2002, 2004; Plohman et al., 2002; Chanet & Meuthyroglobulin and anti-human-TTF-1 antibodies targeting thyroglobulin hormone, was used for the first time for the detection of thyroid
7
30–130
30–120
1.2
1.7
detection of the pituitary hormones (Amemiya, Sogabe, Nozaki,
8
40–130
25–130
1.5
2.6
Takahashi & Kawauchi, 1999) and specific and reliable results were
12
40–190
30–130
1.7
3.4
15
40–220
30–140
1.9
4
19
50–250
50–300
3.6
4.5
achieved. In these studies that utilize different immunostaining techniques, mainly monoclonal rabbit antibodies (Amemiya et al., 1999; ~uela & Northcutt, 2007) were used but also anti-human macroPin phage antibodies were used (Domeneghini et al., 2002). Immunohistochemical methods were previously used for the detection of
thyroid gland development and determination of the initial functional
thyroid gland development in various freshwater fish species such as
activity of this gland and its hormones in larvae of two sturgeon spe-
rainbow trout (Raine & Leatherland, 2000), carp (Geven et al., 2007)
cies were aimed, and differences in the early development stages
and tilapia (Geven et al., 2007; Santos et al., 2015). Alt et al., (2006)
were observed using histological and immunostaining methods.
previously used anti-human immune globulines (T4 and TG) in an
The presence of thyroid hormones was detected at all stages of
immunostaining method and successfully detected the thyroid gland
early development, that is, in mature eggs being ready for fertiliza-
development in the zebra fish (Danio rerio) larvae. Depending on the
tion, in embryos and also in developing fish larvae (Boiko et al.,
results of this study, the success of immune staining in the detection
2002, 2004; Ortiz Delgado et al., 2006; Blanton & Specker, 2007).
of thyroid gland development in fish was also proved. Despite one
Initial thyroid gland development in various marine fish larvae varies
of the two antibodies used in this study, TTF-1 did not provided any
from 1 to 6 days (Tanaka et al., 1995). Yakovleva (1964) determined
positive results in the whole study; previously, Santos et al. (2015)
that the first development of the thyroid follicles in sturgeon larvae
could be able the detect the expression of thyroid receptors in the
started at 3 dph and it was also confirmed with the results of this
ovary of tilapia (Oreochromis niloticus) with this method. They have
study. In this study, early appearance of thyroid follicles was
detected an increase in the thyroid hormone production depending
detected in 3- to 4-day-old stellate sturgeon larvae and 4- to 5-day-
on the maturation of ovaries using another receptor.
old Russian sturgeon larvae. But later stellate sturgeon larvae showed a faster functional activity development.
In this study, using histological and antithyroglobulin immunostaining methods, it was detected that the first thyroid follicles were
Hibiya (1982) reported that the thyroid follicles can be found in
detected on the 3rd dph and the first hormone production was
fish, apart from the connective tissue of the pharyngeal area, in the
detected in the 12th dph in stellate sturgeon larvae. On the contrary,
eye, front kidney and inside big blood vessels. The thyroid gland
thyroid follicles were first formed in the 4th dph and begun to pro-
despite being an organ surrounded by the follicle capsules in Elas-
duce hormones on the 19th dph in Russian sturgeon. Depending on
mobranchii and in a few Teleost fish, in other fish as we also
the previous reports, an increase of more than three times was
observed in this study in sturgeons (Chondrostean species) it com-
detected in the thyroxin level in sturgeon larvae from 14 to 20 dph
monly shows a gland structure composed of the follicles spread
which is a proof of a rapid development of the thyroid gland in the
widely over an area around the ventral aorta (Yakovleva, 1964;
early ontogenesis in Russian sturgeons (Boiko & Grigoryan, 2002;
Chanet & Meunier, 2014). In fish, de-oxygenated blood is carried
Boiko, Vorobeva, Grigoryan & Kornienko, 2004). In this study, as the
by the ventral aorta from the heart to the gills and tetrapods found
first exogenous feeding started, the size of the thyroid gland follicles
in the ascending aorta are connected with the thyroid gland by a
showed an increase and this enlargement in size also increased as
number of vessels (Roberts & Ellis, 2012; Chanet & Meunier, 2014).
the hormone production started.
In a similar way, developing thyroid follicles were also found inside
Sturgeon prelarvae are fed through the yolk sac supply and later
the branches of the ventral aorta in the histological sections of the
first exogenous feeding activities are started with live feed such as
larvae in this study. As stated previously, this is an important fea-
Artemia saline and Daphnia sp. which induces the increase in the
ture which shows that the thyroid gland is fed with blood (Hibiya,
growth rate (Chebanov & Galich, 2013; Chebanov et al., 2011; Dett-
1982).
laff et al.,1993). Similarly, in this study, sturgeon larvae showed a
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F I G U R E 2 Photomicrographs of the thyroid gland of the Russian sturgeon during early development stage. (a, b) Early appearance of thyroid follicles in the ventral aorta vessel (4–5 days old); (c) developing thyroid follicles (7 days old); (d) two thyroid follicles developing inside the vessel (8 days old); (e) an increase in the number of the follicles evolving between two branches of the aorta (15 days old); (f) follicles filled with lumens colloid which finished the development (19 days old) (va) ventral aorta; (tf) thyroid follicle; (c) colloid; (bc) blood cell; (vl) vacuol; (m) melanin granules [Colour figure can be viewed at wileyonlinelibrary.com] relatively slower growth rate during the yolk sac stage, and with the
reported that live feed induces an increase in the hormone produc-
initiation of live feeding stage, the growth rate was also increased.
tion in sturgeons (Boiko & Grigoryan, 2002; Boiko et al., 2004; Che-
During the 20-day sampling study, although the stellate larvae devel-
banov & Galich, 2013; Chebanov et al., 2011). Similarly, in this
oped thyroid glands and started the hormone production earlier than
study, it was detected that the thyroid gland activity showed an
the Russian sturgeons, the latter one showed a greater increase in
increase 4 days after the initiation of the live feeding stage in the
size. A similar slower growth rate and observation of a smaller size
stellate sturgeon and 7 days after the same point in Russian stur-
during the larval stages in stellate sturgeon than the Russian stur-
geon.
geon was previously reported by Dettlaff et al. (1993), but in con-
In fish, a variety of pigments, including melanins, are present in
trast, it was also reported that stellate sturgeon reaches to sexual
melanomacrophage centres (MMCs) that are usually located in the
maturity earlier than the Russian sturgeon (Chebanov & Galich,
haemopoietic tissues such as spleen, kidney and the liver in teleost
2013; Chebanov et al., 2011; Dettlaff et al.,1993). It was previously
dez, Quiroga & Nieto, fish (Agius & Roberts, 2003; Vigliano, Bermu
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ET AL.
5539
F I G U R E 3 Immunostaining of the thyroid tissues of 12-day-old stellate larvae. (a) TG positive result. (b) TTF-1 negative result [Colour figure can be viewed at wileyonlinelibrary.com] 2006). The major function of MMCs is to concentrate the destruc-
Turkey: habitat assessment and restocking” supported by the Min-
tion and recycling of exogenous and endogenous material and this
istry of Food Agriculture and Livestock. We would like to thank all
process originates the melanin, lipofuscin and hemosiderin deposits
project management committee and staff of Yedikır Fish Culture and
found in MMCs. Other functions attributed to MMCs include the
Research Station (Amasya, Turkey), General Directorate of State Hydraulic Works (DS_I).
storage of iron following erythrophagocytosis, the retention of resistant pathogens such as bacterial or parasite spores, and antigen processing during the immune response (Agius & Roberts, 2003). For
REFERENCES
example, multifocal melanomacrophage centres were observed in the liver tissue of cultured A. gueldenstaedtii affected by a bacterial infection caused by Aeromonas hydrophila and Flavobacterium hydatis (Timur, Akayli, Korun & Yardimci, 2010). Interestingly, in contrast to other Teleost fish, these melanin granules which are generally present in the haemopoietic tissues were observed around the thyroid follicles of sturgeon larvae which is an extraordinary case for the taxonomic order of Acipenseriformes. This phenomenon can be explained in these fish, a primitive form of Teleostei. In conclusion, in this study, it was described that the early development stage of the thyroid gland shows histological similarities between two cultured sturgeon species A. stellatus and A. gueldenstaedtii but using immunostaining methods, it was described that A. stellatus shows a faster functional development and begin to produce thyroglobulin hormones earlier than A. gueldenstaedtii. In both sturgeon species, a rapid development in size was observed after the initiation of exogenous feeding and it is also thought that it is closely related to the development of thyroid gland and hormone production. The production of high-quality sturgeon fry and development of their thyroid glands mostly depend on successful first feeding. Hence, an ultimate attention must be shown to the feeding regime of these fish species during rearing in the hatcheries, and when regulating the time of first feeding for the culture of these two sturgeon species, the differences in the thyroid gland development should be taken in care.
ACKNOWLEDGMENTS In this study, sturgeon larvae samples were obtained from FAO: TCP/TUR/3202(D) project, “Recovery of sturgeon population in
Adams, A., & Marin de Mateo, M. (1994). Immunohistochemical detection of fish pathogens. Techniques in Fish Immunology, 3, 133–144. In: J. S. Stolen, T. C. Fletcher, S. L. Kaattari & A. F. Rowley (eds) Agius, C., & Roberts, R. J. (2003). Melano-macrophage centers and their role in fish pathology. Journal of Fish Diseases, 26(9), 499–509. Amemiya, Y., Sogabe, Y., Nozaki, M., Takahashi, A., & Kawauchi, H. (1999). Somatolactin in the white sturgeon and African lungfish and its evolutionary significance. General and Comparative Endocrinology, 114(2), 181–190. Alt, B., Reibe, S., Feitosa, N. M., Elsalini, O. A., Wendl, T., & Rohr, K. B. (2006). Analysis of origin and growth of the thyroid gland in zebrafish. Developmental Dynamics, 235, 1872–1883. Blanton, M. L., & Specker, J. L. (2007). The hypothalamic-pituitary-thyroid (HPT) axis in fish and its role in fish development and reproduction. Critical Reviews in Toxicology, 37, 97–115. Boiko, N. E., & Grigoryan, R. A. (2002). Effect of thyroid hormones on imprinting of chemical signals at early ontogenesis of the sturgeon Acipenser gueldenstaedtii. Journal of Evolutionary Biochemistry and Physiology, 38, 218–222. Boiko, N. E., Vorobeva, O. A., Grigoryan, R. A., & Kornienko, G. G. (2004). Dynamics of thyroid hormones at early stages of develop€ldenstadtii. Journal of Evolutionary ment of the sturgeon Acipenser gu Biochemistry and Physiology, 40(2), 176–181. Chanet, B., & Meunier, F. J. (2014). The anatomy of the thyroid gland among “fishes”: Phylogenetic implications for the vertebrata. Cybium, 38(2), 89–116. Chebanov, M. S., & Galich, E. (2013). Sturgeon hatchery manual. FAO Fisheries and Aquaculture Technical Paper 558. Ankara-Turkey: Food and Agriculture Organization of the United Nations. Chebanov, M., Rosenthal, H., Gessner, J., Van Anrooy, R. V., Doukakis, P., Pourkazemi, M., & Williot, P. (2011). Sturgeon hatchery practices and management for release guidelines. Fao Fisheries and Aquaculture Technical Paper 570. Ankara-Turkey: Food and Agriculture Organization of the United Nations. Dettlaff, T. A., Ginsburg, A. S., & Schmalhausen, O. I. (1993). Development of prelarve. In T. A. Dettlaff, A. S. Ginsburg, & O. I.
5540
|
Schmalhausen (Eds.), Sturgeon fishes developmental biology and aquaculture (pp. 175–185). New York, NY: Springer. Domeneghini, C., Radaelli, G., Bosil, G., Arrighi, S., Giancamillo, A. D., Pazzaglia, M., & Mascarello, F. (2002). Morphological and histochemical differences in the structure of the alimentary canal in feeding and runt (feed deprived) white sturgeons (Acipenser transmontanus). Journal of Applied Ichthyology, 18, 341–346. €e, J. (1995). HisGawlicka, A., Teh, S. J., Hung, S. S., Hinton, D. E., & Nou tological and histochemical changes in the digestive tract of white sturgeon larvae during ontogeny. Fish Physiology and Biochemistry, 14 (5), 357–371. Gessner, J., & Arndt, G. M. (2006). Modification of gill nets to minimize by-catch of sturgeons. Journal of Applied Ichthyology, 22(Suppl. 1), 166–171. Geven, E. J. W., Boogaart, M., Spanings, T., Flik, G., & Klaren, P. H. M. (2007). Comparative thyroidology: Thyroid gland location and iodothyronine dynamics in Mozambique tilapia (Oreochromis mossambicus Peters) and common carp (Cyprinus carpio L.). The Journal of Experimental Biology, 210, 4005–4015. Gorbman, A. (1969). Thyroid function and its control in fishes. In W. S. Hoar, & D. J. Randall (Eds.), Fish physiology, Vol. 2 (pp. 241–274). New York & London: Academic Press. Hibiya, T. (1982). Endocrine system. In T. Hibiya (Ed.), An atlas of fish histology, normal and pathological features (pp. 122–124). Tokyo: Kodansha. Katoh, R., Kawaoi, A., Eri, Miyagi. E., Li, X., Suzuki, K., Nakamura, Y., & Kakudo, K. (2000). Thyroid transcription factor-1 in normal, hyperplastic, and neoplastic follicular thyroid cells examined by immunohistochemistry and nonradioactive in situ hybridization. Modern Pathology, 13(5), 570–576. Memis, D. (2014). Short history of sturgeon caviar production in Turkey. Journal of Applied Ichthyology, 30, 1552–1556. Memis, D., Ercan, E., Celikkale, M. S., Timur, M., & Zarkua, Z. (2009). Growth and survival rate of Russian sturgeon (Acipenser gueldenstaedtii) larvae from fertilized eggs to artificial feeding. Turkish Journal of Fisheries and Aquatic Sciences, 9, 47–52. Ortiz Delgado, J. B., Ruane, N. M., Pous~ao-Ferreira, P., Dinis, M. T., & Sarasquete, C. (2006). Thyroid gland development in Senegalese sole (Solea senegalensis Kaup 1858) during early life stages: A histochemical and immunohistochemical approach. Aquaculture, 260, 346–356. ~uela, C., & Northcutt, R. G. (2007). Immunohistochemical organization Pin of the forebrain in the white sturgeon, Acipenser transmontanus. Brain, Behavior and Evolution, 69, 229–253. Plohman, J. C., Dick, T. A., & Eales, J. G. (2002). Thyroid of lake sturgeon, Acipenser fulvescens II. Deiodination properties, distribution, and effects of diet, growth, and a T3 challenge. General and Comparative Endocrinology, 125, 56–66. Power, D. M., Llewellyn, L., Faustino, M., Nowell, M. A., Bjornsson, B. Th., I. E., Einarsdottir., . . . Sweeney, G. E. (2001). Thyroid hormones
AKAYLI
ET AL.
in growth and development of fish. Comparative Biochemistry and Physiology, 130, 447–459. Raine, J. C., & Leatherland, J. F. (2000). Morphological and functional development of the thyroid tissue in rainbow trout (Oncorhynchus mykiss) embryos. Cell Tissue Research, 301(2), 235–244. Ramos-Vara, J. A., Miller, M. A., Johnson, G. C., & Pace, L. W. (2002). Immunohistochemical detection of thyroid transcription factor-1, thyroglobulin, and calcitonin in canine normal, hyperplastic, and neoplastic thyroid gland. Veterinary Pathology, 39(4), 480–487. Roberts, R. J., & Ellis, A. E. (2012). The anatomy and physiology of teleosts. In R. J. Roberts (Ed.), Fish pathology (pp. 1–17). Oxford: WileyBlackwell. Santos, F. C., Silva, J. F., Boeloni, J. N., Teixeira, E., Turra, E. M., & Serakides, R. N. M. (2015). Morphological and immunohistochemical characterization of angiogenic and apoptotic factors and the expression of thyroid receptors in the ovary of tilapia Oreochromis niloticus in captivity. Pesquisa Veterin aria Brasileira, 35(4), 371–376. Tanaka, M., Tanangonan, J. B., Tagawa, M., Jesus, E. G., Nishida, H., Isaka, M., . . . Hirano, T. (1995). Development of the pituitary, thyroid and interrenal glands and applications of endocrinology to the improved rearing of marine fish larvae. Aquaculture, 135, 111–126. Timur, G., Akayli, T., Korun, J., & Yardimci, R. E. (2010). A study on bacterial haemorrhagic septicemia in farmed young Russian sturgeon in Turkey (Acipencer gueldenstaedtii). Istanbul University Journal of Fisheries & Aquatic Sciences, 25(1), 19–27. dez, R., Quiroga, M. I., & Nieto, J. M. (2006). EviVigliano, F. A., Bermu dence for melano-macrophage centers of teleost as evolutionary precursors of germinal centers of higher vertebrates: An immunohistochemical study. Fish and Shellfish Immunology, 21(4), 467–471. Yakovleva, I. V. (1964). Gistogenez shchitovidnoi zhelezy i gipofiza osetra v svyazi s etapami lichinochnogo razvitiya. [Histogenesis of Thyroid Gland and Hypophysis of Sturgeon in Connection with Stages of Larval Developmwnt]. In Problemly sovremennoi embriologii (Problems in Modern Embriology) (pp. 236–242). Moscow: Izd. Mosk. Gos. Yamano, K., Nomura, K., & Tanaka, H. (2007). Development of thyroid gland and changes in thyroid hormone levels in Leptocephali of Japanese Eel (Anguilla japonica). Aquaculture, 270, 499–504.
How to cite this article: Akayli T, Memisß D, Bozkurt ER. A comparative histological study on early thyroid gland development in Acipenser stellatus and A. gueldenstaedtii larvae in hatchery. Aquac Res. 2017;48:5533–5540. https://doi.org/10.1111/are.13374