Evolution of the branchiostegal membrane and restricted gill openings in Actinopterygian fishes

A phylogenetic survey is a powerful approach for investigating the evolutionary history of a morphological characteristic that has evolved numerous times without obvious functional implications. Restricted gill openings, an extreme modification of the branchiostegal membrane, are an example of such a characteristic. We examine the evolution of branchiostegal membrane morphology and highlight convergent evolution of restricted gill openings. We surveyed specimens from 433 families of actinopterygians for branchiostegal membrane morphology and measured head and body dimensions. We inferred a relaxed molecular clock phylogeny with branch length estimates based on nine nuclear genes sampled from 285 species that include all major lineages of Actinopterygii. We calculated marginal state reconstructions of four branchiostegal membrane conditions and found that restricted gill openings have evolved independently in at least 11 major actinopterygian clades, and the total number of independent origins of the trait is likely much higher. A principal component analysis revealed that fishes with restricted gill openings occupy a larger morphospace, as defined by our linear measurements, than do fishes with nonrestricted openings. We used a decision tree analysis of ecological data to determine if restricted gill openings are linked to certain environments. We found that fishes with restricted gill openings repeatedly occur under a variety of ecological conditions, although they are rare in open‐ocean pelagic environments. We also tested seven ratios for their utility in distinguishing between fishes with and without restricted gill openings, and we propose a simple metric for quantifying restricted gill openings (RGO), defined as a ratio of the distance from the ventral midline to the gill opening relative to half the circumference of the head. Functional explanations for this specialized morphology likely differ within each clade, but its repeated evolution indicates a need for a better understanding of diversity of ventilatory morphology among fishes. J. Morphol. 276:681–694, 2015. © 2015 Wiley Periodicals, Inc.     

Fish gill morphology: inside out

In this short review of fish gill morphology we cover some basic gross anatomy as well as in some more detail the microscopic anatomy of the branchial epithelia from representatives of the major extant groups of fishes (Agnathans, Elasmobranchs, and Teleosts). The agnathan hagfishes have primitive gill pouches, while the lampreys have arch-like gills similar to the higher fishes. In the lampreys and elasmobranchs, the gill filaments are supported by a complete interbranchial septum and water exits via external branchial slits or pores. In contrast, the teleost interbranchial septum is much reduced, leaving the ends of the filaments unattached, and the multiple gill openings are replaced by the single caudal opening of the operculum. The basic functional unit of the gill is the filament, which supports rows of plate-like lamellae. The lamellae are designed for gas exchange with a large surface area and a thin epithelium surrounding a well-vascularized core of pillar cell capillaries. The lamellae are positioned for the blood flow to be counter-current to the water flow over the gills. Despite marked differences in the gross anatomy of the gill among the various groups, the cellular constituents of the epithelium are remarkably similar. The lamellar gas-exchange surface is covered by squamous pavement cells, while large, mitochondria-rich, ionocytes and mucocytes are found in greatest frequency in the filament epithelium. Demands for ionoregulation can often upset this balance. There has been much study of the structure and function of the branchial mitochondria-rich cells. These cells are generally characterized by a high mitochondrial density and an amplification of the basolateral membrane through folding or the presence of an intracellular tubular system. Morphological subtypes of MRCs as well as some methods of MRC detection are discussed.     

Functional anatomy of the internal gills of the tadpole of Litoria ewingii (Anura,Hylidae)

Summary (1) Scanning electron microscopy and vascular casting were used to study the morphology and vascular anatomy of the fully developed internal gills of Litoria ewingii tadpoles. — (2) The four pairs of gills were located in two branchial baskets on either side of the heart. Each gill consisted of a branchial arch with gill tufts projecting ventrally and gill filters running dorsally. The gills bore a variable number of gill tufts in which a complex three-dimensional array of capillary loops, of varying lengths and diameters, was trailed in the path of the ventilatory current. — (3) The evidence presented in this paper suggests that the gill tufts have greater potential as gas exchangers than either the gill filters or skin. — (4) The study revealed structural and functional evidence for the existence of branchial shunts between afferent and efferent branchial arteries.     

Making a master filterer: Ontogeny of specialized filtering plates in silver carp (Hypophthalmichthys molitrix)

Filter feeding fishes possess several morphological adaptations necessary to capture and concentrate small particulate matter from the water column. Filter feeding teleosts typically employ elongated and tightly packed gill rakers with secondary bony or epithelial modifications that increase filtering efficiency. The gill rakers of Hypophthalmichthys molitrix, silver carp, are anatomically distinct from and more complex than the filtering apparatus of other teleostean fishes. The silver carp filtering apparatus is composed of biserial, fused filtering plates used to capture particles ranging in size from 4 to 80 μm. Early in ontogeny, at 15–25 mm standard length (SL), silver carp gill rakers are reminiscent of other more stereotypical teleostean rakers, characterized by individual lanceolate rakers that are tightly packed along the entirety of the branchial arches. At 30 mm SL, secondary epithelial projections and concomitant dermal ossification begin to stitch together individual gill rakers. During later juvenile stages, dermal bone further modifies the individual gill rakers and creates a bony scaffold that supports the now fully fused and porous epithelium. By adulthood, the stitching of bone and complete fusion of the overlying epithelium creates rigid filtering plates with morphologically distinct faces. The inner face of the plates is organized into a net‐like matrix while the outer face has a sponge‐like appearance comprised of differently sized pores. Here, we present morphological data from an ontogenetic series of the filtering apparatus within silver carp. These data inform hypotheses regarding both how these gill raker plates may have evolved from a more basal condition, as well as how this novel architecture allows this species to feed on exceedingly small phytoplankton, particles that represent a greater filtering challenge to the typical anatomy of the gill rakers of fishes.     

The filter pads and filtration mechanisms of the devil rays: Variation at macro and microscopic scales

Three lineages of cartilaginous fishes have independently evolved filter feeding (Lamniformes: Megachasma and Cetorhinus, Orectolobiformes: Rhincodon, and Mobulidae: Manta and Mobula); and the structure of the branchial filters is different in each group. The filter in Rhincodon typus has been described; species within the Lamniformes have simple filamentous filters, but the anatomy and ultrastructure of the branchial filter in the mobulid rays varies and is of functional interest. In most fishes, branchial gill rakers are elongated structures located along the anterior ceratobranchial and/or epibranchial arches; however, mobulid gill rakers are highly modified, flattened, lobe‐like structures located on the anterior and posterior epibranchial elements as well as the ceratobranchials. The ultrastructure of the filter lobes can be smooth or covered by a layer of microcilia, and some are denticulated along the dorsal and ventral lobe surface. Flow through the mobulid oropharyngeal cavity differs from other filter‐feeding fishes in that water must rapidly deviate from the free stream direction. There is an abrupt 90° turn from the initial inflowing path to move through the laterally directed branchial filter pores, over the gill tissue, and out the ventrally located gill slits. The deviation in the flow must result in tangential shearing stress across the filter surface. This implies that mobulids can use cross‐flow filtration in which this shearing force serves as a mechanism to resuspend food particles initially caught by sieving or another capture mode. These particles will be transported by the cross filter flow toward the esophagus. We propose that species with cilia on the rakers augment the shear mediated movement of particles along the filter with ciliary transport. J. Morphol. 274:1026–1043, 2013. © 2013 Wiley Periodicals, Inc.     

Biochemical responses of fish exposed to a harmful dinoflagellate Cochlodinium polykrikoides

To elucidate the ichthyotoxic mechanisms of a harmful dinoflagellate Cochlodinium polykrikoides, biochemical responses of fish exposed to blooms were investigated. Particularly, based on our finding that oxidative damages of gill were associated with fish mortality (J. Plankton Res. 21 (1999) 2105-2115), dysfunction of ion-transporting enzymes and secretion of gill mucus of fish exposed to this bloom species were examined. The susceptibilities of several fishes to C. polykrikoides were different; the active pelagic fishes such as black scraper Thamnaconus septentrionalis, red sea bream Pagrus major, beakperch Oplegnathus fasciatus and seaperch Malakichthys wakiyae, were more vulnerable than the benthic fishes, flounder Paralichthys olivaceus and rockfish Sebastes inermis. In addition, the higher the algal cell density, the higher the fish mortality. When the test fishes were exposed to C. polykrikoides of 5000 cells ml(-1), the transport-related enzymes, carbonic anhydrase and Na(+)/K(+)-ATPase activities were significantly decreased. The activity of carbonic anhydrase was decreased with increasing algal cell density and exposure time. The quantity of total polysaccharide in gill mucus is higher in the fish exposed to C. polykrikoides than in the control fish; the magnitudes were higher in the pelagic fishes than that of benthic fishes. Moreover, a drop of blood pH and oxygen partial pressure (pO(2)) was also observed in red sea bream and flounder subjected to C. polykrikoides. These results suggest that the inactivation of gill transport-related enzymes activities, the fall in blood pO(2) and abnormal secretion of gill mucus by the C. polykrikoides may be one of the principal causes of fish kill.     

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.     

Studies of the biology of the lesser weever fish Trachinus vipera Cuvier

The anatomical adaptations to a benthic mode of life are reviewed and discussed. The functioning of the pectoral, pelvic and anal fins in moving sand from underneath the animal, during burrowing, are described. Jets of water directed downwards from the gill chambers, produce a fluid sand-water mixture which facilitates the functioning of the pelvic fins, and the movement of the head into the sand. The direction of water movements associated with gill ventilation, which are propelled almost exclusively by the branchiostegal rays, are outlined. Inhalation is normally through the mouth, which is protected by papillae, from being blocked by sand. When the mouth is covered with sand, the water flow through it is reduced, and some inhalation occurs through the dorsal margin of the operculum, involving use of the supracliethrum.     

Functional analysis of the musculo‐skeletal system of the gill apparatus in Heptranchias perlo (Chondrichthyes: Hexanchidae)

Musculo‐skeletal morphology is an indispensable source for understanding functional adaptations. Analysis of morphology of the branchial apparatus of Hexanchiform sharks can provide insight into aspects of their respiration that are difficult to observe directly. In this study, I compare the structure of the musculo‐skeletal system of the gill apparatus of Heptranchias perlo and Squalus acanthias in respect to their adaptation for one of two respiratory mechanisms known in sharks, namely, the active two‐pump (oropharyngeal and parabranchial) ventilation and the ram‐jet ventilation. In both species, the oropharyngeal pump possesses two sets of muscles, one for compression and the other for expansion. The parabranchial pump only has constrictors. Expansion of this pump occurs only due to passive elastic recoil of the extrabranchial cartilages. In Squalus acanthias the parabranchial chambers are large and equipped by powerful superficial constrictors. These muscles and the outer walls of the parabranchial chambers are much reduced in Heptranchias perlo , and thus it likely cannot use this pump. However, this reduction allows for vertical elongation of outer gill slits which, along with greater number of gill pouches, likely decreases branchial resistance and, at the same time, increases the gill surface area, and can be regarded as an adaptation for ram ventilation at lower speeds.     

Gill surface area provides a clue for the respiratory basis of brain size in the blacktip shark (Carcharhinus limbatus)

Brain size varies dramatically, both within and across species, and this variation is often believed to be the result of trade-offs between the cognitive benefits of having a large brain for a given body size and the energetic cost of sustaining neural tissue. One potential consequence of having a large brain is that organisms must also meet the associated high energetic demands. Thus, a key question is whether metabolic rate correlates with brain size. However, using metabolic rate to measure energetic demand yields a relatively instantaneous and dynamic measure of energy turnover, which is incompatible with the longer evolutionary timescale of changes in brain size within and across species. Morphological traits associated with oxygen consumption, specifically gill surface area, have been shown to be correlates of oxygen demand and energy use, and thus may serve as integrated correlates of these processes, allowing us to assess whether evolutionary changes in brain size correlate with changes in longer-term oxygen demand and energy use. We tested how brain size relates to gill surface area in the blacktip shark Carcharhinus limbatus. First, we examined whether the allometric slope of brain mass (i.e., the rate that brain mass changes with body mass) is lower than the allometric slope of gill surface area across ontogeny. Second, we tested whether gill surface area explains variation in brain mass, after accounting for the effects of body mass on brain mass. We found that brain mass and gill surface area both had positive allometric slopes, with larger individuals having both larger brains and larger gill surface areas compared to smaller individuals. However, the allometric slope of brain mass was lower than the allometric slope of gill surface area, consistent with our prediction that the allometric slope of gill surface area could pose an upper limit to the allometric slope of brain mass. Finally, after accounting for body mass, individuals with larger brains tended to have larger gill surface areas. Together, our results provide clues as to how fishes may evolve and maintain large brains despite their high energetic cost, suggesting that C. limbatus individuals with a large gill surface area for their body mass may be able to support a higher energetic turnover, and, in turn, a larger brain for their body mass.     

鲻和鲮鳃丝的扫描电镜比较观察

对鲻（Mugil cephalus）和鲮（Cirrhina molitorella）的鳃丝表面结构进行了扫描电镜比较观察,结果表明,鲻鳃丝杆状部比鲮粗．鲻鳃小片高度比鲮低;两者鳃丝表面分泌孔洞口径和密度不同;鲻和鲮细胞外被不同,鲻细胞外被稀疏,鲮的则致密复杂;鳃小片细胞和鳃丝表皮细胞的表面形态存在差异,文章还描述了鳃丝表皮形态特异的细胞。     

Tradeoffs between respiration and feeding in Sacramento blackfish,Orthodon microlepidotus

Synopsis Suspension-feeding fishes use gill structures for both respiration (lamellae) and food capture (rakers). During hypoxic exposure in eutrophic lakes or poorly circulated sloughs, many fishes, including Sacramento blackfish, Orthodon microlepidotus, increase their gill water flows, in part by increasing ventilatory stroke volumes. Stroke volume increases could compromise particle sieving efficiency by spreading interdigitated gill rakers from adjacent gill arches, although blackfish capture food particles by raker-guided water flows to a sticky buccal root. Using van Dam-type respirometers, blackfish respiratory variables and feeding efficiency (Artemia nauplii) were measured under normoxia (> 130 torr PO₂) and hypoxia (60 torr PO₂). Compared with non-feeding, normoxic conditions, gill ventilation volume, frequency, stroke volume, and gape all increased, while O₂ uptake efficiency decreased, during hypoxia and during feeding. O₂ consumption increased during feeding treatments, and % uptake of nauplii showed no difference between normoxic and hypoxic groups. Thus, blackfish display respiratory adaptations, including increased ventilatory stroke volumes, to survive in hypoxic environments such as Clear Lake, California. Importantly, they have also evolved a particle capture mechanism that allows efficient suspension-feeding under both normoxic and hypoxic conditions.     

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.     

Ventilation of the branchial chambers in the amphibious West African freshwater crab,Sudanonautes (Convexonautes) aubryi monodi (Balss, 1929) (Brachyura,Potamonautidae)

The anatomy of the respiratory system of the savanna-zone African freshwater crab, Sudanonautes (Convexonautes) aubryi monodi [Balss, 1929], has been examined and has been found to be adapted for both aerial and aquatic gas exchange. The activities of the scaphognathites and the directions of flow of the ventilatory stream have been recorded in stressed, active and resting specimens during their exposure to a wide range of conditions from deep water to dry land.Ventilation of the branchial chambers during aquatic gas exchange in Sudanonautes kept in deep water is shown to consist of a rapid, predominantly forward water flow similar to that of fully-aquatic species. Ventilation of the branchial chambers during aerial gas exchange in Sudanonautes on land is shown to consist of a relatively slow forward air flow. This flow is continuous in post-operative crabs, pulsatile in active crabs and completely immobile in resting crabs.A second method of ventilation of the branchial chambers during aerial gas exchange is shown to consist of a pulsatile reversed air flow. This occurs (1) when Sudanonautes is kept in very shallow water and active or stressed; (2) when it has recently moved on to land; and (3) when it is completely immersed and exhibiting aerial gas exchange under water. The unusual phenomenon of aerial gas exchange under water is reported here for the first time in any species of crab.Bimodal ventilation of the branchial chambers occurs in stressed or active crabs partly immersed in shallow water. This consists of an alternation between forward water flow and reversed air flow.The morphology of the branchial chambers in Sudanonautes, and observational data on the patterns of ventilation of the branchial chambers, are discussed in relation to those described for other air-breathing decapod crustaceans.     

Embryonic ionocytes in the European sea bass (Dicentrarchus labrax): Structure and functionality

Early ionocytes have been studied in the European sea bass (Dicentrarchus labrax) embryos. Structural and functional aspects were analyzed and compared with those observed in the same conditions (38 ppt) in post hatching stages. Immunolocalization of Na⁺/K⁺‐ATPase (NKA) in embryos revealed the presence of ionocytes on the yolk sac membrane from a stage 12 pair of somites (S), and an original cluster around the first gill slits from stage 14S. Histological investigations suggested that from these cells, close to the future gill chambers, originate the ionocytes observed on gill arches and gill filaments after hatching. Triple immunocytochemical staining, including NKA, various Na⁺/K⁺/2Cl^? cotransporters (NKCCs) and the chloride channel “cystic fibrosis transmembrane regulator” (CFTR), point to the occurrence of immature and mature ionocytes in early and late embryonic stages at different sites. These observations were completed with transmission electronic microscopy. The degree of functionality of ionocytes is discussed according to these results. Yolk sac membrane ionocytes and enteric ionocytes seem to have an early role in embryonic osmoregulation, whereas gill slits tegumentary ionocytes are presumed to be fully efficient after hatching.     

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.     

Nucleolar variation in response to nutritional condition in juvenile pejerrey Odontesthes bonariensis (Valenciennes)

The variations of the nucleolar characteristics size and number were studied in the gill and liver of Odontesthes bonariensis under different feeding regimes in order to test the hypothesis that functional genomes at the nucleolus, which determine variation of size (heterogeneity) in juvenile fishes, are modulated by environmental factors such as food availability. The programme that controls genetic changes of the nucleolar characteristics of the diploid cells of O. bonariensis was different from that described in the diploid cells of cyprinid fishes. No variations of the mean nucleolar number per nucleus were observed in liver or gill cells in relation to the feeding regime. Conversely, significant reduction of the mean nucleolar volume per nucleus ( V _MN) and change in the shape of the frequency distribution of the total nucleolar volume per cell was evident in both cell types in response to starvation or food restriction. Tissue specificity was observed in relation to the absolute values of the nucleolar characteristics; however, the relative behaviour was comparable in digestive and non-digestive tissues. The time-course reduction of V _MN in gill and liver cells of restrictively fed fish followed a negative exponential. A good correlation between V _MN and the condition index of the fish ( K ) was observed after long-term food restriction; however, a faster response of V _MN was observed after short-term fasting events. Results supported the stated hypothesis and showed nucleolar activity as a direct, rapid and sensitive indicator of the nutritional status of the fish.     

Cadmium toxicity in fishes

Cadmium from industrial effluents pollutes sea and river water and hence may effect the fish population therein. The present investigation shows that resistivity is greater in case of air-breathing fishes as compared to non air-breathing fishes with regards to their duration of survival and growth when exposed to a cadmium containing environment. Under sub-acute levels of cadmium exposure, they respond differently so far as the activities of their liver, gill and intestinal lysosomal enzymes are concerned. Though both species show a definite stress condition on cadmium exposure, the two anatomically different fishes respond differently towards carbohydrate metabolism as observed from liver and muscle glycogen content, liver microsomal glucose-6-phosphatase activity and serum glucose level.