Morphology of the digestive tract of the Whitemouth

Acta Zoologica (Stockholm)

doi: 10.1111/azo.12156

Morphology of the digestive tract of the Whitemouth croaker Micropogonias furnieri (Desmarest, 1823) (Perciformes: Sciaenidae) Isabel M. Andrade,1 Juliana P. Guimar~aes,2 Matheus M. Rotundo3 and Renata B. Mari1

1

Marine Animal Morphology Laboratory at Universidade Estadual Paulista “J ulio de Mesquita Filho” – Campus Experimental Litoral Paulista, Pracßa Dom Infante, s/no, 11330-900, S~ao Vicente, S~ao Paulo, Brazil; 2Graduate Studies Program in Coastal and Marine Ecosystem Sustainability, Universidade Santa Cecılia, R. Oswaldo Cruz, 266, 11045-907, Santos, S~ao Paulo, Brazil; 3Zoology Collection at Universidade Santa Cecılia, R. Oswaldo Cruz, 266, 11045-907, Santos, S~ao Paulo, Brazil Keywords: Teleostean fish, sexual maturation, gastrointestinal system, morphology Accepted for publication: 30 November 2015

Abstract Andrade, I.M., Guimar~aes, J.P., Rotundo, M.M., Mari, R.B. 2016. Effect of gonad maturation on the morphology of the digestive tract of the Whitemouth croaker Micropogonias furnieri (Desmarest, 1823) (Perciformes: Sciaenidae). — Acta Zoologica (Stockholm) 00: 000–000.

Studies have shown the feeding diversity of teleostean fish, which is conditioned by environmental characteristics or the biology of the different species. Analysis on the morphology of the digestive system (DS) of fish made it possible for researchers to know the food regimen of several species at different stages of life. On the other hand, it is known that food habits may lead to morphological changes in the DS the same way that different food habits may be imposed by morphological limitations of this system. Among the species of greater commercial importance in Brazil, Micropogonias furnieri is highly representative of fish in south-eastern Brazil. Therefore, the objective of this study was to analyse the morphology of the DS of M. furnieri. Results on the morphology of the DS observed in this study were similar to the patterns determined for the morphology of teleostean fish. In this study, it was observed that the DS of the Whitemouth croaker is directly related with the shape of the peritoneal cavity; these fish showed oesophagus, stomach, pyloric caeca and intestines. The pyloric caeca showed morphological adaptations in relation to sexual maturation, with well-developed caeca found in sexually mature animals. Renata de Britto Mari, Marine Animal Morphology Laboratory at Biosciences Institute, S~ao Paulo State University - UNESP, Coastal Campus, Pracßa Infante Dom Henrique, s/no, 11330-900, S~ao Vicente, S~ao Paulo, Brazil. E-mail: [email protected]

Introduction Fish are the most numerous vertebrates and inhabit different aquatic ecosystems to which few species are able to adapt. A consistent approach to the evaluation of interactive processes in aquatic communities is the knowledge on the diet of these animals, whose feeding range may be influenced by both environmental conditions and individual species biology (Winemiller 1989; Hahn et al. 1997). Studies on trophic ecology revealed considerable feeding versatility of teleostean fish throughout their development, not only among different species, but also among individuals of the same species (Abelha et al. 2001). During the evolutionary process and according to feeding habits, fish developed unique mechanisms to feed and survive, © 2016 The Royal Swedish Academy of Sciences

which are demonstrated by the presence of digestive system (DS) changes or adaptations of the feeding behaviour (Dzhumaliyev 1982; Snorrason et al. 1994; Fanta et al. 2001). Therefore, morphological limitations may impose feeding behaviours to fish. Most of the fish have a simple and undifferentiated DS at the beginning of their larval stage. Later on, digestive organs develop. Structural changes in the DS that take place throughout fish development characterize different functional adaptations to the diets and to the availability of prey (Govoni et al. 1986). Functional changes in digestion, absorption and assimilation of chemical compounds also follow the development of the fish (Dabrowski 1984). Studies on the DS of fish and the respective relationship with feeding habits have enabled researchers to know the food 1

Digestive tract of the Whitemouth croaker Mari et al.

regimen of several species based on proven morphological and functional characteristics of the DS of herbivores, carnivores and omnivores. The most prominent differences are found in the stomach and intestines (Castagnolli 1979). The morphological variations produced by environmental factors on the organism may be permanent, produced by phylogenetic changes, as occurs in adaptations, or may be temporary, produced by the individual ontogenetic cycle and, in these cases, they are called modifications. Therefore, it is of fundamental importance to know the biology of the species and, in particular, the connection between these factors to better understand species performance both in natural ecosystems and in fish farms (Fugi and Hahn 1991; Seixas-Filho et al. 2001). The DS of fish, besides digestive and absorptive processes in its different portions, may have some organs specialized in other functions (Silva et al. 2005), as it was observed, for instance, in the stomach of some species of Loricadidae and in the intestine of Hoplosternum littorale. In this latter fish, besides the digestive function, intestines are involved in the respiratory process (Giamas et al. 2000). In general, fish DS has the classical stratigraphic organization of tubular organs of other vertebrate species. However, the macro- and microscopic structures of the different portions of the DS show, in a very precise way, the nature of the food and the way it is ingested (Moraes and Barbola 1995), justifying, thus, the morphological changes found from the oesophagus to the distal intestine that differentiate these structures from classical descriptions of the DS of other vertebrates. Considering the wide diversity of fish species and the consequent morphological and physiological differentiation, fish nutrition became a wide field of study due to the diverse habits and feeding behaviours. In spite of the studies in the area that accumulate decades of knowledge, many trials are being carried out to relate morphological characteristics of fish DS with feeding habits and behaviours, which may enable inferences related to commercially valuable species in Brazil. Therefore, the objective of this study was to describe the morphological characteristics of the DS of the Whitemouth croaker Micropogonias furnieri, as it is a commercially important species in Brazil and represents a significant proportion of the fish in the southern and south-western seaside of Brazil (Brazil 1981; Carneiro et al. 2005; Seriani et al. 2010; Fischer et al. 2011). Material and Methods Fifty-five specimens of the Whitemouth croaker obtained in commercial fishing activities in the coastal area of the Baixada Santista, S~ao Paulo, Brazil, were used. After fish were collected, they were sent to the Marine Animal Morphology Laboratory at Universidade Estadual Paulista to be analysed. All animals were classified according to their gonadal development stage as immature, maturing and mature 2

Acta Zoologica (Stockholm) 0: 1–8 (February 2016)

(Haimovici 1977; Isaac-Nahum and Vazzoler 1983). Animals were considered immature when their gonads were small, thin, almost colourless and located close to the spine. Maturating species showed larger gonads that were whitish in males and yellowish in female, and took at least a third of the peritoneal cavity. Mature gonads were well developed and took most of the peritoneal cavity. After this classification, topographic and macroscopic description of the DS in situ was carried out. Samples of all DS portions were collected, fixed in 10% formaldehyde and processed to be analysed under light microscopy. After that, samples were included in Paraplastâ (Sigma-Aldrichâ, St. Louis, MO, USA), and 5-lm thick sections were cut and stained by haematoxylin–eosin (HE). Results A total of 55 Whitemouth croakers were analysed. Gonadal development analysis yielded the following results: 30 specimens were immature, with mean total length of 184.69 16.07 cm, and 25 animals were maturing or mature, with mean total length of 266.44 15.22 cm. From the immature fish (30 specimens), 21 were males and nine were females, and among the maturing and mature fish (25 individuals), 12 were males and nine were females. In all M. furnieri individuals analysed, DS organs followed the shape of the peritoneal cavity. In the anterior third of the peritoneal cavity, the anterior intestine, pyloric caeca and second intestinal loop were observed. The anterior intestine was composed by oesophagus and stomach, which were delimited by a little developed cardiac sphincter. The stomach was U-shaped with the mucosa showing longitudinal folds throughout its length (Fig. 1A,B, and C). In the junction between the distal portion of the stomach and the proximal portion of the intestine, a well-developed pyloric sphincter was observed with the presence of pyloric caeca (Fig. 1B,D, and E) that varied in size in both mature and immature fish. Pyloric caeca in M. furnieri were tubular and shaped as cul-de-sacs. In average, ten of them opened to the pyloric region, in the transition of the first intestinal portion. The average number of caeca was constant in all specimens, no matter sexual maturity. However, in animals that were not mature, regardless of sex, the caeca were short (Fig. 1B) with the same length and thickness, arranged in a radial fashion, without going beyond the stomach. In specimens whose gonads were maturating or mature, no matter the sex, it was observed that one of the pyloric caeca was developed and covered the other ones, the stomach, and sometimes, the second intestinal loop, in the shape of a purse. From this larger caecum, there were ramifications of different sizes and numbers (Fig. 1D,E). The medium intestine started caudally after the pyloric sphincter, until it reached the first intestinal loop. In none of the specimens, it reached the gonad region, and it delimited the first intestinal segment. After the first loop, the medium © 2016 The Royal Swedish Academy of Sciences


Mari et al. Digestive tract of the Whitemouth croaker

A

B

C

D

E

Fig. 1——A. Adult Micropogonias furnieri in

ventral view with open peritoneal cavity showing the arrangement of the digestive tract organs. —B. Gastrointestinal tract of juvenile specimen of M. furnieri. —C. Gastrointestinal tract of adult specimen of M. furnieri, showing the two bowel loops (*).—D. Bag formed by the pyloric caeca in sexually mature specimen. —E. Open bag formed by caecum, showing the stomach (and) which was involved by the bag. c, pyloric caeca; f, liver; g, gonads; e, stomach; 1s, first intestinal segment; 2s, second intestinal segment; 3s, third intestinal segment.

© 2016 The Royal Swedish Academy of Sciences

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intestine was located caudally until it formed the second intestinal loop, following a straight path caudally (the third intestinal segment). No sphincter or ileorectal valve was observed, indicating absence of a posterior intestine (Fig. 1A, B and C). The histological analysis of the DS of M. furnieri showed the basic four-layered stratigraphy characteristic of tubular organs: mucosa, submucosa, muscularis externa and serosa (Fig. 2). The mucosa of the digestive tract was made up of simple columnar epithelium without the muscularis mucosa, throughout the digestive tract. In the stomach, the mucosa was made up by longitudinal folds, with the presence of cardiac and fundus glands, and gastric pits throughout the organ. In the caeca and intestinal segments, the mucosa was projected in villi, with the presence of mucus-secreting cells only in the intestine. The submucosa presented dense connective tissue, with blood vessels and mucus glands. The muscularis externa presented a circular (internal) and a longitudinal (external) muscle layer. Nervous cells that were part of the mioenteric nervous plexus were spread between these layers. Discussion External morphology, such as the shape of the body and mouth, and the length of the gastrointestinal tract, is strongly related to the type of feeding habits (Cailliet et al. 1996; Wootton 1998). This is evidenced in M. furnieri, which has a laterally compressed body and a mouth that is turned downwards, favouring the feeding behaviour of the species in the benthonic habitat. There is a strong correlation between the A


organization of the organs in the DS and the size and shape of the peritoneal cavity, a pattern that was observed in the Whitemouth croaker and described in other teleostean species, as well (Suyehiro 1942). It was possible to observe, in their respective regions, the oesophagus, stomach, pyloric caeca and intestine with two loops in the peritoneal cavity. In M. furnieri, the oesophagus was short, a characteristic that was also observed in other Telesostei, such as in the carnivore species Hoplias malabaricus, and in some carnivore Characiforms (Menin and Mimura, 1993; Amaral, 1990). This finding is different from what was observed in other carnivore species, such as Gymnotus carapo, which has a long stomach (Menin, 1989). The stomach is absent in many teleostean families, such as Cyprinidae, Labridae, Gobiidae, Scaridae, Cyprinodontidae and some Poeciliidae (Genten et al., 2009). When it is found, this organ may present a wide variety of shapes, such as M. furnieri that presents a U-shaped fundus-type stomach, as reported by Pessoa et al. (2013) in Hypostomus pusarum. Different from this description, the same study reported a straight stomach in H. malabaricus. The U-shaped fundus-type stomach is classified as an adapted stomach for debris-eating fish (Suyehiro 1942; Moraes et al., 1997), whereas the straight stomach may be related with the ability to store prey (Moraes and Barbola 1995). A Y-shaped, caecum-type stomach was reported in teleostean fish, making it adapted to the ingestion of whole prey, such as in Salminus brasiliensis (Rodrigues and Menin 2008). Studies have associated the stomach with feeding habits of the species, and this organ may be shaped differently according to the diet (Verma et al., 1974). On the other hand, Rios B

Fig. 2—Light microscopy of the stomach of

C

4

D

Micropogonias furnieri. —A. Showing the mucosa (M), lamina propria (LP) and muscular layer (ML). Haematoxylin–eosin HE —B. It is possible to observe the mucosa (M), the lamina propria (LP) and muscular layer (ML). Picrosirius Red —C. In the mucosa (M), it is possible to distinguish gastric pit (arrowhead) and the gastric glands (arrow) is also evident the submucosa (SM). HE —D. Light microscopy of the pyloric caecum of M. furnieri is possible to observe the mucosa (M), the submucosa (SM) and muscular layer (ML). Light microscopy of the intestine of M. furnieri. HE E. Showing the mucosa (M), lamina propria (LP), submucosa (SM) and muscular layer (ML). HE. F. Evidencing the mucosa (M), the submucosa (SM), circular muscle (CM), longitudinal muscle (LM) and myenteric plexus (arrowhead). HE. © 2016 The Royal Swedish Academy of Sciences


intestine was located caudally until it formed the second intestinal loop, following a straight path caudally (the third intestinal segment). No sphincter or ileorectal valve was observed, indicating absence of a posterior intestine (Fig. 1A, B and C). The histological analysis of the DS of M. furnieri showed the basic four-layered stratigraphy characteristic of tubular organs: mucosa, submucosa, muscularis externa and serosa (Fig. 2). The mucosa of the digestive tract was made up of simple columnar epithelium without the muscularis mucosa, throughout the digestive tract. In the stomach, the mucosa was made up by longitudinal folds, with the presence of cardiac and fundus glands, and gastric pits throughout the organ. In the caeca and intestinal segments, the mucosa was projected in villi, with the presence of mucus-secreting cells only in the intestine. The submucosa presented dense connective tissue, with blood vessels and mucus glands. The muscularis externa presented a circular (internal) and a longitudinal (external) muscle layer. Nervous cells that were part of the mioenteric nervous plexus were spread between these layers. Discussion External morphology, such as the shape of the body and mouth, and the length of the gastrointestinal tract, is strongly related to the type of feeding habits (Cailliet et al. 1996; Wootton 1998). This is evidenced in M. furnieri, which has a laterally compressed body and a mouth that is turned downwards, favouring the feeding behaviour of the species in the benthonic habitat. There is a strong correlation between the A


organization of the organs in the DS and the size and shape of the peritoneal cavity, a pattern that was observed in the Whitemouth croaker and described in other teleostean species, as well (Suyehiro 1942). It was possible to observe, in their respective regions, the oesophagus, stomach, pyloric caeca and intestine with two loops in the peritoneal cavity. In M. furnieri, the oesophagus was short, a characteristic that was also observed in other Telesostei, such as in the carnivore species Hoplias malabaricus, and in some carnivore Characiforms (Menin and Mimura, 1993; Amaral, 1990). This finding is different from what was observed in other carnivore species, such as Gymnotus carapo, which has a long stomach (Menin, 1989). The stomach is absent in many teleostean families, such as Cyprinidae, Labridae, Gobiidae, Scaridae, Cyprinodontidae and some Poeciliidae (Genten et al., 2009). When it is found, this organ may present a wide variety of shapes, such as M. furnieri that presents a U-shaped fundus-type stomach, as reported by Pessoa et al. (2013) in Hypostomus pusarum. Different from this description, the same study reported a straight stomach in H. malabaricus. The U-shaped fundus-type stomach is classified as an adapted stomach for debris-eating fish (Suyehiro 1942; Moraes et al., 1997), whereas the straight stomach may be related with the ability to store prey (Moraes and Barbola 1995). A Y-shaped, caecum-type stomach was reported in teleostean fish, making it adapted to the ingestion of whole prey, such as in Salminus brasiliensis (Rodrigues and Menin 2008). Studies have associated the stomach with feeding habits of the species, and this organ may be shaped differently according to the diet (Verma et al., 1974). On the other hand, Rios B

Fig. 2—Light microscopy of the stomach of

C

4

D

Micropogonias furnieri. —A. Showing the mucosa (M), lamina propria (LP) and muscular layer (ML). Haematoxylin–eosin HE —B. It is possible to observe the mucosa (M), the lamina propria (LP) and muscular layer (ML). Picrosirius Red —C. In the mucosa (M), it is possible to distinguish gastric pit (arrowhead) and the gastric glands (arrow) is also evident the submucosa (SM). HE —D. Light microscopy of the pyloric caecum of M. furnieri is possible to observe the mucosa (M), the submucosa (SM) and muscular layer (ML). Light microscopy of the intestine of M. furnieri. HE E. Showing the mucosa (M), lamina propria (LP), submucosa (SM) and muscular layer (ML). HE. F. Evidencing the mucosa (M), the submucosa (SM), circular muscle (CM), longitudinal muscle (LM) and myenteric plexus (arrowhead). HE. © 2016 The Royal Swedish Academy of Sciences


Sardi~ na and Cazorla 2005; Mendoza-Carranza and Vieira 2008; Bertran et al. 2013; Olsson et al. 2013). This ontogenetic change in the diet may be given by the availability of food, changes in the position of the water column, or by morphological changes, such as migration of the mouth, and increased number of barbells and sensory pores (Goncßalves 1997; Mendoza-Carranza and Vieira 2008; Bertran et al. 2013). These definitions are similar to the morphology reported here for the gastrointestinal tract of M. furneri, whose adaptations in length, mucosa projections, and presence of caeca show a carnivore diet. The agreement between the results presented here and the studies on the Whitemouth croaker feeding habits reinforce the important connection between studies of species morphology and behaviour. References Abelha, M. C. F., Agostinho, A. A. and Goulart, E. 2001. Plasticidade tr ofica em peixes de agua doce. – Acta Scientiarum - Biological Sciences 23: 425–434. Alves, M. I. M. and Tome, G. S. 1966. Anatomia e histologia do tubo digestivo da cavala Scomberomorus cavalla (Cuvier, 1829). – ~o de Biologia Marinha 6: 103–108. Arquivos da Estacßa Amaral, A. A. 1990. Anatomia comparativa do aparelho digest orio de Acestrorhynchus britskii Menezes, 1969 e Acestrorhynchus lacustris (Reinhardt, 1874) (Pisces, Characidae, Acestrorhynchidae). – Revista Ceres 37: 277–288. Bertran, C., Jimenez, C., Fierro, P., Pe~ na-Cortes, F., Tapia, J., Hauenstein, E. and Vargas-Chacoff, L. 2013. Alimentaci on de Micropogonias furnieri (Osteichthyes: Sciaenidae) en el lago costero Budi, Sur de Chile. – Revista de biologıa marina y oceanografıa 48: 193–197. Bicca, D. F., Querol, E. and Braccini, M. C. 2006. Aspectos morfol ogicos e histol ogicos do est^ omago de Acestrorhynchus pantaneiro (Menezes, 1992) (Teleostei, Acestrorhynchidae) na bacia do rio Uruguai medio. – Biodiversidade Pampeana 4: 5–10. Brazil, 1981. Ministerio da Agricultura. Laborat orio Nacional de Referência Animal. Metodos analıticos oficiais para controle de produtos de origem Animal e seus Ingredientes, Vol 2, Ministerio da Agricultura, Brasılia, cap.11. Buddington, R. K. and Diamond, J. 1986. Pyloric caeca of fish: a ‘new’ absorptive organ. – American Journal of Physiology 15: G65– G67. Cailliet, G. M., Love, M. S. and Ebeling, A. W. 1996. Fishes: A Field and Laboratory Manual on Their Structure, Identification and Natural History. Waveland, Long Grove. Carneiro, M. H., Castro, P. M. G., Tutui, S. L. S. and Bastos, G. C. C. 2005. Micropogonias furnieri (Desmarest, 1823). Estoque Sud este. In: Cergole, M. C., Avila-da-Silva, A. O. and Rossiwongtschowski, C. L. B. (Eds): Analise das Principais Pescarias Comerciais da Regi~ao Sudeste-Sul do Brasil: Dinâmica Populacional das Especies em Explotacß~ao, pp. 94–100. Serie Documentos REVIZEE, Score Sul, S~ao Paulo, Instituto Oceanografico da Universidade de S~ao Paulo. Castagnolli, N.. 1979. Fundamentos de nutricß~ao de peixes. Piracicaba, Livroceres, pp. 13. Chanet, B., Guintard, C., Boisgard, T., Fusellier, M., Tavernier, C., Betti, E. and Lecointre, G. 2012. Visceral anatomy of ocean sunfish (Mola mola (L., 1758), Molidae, Tetraodontiformes) and angler (Lophius piscatorius (L., 1758), Lophiidae, Lophiiformes) investi-

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Mari et al. Digestive tract of the Whitemouth croaker

Ortêncio-Filho, H., Hahn, N. S., Fugi, R. and Russo, M. R. 2001. Aspectos da alimentacß~ao de Glanidium ribeiroi (Haseman, 1911) (Teleostei, Auchenipteridae), especie endêmica do rio Iguacßu, PR. – Acta Limnologica Brasiliensia 13: 85–92. Pessoa, E. K. R., Da Silva, N. B., Chellappa, N. T., De Souza, A. A. and Chellappa, S. 2013. Morfologia comparativa do trato digest orio dos peixes Hoplias malabaricus e Hypostomus pusarum do acßude Marechal Dutra, Rio Grande do Norte, Brasil. – Biota Amazonica 3: 48–57. Raji, A. R. and Norouzi, E. 2010. Histological and histochemical study on the alimentary canal in walking catfish (Claris batrachus) and piranha (Serrasalmus nattereri). – Iranian Journal of Veterinary Research 11: 255–261. Rios, F. S., Kalinin, A. L., Fernandes, M. N. and Rantin, F. T. 2004. Changes in gut gross morphology of traıra, Hoplias malabaricus (TELEOSTEI, ERYTHRINIDAE) during long-term starvation and after refeeding. – Brazilian Journal of Biology 64: 683–689. Rodrigues, S. S. N. and Menin, E. 2008. Anatomia do tubo digest orio de Leporinus macrocephalus (Characiformes, Anostomidae) em relacß~ao a seu habitar alimentar. – Bioscience Journal 24: 86–95. Sardi~ na, P. and Cazorla, A. L. 2005. Feeding interrelationships and comparative morphology of two young sciaenids co-occurring in South-western Atlantic waters. – Hydrobiologia 548: 41–49. Seixas-Filho, J. T., Bras, J. M., Gomide, A. T. M., Oliveira, M. G. A., Donzele, J. L. and Menin, E. 2001. Anatomia Funcional e Mor fometria do Intestino no Teleostei (Pisces) de Agua Doce Surubim (Pseudoplatystoma coruscans - Agassiz, 1829). – Revista Brasileira de Zootecnia 30: 1670–1680. Seriani, R., Moreira, L. B., Abessa, D. M. E., Abujamara, L. D., Carvalho, N. S. B., Maranho, L. A., Kirschbaum, A. A. and Ranzani-Paiva, M. J. T. 2010. Hematological Analysis of Micropogonias furnieri, Desmarest, 1823, Scianidae, from two estuaries of baixada santista, S~ao Paulo, Brazil. – Brazilian Journal of Oceanography 58: 87–92. Silva, N. B., Gurgel, H. C. B. and Santana, M. D. 2005. Histologia do sistema digest orio de sag€ uiru, Stendachnerina notanota (Miranda Ribeiro, 1937) (Pisces, Curimatidae), do rio Ceara Mirim, Rio Grande do Norte, Brasil. – Boletim do Instituto de Pesca 31: 1–8. Sis, R. F., Ives, P. J., Jones, D. M., Lewis, D. H. and Haensly, W. E. 1979. The microscopic anatomy of the esophagus, stomach and intestine of channel catfish, Ictalurus punctatus. – Journal of Fish Biology 14: 179–186. Snorrason, S. S., Sk ulasons, S., Jonsson, B., Malmquist, H. J., J onasson, P. M., Sandlund, O. T. and Lindem, T. 1994. Trophic specialization in Arctic char Salvelinus alpinus (Pisces; Salmonidae): Morphological divergence and ontogenetic niche shifts. – Biological Journal of the Linnean Society 52: 1–18. Soares, L. S. H. and Vazzoler, A. D. M. 2001. Diel changes in food and feeding activity of sciaenid fishes from the South-western Atlantic, Brazil. – Revista Brasileira de Biologia 61: 197–216. Sodelin, M., Madsen, S. S., Blenstrup, H. and Tipsmark, C. 2000. Time-course changes in the expression of Na+, K+ -ATPase in gills and pyloric caeca of brown trout (Salmo trutta) during acclimation to seawater. – Physiological and Biochemical Zoology 73: 446–453. Suyehiro, Y. A. 1942. A study of the digestive system and feeding habits of fish. – Japanese Journal Zoology 10: 1–303. Takiue, S. and Akiyoshi, H. 2013. Light and scanning electron microscope examination of the digestive tract in peppered moray, Gymnothorax pictus (Elopomorpha). – The Anatomical Record 296: 443–451. Vazzoler, A. E. A. M. 1991. Sıntese de conhecimentos sobre a biologia da corvina, Micropogonias furnieri (Desmarest,1823), da costa do Brasil. – Atl^ antica 13: 55–74.

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