Gill surface area of water-breathing freshwater fish

Summary To provide a hitherto lacking review which focuses on gill surface area of freshwater fish, we collected and analysed morphometric data from the literature. The scaling exponent of gill area ranges from 0.36 to 1.13, with a mean value of 0.76. The absolute values for the largest gill areas are about 5 times as high as those of the smallest. This range resembles that of marine fish, if specially adapted steady swimmers, such as tunnies and some sharks, are excluded. Generally it appears that the gill areas of freshwater fish are smaller than those of comparable marine species. To establish whether a relationship exists between gill area and swimming activity or oxygen content of water, the activity of each species and the oxygen content of its habitat were estimated and checked against the gill area. ANOVA revealed that activity explains the presence of the smallest gill areas only, while oxygen content does not correlate with gill area at all. The morphometric variables determining gill area (total length of filaments, average lamellar density, average lamellar area) are highly correlated; total gill area correlates mainly with lamellar density and to a lesser degree with filament length; lamellar area varies independently. Different populations of the same species exhibit striking differences with respect to gill areas, total length of filaments, average lamellar density and average lamellar area. These differences point to a substantial morphological plasticity of the gill system.     

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.     

Comparative study of gill neuroepithelial cells and their innervation in teleosts and Xenopus tadpoles

Peripheral O₂ chemoreceptors initiate adaptive cardiorespiratory responses to hypoxia in vertebrates. Morphological and physiological evidence suggests that, in fish, neuroepithelial cells (NECs) of the gill perform this role. We conducted a comparative examination in three species of teleosts (zebrafish, goldfish and trout) and larvae of the amphibian Xenopus laevis, using whole-mount gill preparations and confocal immunofluorescence, to elucidate the distribution, morphology and innervation of gill NECs. Nerve fibres were immunolabelled with the neuronal marker zn-12 and were associated with serotonin-immunoreactive NECs in the gills of all species tested. With the exception of trout, innervated NECs were present on all gill arches in the filaments and respiratory lamellae in fish and on homologous structures in Xenopus (i.e. gill “tufts”, including respiratory terminal branches). Thus, the distribution and innervation of NECs of the internal gills of amphibians and teleosts are relatively well conserved, suggesting an important role for gill NECs as O₂ chemoreceptors in aquatic vertebrates. Furthermore, the size and density of gill NECs is variable among teleosts and developmental stages of Xenopus larvae and may be dependent on general gill dimensions or environmental conditions. This report constitutes the first comparative study of gill NECs in fish and amphibians and highlights the significance of gill NECs as an evolutionary model for studying O₂ sensing in vertebrates. We acknowledge the Natural Sciences and Engineering Research Council (NSERC) of Canada for funding through an operating grant to C.A.N., and the NSERC and the Ontario Graduate Scholarship (OGS) program for postgraduate scholarships to M.G.J.     

Morphometry of gill respiratory area in the Baikalian deep-water sculpins Abyssocottus korotneffi and Cottinella boulengeri (Abyssocottidae,Cottoidei)

Abyssocottus korotneffi and Cottinella boulengeri are the deepest-living bottom species among freshwater teleosts. Both species have gill arches with nodulous gill-rakers equipped with sharp denticles. The gill-slit behind the fourth arch is reduced considerably and the hemibranch corresponding to this slit is absent, though some miniature structures resembling reduced filaments were occasionally observed there. The respiratory components of the gill apparatus in both species considered are much reduced, especially in A. korotneffi, because of the moderate number of relatively short gill filaments and the small number of respiratory lamella on them. The allometric relationship between the gill respiratory surface area (GRSA) and body mass (Y = aW^b) is expressed by Y = 328.55 W^0.724 for A. korotneffi (7–22 g) and by Y = 333.15 W^0.902 for C. boulengeri (3–24 g). In adult A. korotneffi, the GRSA index calculated per body weight unit is about 35% lower than that in C. boulengeri, but is 70% higher compared with the bathypelagic golomyanka Comephorus dybowskii previously examined. The data seem to correspond with the difference in biological activity of these species. J. Morphol. 233:105–112, 1997. © 1997 Wiley-Liss, Inc.     

Regional differences in the feeding of the ambush predator Neosebastes pandus and comparisons of diets in the Scorpaenidae,Triglidae and Platycephalidae

This study provides a comprehensive assessment of the dietary composition of the ambush predator Neosebastes pandus and compares the diets of 49 species from 39 studies of three benthic predatory families in the Scorpaeniformes: Scorpaenidae (20 species), Triglidae (19 species) and Platycephalidae (10 species). A total of 275 N. pandus were collected from the west (Rottnest Island) and south (Esperance) coasts of south‐western Australia and the percentage frequency and volumetric contribution of the stomach contents identified. Fish from the west coast consumed a greater mean number of broad taxonomic groups and were more diverse in their diet than fish from the south coast. Cephalopods, brachyurans and teleosts were the largest overall contributors to diet, with teleosts being more important to diets of west‐coast fish and polychaetes for south‐coast fish. This reflects differences in habitat between the two locations. Dietary composition also changed with increasing body size, reflecting morphological changes that allow bigger fish to capture and ingest larger, more mobile prey. Meta‐analysis of the diets of 49 species of scorpaenid, triglid and platycephalid revealed that they feed predominantly on teleosts and large crustaceans. Significant differences in diet were detected among families, with platycephalids being the most distinct and feeding more on teleosts than scorpaenids and triglids.     

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.     

A checklist of parasites of non-native populations of the fish rotan Perccottus glenii (Odontobutidae): Communication II

The fish rotan, Perccottus glenii Dybowski, 1877 (Odontobutidae) is one of the most successful fish invaders during 20th and beginning of 21st century in European and Asian fresh waters. The diversity of its parasites within its invaded range was first reviewed by Sokolov, Reshetnikov, et al. (2014). The current paper analyzes new data from 2013 to 2019 on protistan and metazoan parasites of the non-native populations of this fish. We used information from peer-reviewed journals, difficult to access grey literature and our own recently obtained original data. 45 literature sources were included in the analysis. The newly-available data originate from 95 water bodies of 13 river basins, isolated lakes in West Siberia, and Gulf of Finland, spanning a total of eight countries. A total of 132 recently detected parasite species/taxa are listed in this paper. Each species is presented with its location in/on the host, geographical localities, countries, and according literature sources. When available, number of examined fish as well as prevalence and range of intensity of infection are cited from the original source. This review enlarges contemporary knowledge on parasites of non-native populations of the studied fish species up to 167 species/taxa. We highlight perspectives for further parasitological investigations of this invasive fish.     

Morphometric analysis of the gills of the European eel, Anguilla anguilla

The gills of the European eel, Anguilla unguilla L. were analysed morphometrically. Fresh (unfixed) gills and resin-replica casts of the branchial vascular system were examined. The total gill surface area was found to be proportional to (body mas) 0-715 for fish of between 60 and 1 160 g. This relationship between gill surfxe area and body mass was maintained irrespective of a reduction in body mass produced by fasting. Vessel dimensions were obtained from the vascular casts. Calculations made using these values suggest that the major sites of gill vascular resistance lie at the level of the afferent lamellar arterioles and the secondary lamellae.     

New insights into fish ion regulation and mitochondrion-rich cells

Compared to terrestrial animals, fish have to cope with more-challenging osmotic and ionic gradients from aquatic environments with diverse salinities, ion compositions, and pH values. Gills, a unique and highly studied organ in research on fish osmoregulation and ionoregulation, provide an excellent model to study the regulatory mechanisms of ion transport. The present review introduces and discusses some recent advances in relevant issues of teleost gill ion transport and functions of gill ionocytes. Based on accumulating evidence, a conclusive model of NaCl secretion in gills of euryhaline teleosts has been established. Interpretations of results of studies on freshwater fish gill Na+/Cl- uptake mechanisms are still being debated compared with those for NaCl secretion. Current models for Na+/Cl- uptake are proposed based on studies in traditionally used model species. Many reported inconsistencies are claimed to be due to differences among species, various experimental designs, or acclimation conditions. Having the benefit of advanced techniques in molecular/cellular biology, functional genomics, and model animals, several new notions have recently been raised concerning relevant issues of Na+/Cl- uptake pathways. Several new windows have been opened particularly in terms of molecular mechanisms of ionocyte differentiation and energy metabolite transport between gill cells during environmental challenge.     

Surface ultrastructure of the gill arch of the killifish, Fundulus heteroclitus, from seawater and freshwater, with special reference to the morphology of apical crypts of chloride cells

The surface ultrastructure of the gill arches of the killifish, Fundulus heteroclitus, adapted to seawater or freshwater, was found to be similar to that reported for other euryhaline teleosts. Two rows of gill filaments (about 42 filaments per row) extended posterolaterally, and two rows of gill rakers (about 10 rakers per row) extended anteromedially from each arch. Leaf-like respiratory lamellae protruded along both sides of each filament, from its base to its apex. The distributions, sizes, and numbers of various surface cells and structures were also determined. All surfaces were covered by a mosaic of pavement cells, which measured about 7 X 4 microns and exhibited concentrically arranged surface ridges. Taste buds were especially prominent on the rakers and the pharyngeal surfaces of the first and second gill arches, but were often replaced by horny spines on the third and fourth gill arches. Apical crypts of chloride cells occurred mostly on the surfaces of the gill filaments adjacent to the afferent artery of the filament. In seawater adapted killifish, crypts resembled narrow, deep holes along the borders of adjacent pavement cells, had openings of about 2 microns2, and occurred at a frequency of about 1 per 70 microns2 of surface area. In freshwater fish, the crypts usually had larger openings (about 10 microns2), occurred less frequently (1 per 123 microns2), and exhibited many cellular projections in their interiors. Changes in crypt morphology may be related to the ion transport function of chloride cells.     

Salinity tolerance of two tropical fishes, Oreochromis aureus and O. niloticus. I. Biochemical and morphological changes in the gill epithelium

Cichlids of the genus Oreochromis are fish of economic importance in African countries. They tolerate brackish water, however, with great variations between species. In this work, two species, both from the Ivory Coast but of different origins, O. niloticus (field and laboratory strains) and O. aureus (field strain) were compared during osmotic challenges (10, 20 and 30%o salinity) in order to provide physiological support for their specific behaviour when confronted with natural hypertonic environments. Tolerance to salinity was assessed by correlated observations on gill structure, plasma sodium levels and gill Na⁺/K⁺ ATPase activity. In fresh water (FW), all fish presented a gill epithelium structure characteristic of FW stenohaline fish: no chloride cells (CC) on the lamellae and few CC on the filaments. An increase in external salinity induced the proliferation of CC on filaments, a feature typical of seawater teleosts. This change in gill structure was accompanied by an increase of gill Na⁺/K⁺ ATPase activity. In the most tolerant strains, plasma Na⁺ did not change, indicating successful ion regulation in the hypertonic media. With regard to potential interest of field strains in fish culture, O. aureus acclimated more easily to brackish water than O. niloticus . Interestingly, O. niloticus , kept for several generations in the laboratory, performed best in our challenge studies. Plasma Na⁺ levels and gill CC proliferation upon transfer to an isotonic medium may be the parameters of choice when testing these fish for their response to a salinity change.     

Length-weight relationships of six fish species of tropical lake,Mexico

The length–weight relationships (LWRs) for six native fish species from the Chapala Lake, Mexico, are described in this paper. The fish were caught monthly with the support of local fishermen from different landing sites. The daily catch is obtained using the nasa charalera (pot) and the gill net. Each fisherman can operate 20 pots daily at each fishing site for approximately six or seven months; this pot is a 2 m long cylinder, 0.5 m in diameter, with a mesh opening of 0.5 to 1 cm. Also, each fisherman can set between 10 and 20 gill nets each day at sunset and recover them in the morning, again for six or seven months. The length of the gill net is 30 m or more with a 2 m drop, with a 1 cm mesh size. The study provides basic data, morphometric data on length and weight of native species belonging to the genus Chirostoma. These species are of great importance for the local fishery with the Mesa Central of Mexico.     

Terrestrial locomotion in the climbing perch, Anabas testudineus (Bloch) (Anabantidea, Pisces)

Climbing perches use the tail for forward propulsion when on land. The spiny gill covers are used to obtain purchase on the substratum. Unusually amongst teleosts, the opercular and subopercular bone are not bound strongly together into a single operculum. Instead they are joined only by a thin, flexible membrane, so that the fish has two sections of the gill cover hinged separately; the opercular on the suspensorium and the subopercular on the rearmost part of the lower jaw. The gill covers open very widely and the subopercular rotates ventrally as well as laterally. Two modes of locomotion are employed. Usually Anabus adopts a near-upright posture and alternately drives the left and right spiny suboperculars into the substratum, using the tail to vault over the subopercular (which acts in the manner of a short vaulting pole). During vigorous movement the fish may leave the substratum altogether during the vault. Fatigued fish, or fish which have fallen during climbing, move on their sides, using the tail for propulsion and a single spiny opercular which is repeatedly driven into the substratum. Maximum speeds observed on land corresponded to 1.8 body lengths S^?1. No evidence of involvement of the pelvic fins in locomotion was obtained; the pectorals seemed only to help in tilting the head from side to side and did not contribute significantly to forward propulsion. On mud and tree bark the fish were laterally unstable, often resting on their sides. Grassy substrata provided support and permitted a more upright posture. Slope climbing ability was restricted to 25° when climbing tree bark and 30° when climbing grass. Coupled with lateral instability these observations disqualify the species from any tree-climbing capacity. Anabas can climb vertical obstacles of at least half body length in height by pushing the head against the obstacle, using the spiny gill covers for purchase until one or other subopercular hooks over the top of the barrier. The subopercular is then used as a fulcrum for an upwards vault to clear the obstacle.     

Gill Morphometrics of the Lampreys Lampetra fluviatilis (L.) and Lampetra planeri (Bloch)

Morphometric measurements have been made on various gill components of different stages in the life cycle of the anadromous parasitic lamprey, Lampetra fluviatilis, and its nonparasitic derivative Lampetra planeri. The total gill area, expressed in terms of body weight, of both larval (1462–2717 mm² g^–1) and adult (1402–2337 mm² g^–1) L. fluviatilis are greater than those previously recorded in the rather meagre literature on lamprey gill measurements and are comparable with those found in the most active teleosts. The gills of the two Lampetra species are apparently identical in the larval stages and those of metamorphosing and adult L. planeri are similar to those of metamorphosing L. fluviatilis. Although the pharyngeal arrangement of lampreys differs greatly from that of teleosts, there are many features of the gills indicative of convergence between the two groups. Thus, in a given stage in the life cycle of lampreys, the secondary lamellae on either side of the filaments also alternate, become more widely spaced as the filament length increases and increase in area as the body weight becomes greater. Furthermore, the fractional cumulative increase in secondary lamellae area along a line following the presumed direction of water flow is also represented by a sigmoid curve. While at metamorphosis the pharynx becomes considerably modified to accommodate the change from a unidirectional to a tidal respiratory water flow, the total gill areas of the ammocoete are similar to those of metamorphosing stages which have attained adult characteristics. However, there are clearly differences in some of the components that influence and contribute towards the total gill area. Thus, in terms of body weight, the number and total length of the filaments and the total number of secondary lamellae, together with the number of secondary lamellae found on a given distance of filament, are greater in late metamorphosing stages, while the reverse is true for the average bilateral area of the secondary lamellae which is considerably greater in ammocoetes.     

Morphometries of the respiratory organs of the Indian green snake-headed fish, Channa punctata

Measurements of the dimensions of the different gills and the suprabranchial chambers have been made and the data analysed with respect to body weight using logarithmic transformations (Y = aW^b). The slope (b) for area of the total gill surface is 0–592 and for the supra-branchial chamber 0–696, and their combined respiratory surface: 0–623. The slope values for the surface areas of the 1st, 2nd, 3rd and the 4th gill arches were 0–595,0–578,0–614 and 0–572 respectively.
The slope for secondary lamellae/mm is –0138 and that for the bilateral surface area of an average-sized lamella 0–304.
These results indicate differences in growth patterns for the dimensions of the different gills. The growth-related decrease in the number of secondary lamellae/mm and size of an average secondary lamella together with evidence from "drowning" experiments and diffusing capacity calculation, suggest that this fish is better adapted for aquatic respiration than Anabas or Saccobranchus. The slopes for the total respiratory surface area and gill area seem to be comparatively low in this species.     

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.     

Surface area of the respiratory organs of the Climbing perch, Anabas testudineus (Pisces: Anabantidae)

Measurements have been made of the surface area of the gills and accessory respiratory organs of Anabas in the weight range 1–120 g, and the data analysed with respect to body weight using logarithmic transformations. The slope of the regression line for total gill area (0–615) is less than that found in most fish, the number of secondary lamellae/mm decreased more rapidly with body weight than for most water-breathing species (h = -0.152). The gill area of Anabas is relatively small but when the area of the accessory organs is added, the total respiratory area is of the same order as inactive water-breathing fish. The regression coefficient for combined areas of labyrinthine organs and lining of the suprabranchial chambers (0.713) exceeds that for the gills and together with other evidence (including estimates of diffusing capacity from morphological measurements), indicates an increasing importance of air-breathing of larger specimens. The average surface area of the accessory organs available for 1 ml of air within the suprabranchial chambers was found to be 2226 mm².     

Length–weight relationship of six notothenioid species from sub‐Antarctic waters (Beagle Channel,Argentina)

This study presents length‐weight relationships (LWR) for six species of fishes of the Suborder Notothenioidei that inhabit the sub‐Antarctic waters of the Beagle Channel (Argentina). These species represent five of the nine families of this Suborder. The specimens belong to historical fish collections in the area (from 1987 to 1990) using gill and trammel nets. All species but Eleginops maclovinus had no previous LWR estimates. The coefficient of determination (r²) ranged from 0.91 to 0.99 and b values ranged from 2.74 to 3.2. Harpagifer bispinis was the only species with a b value lower than three. This information is useful to predict the weight from the length data and to provide insights into the ecology of sub‐Antarctic nototheniod fish.     

Review: Assessing fish welfare in research and aquaculture,with a focus on European directives

The number of farmed fish in the world has increased considerably. Aquaculture is a growing industry that will in the future provide a large portion of fishery products. Moreover, in recent years, the number of teleost fish used as animal models for scientific research in both biomedical and ecological fields has increased. Therefore, it is increasingly important to implement measures designed to enhance the welfare of these animals. Currently, a number of European rules exist as requirements for the establishment, care and accommodation of fish maintained for human purposes. As far as (teleost) fish are concerned, the fact that the number of extant species is much greater than that of all other vertebrates must be considered. Of further importance is that each species has its own specific physical and chemical requirements. These factors make it difficult to provide generalized recommendations or requirements for all fish species. An adequate knowledge is required of the physiology and ecology of each species bred. This paper integrates and discusses, in a single synthesis, the current issues related to fish welfare, considering that teleosts are target species for both aquaculture and experimental models in biological and biomedical research. We first focus on the practical aspects, which must be considered when assessing fish welfare in both research and aquaculture contexts. Next, we address husbandry and the care of fish housed in research laboratories and aquaculture facilities in relation to their physiological and behavioural requirements, as well as in reference to the suggestions provided by European regulations. Finally, to evaluate precisely which parameters described by Directive 2010/63/EU are reported in scientific papers, we analysed 82 articles published by European researchers in 2014 and 2015. This review found that there is a general lack of information related to the optimal environmental conditions that should be provided for the range of species covered by this directive.