Functional morphology of the sonic apparatus in Ophidion barbatum (Teleostei, Ophidiidae)

Most soniferous fishes producing sounds with their swimbladder utilize relatively simple mechanisms: contraction and relaxation of a unique pair of sonic muscles cause rapid movements of the swimbladder resulting in sound production. Here we describe the sonic mechanism for Ophidion barbatum, which includes three pairs of sonic muscles, highly transformed vertebral centra and ribs, a neural arch that pivots and a swimbladder whose anterior end is modified into a bony structure, the rocker bone. The ventral and intermediate muscles cause the rocker bone to swivel inward, compressing the swimbladder, and this action is antagonized by the dorsal muscle. Unlike other sonic systems in which the muscle contraction rate determines sound fundamental frequency, we hypothesize that slow contraction of these antagonistic muscles produces a series of cycles of swimbladder vibration.     

Capillostrongyloides arapaimae sp. n. (Nematoda: Capillariidae), a new intestinal parasite of the arapaima Arapaima gigas from the Brazilian Amazon

A new nematode species, Capillostrongyloides arapaimae sp. n., is described from the intestine and pyloric caeca of the arapaima, Arapaima gigas (Schinz), from the Mexiana Island, Amazon river delta, Brazil. It is characterized mainly by the length of the spicule (779-1,800 microm), the large size of the body (males and gravid females 9.39-21.25 and 13.54-27.70 mm long, respectively) and by the markedly broad caudal lateral lobes in the male. It is the third species of genus Capillostrongyloides reported to parasitize Neotropical freshwater fishes.     

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     

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.     

Phylogenetic Studies of Complete Mitochondrial DNA Molecules Place Cartilaginous Fishes Within the Tree of Bony Fishes

It is commonly acknowledged that cartilaginous fishes, Chondrichthyes, have a basal position among the Gnathostomata (jawed vertebrates). In order to explore this relationship we have sequenced the complete mitochondrial genome of the spiny dogfish, Squalus acanthias, and included it in a phylogenetic analysis together with a number of bony fishes and amniotes. The phylogenetic reconstructions placed the dogfish among the bony fishes. Thus, and contrary to the common view, the analyses have shown that the position of the sharks is not basal among the gnathostomes. The presently recognized phylogenetic position of the dogfish was identified irrespective of the outgroup used, echinoderms or agnathan fishes. The lungfish was the most basal gnathostome fish, while the teleosteans had an apical position in the piscine tree. A basal position of the dogfish among the gnathostomes was statistically rejected, but the phylogenetic relationship among the coelacanth, spiny dogfish, and teleosts was not conclusively resolved. The findings challenge the current theory that sharks and other chondrichthyans, if monophyletic, are the sister group to all other extant gnathostomes. The results open to question the status of several morphological characters commonly used in piscine phylogenetic reconstruction, most notably the presence versus absence of endochondral bone in the endoskeleton, the macromeric versus micromeric structure of the exoskeleton, and the presence/absence of swimbladder and/or lung. The study also confirmed recent findings demonstrating that the origin of the amniotes is deeper than the diversification of extant bony fishes. Received: 12 March 1998 / Accepted: 12 June 1998     

The evolution of the premaxillary protrusion system in some teleostean fish groups

Changes in the acanthopteran (acanthopterygian) system of premaxillary protrusion are traced from its incipient representation in the iniomous (myctophiform) genus Aulopus to its fully evolved form in the percoids. Two complementary components of the system are differentiated. One is the protrusion of the premaxillary, brought about primarily by the anteroventral movement of a ligament attached to the rostral cartilage. The second, which distinguishes the acanthopteran system from other types of jaw protrusion, is the emplacement of a bony maxillary wedge between the skull and the protruded premaxillary.
The acanthopteran type of protrusion appears to have evolved in large-mouthed fishes, with the lateral expansion of the gape that occurs in such forms a fundamental element of this system's mechanics. The modifications that occur in small-mouthed fishes with little or no lateral expansion of the gape are discussed.
Premaxillary protrusion was investigated in available fish groups sometimes placed between the iniomous fishes and the percoids in classifications. Of these groups, the beloniform and cyprinodont fishes have developed protrusion systems of non-acanthopteran types.     

Activity and inhibition of carbonic anhydrase in Amia calva, a bimodal-breathing holostean fish

Carbonic anhydrase (CA) activity was measured in the respiratory swimbladder, gill filaments and red blood cells of the primitive air-breathing holostean fish, the bowfin, Amia calva . The activity of swimbladder CA, relative to gill and red cell CA activities, was within the range reported previously for unimodally-breathing fishes and was comparable to the CA activities reported for the air-breathing organs of teleosts. It is unlikely that carbon dioxide excretion across the bowfin swimbladder is limited to the uncatalyzed rate of HCO₃-dehydration. Bowfin blood plasma lacked any endogenous inhibitor(s) of CA, in contrast with information on teleostean fishes. This absence may have interesting phylogenetic implications and may offer some potential for investigating the nature and physiological role of plasma CA inhibitors.     

Assessing CITES non-detriment findings procedures for Arapaima in Brazil

Arapaima are listed as endangered fishes according to the Convention on International Trade of Endangered Species of Wild Fauna and Flora (CITES), thus their international trade is regulated by non-detriment finding (NDF) procedures. The authors critically assessed Brazil's regulations for NDF procedures for Arapaima using IUCN's checklist for making NDFs, and found that those regulations cannot ensure the sustainability of Arapaima populations. Arapaima are among the largest fishes in the world, migrate short distances among several floodplain habitats, and are very vulnerable to fishing during spawning. They are threatened mainly by overfishing. The fishery is largely unregulated because government regulations on size, season, and even moratoriums on capture have been very poorly enforced. Arapaima remain poorly understood and the taxonomy and geographical distribution of the genus remain uncertain. There are no data on catch levels or status of wild populations, although available information suggests they are in decline. Brazil's NDF procedures for specimens originating in the wild are inadequate as they rely on 'technical opinion reports', which do not necessarily require scientific evidence. Furthermore, Brazil's NDF procedures exempt the need for NDF reports on 'captive' specimens; however, 'captive' specimens originating in the wild and raised in captivity can be exported because regulations do not specify that they must be 'captive-bred'. Six suggestions are offered to improve the reliability of NDF procedures for Arapaima in Brazil, emphasizing the utility of participatory monitoring and adaptive harvesting to strengthen much needed harvest control capacity in other tropical fisheries.     

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.     

Electrosensory ampullary organs are derived from lateral line placodes in cartilaginous fishes

Ampullary organ electroreceptors excited by weak cathodal electric fields are used for hunting by both cartilaginous and non-teleost bony fishes. Despite similarities of neurophysiology and innervation, their embryonic origins remain controversial: bony fish ampullary organs are derived from lateral line placodes, whereas a neural crest origin has been proposed for cartilaginous fish electroreceptors. This calls into question the homology of electroreceptors and ampullary organs in the two lineages of jawed vertebrates. Here, we test the hypothesis that lateral line placodes form electroreceptors in cartilaginous fishes by undertaking the first long-term in vivo fate-mapping study in any cartilaginous fish. Using DiI tracing for up to 70 days in the little skate, Leucoraja erinacea, we show that lateral line placodes form both ampullary electroreceptors and mechanosensory neuromasts. These data confirm the homology of electroreceptors and ampullary organs in cartilaginous and non-teleost bony fishes, and indicate that jawed vertebrates primitively possessed a lateral line placode-derived system of electrosensory ampullary organs and mechanosensory neuromasts.     

Swimming behavior in relation to buoyancy in an open swimbladder fish, the Chinese sturgeon

The swimbladder of fishes is readily compressed by hydrostatic pressure with depth, causing changes in buoyancy. While modern fishes can regulate buoyancy by secreting gases from the blood into the swimbladder, primitive fishes, such as sturgeons, lack this secretion mechanism and rely entirely on air gulped at the surface to inflate the swimbladder. Therefore, sturgeons may experience changes in buoyancy that will affect their behavior at different depths. To test this prediction, we attached data loggers to seven free-ranging Chinese sturgeons Acipenser sinensis in the Yangtze River, China, to monitor their depth utilization, tail-beating activity, swim speed and body inclination. Two distinct, individual-specific, behavioral patterns were observed. Four fish swam at shallow depths (7–31 m), at speeds of 0.5–0.6 m s⁻¹, with ascending and descending movements of 1.0–2.4 m in amplitude. They beat their tails continuously, indicating that their buoyancy was close to neutral with their inflated swimbladders. In addition, their occasional visits to the surface suggest that they gulped air to inflate their swimbladders. The other three fish spent most of their time (88–94%) on the river bottom at a depth of 106–122 m with minimum activity. They occasionally swam upwards at speeds of 0.6–0.8 m s⁻¹ with intense tailbeats before gliding back passively to the bottom, in a manner similar to fishes that lack a swimbladder. Their bladders were probably collapsed by hydrostatic pressure, resulting in negative buoyancy. We conclude that Chinese sturgeons behave according to their buoyancy, which varies with depth due to hydrostatic compression of the swimbladder.     

Development of the respiratory swimbladder of Pangasius sutchi

The swimbladder of Pangusius sutchi first appears on the dorsal surface of the oesophagus at about 5 days after hatching. The swimbladder has double chambers when it is separated by a medial septum at 8–10 days. Alveoli start to develop and function in air-breathing at 12–14 days. Their number is increased by subdivision, and the respiratory portion grows towards the centre. Morphometric analysis shows that the swimbladder increases in respiratory surface, volume and surface area: volume ratio during development. On a histological basis, the development of the swimbladder is divided into three distinct periods: a blind tube, a double chamber and an alveolus period. It is characteristic that the flat epithelial cell arises from a primordial cuboidal cell and that a double capillary system is arranged in the interalveolar septa. Multilamellar bodies appear and a blood-air barrier is established when the swimbladder becomes functional.     

The contribution of the swimbladder to buoyancy in the adult zebrafish (Danio rerio): a morphometric analysis

Many teleost fishes use a swimbladder, a gas-filled organ in the coelomic cavity, to reduce body density toward neutral buoyancy, thus minimizing the locomotory cost of maintaining a constant depth in the water column. However, for most swimbladder-bearing teleosts, the contribution of this organ to the attainment of neutral buoyancy has not been quantified. Here, we examined the quantitative contribution of the swimbladder to buoyancy and three-dimensional stability in a small cyprinid, the zebrafish (Danio rerio). In aquaria during daylight hours, adult animals were observed at mean depths from 10.1 +/- 6.0 to 14.2 +/- 5.6 cm below the surface. Fish mass and whole-body volume were linearly correlated (r(2) = 0.96) over a wide range of body size (0.16-0.73 g); mean whole-body density was 1.01 +/- 0.09 g cm(-3). Stereological estimations of swimbladder volume from linear dimensions of lateral X-ray images and direct measurements of gas volumes recovered by puncture from the same swimbladders showed that results from these two methods were highly correlated (r(2) = 0.85). The geometric regularity of the swimbladder thus permitted its volume to be accurately estimated from a single lateral image. Mean body density in the absence of the swimbladder was 1.05 +/- 0.04 g cm(-3). The swimbladder occupied 5.1 +/- 1.4% of total body volume, thus reducing whole-body density significantly. The location of the centers of mass and buoyancy along rostro-caudal and dorso-ventral axes overlapped near the ductus communicans, a constriction between the anterior and posterior swimbladder chambers. Our work demonstrates that the swimbladder of the adult zebrafish contributes significantly to buoyancy and attitude stability. Furthermore, we describe and verify a stereological method for estimating swimbladder volume that will aid future studies of the functions of this organ.     

The origin and evolution of the surfactant system in fish: insights into the evolution of lungs and swim bladders

Several times throughout their radiation fish have evolved either lungs or swim bladders as gas-holding structures. Lungs and swim bladders have different ontogenetic origins and can be used either for buoyancy or as an accessory respiratory organ. Therefore, the presence of air-filled bladders or lungs in different groups of fishes is an example of convergent evolution. We propose that air breathing could not occur without the presence of a surfactant system and suggest that this system may have originated in epithelial cells lining the pharynx. Here we present new data on the surfactant system in swim bladders of three teleost fish (the air-breathing pirarucu Arapaima gigas and tarpon Megalops cyprinoides and the non-air-breathing New Zealand snapper Pagrus auratus). We determined the presence of surfactant using biochemical, biophysical, and morphological analyses and determined homology using immunohistochemical analysis of the surfactant proteins (SPs). We relate the presence and structure of the surfactant system to those previously described in the swim bladders of another teleost, the goldfish, and those of the air-breathing organs of the other members of the Osteichthyes, the more primitive air-breathing Actinopterygii and the Sarcopterygii. Snapper and tarpon swim bladders are lined with squamous and cuboidal epithelial cells, respectively, containing membrane-bound lamellar bodies. Phosphatidylcholine dominates the phospholipid (PL) profile of lavage material from all fish analyzed to date. The presence of the characteristic surfactant lipids in pirarucu and tarpon, lamellar bodies in tarpon and snapper, SP-B in tarpon and pirarucu lavage, and SPs (A, B, and D) in swim bladder tissue of the tarpon provide strong evidence that the surfactant system of teleosts is homologous with that of other fish and of tetrapods. This study is the first demonstration of the presence of SP-D in the air-breathing organs of nonmammalian species and SP-B in actinopterygian fishes. The extremely high cholesterol/disaturated PL and cholesterol/PL ratios of surfactant extracted from tarpon and pirarucu bladders and the poor surface activity of tarpon surfactant are characteristics of the surfactant system in other fishes. Despite the paraphyletic phylogeny of the Osteichthyes, their surfactant is uniform in composition and may represent the vertebrate protosurfactant.     

Rapid and inexpensive analysis of genetic variability in Arapaima gigas by PCR multiplex panel of eight microsatellites

The aim of the present study was the development of a multiplex genotyping panel of eight microsatellite markers of Arapaima gigas, previously described. Specific primer pairs were developed, each one of them marked with either FAM-6, HEX or NED. The amplification conditions using the new primers were standardized for a single reaction. The results obtained demonstrate high heterozygosity (average of 0.69) in a Lower Amazon population. The multiplex system described can thus be considered a fast, efficient and inexpensive method for the investigation of genetic variability in Arapaima populations.     

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.     

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.     

Hydrogen shuttles in air versus water breathing fishes.

1. The malate-aspartate cycle was demonstrable in subcellular preparations of hearts from Arapaima, Lepidosiren, and Synbranchus (obligate air breathers), Hoplerythriunus (facultative air breather), and Osteoglossum and Hoplias (obligate water breathers). 2. Although no respiratory evidence for significant alpha-glycerophosphate cycle participation could be shown in the air breathers, this cycle was demonstrable in hearts of water breathers. 3. In agreement with the O2 uptake studies, it was possible to reconstruct the malate-aspartate, but not the alpha-glycerophosphate cycle, in isolated mitochondria from air breathers, while both shuttles could be reconstructed with heart mitochondria in the case of water breathing fishes.     

Evolution of muscle activity patterns driving motions of the jaw and hyoid during chewing in Gnathostomes

Although chewing has been suggested to be a basal gnathostome trait retained in most major vertebrate lineages, it has not been studied broadly and comparatively across vertebrates. To redress this imbalance, we recorded EMG from muscles powering anteroposterior movement of the hyoid, and dorsoventral movement of the mandibular jaw during chewing. We compared muscle activity patterns (MAP) during chewing in jawed vertebrate taxa belonging to unrelated groups of basal bony fishes and artiodactyl mammals. Our aim was to outline the evolution of coordination in MAP. Comparisons of activity in muscles of the jaw and hyoid that power chewing in closely related artiodactyls using cross-correlation analyses identified reorganizations of jaw and hyoid MAP between herbivores and omnivores. EMG data from basal bony fishes revealed a tighter coordination of jaw and hyoid MAP during chewing than seen in artiodactyls. Across this broad phylogenetic range, there have been major structural reorganizations, including a reduction of the bony hyoid suspension, which is robust in fishes, to the acquisition in a mammalian ancestor of a muscle sling suspending the hyoid. These changes appear to be reflected in a shift in chewing MAP that occurred in an unidentified anamniote stem-lineage. This shift matches observations that, when compared with fishes, the pattern of hyoid motion in tetrapods is reversed and also time-shifted relative to the pattern of jaw movement.     

The skeletal kinematics of lung ventilation in three basal bird taxa (emu, tinamou, and guinea fowl)

In vivo visceral and skeletal kinematics of lung ventilation was examined using cineradiography in two palaeognaths, the emu (Dromaius novaehollandiae) and the Chilean tinamou (Nothoprocta perdicaria), and a basal neognath, the helmeted guinea fowl (Numida meleagris). Upon inspiration, the thorax expands in all dimensions. The vertebral ribs swing forward and upward, thereby increasing the transverse diameter of the trunk. The consistent location of the parapophysis throughout the dorsal vertebral series, ventral and cranial to the diapophysis, ensures a relatively uniform lateral expansion. An increase in the angle between the vertebral and the sternal ribs causes the sternal ribs to push the sternum ventrally. Owing to the greater length of the caudal sternal ribs, the caudal sternal margin is displaced further ventrally than the cranial sternal margin. When observed in lateral view, sternal movement is not linear, but elliptical. The avian thorax is highly constrained in its movement when compared with crocodylians, the other extant archosaur clade. Birds lack a lumbar region and intermediate ribs. Sternal ribs are completely ossified, and have a bicondylar articulation with the sternum. Considering the importance of pressure differences between cranial and caudal air sac complexes for the generation of unidirectional air flow in the avian lung, it is hypothesized that a decrease in the degrees of freedom of movement of the avian trunk skeleton, greater expansion of the ventrocaudal trunk region, and elliptical sternal movement may represent specific adaptations for fine-tuned control over air flow within the complex avian pulmonary system.