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Histology of corpuscles of Stannius in fish ( tarichi Güldenstädt, 1814) ()

Article in Anatomia Histologia Embryologia · March 2021 DOI: 10.1111/ahe.12645

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ORIGINAL ARTICLE

Histology of corpuscles of Stannius in Lake Van (Alburnus tarichi Güldenstädt, 1814) (Cyprinidae)

Burak Kaptaner1 | Güler Ünal2 | Emine Doğan3 | Handan Aykut3

1Department of Biology, Faculty of Science, University of Van Yuzuncu Yil, Van, Turkey Abstract 2Department of Child Development, Faculty In the present study, the location, histology and number of corpuscles of Stannius of Healthy Sciences, University of Aydın (Sc), which are endocrine glands associated with the kidneys of teleost fish, were Adnan Menderes, Aydın, Turkey 3Department of Biology, Institute of Natural investigated for the first time in Lake Van fish (Alburnus tarichi), an anadromous and and Applied Sciences, University of Van endemic inhabiting Turkey's Lake Van Basin. The Sc, which were ovoid or spheroid Yuzuncu Yil, Van, Turkey and white or cream in colour, were found to vary in number between three and five Correspondence among the examined fish. The glands were located in the caudal part of the kidney, Burak Kaptaner, University of Van Yuzuncu Yil, Faculty of Science, Department of and either partially or completely embedded, and found to be present on both the Biology, 65080 Tuşba, Van, Turkey. ventral and dorsal surface of either side of the caudal part of the kidney. The Sc were Emails: [email protected]; bkaptaner@ yyu.edu.tr surrounded by a connective tissue capsule that penetrated and divided the gland into incomplete lobules. Two types of cells were determined in the parenchyma of the gland. Type-I cells were predominant throughout the parenchyma and larger than the second (type-II). In the type-I cells, the cytoplasm was observed as weakly or mod- erately eosinophilic with haematoxylin and eosin staining and weakly or moderately acidophilic with Mallory's triple staining. In the type-I cells, the cytoplasm exhibited weak to moderate periodic acid-Schiff staining and slight or uniform staining with aldehyde fuchsin. The type-II cells were round, had a darkly stained spherical nucleus and were dispersed among the type-I cells. They displayed no cytoplasmic staining with the abovementioned stains.

KEYWORDS Alburnus tarichi, corpuscles of Stannius, histology, Lake Van fish

1 | INTRODUCTION and calcium excretion (Butler, 1993), and reduced blood pressure levels (Jones et al. 1966) in fish. Corpuscles of Stannius (Sc) are very small endocrine glands that are The number and anatomical localization of the Sc in the kid- associated with the kidneys in teleostean and holostean fish. They neys may vary among the fish species (Bedjargi & Kulkarni, 2014a; synthesize and secrete a glycoprotein hormone called stannio- Krishnamurthy & Bern, 1969). Although previous ultrastructural calcin, which is involved in the maintenance of calcium and phos- and histological studies reported two different cell types constitut- phate homeostasis via the gills, gut and kidneys (Meats et al., 1978; ing the gland in general (Abu Zinadah et al., 2006; Bhattacharyya Lu et al., 1994; Wagner & Dimattia, 2006). Physiological studies & Butler, 1978; Chakrabarti & Banerjee, 2016; Krishnamurthy & conducted in the past have reported that stanniectomy resulted Bern, 1969; Wendelaar Bonga & Greven, 1975; Wendelaar Bonga in hypercalcemia (Fontaine, 1964), changes in the electrolyte con- et al., 1977; Wendelaar Bonga et al., 1980), only a single type or centrations of the plasma and tissue (Butler, 1969, 1972; Butler & a third type of cell has been reported in the glands of some fish Cadinouche, 1995; Chan et al., 1969), increased renal magnesium species (Ahmad et al., 2002; Bedjargi & Kulkarni, 2014a, 2014b;

404 | © 2020 Wiley-VCH GmbH wileyonlinelibrary.com/journal/ahe Anat Histol Embryol. 2021;50:404–410. KAPTANER et al. | 405

Pinheiro et al., 1987). The staining pattern of the cell types in the staining with haematoxylin and eosin (H&E), Mallory's triple (MT) gland using histological stains, such as periodic acid-Schiff (PAS) and (Crossmon, 1937), PAS and haematoxylin (PAS&H) (Mcmanus, 1948) aldehyde fuchsin (AF) may also differentiate between fish species and modified AF (Halmi, 1952) was conducted. For counterstaining (Krishnamurthy & Bern, 1969). of the sections with AF staining, neutral red was used. Entellan was Lake Van fish (Alburnus tarichi Güldenstädt, 1814) is an anadro- used to mount the preparations, and they were then examined using mous Cyprinid species endemic to Turkey's Lake Van Basin. It inhab- Leica DMI 6000B and DM500 microscopes, and then, photographs its the extreme living environment of Lake Van, which comprises were captured. highly alkaline (total alkalinity of 153 meq/L; pH 9.8) and brackish (total salinity of 0.22%) water. However, the Lake Van fish (A. tari- chi) possesses physiological capabilities that have allowed to adapt 2.3 | Morphometrical analyses and cell counting to the living conditions in lake, which are quite harsh (Danulat & Selcuk, 1992). The Lake Van fish is also an anadromous fish that mi- The diameters of the dissected glands (n = 20) from the fish were grates to freshwater streams to spawn. Apart from its biologically measured on the captured photographs at 200× magnification, using important properties, it is also a commercial species, with an annual imagej 1.46 software (https://imagej.nih.gov/ij/downl​oad.html). The catch of 8,600 tons (Kaptaner & Kankaya, 2013; Sen et al., 2015). To discrimination of the cell types was conducted using to the nucleus– date, no studies regarding the histological organization of Sc in Lake cytoplasm diameter and staining morphology. The cytoplasm and Van fish have been conducted. In the present study, it was aimed to nucleus diameters of the cell types were measured manually, also investigate the localization, number and microscopic anatomy of the using imagej software. For each cell type, a total of 75 cells from 3 gland in this endemic and biologically important species, and learn fish, of both sexes, were used in the cytoplasmic and nuclear diam- how they differed from other fish species. The results, reported for eter measurements. For estimation of the percentage of the cell the first time herein, will contribute to basic knowledge for future types in the parenchyma of the gland, 5 randomly chosen optical 2 studies. areas, each measuring 30,500 µm , with no intersection points in one section, were captured at 630× magnification from the H&E- stained sections of three fish, from both sexes. At least 1,250 cells 2 | MATERIALS AND METHODS from each fish were counted using the cell counter plugin of imagej software, and then, the percentage of each cell type was calculated 2.1 | Fish for both sexes.

In this study, 12 mature Lake Van fish (eight females and four males), with a fork length of 18–20 cm and total weight of between 2.4 | Statistical analyses 80 and 100 g, were examined. The fish used as the study material were caught by professional fishermen during the fishing season spss Statistics for Windows 16.0 (SPSS Inc.) was used to statistically (September 2020), in Lake Van (43°13′E, 38°26′N). The freshly evaluate data from the nucleus–cytoplasm diameter and percentage killed fish under natural circumstances were used for subsequent of cell types in both sexes. Statistical evaluation of the mean differ- histological procedures. In accordance with the regulations stipu- ences between the two groups was performed using the Student lated by the Turkish Ministry of Forestry and Water Affairs, ap- unpaired t test. The results were presented as the mean ± stand- proval for post-mortem tissue usage was not required by the ard deviation. Statistical significance was accepted as p < .05 and Animal Experiments Local Ethics Committee (The Official Gazette p < .001. of Republic of Turkey on 15 February 2014, No: 28914); however, a decision protocol was issued by the Ethics Committee of Van Yuzuncu Yil University (VAN YUHADYEK) under decision number: 3 | RESULTS VAN YUHADYEK–2020/10-01). The Sc located were either partially or completely embedded in the caudal part of the mesonephric kidney (Figure 1a). The glands 2.2 | Histological procedures were small and spheroid or ovoid, and white or cream in colour. They were located on both the ventral and dorsal of the right and Immediately following the death of the fish, the Sc were removed left side of the caudal part of the kidney (Figure 1b,c). The number from the kidneys. Next, Bouin's solution was used to fix the tissues of Sc varied from 3 to 5 among the examined kidneys of the Lake for 24 hr at 4°C. After which, a graduated ethanol series was used Van fish (Figure 1d). The diameter of the gland varied between to dehydrate the tissues, and then, they were embedded in paraf- 0.65 and 1.61 mm (Figure 1d,e), one or two of which were ob- fin. As a next step, tissue sections measuring 5 µm thick were cut served to be larger than the others. There were no differences in and placed onto slides containing an adhesive coating (Marienfeld the number, shape or location of the glands with regard to the sex GmbH). After deparaffinization and rehydration of the tissues, of the fish. 406 | KAPTANER et al.

FIGURE 1 Photographs displaying anatomical locations of the Sc in the kidneys of Lake Van fish. Two Sc, partially embedded in the caudal part of kidney on the ventral surface, are indicated with yellow arrows in (a) and (b). One Sc, located on the dorsal surface of the caudal kidney, can be seen in (c) (yellow arrow). Five Sc are indicated with yellow arrows in the caudal region of the kidney of a Lake Van fish, one of which is larger than the others (d) (a)

(b) (c) (d)

(type-II). Observation of the type-I revealed that they were rounded or polygonal and possessed a slightly basophilic and round nucleus with a conspicuous nucleolus. In the type-I cells, the cytoplasm was determined as weakly or moderately eosinophilic with H&E staining (Figure 3a) and weakly or moderately acidophilic with MT staining (Figure 3b). A similar staining pattern was also observed with PAS staining, where the cells displayed weak to moderate staining in their cytoplasm (Figure 3c). On the other hand, in the cytoplasms of the type-I cells, slight and uniform staining was observed with AF stain- ing (Figure 3d). The type-II cells were round and had a darkly stained spherical nucleus (Figure 3a). The cytoplasms of the cells were not observed as eosinophilic with H&E staining or acidophilic with MT staining (Figure 3b). Moreover, no PAS or AF staining was detected in the cytoplasms of the type-II cells (Figure 3c,d). No histological difference was observed between the sexes in terms of the number and staining pattern of the type-I and type-II cells. FIGURE 2 General view of the histological section of one Sc in The cytoplasmic/nuclear diameter of the type-I and type-II a Lake Van fish that is partially embedded in the caudal part of the cells is shown in Figure 4. The cytoplasmic/nuclear diameter of the kidney (k). The gland is encapsulated by a connective tissue capsule, type-I cells were determined to be significantly to be larger when in which the collagen fibres are stained in blue (arrow). Adipose compared to the type-II cells, in both sexes (p < .001). In the males, tissue (at) can be seen in the junction of the kidney and the gland the cytoplasmic diameters of the type-I and type-II cells were deter- (MT staining) mined as 7.51 ± 1.11 µm and 4.78 ± 0.52 µm, respectively, while the nucleus diameters of the type-I and type-II cells were measured as 4.57 ± 0.49 µm and 3.09 ± 0.23 µm, respectively (Figure 4a). In the The histological examination of the gland showed that it was females, the cytoplasmic diameters of the type-I and type-II cells surrounded by a connective tissue capsule (Figure 2). The fibrous were determined as 7.13 ± 0.91 µm and 4.71 ± 0.47 µm, respectively, connective tissue penetrated and divided the gland into incomplete while the nucleus diameters of the type-I and type-II cells were mea- lobules or smaller lobules (Figure 3a,b). The connective tissue com- sured as 4.55 ± 0.46 µm and 3.16 ± 0.29 µm, respectively (Figure 4b). ponents were observed to be well-stained with MT, PAS and AF On the other hand, the cytoplasmic/nuclear diameters of the same (Figure 3b–d). The gland was richly vascularized, and capillaries or cell type did not show any significant differences among the male sinusoids, including blood cells, were present among the connective and female fish (p > .05). tissue septa extending to the lobes and lobules (Figure 3a,b). Two The type-I cells were predominantly present throughout the types of cells were determined in the parenchyma of the gland. parenchyma of the gland, while the type-II cells were dispersed The first type (type-I) was observed to be larger than the second among the type-I cells in the male and female fish. The percentages KAPTANER et al. | 407

(a) (b)

(c) (d)

FIGURE 3 Representative photomicrographs of the histological sections of the Sc of Lake Van fish with H&E (a), MT (b), PAS&H (c) and AF (d) staining. In (a), some larger type-I cells with weakly or moderately eosinophilic cytoplasma and slightly basophilic nuclei are indicated with black arrows, while some type-II cells that exhibit no eosin staining in their cytoplasma and have dark round nuclei are indicated with yellow arrows. The capillaries, including the erythrocytes, can be seen among the connective tissue septa. In (b), well-stained fibrous connective tissue penetrating and dividing the gland into incomplete lobules are indicated with arrowheads and some acidophilic type-I cells are indicated with black arrows, while type-II cells that exhibit no cytoplasmic staining are indicated by yellow arrows. In (c), type-I cells displaying weak or moderate positive cytoplasmic staining with PAS are indicated by black arrows, while type-II cells exhibiting no cytoplasmic staining are indicated by yellow arrows. The connective tissue septa were stained in deep magenta (arrow). In (d), uniform and slight cytoplasmic staining with AF were observed in the type-I cells (black arrows); however, the type-II cells displayed no cytoplasmic staining with AF (yellow arrows). The connective tissue septa were stained darkly with AF (arrow)

FIGURE 4 Cytoplasmic and nuclear diameters of the type-I and type-II cells in the male (a) and female fish (b). Significant differences (*) were determined among the type-I and type-II cells in terms of the cytoplasmic and nuclear diameters in both sexes (p < .001). No significant changes were observed in the cytoplasmic and nuclear diameters of same cell type among the males and females

of type-I and type-II cells were determined to be 91.94 ± 1.10% and 8.06 ± 1.10, respectively, in the male fish, while they were 4 | DISCUSSION 93.46 ± 0.37% and 6.54 ± 0.37, respectively, in the female fish. The percentages of both cell types did not show any significant differ- The present study comprised the first investigation of the location, ences in either of the sexes (Figure 5). histology and number of Sc in Lake Van fish. The results showed that 408 | KAPTANER et al.

structures, rather than a posterior migration. In a comparative study with 47 fish species, it was suggested that the number and location of the Sc on kidney was associated with the taxonomic position of the fish (Bauchot, 1953). The histological examinations conducted herein displayed that the Sc in the Lake Van fish were surrounded by a thin connective tissue that penetrated and divided the glands into incomplete lobes or smaller lobules. The connective tissue septa were determined to be well-vascularized by capillaries or sinusoids. Similar findings were also reported by other researchers in different fish species (Abu Zinadah et al., 2006; Cohen et al., 1975; Karkit et al., 2019; Krishnamurthy & Bern, 1969). Well vascularization of the parenchyma of the glands might be attributed to the function and activity of the FIGURE 5 Percentages of the type-I and type-II cells in the gland (Jones et al., 1969). According to the morphological and histo- male and female fish. No significant changes were observed in the percentage of either cell type among the males and females chemical staining properties, 2 types of gland cells were described in this study. Predominating type-I cells were larger than the type-II cells and displayed weak or moderate acidophilic, and PAS+ or AF+ 3 to 5 Sc were located on either side of the caudal part of the kid- staining in their cytoplasms, while the cytoplasms of the type-II cells ney, both ventrally and dorsally. Similarly, Sc have been reported to were not stained with those stains. In general, two types of cells be found in the posterior end of the kidney in many teleost species have been observed in the parenchyma of the Sc in different tele- (Abu Zinadah et al., 2006; Bedjargi & Kulkarni, 2014a; Bhattacharyya ost species (Abu Zinadah et al., 2006; Bhattacharyya & Butler, 1978; & Butler, 1978; Cohen et al., 1975; Karkit et al., 2019; Krishnamurthy Chakrabarti & Banerjee, 2016; Karkit et al., 2019; Krishnamurthy & & Bern, 1969; Oguri, 1966; Tomasulo et al., 1970; Wendelaar Bonga Bern, 1969; Wendelaar Bonga & Greven, 1975; Wendelaar Bonga et al., 1977). The number of Sc in adult fish could vary between spe- et al., 1977; Wendelaar Bonga et al., 1980). Staining of the cells of cies, and even among individuals of the same species. Krishnamurthy the Sc with PAS or AF was previously reported in different species and Bern (1969) reported 4–6 Sc in Salmo gairdnerii; from 4 to 5 Sc in (Bedjargi & Kulkarni, 2014b; Krishnamurthy & Bern, 1969; Nadkarni Oncorhynchus tshawytscha; 4 Sc in Oncorhynchus kisutch; 2, 3 or 4 Sc in & Gorbman, 1966; Prasad et al., 2017), and the staining pattern may Atherinopsis californiensis; 3 Sc in Sebastodes auriculatus and Ophiodon have differentiated depending on the fish species. In one such study, elongatus; 1 or 2 in Tilapia mossambica; and 2 Sc in the other exam- the granules were reported to be stained as PAS+/AF+, PAS+/AF− or ined fish, comprising Oncorhynchus nerka, Carrasius auratus, Conger PAS−/AF+, or as 2 distinct types of granules, where one was AF+ and bowersi, Gymnothorax flavimarginatus, Roccus saxatilis, Merluccius pro- PAS−, while the other was PAS+ and AF−, which occurred within indi- ductus, Cymatogaster aggregata, Embiotoca jacksoni, Hyperprosopon vidual Sc cells (Krishnamurthy & Bern, 1969). ellipticum, Scopaenichthys marmoratus, Hysurus caryi, Phanerodon In conclusion, it was determined that 3–5 Sc were located ven- furcatus, Rhacochilus vacca, Gillichthys mirabilis, Hexagrammos deca- trally and dorsally on either side of the caudal part of the kidney. grammus, Artedius notospilotus, Leptocottus armatus, Citharichthys Two types of cells existed in the parenchyma of the gland. Type-I sordidus, Eopsetta jordani and Platichthys stellatus. The number of Sc cells displayed eosinophilic or acidophilic staining with H&E and varied from 6 to 8 in Salmo salar (Bauchot, 1953) and 4–5 in Opsanus MT, respectively, and weak or moderate positive staining with tau (Bhattacharyya & Butler, 1978). In a study comparing the his- PAS and AF, while the type-II cells showed no staining with any of tology of the Sc between freshwater fish (Channa marulius, Channa these stains. Due to being an anadromous fish species, a detailed punctatus, Clarias gariepinus, Labeo rohita, Notopterus notopterus and study is needed to learn how those cells differ in terms of their T. mossambica) and sea water fish (Hemiramphus far, Parastromateus number and staining characteristics in the brackish and highly al- niger, Pampus argenteus, Rastrelliger kanagurta, Scoliodon laticaudus kaline waters of Lake Van and in the connected freshwater river and Sillago sihama), 2 Sc in each examined fish species were reported environments during reproductive migration. Thus, this study will (Bedjargi & Kulkarni, 2014a). In another study, a pair of Sc were ob- provide basic and essential knowledge for studies on this topic served in Oreochromis niloticus and Epinephilus tuvina (Abu Zinadah thought in the future. et al., 2006), N. notopterus (Bedjargi & Kulkarni, 2014b) and C. garie- pinus (Karkit et al., 2019). Garret (1942) proposed a phylogenetic CONFLICT OF INTEREST progression wherein number of organs reduced during the evolution The authors declare that there are no conflicts of interest. of Holostei and Telostei, and the Sc moved to the posterior third of the mesonephros or extreme posterior end of the body cavity, com- DATA AVAILABILITY STATEMENT pletely behind the kidney (in some specialized groups), as a result of The data that support the findings of this study are available from shortening of the body cavity and anterior progression of the visceral the corresponding author upon request. KAPTANER et al. | 409

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