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Morphology of the Air-Breathing Stomach of the Catfish Hypostomus Plecostomus

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Morphology of the Air-Breathing Stomach of the Catfish Hypostomus Plecostomus JOURNAL OF MORPHOLOGY 257:147–163 (2003) Morphology of the Air-Breathing Stomach of the Catfish Hypostomus plecostomus Dagmara Podkowa and Lucyna Goniakowska-Witalin´ ska* Department of Comparative Anatomy, Institute of Zoology, Jagiellonian University, 30-060 Krako´w, Poland ABSTRACT Histological and ultrastructural investiga- round, with a diameter ranging from 88–177 nm, while tions of the stomach of the catfish Hypostomus plecosto- elongated ones, 159–389 nm long, are rare. EC of type III mus show that its structure is different from that typical are numerous and also closed. The whole cytoplasm is of the stomachs of other teleostean fishes: the wall is thin filled with large DCV: round, with a diameter from 123– and transparent, while the mucosal layer is smooth and 283 nm, and oval, 230–371 nm long, both with a core of devoid of folds. The epithelium lining the whole internal irregular shape and a wide, irregular halo. EC are in- surface of the stomach consists of several types of cells, the volved in the regulation of digestion and probably local gas most prominent being flattened respiratory epithelial exchange. In conclusion, the thin-walled stomach of Hy- cells. There are also two types of gastric gland cells, three postomus plecostomus, with its rich network of capillaries, types of endocrine cells (EC), and basal cells. The epithe- has a morphology suggesting it is an efficient organ for air lial layer is underlain by capillaries of a diameter ranging breathing. J. Morphol. 257:147–163, 2003. from 6.1–13.1 ␮m. Capillaries are more numerous in the © 2003 Wiley-Liss, Inc. anterior part of the stomach, where the mean number of capillary sections per 100 ␮m of epithelium length is 4, KEY WORDS: air breathing; stomach; ultrastructure; en- compared with 3 in the posterior part. The cytoplasm of docrine cells; Hypostomus plecostomus the epithelial cells, apart from its typical organelles, con- tains electron-dense and lamellar bodies at different stages of maturation, which form the sites of accumulation of surfactant. Small, electron-dense vesicles containing In water, the gills of fishes are the main gas ex- acidic mucopolysaccharides are found in the apical parts change organ. The amount of oxygen dissolved in of some respiratory epithelial cells. Numerous gastric water fluctuates continuously. The oxygen concen- glands (2 glands per 100 ␮m of epithelium length), com- tration in water varies, especially in tropical areas, posed of two types of pyramidal cells, extend from the where the elevated water temperature reduces oxy- surface epithelium into the subjacent lamina propria. The gen solubility. Shallow, stagnant waters, swamps, gland outlets, as well as the apical cytoplasm of the cells and waters which dry up seasonally are habitats are Alcian blue-positive, indicating the presence of acidic mucopolysaccharides. Zymogen granules have not been characterized by low oxygen levels. In tropical wa- found, but the apical parts of cells contain vesicles of ters there are no vertical currents, which are vital variable electron density. The cytoplasm of the gastric for the transport of dissolved oxygen to lower gland cells also contains numerous electron-dense and depths. In hypoxic (oxygen deficient) environments, lamellar bodies. Gastric gland cells with electron-dense gills are not sufficient for gaseous exchange and cytoplasm and tubulovesicular system are probably in- several fish species additionally take up oxygen di- volved in the production of hydrochloric acid. Fixation rectly from the atmosphere through well- with tannic acid as well as with ruthenium red revealed a vascularized accessory respiratory organs (Graham, thin layer of phospholipids and glycosaminoglycans cover- 1997). ing the entire inner surface of the stomach. In regions of the epithelium where the capillaries are covered by the Among 430 families of teleostean fishes, accessory thin cytoplasmic sheets of the respiratory epithelial cells, respiratory organs have evolved in 42 families and a thin air–blood barrier (0.25–2.02 ␮m) is formed, thus in more than 350 species (Graham, 1997). There is a enabling gaseous exchange. Relatively numerous pores great diversity in the structure of these organs: closed by diaphragms are seen in the endothelium lining the apical and lateral parts of the capillaries. Between gastric gland cells, solitary, noninnervated endocrine cells (EC) of three types were found. EC are characterized by Contract grant sponsor: the State Committee for Scientific Re- lighter cytoplasm than the surrounding cells and they search (KBN); Contract grant number: DS/14/IZ/2001. contain dense core vesicles (DCV) with a halo between the electron-dense core and the limiting membrane. EC of *Correspondence to: Lucyna Goniakowska-Witalin´ ska, Department of Comparative Anatomy, Institute of Zoology, Jagiellonian Univer- type I are the most abundant. They are of an open type, sity, R. Ingardena 6, 30-060 Krako´w, Poland. reaching the stomach lumen. The round DCV of this type, E-mail: [email protected] with a diameter from 92–194 nm, have a centrally located core surrounded by a narrow halo. EC of type II are rarely observed and are of a closed type. They possess two kinds of DCV with a very narrow halo. The majority of them are DOI: 10.1002/jmor.10102 © 2003 WILEY-LISS, INC. 148 D. PODKOWA AND L. GONIAKOWSKA-WITALIN´ SKA finger-like protrusions of the mucosal layer in The catfish Hypostomus plecostomus, from the branchial chambers; paired air sacs extending from family Loricariidae, is a bottom-dweller which branchial chambers; the labyrinth — folded mucosa reaches more than 30 cm in length. The native range of suprabranchial chambers (Munshi and Hughes, of the genus Hypostomus extends from the Rio de la 1992); well-vascularized epithelium lining the buc- Plata system throughout Panama and Costa Rica. copharynx (Singh et al., 1991); as well as various This catfish swims to the surface of the water and types of airbladders (Liem, 1989; Podkowa and gulps air, which is then stored in the stomach (Cart- Goniakowska-Witalin´ ska, 1998). Some parts of the er, 1935; Armbruster, 1998). Behavioral and physi- digestive tract can also be used for gas exchange. In ological studies (Gee, 1976) showed that H. plecos- Dalia pectoralis (Umbriidae) (Crawford, 1974), this tomus initiates air-breathing at low water oxygen function is served by the posterior part of the esoph- tensions. The detailed physiological examination agus. Among catfishes, there are two families of carried out by Graham and Baird (1982) confirmed bottom-dwellers inhabiting South American fresh- that the catfish uses gills for gaseous exchange, but waters that have digestive tracts modified for air is a facultative air breather. breathing. Many genera from the family Loricari- In the light of the foregoing physiological re- idae, including Ancistrus, Chaetostoma, Hyposto- search, it seemed interesting to examine the histol- mus, Liposarcus, Loricaria, Loricariichthys, Rhinel- ogy and ultrastructure of the stomach of the catfish epis, Rhineloricaria, Pogonopoma, Pogonopomoides, Hypostomus plecostomus to check whether its struc- Pterygoplichthys, and Sturisoma, have evolved mod- ture is modified for air breathing. ifications of the stomach which enable its usage as an accessory respiratory organ (Carter and Beadle, MATERIALS AND METHODS 1931; Gradwell, 1971; Gee, 1976; Silva et al., 1997; Armbruster, 1998; Satora, 1998; Takasusuki et al., Five young specimens of the catfish Hypostomus plecostomus, 1998; Oliveira et al., 2001). Pygidium (Armbruster, 1.7–2.7 g, were used for the observations. They were obtained from a local pet shop. Prior to the experiment the fishes were kept 1998) and Eremophilus mutisii (Cala, 1987) of the in an aquarium at 23–25°C for 3 weeks and fed with Tetramin, a family Trichomycteridae also use the digestive tract tropical fish food. The specimens were previously anesthetized in in respiration. 0.1% MS 222 (3-amino-benzoin acid ethyl ester), killed by decap- The posterior intestine is used for gas exchange by itation, and their stomachs were removed by dissection. some catfishes belonging to the Callichthyidae, e.g., Hoplosternum thoracatum (Huebner and Chee, Light Microscopy (LM) 1978), Corydoras aeneus (Kramer and McClure, 1980; Podkowa and Goniakowska-Witalin´ ska, Stomachs from two specimens were immersed in Bouin’s fixa- tive for 24 h, dehydrated in ethanol, and embedded in paraffin. 2002), and Brochis splendens (Gee and Graham, Sections 6 ␮m thick were stained routinely with hematoxylin/ 1978). Some species of Cobitidae also use the poste- eosin and with Passini stain (Goniakowska-Witalin´ ska and Ku- rior intestine for air breathing, including Misgurnus biczek, 1998). Histochemical studies were performed by the peri- fossilis (Jasin´ ski, 1973), Lepidocephalus guntea (Ya- odic acid Schiff (PAS) reaction for neutral mucopolysaccharides and by Alcian blue staining at pH 2.5 for acidic mucopolysaccha- dav and Singh, 1980), and M. anguilicaudatus (Mc- rides (Kiernan, 1990). Mahon and Burggren, 1987). Although several physiological and behavioral studies concerning respiration in air-breathing spe- Transmission Electron Microscopy (TEM) cies have been made, only a few reports have dealt The stomachs were fixed with bubbles of air in their lumen. with the histology and ultrastructure of accessory After1hoffixation the stomachs were cut into pieces and fixed respiratory organs in the digestive tract. Histologi- for a further hour. One stomach was fixed in an isoosmotic solu- cal studies
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