Gill morphometrics in relation to gas transfer and ram ventilation in high‐energy demand teleosts: Scombrids and billfishes

This comparative study of the gill morphometrics in scombrids (tunas, bonitos, and mackerels) and billfishes (marlins, swordfish) examines features of gill design related to high rates of gas transfer and the high‐pressure branchial flow associated with fast, continuous swimming. Tunas have the largest relative gill surface areas of any fish group, and although the gill areas of non‐tuna scombrids and billfishes are smaller than those of tunas, they are also disproportionally larger than those of most other teleosts. The morphometric features contributing to the large gill surface areas of these high‐energy demand teleosts include: 1) a relative increase in the number and length of gill filaments that have, 2) a high lamellar frequency (i.e., the number of lamellae per length of filament), and 3) lamellae that are long and low in profile (height), which allows a greater number of filaments to be tightly packed into the branchial cavity. Augmentation of gill area through these morphometric changes represents a departure from the general mechanism of area enhancement utilized by most teleosts, which lengthen filaments and increase the size of the lamellae. The gill design of scombrids and billfishes reflects the combined requirements for ram ventilation and elevated energetic demands. The high lamellar frequencies and long lamellae increase branchial resistance to water flow which slows and streamlines the ram ventilatory stream. In general, scombrid and billfish gill surface areas correlate with metabolic requirements and this character may serve to predict the energetic demands of fish species for which direct measurement is not possible. The branching of the gill filaments documented for the swordfish in this study appears to increase its gill surface area above that of other billfishes and may allow it to penetrate oxygen‐poor waters at depth. J. Morphol. 2010. © 2009 Wiley‐Liss, Inc.     

Functional morphology of the gills of the shortfin mako,Isurus oxyrinchus,a lamnid shark

This study examines the functional gill morphology of the shortfin mako, Isurus oxyrinchus, to determine the extent to which its gill structure is convergent with that of tunas for specializations required to increase gas exchange and withstand the forceful branchial flow induced by ram ventilation. Mako gill structure is also compared to that of the blue shark, Prionace glauca, an epipelagic species with lower metabolic requirements and a reduced dependence on fast, continuous swimming to ventilate the gills. The gill surface area of the mako is about one‐half that of a comparably sized tuna, but more than twice that of the blue shark and other nonlamnid shark species. Mako gills are also distinguished from those of other sharks by shorter diffusion distances and a more fully developed diagonal blood‐flow pattern through the gill lamellae, which is similar to that found in tunas. Although the mako lacks the filament and lamellar fusions of tunas and other ram‐ventilating teleosts, its gill filaments are stiffened by the elasmobranch interbranchial septum, and the lamellae appear to be stabilized by one to two vascular sacs that protrude from the lamellar surface and abut sacs of adjacent lamellae. Vasoactive agents and changes in vascular pressure potentially influence sac size, consequently effecting lamellar rigidity and both the volume and speed of water through the interlamellar channels. However, vascular sacs also occur in the blue shark, and no other structural elements of the mako gill appear specialized for ram ventilation. Rather, the basic elasmobranch gill design and pattern of branchial circulation are both conserved. Despite specializations that increase mako gill area and efficacy relative to other sharks, the basic features of the elasmobranch gill design appear to have limited selection for a larger gill surface area, and this may ultimately constrain mako aerobic performance in comparison to tunas. J. Morphol. 271:937–948, 2010. © 2010 Wiley‐Liss, Inc.     

Structures and immunolocalization of Na+, K+ -ATPase, Na+ /H+ exchanger 3 and vacuolar-type H+ -ATPase in the gills of blennies (Teleostei: Blenniidae) inhabiting rocky intertidal areas

The structure and immunolocalization of the ion transporters Na(+) ,K(+) -ATPase (NKA), Na(+) /H(+) exchanger (NHE3) and vacuolar-type H(+) -ATPase (VHA) were examined in the gills of teleosts of the family Blenniidae, which inhabit rocky shores with vertical zonation in subtropical seas. These features were compared among the following species with different ecologies: the amphibious rockskipper blenny Andamia tetradactylus, the intertidal white-finned blenny Praealticus tanegasimae and the purely marine yaeyama blenny Ecsenius yaeyamaensis. Light and electron microscopic observations indicated that thick gill filaments were arranged close to each other and alternately on two hemibranches of a gill arch in the opercular space of A. tetradactylus. Many mucous cells (MC) and mitochondrion-rich cells (MRC) were present in the interlamellar regions of the gill filament. An immunohistochemical study demonstrated that numerous NKA, NHE3 and some VHA were located predominantly on presumed MRCs of gill filaments and at the base of the lamellae. Analyses using serial (mirror image) sections of the gills indicated that only a few NKA immunoreactive cells (IRC) were colocalized with VHA on some MRCs in the filaments. In the gills of P. tanegasimae, NKA- and NHE3-IRCs were observed in the interlamellar region of the filaments and at the base of the lamellae. VHA-IRCs were located sparsely on the lamellae and filaments. In the gills of E. yaeyamaensis, the lamellae and filaments were thin and straight, respectively. MCs were located at the tip as well as found scattered in the interlamellar region of gill filaments. NKA-, NHE3- and VHA-IRCs were moderately frequently observed in the filaments and rarely on the lamellae. This study shows that the structure and distribution of ion transporters in the gills differ among the three blennid species, presumably reflecting their different ecologies.     

Gross structure of the respiratory organs and dimensions of the gill in the mud–skipper, Periophthalmodon schlosseri (Bleeker)

In Periopkrlialnwdon scldosseri the respiratory organs consist of the gills, the suprabranchial and opercular chambers. The gills are more suited for aerial than aquatic respiration as is shown by the presence of the vascular papillae, blood sinusesand dilated blood vessels in their lamellae. The gill lamellae possess a surface coat of sulphated mucopolysaccharides that prevents water loss during exposure to the air. The filaments of the outer hemibranchs in the first gill arch are reduced to nearly one quarter of those of its posterior hemibranch. The gill area in relation to body weight shows a high slope value ( b =0·93).     

鲤鳃表面结构扫描电镜研究

鲤的鳃丝表面显示了由三边形一六边形不等的表皮细胞,呈现出各种图案式的结构。     

Gill-derived glands in glandulocaudine fishes (teleostei: Characidae: Glandulocaudinae)

The Glandulocaudinae is a subfamily of neotropical characid fishes from Central and South America. A unifying feature of the subfamily is the caudal gland, found almost exclusively in males. The gland consists of tissue on the base of the caudal fin covered in part by hypertrophied scales. Scale movement as the caudal fin is flexed appears to facilitate the release of chemical compounds from the glandular tissue. We describe here a different structure, found in the gill cavity of mature males in 12 of 17 glandulocaudine genera examined. Termed a gill gland, it develops as a male secondary sex character and appears morphologically suited to release chemical signals. The gland forms by the growth of tissue over and around 4-13 anterior gill filaments on the first gill arch, forming chambers with ventral openings. Within the gland chambers, gill secondary lamellae usually shorten and may disappear. When secondary lamellae persist, simple columnar epithelial cells develop between them. In the absence of secondary lamellae, the gland chambers are lined with a simple cuboidal or columnar epithelium. Gland size and the degree of gill modification vary among species. Gill glands appear absent in five glandulocaudine genera, suggesting character reversals based on current phylogenetic hypotheses and systematic classification. Gill gland morphology suggests that this structure releases chemical compounds into the gill current. The presence of gill glands only in mature males suggests a function in reproduction and/or male aggression. Together with studies of the caudal gland, this research suggests that chemical signals may play important roles in glandulocaudine reproduction.     

Gill remodelling during terrestrial acclimation in the amphibious fish Polypterus senegalus

Fishes are effectively weightless in water due to the buoyant support of the environment, but amphibious fishes must cope with increased effective weight when on land. Delicate structures such as gills are especially vulnerable to collapse and loss of surface area out of water. We tested the ‘structural support’ hypothesis that amphibious Polypterus senegalus solve this problem using phenotypically plastic changes that provide mechanical support and increase stiffness at the level of the gill lamellae, the filaments, and the whole arches. After 7 d in terrestrial conditions, enlargement of an inter-lamellar cell mass filled the water channels between gill lamellae, possibly to provide structural support and/or reduce evaporative water loss. Similar gill remodelling has been described in several other actinopterygian fishes, suggesting this may be an ancestral trait. There was no change in the mechanical properties or collagen composition of filaments or arches after 7 days out of water, but 8 months of terrestrial acclimation caused a reduction in gill arch length and mineralized bone volume. Thus, rather than increasing the size and stiffness of the gill skeleton, P. senegalus may instead reduce investment in supportive gill tissue while on land. These results are strikingly similar to the evolutionary trend of gill loss that occurred during the tetrapod invasion of land, raising the possibility that genetic assimilation of gill plasticity was an underlying mechanism.     

Unique adaptations of the metabolic biochemistry of tunas and billfishes for life in the pelagic environment

Synopsis Virtually all characteristics of tunas and billfishes reflect their highly charged lifestyles as apex predators in the oceanic pelagic environment. The adaptations they possess for efficient and rapid swimming, efficient and rapid food processing, turnover of nutrients and storage and mobilization of internal fuel supplies, and for rapid recovery rates, are discussed. Overall, tunas and billfishes are designed for high performance, at both sustainable and burst swimming speeds, but there are several differences between tunas and billfishes. Tunas' aerobic metabolic capacities exceed those of ectothermic fishes, including billfishes and other scombrids, by virtue of their elevated red muscle temperatures, and because heart and white muscle aerobic capacities are significantly greater in tunas. The adaptations for high performance involve some costs, including the need for a constant high energy input to sustain high metabolic rates, high activity levels, and endothermy, Yet, tunas and billfishes have adopted successful lifestyles, as evidenced by their large numbers and biomass within the marine environment. Although our knowledge of these fishes has increased dramatically during the past 15 years, there are major gaps in our understanding of the metabolic biochemistry and physiology of these fishes, and these are highlighted so that additional research can be directed towards filling these gaps.Paper from the International Union of Biological Societies symposium The biology of tunas and billfishes: an examination of life on the knife edge, organized by Richard W. Brill and Kim N. Holland.     

Gills of the medaka (Oryzias latipes): A scanning electron microscopy study

The general morphology and surface ultrastructure of the gills of adult and larvae medaka (Oryzias latipes) were studied in freshwater and seawater using scanning electron microscopy. The gills of all examined fish were structurally similar to those of other teleosts and consisted of four pairs of arches supporting (i) filaments bearing lamellae and (ii) rakers containing taste buds. Three cell types, specifically pavement cells, mitochondria‐rich cells (MRCs), and mucous cells, constituted the surface layer of the gill epithelium. Several distinctive characteristics of medaka gills were noted, including the presence of regularly distributed outgrowth on the lamellae, enlarged filament tips, the absence of microridges in most pavement cells in the filament and lamellae and the presence of MRCs in the arch at the filament base. A rapid mode of development was recorded in the gills of larval fish. At hatching, the larvae already had four arches with rudimentary filaments, rakers, and taste buds. The rudimentary lamellae appeared within 2 days after hatching. These results suggest the early involvement of larval gills in respiratory and osmoregulation activities. The responses of the macrostructures and microstructures of gills to seawater acclimation were similar in larvae and adult fish and included modification of the apical surface of MRCs, confirming the importance of these cells in osmoregulation. The potential roles of these peculiarities of the macrostructures and microstructures of medaka gills in the major functions of this organ, such as respiration and osmoregulation, are discussed.     

Microhabitats of gill parasites (Monogenea and copepoda) of teleosts (Scomberoides spp.)

Ramasamy P., Ramalingam K., Hanna R. E. B. and Halton D. W. 1985. Microhabitat of gill parasites (Monogenea and Copepoda) of teleosts (Scomberoides spp.). International Journal for Parasitology15: 385–397. The parasites Vallisia indica, Allodiscocotyla chorinemi, Heterapta chorinemi, and Dionchus remorae exhibited site specificity on the gills of Scomberoides commersonianus, S. tol, S. lysan and S. tala, whereas the copepod Caligus sp. did not. Observations on site preference revealed microhabitat differences along the length of gill filaments, along the anterio-posterior axis of the gill, between external and internal gill filaments and on different gill arches. Site preference varied with parasite density on each gill and host. An interspecific association test between pairs of species revealed, in some cases, a positive association, and in other cases a negative association. There were apparently no association? between certain pairs of species. A comparison of intensity within pairs of parasite species infecting the same host revealed either an inverse or a direct correlation. The numerical dominance and prevalence of parasites differed on each host species. This study indicates that intra- and interspecific competition may occur among the gill parasites. The direction and speed of ventilation water-currents and certain intrinsic factors of the parasite themselves may determine their microhabitat restriction on the gills.     

Functional morphology of gills and respiratory area of two active rheophilic fish species, Plagioscion squamosissimus and Prochilodus scrofa

Measurements of gill dimensions were carried out on two ecologically distinct active rheophilic teleost species, the curvina Plagioscion squamosissimus and the curimbatá Prochilodus scrofa , and were analysed in relation to body mass according to the equation Y=aW^b . The gill respiratory areas of P. squamosissimus and P. scrofa were large as expected for active fish and increased with increasing body mass ( b =0.70 and 0.72, respectively) showing no significant difference between them. However, the large respiratory area of both species was realized in a different way revealing an adaptation to the plasticity of head components related to feeding habits. Consequently, significant differences were found between the number and average length of gill filaments and the bilateral area of secondary lamellae. The respiratory area of P. scrofa was due mainly to larger bilateral surface area of the secondary lamellae and its growth coefficient ( b =0.51) that was significantly higher ( P <0.05) than that found for P. squamosissimus ( b = 0.36). The frequency of secondary lamellae mm⁻¹ of filament was similar in both species (22 ± 2 on one side of gill filament). The dimensions of gill components and the respiratory area of these species suggest a complex interaction between head form, and feeding habits related to the functional morphology of the gills to meet the oxygen requirements of each species.     

Histomorphological alterations in organs of the plaicePleuronectes obscurus from a polluted part of Peter the Great Bay, Sea of Japan

This paper describes the results of a histological study of the internal organs of the plaicePleuronectes obscurus from a polluted part of Amurskii Bay, Sea of Japan. A variety of histomorphological alterations were found in the gills and liver, while the kidney and spleen were affected to a lesser degree. The most frequent lesions in gills were edemas of gill lamellae, epithelial detachments, fusions of the secondary lamellae, hypertrophies and hyperplasias of respiratory cells, pigment accumulations, the presence of parasites, increased quantities of mucous cells, lymphocyte infiltrations, and disturbances of blood circulation. Characteristic morphological changes in the liver were lipid and hydropic dystrophy, pigment accumulation, and the presence of regenerative and necrotic foci. Telangiectasia, globate filaments, and xenomas were found in the gills ofP. obscurus for the first time. These morphological alterations appear to be a result of the chronic effect of pollution in Amurskii Bay.     

On the conservative nature of the gill filaments of sharks

Synopsis Gill filaments of one highly active and two less active shark species exhibit a conservative morphological scheme including such features as branchial canopies, marginal lamellar projections, and enlarged, discrete outer marginal lamellar channels and lateral lamellar sinuses. The specific spatial orientation of the secondary lamellae respective to one another, the gill filaments, and the interbranchial septa create what appears as one-way interfilament water channels, suggesting the presence of an efficient branchial countercurrent system. It is proposed that the fortified structure of shark gills allows many shark species to ventilate passively without having evolved gill filament modifications as apparently did some highly active teleosts. This in turn may have expedited the evolution of lamnid shark species through pre-adaptation to a swift oceanic lifestyle.     

Gill area and dimensions of gilthead sea bream Sparus aurata L.

Detailed measurements of gill area and constituent variables (total filament length, lamellar frequency and bilateral area) were performed on both hemibranchs of all eight arches in six specimens of gilthead sea bream Sparus aurata (mean ±s.e . 49·9 ± 0·2 g). Shrinkage was also quantified and results were corrected accordingly. Filament number decreased from the first to the fourth gill arch, and average bilateral area of secondary lamellae was higher in the second and third arches. Total and mean filament length, total number of secondary lamellae and total gill area (A_TG) were lower in posterior than in anterior hemibranchs of the second, third and fourth gill arches; while the opposite was observed for the first arch. Lamellar frequency was increased in posterior hemibranchs of all arches compared to that in anterior hemibranchs, especially at the fourth arch. Comparison of the actually measured A_TG and constituent variables with estimates revealed that the third gill arch is the most representative for appropriate measurements and that any of its components (even one hemibranch) approximates the best A_TG (within the range of 0·2–4·3%, P > 0·05) and related dimensions. Consequently, necessary measurements were restricted to the posterior hemibranch of the third gill arch, and A_TG and dimensions (y) were estimated in 21 specimens (23·5–217·6 g) and correlated to body mass (M) according to the allometric equation y = aM^b. As fish increased in size, A_TG (b= 0·664), total (b= 0·425) and mean (b= 0·323) filament length, total number of filaments (b= 0·103) and secondary lamellae (b= 0·377), as well as average lamellar bilateral area (b= 0·288), increased, while the opposite was observed for lamellar frequency (b=?0·049) and mass‐specific area (b=?0·336). Data obtained are discussed in relation to S. aurata activity and living ethology.     

The gill of fish larvae. Is it primarily a respiratory or an ionoregulatory structure?

Based on surface area and chloride cell number, rainbow trout Oncorhynchus mykiss gills appear initially to be more important in terms of ion balance than gas exchange. Chloride cells appear on the gill 3–6 days before hatch at 10°C. This is about 9 days before secondary lamellae, the definitive adult gas exchange structure, begin to form. At hatch, 22% of all chloride cells but only 7% of total surface area are located on the gill. This discrepancy gradually diminishes but even at complete yolk absorption the gill still seems to be about twice as important in terms of ion balance (75% of chloride cells) as gas exchange (37% of total surface area represented by gill filaments and lamellae combined). Surface area measurements and chloride cell counts reported in the literature for larvae of other species show a similar pattern suggesting that this may be a general phenomenon. If true, the implications are profound not only for developmental physiologists but also for those interested in the evolutionary history of gills and their function in adult fish.     

Scanning electron microscopy of the gills of a freshwater catfish,Rita Rita

Variations in the gross morphology and surface architecture of the gill filaments and secondary lamellae of a freshwater catfish (Rita rita) have been investigated using scanning electron microscopy. Heterogeneity of the gill has been correlated with the distribution of lamellar water-flow at different regions of a gill filament. Higher lamellar water flow (cc/pore/cmH₂O/sec) was estimated for the middle region of the filaments. The filaments are covered with epithelial cells whose surface is provided with well-developed microridges. The lamellae are generally covered with microvillous epithelial cells. The variations in surface architecture of the gill filaments and secondary lamellae have been correlated with their probable functions.     

Structural organization of the gills in pipefish (Teleostei,Syngnathidae)

Summary The morphology and structural features of the gills of the two Western Baltic pipefish Nerophis ophidion and Syngnathus rostellatus were investigated using scanning electron microscopy. The general anatomy of the gills complies with the general pattern in fish. Several adaptations though, show the highly specialized nature of pipefish gills. The filaments are extremely short, few in number and carry only a few lamellae due to the limited space in the branchial cavity. The lamellae have a widely projecting form yet still have a small area in comparison to other fish. Gill irrigation is performed by a specialized pumping mechanism which forces respiratory water through the small but densely packed gill sieve. Although both species live in the same habitat and belong to the same family, differences in gill morphology were found and are related to different lifestyles. S. rostellatus is the more active species and therefore has more filaments per gill arch, more lamellae per filament, wider projecting lamellae and a more extreme utilisation of available space in the gill cavity through a very densely packed gill sieve. N. ophidion has a stationary mode of life and therefore has a less extreme gill anatomy.     

Gill‐derived glands in species of Astyanax (Teleostei: Characidae)

The presence of a gill‐derived gland is herein reported for the first time in males of species of Astyanax and related genera; they are described through histological cuts and SEM. The gill‐derived glands described for the Characidae, when fully developed, present a similar structure in different species. The main external feature of gill‐derived glands is the fusion of anteriormost gill filaments on the ventral branch of first gill arch. This fusion is caused by squamous stratified epithelial tissue that covers adjacent filaments, forming a series of chambers. In the region where the gill‐derived gland develops, the secondary lamellae of the gill filaments are much reduced or completely atrophied being characterized by the presence of glandular cells forming nests.     

The evolution of thunniform locomotion and heat conservation in scombrid fishes: New insights based on the morphology of Allothunnus fallai

Two significant functional differences–a more anterior and internally positioned red myo‐tomal muscle mass and modification of the red‐muscle vascular supply to form counter‐current heat exchangers–distinguish the tunas (tribe Thunnini) from other species in the teleost family Scombridae. Neither of these characteristics is found in the bonitos (tribe Sardini), the sister group to the Thunnini. The most recent scombrid classification places the slender tuna, Allothunnus fallai, in the tribe Sardini, but some earlier studies suggested that this species should be a member of the Thunnini. Allothunnus fallai does not possess the lateral subcutaneous arteries and veins or the lateral heat‐exchanging retia typical of tunas. However, we have found that this species has a highly modified central circulation (dorsal aorta, post cardinal vein, and associated branch vessels) similar to the central heat‐exchanging retia of certain tunas, an enlarged haemal arch to accommodate this structure, and the anterior, internal placement of red muscle characteristic of tunas. With these new characters, phylogenetic reconstructions based on parsimony place A. fallai as the sister taxon to the tunas, establish that it is the most basal tuna species, and support the hypothesis that the derivation of tunas from a bonito‐like ancestor occurred through selection for an integrated set of characteristics affecting locomotion and endothermy. The major features of this hypothesis are as follows. (1) Selection for continuous, steady, and efficient swimming resulted in changes in body shape (the result of enlargement of the anterior myotomes, the anterior and internal shift of red muscle, and a narrowing of the caudal peduncle) which increased streamlining and led to the adoption of the thunniform swimming mode unique to the tunas. (2) Alterations in blood supply necessitated by the anterior shift in red muscle led to the interdigitation of numerous arterial and venous branches which set the stage for heat conservation. (3) The evolution of endothermy, together with thunniform swimming, contributed significantly to the ecological radiation and diversification of tunas during the Early Tertiary Period. Our studies of A fall thus suggest that the shift in red muscle position and changes in central circulation preerded the evolution of red‐muscle endothermy. Co‐evolutionary changes in red muscle quantity and distribution and in vascular specializations for heat conservation have led to different macroevolutionary trajectories among the now five genera and 14 tuna species of tunas and appear to reflect the influence of changing paleocological and paleoccanographic conditions, including cooling, that occurred in the Tertiary     

The source of lamellar mitochondria-rich cells in the air-breathing fish, Trichogaster leeri

Pavement cells and the mitochondria-rich cells (MRCs) are two of the main types of cells in fish gill epithelia. The pavement cells are generally responsible for gas exchange and MRCs for ion regulation. MRCs are found especially in the trailing edge and the interlamellar region of gill filament. In some species, MRCs are also observed in the gill lamellae. A previous study reported the likelihood of having lamellar MRCs in air-breathing fishes. Nevertheless, the source of lamellar MRCs is unclear. We used the air-breathing fish, Trichogaster leeri, to investigate the source of proliferated cells on the lamellae when 5-bromo-2-deoxyuridine (BrdU) was injected at different times before fish were sampled from deionized water. There were two major findings in this study. First, undifferentiated cells were found in the lamellae, as well as in the filaments. And, within 12-24 hr, a proliferated cell, identified as BrdU cell, could differentiate to an MRC in the gill lamellae. Second, the filaments and the lamellae in T. leeri responded to ionic stress differently but the proportion of the proliferated MRCs to the BrdU cells remained constant. Our results suggested that the lamellar MRCs were mainly differentiated from the cells that proliferated earlier from the lamellae.