Swimbladder form in clupeoid fishes

The general form of the swimbladder is described and illustrated for representatives of 50 out of the 82 genera of clupeoid fishes (families Chirocentridae, Clupeidae, Pristigasteridae and Engraulididae of the suborder Clupeoidei), based mainly on preserved specimens. There is a remarkable diversity of shape, volume and silvering, as well as many curious specializations. The point of origin of the pneumatic duct from the gut, the presence or absence of an anal duct, and the length and diameter of the pre-coelomic ducts are noted, with attempts to explain their functional significance in terms of feeding and vertical migration. Specializations such as dorsal or lateral pockets, post-coelomic diverticula and internal muscular processes may be connected with sound production. The taxonomic implications of this diversity of swimbladder form are explored but, while some intra-and intergeneric relationships arc either confirmed or challenged, the swimbladder gives little help at suprageneric levels.     

ANATOMY OF THE SWIMBLADDERS OF SEVEN FAMILIES OF TRANSVAAL FRESHWATER FISHES

SUMMARY

IN the genera Barbus and Labeo of the family Cyprinidae there is a typical twolobed, cylindrical swimbladder: a shorter anterior and a longer posterior lobe, connected by an isthmus. The pneumatic duct passes from the anteroventral end of the posterior lobe to the oesophagus. In the genus Labeo two spiral bands encircle the posterior lobe twice. No rete mirabile, nor any indication of a gas gland, was observed.

The species Hydrocynus vittutus of the family Characidae has a very similarly shaped swimbladder to that of the Cyprinidea. Inside the anterior lobe, however, there is a peculiar structure, which is evidently the gas glad, although a rete mirabile was not observed.

In the families of the Siluriformes, studied, with the exception of the Clariidae, a single lobed, heartshaped swimbladder is present. It is divided by a longitudinal and a transverse. septum into three chambers: an anterior, a right and a left posterior chamber. The pneumatic duct originates from the medial posteroventral part of the anterior chamber. In Clarias gariepinus the two-lobed, right and left lobed, swimbladder lies in a bony capsule, which is attached transversely to the posteroventral part of the skull. In all the Siluriformes, studied, no trace of a gas gland, nor of a rete mirabile was found.

The Cichlid swimbladder has no pneumatic duct, nor any other exit, hence it is physoclistic. In the Cichlids the retroperitoneal position of the swimbladder is accentuated, as the peritoneum and the outer tectum of the swimbladder have united to form a thick, tough membrane, which divides the body cavity into a distinct ventral, or visceral cavity, and a dorsal, or swimbladder cavity. The swimbladder cavity acts as an outer swimbladder. It contains an inner, smaller bladder whose internal ventro-anterior surface is covered with arborescently arranged patches of gas glands.

The attachment of the swimbladder to the tripus and also to the ossa suspensoris is discussed.     

Development and function of the swimbladder-inner ear-lateral line system in the Atlantic menhaden,Brevoortia tyrannus (Latrobe)*

The swimbladder-acoustico-lateralis system of the Atlantic menhaden, Brevoortia tyrannus, is described and compared with that of the Atlantic herring, Clupea harengus. The system develops in the larva at a much earlier stage than the herring, being functional by about 2 mm tl. The volume of the gas-filled pro-otic bullae is five times that of the herring, and the gas ducts to the swimbladder, instead of being short and separate, are three times the length and join to form a common duct well in front of the swimbladder. The menhaden swimbladder is baggy and totally compliant when subjected to pressure changes. There is no toughened anterior end as in the herring, but the swimbladder is steeply angled in the body cavity, causing gas to collect at the anterior end after a pressure increase, unless the fish is diving very steeply. The guanine content of the swimbladder is comparable with that of the herring and makes the wall very impervious to gas diffusion. When subjected to quick pressure increases and decreases, the pro-otic membrane returns to its flat position with a time constant of 31-44 s. Very large quick pressure changes of about 3 atm burst the pro-otic membrane in adult fish but not in larvae.     

Development of the swimbladder in the European eel (Anguilla anguilla)

The swimbladder of the adult eel, Anguilla anguilla, with its bipolar countercurrent system, the rete mirabile, is a widely used model for swimbladder function, but very little is known about the development of this swimbladder. Our histological studies on the developing swimbladder revealed that during metamorphosis the swimbladder becomes present as a dorsal outgrowth of the esophagus. It is filled with surfactant, and gas was not detected in the swimbladder. In the young glass-eel, the epithelial (gas gland) cells of the swimbladder are columnar, but do not yet have the typical basolateral labyrinth established in adult animals. Few blood vessels are found in the swimbladder tissue, and the submucosa is present as a thick layer of connective tissue, giving a large diffusion distance between blood vessel and swimbladder lumen. Within the next 2 or 3 months of development, gas gland cells develop their typical basolateral labyrinth, and the thickness of the submucosa is significantly reduced, resulting in a short diffusion distance between blood vessels and the swimbladder lumen. The first filling of the swimbladder with gas is observed while the gas gland cells are still in a poorly differentiated status and it appears unlikely that these cells can accomplish their typical role in gas deposition. The presence of small gas bubbles in the swimbladder as well as in the ductus pneumaticus at the time of initial swimbladder inflation suggests that the swimbladder is filled by air gulping or possibly by taking up gas bubbles from the water.     

Ontogeny of body density and the swimbladder in yellowtail kingfish Seriola lalandi larvae

The ontogeny of larval body density and the morphological and histological events during swimbladder development were investigated in two cohorts of yellowtail kingfish Seriola lalandi larvae to understand the relationship between larval morphology and body density. Larvae <3 days post hatch (dph) were positively buoyant with a mean ± s.d . body density of 1·023 ± 0·001 g cm^?3. Histological evidence demonstrated that S. lalandi larvae are initially transient physostomes with the primordial swimbladder derived from the evagination of the gut ventral to the notochord and seen at 2 dph. A pneumatic duct connected the swimbladder to the oesophagus, but degenerated after 5 dph. Initial swimbladder (SB) inflation occurred on 3 dph, and the inflation window was 3–5 dph when the pneumatic duct was still connected to the gut. The swimbladder volume increased with larval age and the epithelial lining on the swimbladder became flattened squamous cells after initial inflation. Seriola lalandi developed into a physoclist with the formation of the rete mirabile and the gas‐secreting gland comprised low‐columnar epithelial cells. Larvae with successfully inflated swimbladders remained positively buoyant, whereas larvae without SB inflation became negatively buoyant and their body density gradually reached 1·030 ± 0·001 g cm^?3 by 10 dph. Diel density changes were observed after 5 dph, owing to day time deflation and night‐time inflation of the swimbladder. These results show that SB inflation has a direct effect on body density in larval S. lalandi and environmental factors should be further investigated to enhance the rate of SB inflation to prevent the sinking death syndrome in the early life stage of the fish larvae.     

Comparative study of X-ray computerised tomography and conventional X-ray methods in diagnosis of swimbladder infection in eels caused by Anguillicola crassus

To date, swimbladder lesions due to Anguillicola crassus infection of the European eel Anguilla anguilla have so far been studied only by conventional X-ray methods. This is the first study to report the use of computerised tomography (CT) for studying lesions induced by anguillicolosis. Of 50 eels caught by electrofishery from Lake Balaton, Hungary, in autumn 2002 and pre-selected by a conventional X-ray method, 22 specimens were examined with a Siemens Somatom Plus S40 spiral CT scanner. Tomograms, radiographs and photographs of 5 of these, showing anguillicolosis-induced swimbladder lesions of varying severity, are presented. Computerised tomograms provide information on the inner structure, air content and wall thickness of the swimbladder as well as on the number of worms it contains. When the swimbladder is not severely affected or not completely filled with worms, computerised tomography provides adequate data on the shape of the swimbladder, thickness of the swimbladder wall and the location of worms in the lumen. However, in more severe cases, i.e. when the swimbladder is tightly packed with worms or contains no air as a result of wall-thickening, this method fails to determine the number and location of helminths or the thickness of the swimbladder wall.     

Histopathological changes in the swimbladder wall of the European eel Anguilla anguilla due to infections with Anguillicola crassus

The histopathological changes in swimbladders of European eels naturally and experimentally infected with Anguillicola crassus were studied using transmission and scanning electron microscopy. During the course of probably several infections swimbladders undergo characteristic changes. In addition to the thickening of the entire swimbladder wall, and to the folded internal surface of this organ, inflammation, migration of white blood cells, fibrosis and changes in the epithelial cells are frequently seen. Epithelial cells tend to proliferate heavily and form hyperplastic tissues; these processes are accompanied by changes in the internal structure of the cells. The normally cubic cells become spherical or columnar and form folds facing the lumen of the swimbladder. As a consequence, most of these cells lose contact with the blood vessels and show no strict polarity. In heavily affected swimbladders the basal labyrinth of the epithelial cells is reduced, i.e. becomes shorter and less densely packed. The lamina propria shows severe fibrosis with infiltration of white blood cells. Larvae of A. crassus, inhabiting the wall of the swimbladder, were found to be surrounded by cell debris, but this local necrosis does not affect the entire swimbladder in its overall structure. These histological findings can partly explain changes in the gas composition in eels infected with A. crassus.     

The occurrence and distribution of peptide- or 5-HT-containing nerves in the swimbladder of four different species of teleosts (Gadus morhua,Ctenolabrus rupestris,Anguilla anguilla,Salmo gairdneri)

Summary The innervation of the swimbladder in four different teleost species has been studied by the use of immunohistochemical methods. The teleosts examined belong to two different groups regarding their swimbladder morphology: physoclists (the cod, Gadus morhua and the goldsinny wrasse, Ctenolabrus rupestris) and physostomes (the eel, Anguilla anguilla and the rainbow trout, Salmo gairdneri). Vasoactive intestinal polypeptide-like immunoreactivity was demonstrated in nerves of the swimbladder walls of all four species, and in the gas glands of the cod and the goldsinny wrasse. Substance P-like immunoreactivity was shown in swimbladders of the cod, eel and rainbow trout but not the goldsinny wrasse. Immunoreactivity to met-enkephalin antiserum was revealed in the swimbladder walls of the eel and the goldsinny wrasse, while neurotensin-like immunoreactivity was present in the goldsinny wrasse and rainbow trout swimbladders. Neurotensin-like immunoreactivity was also seen in the gas gland of the goldsinny wrasse. 5-Hydroxytryptamine immunoreactivity was found in endocrine cells in the pneumatic duct of the eel and in the swimbladder walls of the goldsinny wrasse and the rainbow trout. In conclusion, all teleosts examined showed a very close resemblance in the peptidergic/tryptaminergic innervation of the swimbladder to that of the gut, inasmuch as the immunoreactivity present in the swimbladders always occurred in the gut of the same species.     

A finite interval of initial swimbladder inflation in Latris lineata revealed by sequential removal of water‐surface films

A finite interval of initial swimbladder inflation in striped trumpeter Latris lineata larvae occurred over 4 days at 16° C. Water‐surface films were removed on different days to form treatments: 4, 8, 9, 10, 11 and 12 days post hatching, dph (day 4, 8, 9, 10, 11 and 12 treatments, respectively). No swimbladder inflation was recorded prior to water‐surface film removal. When the water‐surface films were removed in day 4 and 8 treatments, initial swimbladder inflation was first recorded in larvae 9 dph at mean ± s .e . 35·0 ± 5·4%(n = 4) and 45·0 ± 7·9%, respectively. Water‐surface film removal at days 9, 10 and 11, resulted in initial swimbladder inflation the following day at 62·5 ± 2·5, 62·5 ± 7·2 and 11·3 ± 5·5% in larvae 10, 11 and 12 dph, respectively. No swimbladder inflation was recorded following water‐surface film removal on day 12. There was no significant difference in initial inflation among larvae in day 4, 8, 9 and 10 treatments, ranging from 65·0 ± 4·1 to 73·8 ± 6·9%(P > 0·05). Initial inflation was significantly lower in the day 11 treatment (11·3 ± 5·5%)(P < 0·05). During the inflation interval (9–12 dph) swimbladders displayed one of three morphologies; liquid dilation, gas inflated and collapsed. Collapse of the swimbladder lumen was first apparent in larvae without swimbladder inflation from 11 dph and progressively developed thereafter in all larvae with non‐inflated swimbladders. Larvae >6·1 mm standard length lost the ability to undergo initial swimbladder inflation. This study demonstrates that the interval for initial swimbladder inflation in striped trumpeter is short, finite and related to larval size. The end of the inflation interval was marked by onset of abnormal swimbladder morphologies, but not to closure of the pneumatic duct.     

Different on the inside: extreme swimbladder sexual dimorphism in the South Asian torrent minnows

The swimbladder plays an important role in buoyancy regulation but is typically reduced or even absent in benthic freshwater fishes that inhabit fast flowing water. Here, we document, for the first time, a remarkable example of swimbladder sexual dimorphism in the highly rheophilic South Asian torrent minnows (Psilorhynchus). The male swimbladder is not only much larger than that of the female (up to five times the diameter and up to 98 times the volume in some cases), but is also structurally more complex, with multiple internal septa dividing it into smaller chambers. Males also exhibit a strange organ of unknown function or homology in association with the swimbladder that is absent in females. Extreme sexual dimorphism of non-gonadal internal organs is rare among vertebrates and the swimbladder sexual dimorphisms that we describe for Psilorhynchus are unique among fishes.     

Histological study of the development of the embryo and early larva of Oreochromis niloticus (Pisces: Cichlidae)

The developmental stages of Oreochromis niloticus are similar to those described in other mouth-breeding tilapias except that, as in zebrafish, no cavity was found in the blastula. Variation in the rate of development of the embryo and larva of O. niloticus was found within a clutch of eggs as well as between clutches. Hatching glands are described for the first time in tilapias. They are widely distributed within the ectoderm covering the head, body, tail, and surface of the yolk sac near its attachment to the embryo. Timing of larval development is similar to that in other mouthbrooding tilapias, but is slower than that found in substrate-spawning tilapias. A pneumatic duct connects the swimbladder to the digestive tract and swimbladder inflation and initiation of feeding occurs at about the same time. The digestive tract of the larva 8 and 9 days after fertilization is similar to that found in the adult, except that there are no digestive glands. An endocrine pancreatic islet was first seen 76 h after fertilization. A prominent thymus gland is present at 100 h. Hematopoietic tissue develops in the vicinity of the pronephros during early larval development. A spleen develops later, 7 days after fertilization.     

Auditory role of lateral trunk channels in cobitid fishes

In cobitid fishes the anterior part of the swimbladder is encapsulated by bone to varying extent. This might diminish the auditory sensitivity of these otophysine fishes by reducing the vibrations of the swimbladder wall in the sound field. However, according to prior studies the auditory thresholds of the cobitid Botia modesta is similar to that of other otophysine fishes. According to anatomical investigation B. modesta has a cranial encapsulation of the anterior part of the swimbladder (camera aerea Weberiana) as expected and in addition special channels stretching laterally from the swimbladder to the outer body wall. These lateral trunk channels are filled with fat and lymph. They form a muscle-free acoustic window beneath the skin, which could be demonstrated by measuring the auditory brainstem response at 400 Hz, 800 Hz, 1500 Hz, and 3000 Hz. Filling the lateral trunk channels with wettex (cotton/rayon staple) resulted in an increase of the auditory thresholds by 13.6–17.6 dB, indicating mechanical damping of the swimbladder. Our experiments demonstrate that the intact lateral trunk channels enhance the hearing sensitivity of cobitid fishes. Accepted: 15 December 1999     

Cytochemical study of the lamellar bodies in the swimbladder of the toadfish Opsanus tau L.

Summary The columnar epithelial cells of the gas gland in the swimbladder of the toadfish, Opsanus tau L., contain lamellar bodies that resemble the lamellar bodies found in epithelial cells of vertebrate lungs. Cytochemical assays indicate that swimbladder lamellar bodies are soluble in chloroform-methanol solution, react with tricomplex flocculation solution (indicating a phospholipid component), exhibit a positive reaction for cholesterol when exposed to digitonin, and contain acid phosphatase.The anterior chamber of the toadfish swimbladder is lined by an extracellular layer. Digitonin-cholesterol crystals are found in this layer when the swimbladder is treated with digitonin. A ruthenium red positive layer is also present in the anterior chamber of the toadfish swimbladder.The structure and cytochemistry of swimbladder lamellar bodies are compared with those of vertebrate lung lamellar bodies. Similarities between the extracellular layer in the swimbladder and the extracellular layer in lungs are also noted.Supported in part by a grant No 1 R23 HL 19593-01 from the National Institutes of Health     

Functional morphology of the sonic apparatus in the fawn cusk-eel Lepophidium profundorum (Gill, 1863)

Recent reports of high frequency sound production by cusk-eels cannot be explained adequately by known mechanisms, i.e., a forced response driven by fast sonic muscles on the swimbladder. Time to complete a contraction-relaxation cycle places a ceiling on frequency and is unlikely to explain sounds with dominant frequencies above 1 kHz. We investigated sonic morphology in the fawn cusk-eel Lepophidium profundorum to determine morphology potentially associated with high frequency sound production and quantified development and sexual dimorphism of sonic structures. Unlike other sonic systems in fishes in which muscle relaxation is caused by internal pressure or swimbladder elasticity, this system utilizes antagonistic pairs of muscles: ventral and intermediate muscles pull the winglike process and swimbladder forward and pivot the neural arch (neural rocker) above the first vertebra backward. This action stretches a fenestra in the swimbladder wall and imparts strain energy to epineural ribs, tendons and ligaments connected to the anterior swimbladder. Relatively short antagonistic dorsal and dorsomedial muscles pull on the neural rocker, releasing strain energy, and use a lever advantage to restore the winglike process and swimbladder to their resting position. Sonic components grow isometrically and are typically larger in males although the tiny intermediate muscles are larger in females. Although external morphology is relatively conservative in ophidiids, sonic morphology is extremely variable within the family.     

Morphology and histology of the swimbladder and infrastructure of respiratory epithelium in the air-breathing catfish, Pangasius sutchi (Pangasiidae)

The swimbladder of Pangasius sutchi is made up of fibrosa, collagenic fibre walls and mucosa; its walls extend into the lumen to form dense respiratory alveoli, with the inner surface covered by a highly vascularized respiratory epithelium. The thin epithelial cells have the structural characteristics and function of type I and type II cells of lung alveoli in higher mammals. These cells and the endothelial cells compose the barrier through which gases must pass in the exchange between blood and air. The study shows that the swimbladder of P. sutchi is an important accessory respiratory organ.     

Impacts of the swimbladder nematode Anguillicola crassus on Anguilla anguilla: variations in liver and spleen masses

Variations in the liver and spleen masses of the eel Anguilla anguilla were analysed in relation to the parasite load of Anguillicola crassus at autopsy (current infection by swimbladder lumen worms) and in relation to the severity of damage observed in the swimbladder (a way of assessing the intensity of past infections). None of these measures of parasite pressure were shown to account for variation in the relative liver mass, either when controlling for somatic mass or eel age. In marked contrast, a significant increase in spleen size was revealed in eels harbouring many lumen worms and also in eels with severe damage in the swimbladder. Splenic enlargement was nearly two‐fold higher among severely affected eels (harbouring more than seven lumen parasites and showing severe damage in the swimbladder) than among infection‐free eels (no lumen parasites and no pathological signs in the swimbladder). Several possible hypotheses are reviewed before arguing for an adaptive host response involving the haematological and immunological functions of the spleen. Indeed, among eels with no pathological signs in the swimbladder, the relative spleen mass was positively associated with the mass of lumen parasites, which suggests a hyper‐synthesis of blood cells by the spleen in response to the bloodsucking activity of lumen worms. Nevertheless, among eels with no lumen parasites at autopsy, there was still an increase in spleen size in relation to the severity of the swimbladder damage, which also suggests a hyper‐synthesis of splenic immune cells (lymphocytes and macrophages) in reaction to damaged tissues and particularly to larvae in the swimbladder wall.     

Aspiratory respiration in Arapaima gigas (Teleostei, Osteoglossomorpha): A reappraisal

Recently it has been hypothesized that the osteoglossoid fish Arapaima gigas is unique amongst air-breathing bony fishes in that it ventilates its respiratory swimbladder by aspiration. Aspiration, it was suggested, is effected by a diaphragm-like septum lying below the swimbladder, and activated through lateral movement of the ribs.
By using both high-speed X-ray and light cinematography this hypothesis can be refuted. Furthermore, dissection shows that the presumed anatomical basis for aspiration stems from a misinterpretation of the usual retroperitoneal position of the swimbladder, and that the ribs are capable of only a very restricted lateral movement. Arapaima gigas , like other bony fishes with a respiratory swimbladder, ventilates that organ by means of a buccopharyngeal pump.
The principal afferent vascular supply to the swimbladder is, however, unusual since it stems from the caudal vein via the renal-portal system. This and other aspects of swimbladder structure and anatomy may throw further light on the interrelationships of osteoglossoid fishes.     

Perturbation of zebrafish swimbladder development by enhancing Wnt signaling in Wif1 morphants

Wnt signaling plays critical roles in development of both tetrapod lung and fish swimbladder, which are the two evolutionary homologous organs. Our previous data reveal that down-regulation of Wnt signaling leads to defective swimbladder development. However, the effects of up-regulation of Wnt signaling on swimbladder development remain unclear. By knockdown of the Wnt protein inhibitory gene wif1, we demonstrated that up-regulation of Wnt signaling also resulted in perturbed development of the swimbladder. Specifically, the growth of epithelium and mesenchyme was greatly inhibited, the smooth muscle differentiation was abolished, and the organization of mesothelium was disturbed. Furthermore, our data reveal that it is the reduced cell proliferation, but not enhanced apoptosis, that contributes to the disturbance of swimbladder development in wif1 morphants. Blocking Wnt signaling by the Wnt antagonist IWR-1 did not affect wif1 expression in the swimbladder, but complete suppression of Hedgehog signaling in smo-/- mutants abolished wif expression, consistent with our earlier report of a negative feedback regulation of Wnt signaling in the swimbladder by the Hedgehog signaling. Our works established the importance of proper level of Wnt signaling for normal development of swimbladder in zebrafish.