- Email: [email protected]
LM and SEM study on the swordfish (Xiphias gladius) tongue
Tissue and Cell xxx (xxxx) xxx–xxx
Contents lists available at ScienceDirect
Tissue and Cell journal homepage: www.elsevier.com/locate/tice
LM and SEM study on the swordfish (Xiphias gladius) tongue ⁎
Francesco Abbate , Maria Cristina Guerrera, Mauro Cavallaro, Giuseppe Montalbano, Antonino Germanà, Maria Levanti Department of Veterinary Sciences, University of Messina, Italy
A R T I C L E I N F O
A B S T R A C T
Keywords: Tongue Fish Scanning electron microscopy Light microscopy
Swordfish (Xiphias gladius L. 1758) is a predatory and migratory fish. Its characteristic feature is a flat and sharp upper jaw forming a “sword”. The adaptation of vertebrates, including fish, to their environment is strictly related to the capacity of feeding and is carried out by often severe modifications of the anatomy of the buccal cavity, especially of the tongue. The aim of this study is, using light and scanning electron microscopy and considering that no data are so far available about the morphology of the tongue in this species, to analyse the anatomical characteristics of the tongue, especially its dorsal surface. The tongue shows a triangular shape and an apex, a body and a root. By SEM the presence of several small denticles and filiform papillae on the lateroventral body was demonstrated while no taste buds or other sensitive structures are observed. LM shows a squamous stratified epithelium, becoming simple cuboidal around the denticles. Therefore this study could add further data to the knowledges of the fish oral cavity morphology supporting the hypothesis that the modifications and evolution of the tongue anatomy are, also in fish, related to the environment and especially to the feeding habits.
1. Introduction Swordfish (Xiphias gladius L. 1758) is a horizontally migrating pandemic fish distributed through tropical and temperate parts of the Atlantic, Pacific, and Indian Oceans (IUCN, 2011). It’s depth distribution ranges from near the surface to a depth of 550 m (Collette et al., 2011). The Mediterranean swordfish populations constitute a unique stock, distinct from the Atlantic ones with different growth and maturity characteristics (Tsimenides and Tserpes, 1989; Tserpes and Tsimenides, 1995). The fish is an extremely versatile predator characterized by a long, flat rostrum and capable of exploiting various trophic resources. It predates mainly pelagic fishes especially at the juvenile stage, later, as adult predates crustaceans and cephalopods. Its best-known feature is the great development of the upper jaw which forms the typical flat and sharp “sword”, long about 1/3 of the body. The lower jaw is elongated and pointed, but has a much shorter length compared to the upper one (Tortonese, 1975; Peristeraki et al., 2005). The ethology of the predation in this species is poorly described considering that, being a cosmopolitan, solitary and aggressive predator, it is quite difficult to make observations regarding its behaviour. The peculiar aspect of the upper jaw impressively affects the predatory techniques. In fact, the animal uses the long rostrum as an instrument of aggression to stun the prey and then swallowing them whole
⁎
(Tortonese, 1975). This second stage of the predatory technique is ensured by a rather wide buccal cavity without teeth in the adult stage. It’s well known that the adaptation of vertebrates to their environment is strictly related to the capacity of feeding. The modifications of the oral cavity morphology are in close relationship with different feeding habits. In vertebrates a very important role in the food processing within the buccal cavity is carried out by the tongue. Numerous data are present on the morphology of the fish oral cavity (for review see Kapoor and Khanna, 1994; Horn, 1998) The different morphological characteristics of the tongue and the buccal cavity were previously demonstrated in different species of fish (Yashpal et al., 2006; Collar et al., 2009; Abbate et al., 2006, 2012a,b; Price et al., 2010; Guerrera et al., 2015; El Bakary, 2014; Dos Santos et al., 2015; Sadeghinezhad et al., 2015; Elgendy et al., 2016; Mahmoud et al., 2016). Taste buds, teeth and mucous cells characterized the tongue morphology in some teleosts of commercial interest and their presence and localization varied among species (Levanti et al., 2017). Some other investigations in vertebrates, like birds (Jackowiak et al., 2010, 2011; Erdoğan and Alan, 2012; Erdoğan and Iwasaki, 2014; Skieresz-Szewczyk and Jackowiak, 2017, 2016) and reptiles (Bels and Baltus, 1988; Schwenk and Bell, 1988; Iwasaki, 1990, 2002; Abbate et al., 2008, 2009, 2010; Herrel et al., 2014) and also very recent data on different mammals (Emura and Sugiyama, 2016; Emura, 2016a,b; Erdoğan et al., 2016a,b)
Corresponding author. E-mail address: [email protected] (F. Abbate).
http://dx.doi.org/10.1016/j.tice.2017.09.007 Received 27 June 2017; Received in revised form 26 September 2017; Accepted 26 September 2017 0040-8166/ © 2017 Elsevier Ltd. All rights reserved.
Please cite this article as: Abbate, F., Tissue and Cell (2017), http://dx.doi.org/10.1016/j.tice.2017.09.007
Tissue and Cell xxx (xxxx) xxx–xxx
F. Abbate et al.
contributed to an interesting comparative analysis. Considering that no data are present in literature about the morphology of the swordfish tongue, the aim of this study was to analyse by scanning electron and light microscopy the anatomical characteristics of the swordfish tongue, especially its dorsal surface, to give a further contribution to the knowledge of the organ deputed to swallowing the preys. 2. Material and methods The samples of swordfish tongue (N = 5) were obtained with the help of fishermen of the Straight of Messina. Their heads were taken after fishing and the oral cavity was exposed by means of the disarticulation of the temporo-mandibular joint. The tongues were withdrawn and, to better observe the morphological details, were washed in 5% neutral Extran (Merck, Damstadt, Germany), a cleansing solution used to remove the mucus. Therefore the samples were fixed in 2.5% glutaraldehyde in Sörensen phosphate buffer 0.1 M. After several rinsing in the same buffer, they were dehydrated in a graded alcohols series, critical-point dried in a Balzers CPD 030, sputter coated with 3 nm gold in a Balzers BAL-TEC SCD 050 and examined under a Zeiss EVO LS 10. For light microscopy the tongues were fixed in Bouin’s liquor for 24 h, dehydrated and routinely embedded in paraffin. Frontal, horizontal and sagittal serial sections of 10 μm thick were obtained, mounted on microscope slides, and processed for Masson Trichrome staining. Three different stains were used: Weigert’s iron hematoxylin for nuclei, a mixture of acid dyes for cytoplasm and aniline blue for connective tissue. After rinsing in distilled water, the sections were submitted to the reagents, repeatedly washed in distilled water and rapidly dehydrated through ascending alcohols, clarified in xylene and mounted. Figures were obtained under a Leica DMRB light microscope.
Fig. 1. Gross anatomy of swordfish tongue. Dorsal view divided in three areas: (a) the apex; (b) the body; (r) the enlarged root. Two areas along the lateral edges of the apex and the body are rough to the touch (arrows); the medial part of the apex and the body, as well as the whole root surface appear to have a velvety aspect (asterisks). Scale bar: 1 cm.
3. Results higher magnification (Fig. 5b).
3.1. Macroscopical anatomy
3.3. Light microscopy
The swordfish tongue is an elongated and triangular organ that can be divided into three main areas, viz. an apex, a body and a root. With an apex it fits to the lower jaw that ends with a tip. Its anterior part of its body is dorsoventrally flattened. Dorsally, the whole body of the tongue is divided into two distinct areas. The first one is along the lateral edges converging medially at the apex level, rough to the touch (arrows) and the second area is a paler median triangular area with a basis directed to the pharynx, with a velvety aspect. The root is wide with a lateral and a medial part and joined to the lower jaw at the base (Fig. 1). (Results).
The tunica mucosa lines the lingual dorsal surface and the epithelium is squamous stratified nonkeratinized with an abundant loose connective tissue projecting to the bases of it. In the apex small conical denticles on different levels and at different steps of eruption are present (fig. 2c). Aborally the shape and size of the denticles change, and they are smaller than the apex with evident smoother tips (fig. 2d). The tunica mucosa of the body is formed by simple cuboidal epithelium wherein denticles are embedded (fig. 3c).Whereas in the lateral areas, the canine-like denticles are protruding out above the cuboidal epithelium (fig. 3d). Filiform papillae can be observed on the latero-ventral areas of the body and the connective tissue projects to the bases of the epithelium (fig. 5c).
3.2. Scanning electron microscopy The apex of the tongue is characterized by numerous small denticles, aborally directed and with a conical shape, organized on different rows and levels forming areas marked by grooves (Fig. 2a). The shape and size of the conical denticles change in the body (aboral part of the apex) becoming thickened, sparse with a hooked tip (Fig. 2b). The lateral part of the body of the tongue shows several canine-like denticles with a sharp tip, aborally directed (Fig. 3a), whereas in the medial surface plicae of the mucosa surround several denticles (Fig. 3b). In the root of the tongue, the lateral one is characterized by the presence of hooked thickened denticles, variously directed (fig. 4a) and the boundaries with the medial one are evident (fig. 4b) for the presence of several polygonal areas marked by plicae of the lingual mucosa. Several denticles are uniformly distributed in zones well defined by septa (fig. 4b) and, medially, slightly hollowed with denticles arranged in small circular zones surrounded by evident plicae. In the latero-ventral surface of the tongue, several filiform papillae are also present (fig. 5a), resembling to finger like structure with microridges on their surface on
4. Discussion In this study a description of the dorsal surface of the tongue in the swordfish is carried out for the first time. In the swordfish the mechanics of food ingestion are in close relationships especially with the aspect of the upper jaw similar to a sword, used to stun the prey that is wholly ingested. Since several years it is well known that no teeth are present in the adult swordfish oral cavity, but only in the larval stage, when the rostrum is not present (Padoa, 1956). Nevertheless no data are so far available about the anatomical features of the tongue, especially regarding its dorsal surface. Our results clearly show the presence of several small denticles and it can be hypothesized that they are used to firmly grasp the prey before the ingestion. Also the presence of filiform papillae on the latero-ventral areas of the lingual body could be related to this mechanism of food ingestion, playing a possible role in 2
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Fig. 2. Scanning Electron Microscopy (SEM): (a) The aboral part of the apex with numerous small denticles, aborally directed, with a conical shape, present on different rows and levels; (b) Thickened conical denticles in the lateral (asterisk) and, smaller, in the medial portions (hashtag). Light microscopy (LM): (c) Longitudinal section with the occurrence of denticles characterized by hooked tip, oro-aborally oriented (asterisks); (d) Longitudinal section of the lateral (asterisk) and medial (hashtag) lingual portions with the connective tissue (CT) forming the submucosa. Denticles are indicated by arrows. Scale bar: (a,c,d) 200 μm; (b) 30 μm.
Fig. 3. SEM: (a) In the lateral part of the body plicae of the mucosa are evident beside the denticles (arrows); (b) the medial part of the body characterized by the presence of hooked thickened denticles (canine-like), variously directed; LM: (c) Longitudinal section of the lateral part of the body with simple cuboidal epithelium (arrows) surrounding denticles (asterisks) (d) Longitudinal section showing caninelike denticles with hooked tips, aborally oriented. Scale bar:(a) 300 μm; (b,c) 100 μm; (d) 30 μm.
Fig. 4. SEM: (a) The border between the lateral and the medial part of the body. (b) Medial part of the body: the lingual dorsal surface divided in zones well defined by septa. LM: (c) Longitudinal section of the border between the lateral and the medial part of the body. (d) Longitudinal section with denticles surrounded by the tunica mucosa. Scale bar:(a,b,c) 200 μm; (d) 30 μm.
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Fig. 5. SEM: (a,b) The latero-ventral surface completely covered by filiform papillae. At higher magnification a typical aspect resembling hand fingers with microridges on their surface is evident. LM: (c) Longitudinal section showing filiform papillae on the latero-ventral surface. The connective tissue projects to the basis of the epithelium with vessels (arrowhead). Scale bar: (a) 20 μm; (b) 200 μm; (c) 100 μm.
the food prehension and water filtration. No taste buds or other sensitive structures were revealed on the dorsal surface of the tongue and their absence could demonstrate a limited taste capacity in a fish that usually ingest quickly the prey without a discrimination among different nourishments. Therefore, the eventual rejection of food demonstrated on other species cannot be expected in case of sword fish (Abbate et al., 2012a,b; Kubitza and Lovshin, 1997; Yashpal et al., 2009). The characteristic of the presence of a rostrum is unique in this species and can be compared, among the enormous number of fish species, only with the marlin (Istiophoridae). The obtained results are in agreement with previous reports on different teleosts (Abbate et al., 2012a,b; Guerrera et al., 2015; Levanti et al., 2017) and confirm that a true tongue with peculiar morphological characteristics is present. The obtained results, compared with other species of studied teleosts and considering the particular morphological aspect of the upper jaw, could give a contribution to the knowledges of the fish oral cavity morphology and to the hypothesis of modifications and evolution of the tongue anatomy related to the environment and especially to the feeding habits.
Collar, D.C., O’Meara, B.C., Wainwright, P.C., Near, T.J., 2009. Piscivory limits diversification of feeding morphology in centrarchid fishes. Evolution 63, 1557–1573. Collette, B., Acero, A., Amorim, A.F., Bizsel, K., Boustany, A., Canales Ramirez, C., Cardenas, G., Carpenter, K.E., de Oliveira Leite Jr, N., Di Natale, A., Die, D., Fox, W., Fredou, F.L., Graves, J., Guzman-Mora, A., Viera Hazin, F.H., Hinton, M., Juan Jorda, M., Minte Vera, C., Miyabe, N., Montano Cruz, R., Masuti, E., Nelson, R., Oxenford, H., Restrepo, V., Salas, E., Schaefer, K., Schratwieser, J., Serra, R., Sun, C., Teixeira Lessa, R.P., Pires Ferreira Travassos, P.E., Uozumi, Y., Yanez, E., 2011. Xiphias Gladius. IUCN Red List of Threatened Species. Version 2011.2. International Union for Conservation of Nature (Retrieved). Dos Santos, M.L., Arantes, F.P., Pessali, T.C., Dos Santos, J.E., 2015. Morphological, histological and histochemical analysis of the digestive tract of Trachelyopterusstriatulus (Siluriformes: auchenipteridae). Zoologia 32 (4), 296–305. El Bakary, N.E.S.R., 2014. Morphological study of the asymmetrical buccal cavity of the flatfish common solea (Soleasolea) and its relation to the type of feeding. Asian Pac. J. Trop. Biomed. 4 (1), 13–17. Elgendy, S.A.A., Alsafy, M.A.M., Tanekhy, M., 2016. Morphological characterization of the oral cavity of the gilthead seabream (Sparus aurata) with emphasis on the teethage adaptation. Microsc. Res. Tech. 79 (3), 227–236. Emura, S., Sugiyama, K., 2016. Morphology of the lingual papillae of the Asian shortclawed otter. Okajimas Folia Anat. Jpn. 93 (3), 105–110. Emura, S., 2016a. Morphology of the lingual papillae in the eastern grey kangaroo. Okajimas Folia Anat. Jpn. 93 (2), 53–57. Emura, S., 2016b. Morphology of the lingual papillae of the eland (Taurotragus oryx). Okajimas Folia Anat. Jpn. 93 (3), 99–103. Erdoğan, S., Alan, A., 2012. Gross anatomical and scanning electron microscopic studies of the oropharyngeal cavity in the European magpie (Pica pica) and the common raven (Corvus corax). Microsc. Res. Tech. 75 (3), 379–387. Erdoğan, S., Iwasaki, S., 2014. Function-related morphological characteristics and specialized structures of the avian tongue. Ann. Anat. 196 (2–3), 75–87. Erdoğan, S., Lima, M., Pérez, W., 2016a. Anatomical and scanning electron microscopic study of the tongue in the meerkat (Suricata suricatta, schreber, 1776). Anat. Histol. Embryol. 45 (1), 51–59. Erdoğan, S., Villar Arias, S., Pérez, W., 2016b. Morphofunctional structure of the lingual papillae in three species of South American Camelids: alpaca, guanaco, and llama. Microsc. Res. Tech. 79 (2), 61–71. Guerrera, M.C., Montalbano, G., Germanà, A., Maricchiolo, G., Ciriaco, E., Abbate, F., 2015. Morphology of the tongue dorsal surface in white sea bream (Diplodus sargus sargus). Acta Zool. 96, 236–241. Herrel, A., Redding, C.L., Meyersm, J.J., Nishikawa, K.C., 2014. The scaling of tongue projection in the veiled chameleon, Chamaeleo calyptratus. Zoology 117 (4), 227–236. Horn, M.H., 1998. Feeding and digestion. In: Evans, D.H. (Ed.), The Physiology of Fishes, pp. 43–63 (Boca Raton). Iwasaki, S., 1990. Fine structure of the dorsal lingual epithelium of the lizard, Gekkojaponicus (Lacertilia, Gekkonidae). Am. J. Anat. 187, 12–20. Iwasaki, S., 2002. Evolution of the structure and function of the vertebrate tongue. J. Anat. 201, 1–13. Jackowiak, H., Skieresz-Szewczyk, K., Kwieciński, Z., Trzcielińska-Lorych, J., Godynicki,
References Abbate, F., Germanà, G.P., De Carlos, F., Montalbano, G., Laurà, R., Levanti, M.B., Germanà, A., 2006. The oral cavity of the adult zebrafish (Danio rerio). Anat. Histol. Embryol. 35, 299–304. Abbate, F., Latella, G., Montalbano, G., Guerrera, M.C., Levanti, M.B., Ciriaco, E., 2008. Scanning electron microscopical study of the lingual epithelium of green iguana (Iguana iguana). Anat. Histol. Embryol. 37, 314–316. Abbate, F., Latella, G., Montalbano, G., Guerrera, M.C., Germanà, G.P., Levanti, M.B., 2009. The lingual dorsal surface of the blue-tongue skink (Tiliqua scincoides). Anat. Histol. Embryol. 38, 348–350. Abbate, F., Guerrera, M.C., Montalbano, G., Zichichi, R., Germanà, A., Ciriaco, E., 2010. Morphology of the lingual dorsal surface and oral taste buds in Italian lizard (Podarcissicula). Anat. Histol. Embryol. 39, 167–171. Abbate, F., Guerrera, M.C., Montalbano, G., De Carlos, F., Suarez, A.A., Ciriaco, E., Germanà, A., 2012a. Morphology of the European seabass (Dicentrarchuslabrax) tongue. Microsc. Res. Tech. 75, 643–649. Abbate, F., Guerrera, M.C., Montalbano, G., Ciriaco, E., Germanà, A., 2012b. Morphology of the tongue dorsal surface of gilthead seabream (Sparusaurata). Microsc. Res. Tech. 75, 1666–1671. Bels, V.L., Baltus, I., 1988. The influence of food items on the feeding cycle in Anolisequestris (Reptilia: iguanidae). Co-peia 2, 479–481.
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Evolution 64, 3057–3068. Sadeghinezhad, J., Rahmati-Holasoo, H., Fayyaz, S., Zargar, A., 2015. Morphological study of the northern pike (Esoxlu-cius) tongue. Anat. Sci. Int. 90 (4), 235–239. Schwenk, K., Bell, D.A., 1988. A cryptic intermediate in the evolution of chameleon tongue projection. Experientia 44, 697–700. Skieresz-Szewczyk, K., Jackowiak, H., 2016. Morphofunctional study of the tongue in the domestic duck (Ana-splatyrhynchos f. domestica: anatidae): LM and SEM study. Zoomorphology 135, 255–268. Skieresz-Szewczyk, K., Jackowiak, H., 2017. Development of mechanical papillae of the tongue in the domestic goose (Anser anser f. domestica) during the embryonic period. Protoplasma 254 (1), 147–160. Tortonese, E., 1975. Fauna d’Italia. (Osteitti. Ed. Calderini). Tserpes, G., Tsimenides, N., 1995. Determination of age and growth of swordfish, Xiphias gladius L. 1758, in the eastern Mediterranean using anal-fin spines. Fish. Bull. 93, 594–602. Tsimenides, N., Tserpes, G., 1989. Age determination and growth of swordfish Xiphias gladius L., 1758 in the Aegean Sea. Fish. Res. 8 (2), 159–168. Yashpal, M., Kumari, U., Mittal, S., Mittal, A.K., 2006. Surface architecture of the mouth cavity of a carnivorous fish Rita rita (Hamilton, 1822) (Siluriformes. Bagridae). Belg. J. Zool. 136, 155–162. Yashpal, M., Kumari, U., Mittal, S., Mittal, A.K., 2009. Morphological specializations of the oral cavity in relation to the food and feeding habit of a carp Cirrhinusmrigala: a scanning electron microscopic investigation. J. Morphol. 270, 714–728.
S., 2010. Functional morphology of the tongue in the nutcracker (Nucifragacaryocatactes). Zool. Sci. 27, 589–594. Jackowiak, H., Skieresz-Szewczyk, K., Godynicki, S., Iwasaki, S., Meyer, W., 2011. Functional morphology of the tongue in the domestic goose (Anseranser f. domestica). Anat. Rec. 294, 1574–1584. Kapoor, B.G., Khanna, B., 1994. The alimentary canal of teleosts: a brief survey of structure and function. In: Singh, H.R. (Ed.), Advances in Fish Biology. Hindustan Publishing Corporation, Delhi, pp. 12–24. Kubitza, F., Lovshin, L.L., 1997. The use of freeze-dried krill to feed train largemouth bass (Micropterussalmoides): Feeds and training strategies. Aquaculture 148, 299–312. Levanti, M., Germanà, A., Montalbano, G., Guerrera, M.C., Cavallaro, M., Abbate, F., 2017. The tongue dorsal surface in fish: a comparison among three farmed species. Anat. Histol. Embryol. 46 (2), 103–109. Mahmoud, U.M., Essa, F., Sayed, A.E.-D.H., 2016. Surface architecture of the oropharyngeal cavity and the digestive tract of Mulloidichthys flavolineatus from the red sea, Egypt: a scanning electron microscope study. Tissue Cell 48 (6), 624–633. Padoa, E., 1956. Fauna e flora del Golfo di Napoli. Uova: larve e stadi giovanili di teleostei. Scombriformes 38, 471–521. Peristeraki, P., Tserpesand, G., Lefhaditou, E., 2005. What cephalopod remains from Xiphias gladius stomachs can imply about predator-prey interactions in the Mediterranean Sea? J. Fish Biol. 67, 549–554. Price, S.A., Wainwright, P.C., Bellwood, D.R., Kazancioglu, E., Collar, D.C., Near, T.J., 2010. Functional innovations and morphological diversification in parrotfishes.
5
Contents lists available at ScienceDirect
Tissue and Cell journal homepage: www.elsevier.com/locate/tice
LM and SEM study on the swordfish (Xiphias gladius) tongue ⁎
Francesco Abbate , Maria Cristina Guerrera, Mauro Cavallaro, Giuseppe Montalbano, Antonino Germanà, Maria Levanti Department of Veterinary Sciences, University of Messina, Italy
A R T I C L E I N F O
A B S T R A C T
Keywords: Tongue Fish Scanning electron microscopy Light microscopy
Swordfish (Xiphias gladius L. 1758) is a predatory and migratory fish. Its characteristic feature is a flat and sharp upper jaw forming a “sword”. The adaptation of vertebrates, including fish, to their environment is strictly related to the capacity of feeding and is carried out by often severe modifications of the anatomy of the buccal cavity, especially of the tongue. The aim of this study is, using light and scanning electron microscopy and considering that no data are so far available about the morphology of the tongue in this species, to analyse the anatomical characteristics of the tongue, especially its dorsal surface. The tongue shows a triangular shape and an apex, a body and a root. By SEM the presence of several small denticles and filiform papillae on the lateroventral body was demonstrated while no taste buds or other sensitive structures are observed. LM shows a squamous stratified epithelium, becoming simple cuboidal around the denticles. Therefore this study could add further data to the knowledges of the fish oral cavity morphology supporting the hypothesis that the modifications and evolution of the tongue anatomy are, also in fish, related to the environment and especially to the feeding habits.
1. Introduction Swordfish (Xiphias gladius L. 1758) is a horizontally migrating pandemic fish distributed through tropical and temperate parts of the Atlantic, Pacific, and Indian Oceans (IUCN, 2011). It’s depth distribution ranges from near the surface to a depth of 550 m (Collette et al., 2011). The Mediterranean swordfish populations constitute a unique stock, distinct from the Atlantic ones with different growth and maturity characteristics (Tsimenides and Tserpes, 1989; Tserpes and Tsimenides, 1995). The fish is an extremely versatile predator characterized by a long, flat rostrum and capable of exploiting various trophic resources. It predates mainly pelagic fishes especially at the juvenile stage, later, as adult predates crustaceans and cephalopods. Its best-known feature is the great development of the upper jaw which forms the typical flat and sharp “sword”, long about 1/3 of the body. The lower jaw is elongated and pointed, but has a much shorter length compared to the upper one (Tortonese, 1975; Peristeraki et al., 2005). The ethology of the predation in this species is poorly described considering that, being a cosmopolitan, solitary and aggressive predator, it is quite difficult to make observations regarding its behaviour. The peculiar aspect of the upper jaw impressively affects the predatory techniques. In fact, the animal uses the long rostrum as an instrument of aggression to stun the prey and then swallowing them whole
⁎
(Tortonese, 1975). This second stage of the predatory technique is ensured by a rather wide buccal cavity without teeth in the adult stage. It’s well known that the adaptation of vertebrates to their environment is strictly related to the capacity of feeding. The modifications of the oral cavity morphology are in close relationship with different feeding habits. In vertebrates a very important role in the food processing within the buccal cavity is carried out by the tongue. Numerous data are present on the morphology of the fish oral cavity (for review see Kapoor and Khanna, 1994; Horn, 1998) The different morphological characteristics of the tongue and the buccal cavity were previously demonstrated in different species of fish (Yashpal et al., 2006; Collar et al., 2009; Abbate et al., 2006, 2012a,b; Price et al., 2010; Guerrera et al., 2015; El Bakary, 2014; Dos Santos et al., 2015; Sadeghinezhad et al., 2015; Elgendy et al., 2016; Mahmoud et al., 2016). Taste buds, teeth and mucous cells characterized the tongue morphology in some teleosts of commercial interest and their presence and localization varied among species (Levanti et al., 2017). Some other investigations in vertebrates, like birds (Jackowiak et al., 2010, 2011; Erdoğan and Alan, 2012; Erdoğan and Iwasaki, 2014; Skieresz-Szewczyk and Jackowiak, 2017, 2016) and reptiles (Bels and Baltus, 1988; Schwenk and Bell, 1988; Iwasaki, 1990, 2002; Abbate et al., 2008, 2009, 2010; Herrel et al., 2014) and also very recent data on different mammals (Emura and Sugiyama, 2016; Emura, 2016a,b; Erdoğan et al., 2016a,b)
Corresponding author. E-mail address: [email protected] (F. Abbate).
http://dx.doi.org/10.1016/j.tice.2017.09.007 Received 27 June 2017; Received in revised form 26 September 2017; Accepted 26 September 2017 0040-8166/ © 2017 Elsevier Ltd. All rights reserved.
Please cite this article as: Abbate, F., Tissue and Cell (2017), http://dx.doi.org/10.1016/j.tice.2017.09.007
Tissue and Cell xxx (xxxx) xxx–xxx
F. Abbate et al.
contributed to an interesting comparative analysis. Considering that no data are present in literature about the morphology of the swordfish tongue, the aim of this study was to analyse by scanning electron and light microscopy the anatomical characteristics of the swordfish tongue, especially its dorsal surface, to give a further contribution to the knowledge of the organ deputed to swallowing the preys. 2. Material and methods The samples of swordfish tongue (N = 5) were obtained with the help of fishermen of the Straight of Messina. Their heads were taken after fishing and the oral cavity was exposed by means of the disarticulation of the temporo-mandibular joint. The tongues were withdrawn and, to better observe the morphological details, were washed in 5% neutral Extran (Merck, Damstadt, Germany), a cleansing solution used to remove the mucus. Therefore the samples were fixed in 2.5% glutaraldehyde in Sörensen phosphate buffer 0.1 M. After several rinsing in the same buffer, they were dehydrated in a graded alcohols series, critical-point dried in a Balzers CPD 030, sputter coated with 3 nm gold in a Balzers BAL-TEC SCD 050 and examined under a Zeiss EVO LS 10. For light microscopy the tongues were fixed in Bouin’s liquor for 24 h, dehydrated and routinely embedded in paraffin. Frontal, horizontal and sagittal serial sections of 10 μm thick were obtained, mounted on microscope slides, and processed for Masson Trichrome staining. Three different stains were used: Weigert’s iron hematoxylin for nuclei, a mixture of acid dyes for cytoplasm and aniline blue for connective tissue. After rinsing in distilled water, the sections were submitted to the reagents, repeatedly washed in distilled water and rapidly dehydrated through ascending alcohols, clarified in xylene and mounted. Figures were obtained under a Leica DMRB light microscope.
Fig. 1. Gross anatomy of swordfish tongue. Dorsal view divided in three areas: (a) the apex; (b) the body; (r) the enlarged root. Two areas along the lateral edges of the apex and the body are rough to the touch (arrows); the medial part of the apex and the body, as well as the whole root surface appear to have a velvety aspect (asterisks). Scale bar: 1 cm.
3. Results higher magnification (Fig. 5b).
3.1. Macroscopical anatomy
3.3. Light microscopy
The swordfish tongue is an elongated and triangular organ that can be divided into three main areas, viz. an apex, a body and a root. With an apex it fits to the lower jaw that ends with a tip. Its anterior part of its body is dorsoventrally flattened. Dorsally, the whole body of the tongue is divided into two distinct areas. The first one is along the lateral edges converging medially at the apex level, rough to the touch (arrows) and the second area is a paler median triangular area with a basis directed to the pharynx, with a velvety aspect. The root is wide with a lateral and a medial part and joined to the lower jaw at the base (Fig. 1). (Results).
The tunica mucosa lines the lingual dorsal surface and the epithelium is squamous stratified nonkeratinized with an abundant loose connective tissue projecting to the bases of it. In the apex small conical denticles on different levels and at different steps of eruption are present (fig. 2c). Aborally the shape and size of the denticles change, and they are smaller than the apex with evident smoother tips (fig. 2d). The tunica mucosa of the body is formed by simple cuboidal epithelium wherein denticles are embedded (fig. 3c).Whereas in the lateral areas, the canine-like denticles are protruding out above the cuboidal epithelium (fig. 3d). Filiform papillae can be observed on the latero-ventral areas of the body and the connective tissue projects to the bases of the epithelium (fig. 5c).
3.2. Scanning electron microscopy The apex of the tongue is characterized by numerous small denticles, aborally directed and with a conical shape, organized on different rows and levels forming areas marked by grooves (Fig. 2a). The shape and size of the conical denticles change in the body (aboral part of the apex) becoming thickened, sparse with a hooked tip (Fig. 2b). The lateral part of the body of the tongue shows several canine-like denticles with a sharp tip, aborally directed (Fig. 3a), whereas in the medial surface plicae of the mucosa surround several denticles (Fig. 3b). In the root of the tongue, the lateral one is characterized by the presence of hooked thickened denticles, variously directed (fig. 4a) and the boundaries with the medial one are evident (fig. 4b) for the presence of several polygonal areas marked by plicae of the lingual mucosa. Several denticles are uniformly distributed in zones well defined by septa (fig. 4b) and, medially, slightly hollowed with denticles arranged in small circular zones surrounded by evident plicae. In the latero-ventral surface of the tongue, several filiform papillae are also present (fig. 5a), resembling to finger like structure with microridges on their surface on
4. Discussion In this study a description of the dorsal surface of the tongue in the swordfish is carried out for the first time. In the swordfish the mechanics of food ingestion are in close relationships especially with the aspect of the upper jaw similar to a sword, used to stun the prey that is wholly ingested. Since several years it is well known that no teeth are present in the adult swordfish oral cavity, but only in the larval stage, when the rostrum is not present (Padoa, 1956). Nevertheless no data are so far available about the anatomical features of the tongue, especially regarding its dorsal surface. Our results clearly show the presence of several small denticles and it can be hypothesized that they are used to firmly grasp the prey before the ingestion. Also the presence of filiform papillae on the latero-ventral areas of the lingual body could be related to this mechanism of food ingestion, playing a possible role in 2
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Fig. 2. Scanning Electron Microscopy (SEM): (a) The aboral part of the apex with numerous small denticles, aborally directed, with a conical shape, present on different rows and levels; (b) Thickened conical denticles in the lateral (asterisk) and, smaller, in the medial portions (hashtag). Light microscopy (LM): (c) Longitudinal section with the occurrence of denticles characterized by hooked tip, oro-aborally oriented (asterisks); (d) Longitudinal section of the lateral (asterisk) and medial (hashtag) lingual portions with the connective tissue (CT) forming the submucosa. Denticles are indicated by arrows. Scale bar: (a,c,d) 200 μm; (b) 30 μm.
Fig. 3. SEM: (a) In the lateral part of the body plicae of the mucosa are evident beside the denticles (arrows); (b) the medial part of the body characterized by the presence of hooked thickened denticles (canine-like), variously directed; LM: (c) Longitudinal section of the lateral part of the body with simple cuboidal epithelium (arrows) surrounding denticles (asterisks) (d) Longitudinal section showing caninelike denticles with hooked tips, aborally oriented. Scale bar:(a) 300 μm; (b,c) 100 μm; (d) 30 μm.
Fig. 4. SEM: (a) The border between the lateral and the medial part of the body. (b) Medial part of the body: the lingual dorsal surface divided in zones well defined by septa. LM: (c) Longitudinal section of the border between the lateral and the medial part of the body. (d) Longitudinal section with denticles surrounded by the tunica mucosa. Scale bar:(a,b,c) 200 μm; (d) 30 μm.
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Fig. 5. SEM: (a,b) The latero-ventral surface completely covered by filiform papillae. At higher magnification a typical aspect resembling hand fingers with microridges on their surface is evident. LM: (c) Longitudinal section showing filiform papillae on the latero-ventral surface. The connective tissue projects to the basis of the epithelium with vessels (arrowhead). Scale bar: (a) 20 μm; (b) 200 μm; (c) 100 μm.
the food prehension and water filtration. No taste buds or other sensitive structures were revealed on the dorsal surface of the tongue and their absence could demonstrate a limited taste capacity in a fish that usually ingest quickly the prey without a discrimination among different nourishments. Therefore, the eventual rejection of food demonstrated on other species cannot be expected in case of sword fish (Abbate et al., 2012a,b; Kubitza and Lovshin, 1997; Yashpal et al., 2009). The characteristic of the presence of a rostrum is unique in this species and can be compared, among the enormous number of fish species, only with the marlin (Istiophoridae). The obtained results are in agreement with previous reports on different teleosts (Abbate et al., 2012a,b; Guerrera et al., 2015; Levanti et al., 2017) and confirm that a true tongue with peculiar morphological characteristics is present. The obtained results, compared with other species of studied teleosts and considering the particular morphological aspect of the upper jaw, could give a contribution to the knowledges of the fish oral cavity morphology and to the hypothesis of modifications and evolution of the tongue anatomy related to the environment and especially to the feeding habits.
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