Functional morphology of the feeding apparatus,feeding constraints,and suction performance in the nurse shark Ginglymostoma cirratum

The nurse shark, Ginglymostoma cirratum, is an obligate suction feeder that preys on benthic invertebrates and fish. Its cranial morphology exhibits a suite of structural and functional modifications that facilitate this mode of prey capture. During suction‐feeding, subambient pressure is generated by the ventral expansion of the hyoid apparatus and the floor of its buccopharyngeal cavity. As in suction‐feeding bony fishes, the nurse shark exhibits expansive, compressive, and recovery kinematic phases that produce posterior‐directed water flow through the buccopharyngeal cavity. However, there is generally neither a preparatory phase nor cranial elevation. Suction is generated by the rapid depression of the buccopharyngeal floor by the coracoarcualis, coracohyoideus, and coracobranchiales muscles. Because the hyoid arch of G. cirratum is loosely connected to the mandible, contraction of the rectus cervicis muscle group can greatly depress the floor of the buccopharyngeal cavity below the depressed mandible, resulting in large volumetric expansion. Suction pressures in the nurse shark vary greatly, but include the greatest subambient pressures reported for an aquatic‐feeding vertebrate. Maximum suction pressure does not appear to be related to shark size, but is correlated with the rate of buccopharyngeal expansion. As in suction‐feeding bony fishes, suction in the nurse shark is only effective within approximately 3 cm in front of the mouth. The foraging behavior of this shark is most likely constrained to ambushing or stalking due to the exponential decay of effective suction in front of the mouth. Prey capture may be facilitated by foraging within reef confines and close to the substrate, which can enhance the effective suction distance, or by foraging at night when it can more closely approach prey. J. Morphol., 2008. © 2008 Wiley‐Liss, Inc.     

Histochemical analysis of glycoproteins in the secretory cells in the gill epithelium of a catfish, Rita rita (Siluriformes, Bagridae)

Glycoproteins (GPs) were visualised histochemically in the secretory cells – the mucous goblet cells (the type A and the type B), the serous goblet cells, the club cells and the epithelial cells in the gill epithelium of Rita rita. The type A mucous goblet cells, the type B mucous goblet cells and the epithelial cells elaborate GPs with oxidizable vicinal diols and GPs with sialic acid residue without O-acyl substitution. In addition, GPs with O-sulphate esters are elaborated by the type A and GPs with O-acyl sugars by the type B mucous goblet cells. GPs are absent in the serous goblet cells and are with oxidizable vicinal diols in low moieties in the club cells. The analysis of the results elucidates interesting differences in the composition and concentration of GPs in the mucus elaborated by the epithelium of the gill arches and the gill rakers; and the gill filaments and the secondary lamellae indicating the potential importance of the glycoproteins at these locations. GPs elaborated on the surfaces of the gill arches and the gill rakers could be associated to assist in feeding activities and on the surfaces of the gill filaments and the secondary lamellae in the respiratory activity.     

Ultrastructure of a complex epithelial system: The pharyngeal lining of the larval lamprey Petromyzon marinus

Electron microscopy shows that the pharyngeal lining of the larval lamprey Petromyzon marinus is a structurally complex epithelial system that can be separated into eight epithelial types: gill lamellar, gill interlamellar, goblet cell, protective, terminal (taste) bud, preciliated, ciliated in tracts, and ciliated in grooves. Furthermore, these epithelial types encompass at least sixteen different cell types based on ultrastructure and, in some cases, correlative histochemistry (PAS, Alcian blue). Common to nearly all the epithelial types are basal cells and intermediate cells. These two cell types are seen as undifferentiated. Among mature cells, structural specialization as proceeded in three directions: (1) elaboration of mitochondria, probably related to molecular transport (ion-uptake cells, chloride cells); (2) ciliogenesis (preciliated and ciliated cell types); and (3) production of mucous secretory granules (mucous-platelet cells, goblet cells, superficial protective cells, columnar mucous cells, “cobblestone” cells, and marginal and dark cells in the terminal buds). Many of the functions of the cell types relate to the process of suspension feeding in this animal.     

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.     

Ultrastructure aspects of Brycon gouldingi (Teleostei,Characidae) related to swimming ability and feeding during larval development

The larval ultrastructure of Brycon gouldingi related to swimming and feeding from hatching to total yolk absorption is described from scanning electron micrographs. Newly hatched larvae (time zero) had no mouth opening, undefined optic vesicles, an olfactory plate visible as a shallow depression, rudimentary gill arches, neural groove, embryonic fin and a primary neuromast in the dorsal region of the head. At the time of yolk absorption, 55 h post hatching, the larvae presented an optic vesicle comprising an optic cup and crystalline lens; a mouth with tongue, tapered teeth and taste buds; a ciliated olfactory cavity; branched gill arches; filled neural groove signalling central nervous system development; caudal, pectoral, dorsal and anal fins; and neuromasts distributed throughout the head and body. These characters are related to prey capture and swimming ability, key aspects of survival during the larval stage. The results of this study provide important information for exploitation and aquaculture of B. gouldingi.     

白鲟消化道形态学与组织学的初步观察

白鲟消化道具有肉食性鱼类的典型特征,其口咽腔结构既适合捕食又适合吞食与滤食水生动物。咽后消化道可分为食道、胃后行支、胃前行支、小肠、瓣肠、直肠与肛门。幽门盲囊似一致密器官,小肠与瓣肠连接处有一特殊淋巴器官,肛门两侧有腹孔。白鲟口咽腔被覆层扁平上皮,上皮内有味蕾分布。咽后消化道组织分层为粘膜(无粘膜肌层)、粘膜下层(小肠及瓣肠前部无)、肌层与外膜。粘膜上皮为单层柱状上皮,由纤毛柱状细胞、一般柱状细胞和杯状细胞组成,其间还散在有颗粒细胞和游走细胞。食道后部与胃的一般柱状细胞为分泌粘液的细胞,肠内的一般柱状细胞为吸收细胞。胃后行支及部分前行支固有膜内有消化腺,其余各部的固有膜为致密层。小肠前中部粘膜形成蜂窝状粘膜窦,无肠腺。除食道前部肌层中有横纹肌外,其余部的肌层均为平滑肌。外膜内结缔组织有的致密有的疏松,外膜表面细胞柱状或立方形或扁平。     

Fine structure of the branchial epithelium in the teleost Oreochromis niloticus

We have studied the gill epithelium of Oreochromis niloticus using transmission electron microscopy with the particular interested relationship between cell morphology and osmotic, immunoregulatory, or other non‐regulatory functions of the gill. Pavement cells covered the filament epithelium and lamellae of gills, with filament pavement cells showing distinct features from lamellar pavement cells. The superficial layer of the filament epithelium was formed by osmoregulatory elements, the columnar mitochondria‐rich, mucous and support cells, as well as by their precursors. Light mitochondria‐rich cells were located next to lamellae. They exhibited an apical crypt with microvilli and horizontal small dense rod‐like vesicles, sealed by tight junctions to pavement cells. Dark mitochondria‐rich cells had long dense rod‐like vesicles and a small apical opening sealed by tight junctions to pavement cells. The deep layer of the filament epithelium was formed by a network of undifferentiated cells, containing neuroepithelial and myoepithelial cells, macrophage and eosinophil‐like cells and their precursors, as well as precursors of mucous cells. The lateral‐basal surface was coated by myoepithelial cells and a basal lamina. The lamellar blood lacunae was lined by pillar cells and surrounded by a basal lamina and pericytes. The data presented here support the existence of two distinct types of pavement cells, mitochondria‐rich cells, and mitochondria‐rich cells precursors, a structural role for support cells, a common origin for pavement cells and support cells, a paracrine function for neuroepithelial cells in the superficial layer, and the control of the lamellar capillary base by endocrine and contractile cells. Data further suggest that the filament superficial layer is involved in gill osmoregulation, that may interact, through pale mitochondria‐rich cells, with the deep layer and lamellae, whereas the deep layer, through immune and neuroendocrine systems, acts in the regeneration and defense of the tissue. J. Morphol. 2010. © 2010 Wiley‐Liss, Inc.     

An analysis of a specialized feeding mechanism of the spined loach, Cobitis taenia (L.), and a description of the related structures

Aquarium observations and gut analyses of the spined loach, Cobitis taenia , suggested the use of a technique by which small items of food could be removed from an almost constant stream of substrate, taken in through the mouth and passed out through the gills. The small amount of indigestible substrate present in the gut contents indicated a very high efficiency level for the process. Photographic investigation revealed a two phased feeding cycle based on the respiratory pumps, consisting of an induction/separation phase and an expulsion/swallowing phase. A morphological study showed large concentrations of mucus secreting goblet cells on the roof of the anterior buccopharyngeal cavity. Other morphological adaptations were noted which resulted in a narrowing of the anterior buccal cavity and a widening of the posterior part along with an increase in the distance between the gill rakers. In the light of this information a method of separation based on differential densities of particles being trapped in a constant stream of mucus is postulated.     

Identification and immunocytochemical localization of two different carbonic anhydrase isoenzymes in teleostean fish erythrocytes and gill epithelia

Summary Carbonic anhydrase was purified from the gills (CAB) of the rainbow trout Salmo gairdneri and from erythrocytes (CAE) of the fresh water carp Cyprinus carpio. The purification of the isozymes was confirmed by SDS acrylamide gel electrophoresis. Antibodies against the purified CAB and CAE were then raised in rabbits. Specificity was verified by immunoblotting. No cross-reaction was found between them, using the immunodot technique. CAB antiserum was used to specifically localize gill CA in the trout. Immunoperoxidase labelling revealed a concentration of enzyme on the apical region of the outer layer of the gill epithelial cells. The inner layer of the epithelium was only weakly positive. Results obtained using the immuno-gold technique confirmed the immunoperoxidase labelling: there was a concentration of label in the apical regions of chloride cells. In mucous cells, only the mucous granules were labelled. In the lamellae, the label was distributed in the apical part of the pavement cells. The villi and microplicae were strongly positive. CAE antiserum stained the red blood cells. The discrepancy between histochemical localization in the gill or in the opercular skin of killifish and our present immunolocalization was discussed.It was concluded that the most typical localization of CA is on the apical surface of the lamellar epithelium lying in contact with the environment. The result suggests that one of the main roles of gill CA may be to facilitate the diffusion of CO₂ from blood to water.     

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.     

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.     

Structural changes in gills of Lost River suckers exposed to elevated pH and ammonia concentrations

The Lost River sucker (Deltistes luxatus) is a federally listed, endangered fish that occurs primarily in Upper Klamath Lake-a hypereutrophic lake in southern Oregon, USA. A decline of the sucker population in the lake over the past few decades has been partly attributed to adverse water quality conditions, including elevated pH and ammonia concentrations that occur during summer cyanobacterial blooms. We quantitatively analyzed structural changes in gills of larval Lost River suckers after they were exposed to elevated pH and ammonia concentrations for 30 d. Exposure to pH as high as 10 caused no observed structural changes. However, lamellar thickness and O(2) diffusion distance increased significantly (P<0.05) at ammonia concentrations that did not significantly decrease survival, growth, whole-body ion concentrations, or swimming performance. Additionally, we qualitatively observed increases in the frequency of hyperplasic and hypertrophic mucous cells, tissue damage, epithelial lifting, and infiltration of white blood cells into paracellular lymphatic spaces at the highest sublethal ammonia concentration. These observed gill changes typically indicate compromised respiratory and ionoregulatory capacity, although such effects were not manifested in the assays we performed. Regardless, these structural gill changes appear to be a more sensitive indicator of exposure to elevated ammonia concentrations than are more traditional sublethal indices. Therefore, gill histopathology might be a relevant early-warning monitoring tool of the health of Lost River suckers in Upper Klamath Lake, and other species in similar eutrophic systems.     

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.     

The symbiotic water mite Unionicola formosa (Acari: Unionicolidae) ingests mucus and tissue of its molluscan host

Unionicola formosa is a symbiotic water mite that passes most of its life cycle in the mantle cavity of freshwater mussels. Although mites of this genus are often referred to as parasitic, little is known about their nutritional biology. A few species reportedly pierce the gill of a host mussel and ingest tissue or hemolymph. The present study was undertaken to identify possible sources of nutrition for U. formosa. To determine if mites ingested particulate matter in the mucous strand produced by a mussel during feeding, mussels with resident mites were exposed to a suspension of fluorescent microspheres. There was no evidence that U. formosa ingested the beads. Histochemical staining did, however, indicate a mucous material present in the midgut of the mites. Sodium dodecyl sulfate-polyacrylamide gel electrophoretic assays revealed a high molecular weight component, consistent with a mucopolysaccharide, present both in the mussel gill and the mites. Results from western blots and an immunoaffinity binding assay with antibodies against mussel gill tissue and hemolymph also indicated that mites ingested host tissue. Whereas U. formosa probably does not ingest particulate material acquired by its host's suspension feeding, it is apparent that this mite utilizes host mucus, gill tissue, or hemolymph for at least part of its nutrition.     

The structure of the gill of the trout,Salmo gairdneri (Richardson)

Summary A light and electron microscopic study was made of the structure of the gill arch, filament and secondary lamella of Salmo gairdneri R. Blood pathways through the gill were traced from serial histological sections, and from the examination of ink perfused tissue and perspex casts formed following resin injection of the circulatory system.The epithelium covering the gill consists of unspecialized, dark, chloride and mucous cells. The distribution of specialized cells appears to be related to gill function. The basement membrane underlying the epithelium consists of three layers, the inner collagen layer being continuous with the connective tissue core of the gills.Blood supply to the secondary lamellar respiratory surface is via branchial, filament and secondary lamellar arteries. Blood spaces of the secondary lamellae are delimited by pillar cells containing what appears to be contractile material. The marginal channel of each lamella is bounded distally by cells of endothelial origin. A network of lymph spaces within the filaments connects with efferent branchial arteries. Nutritionary capillaries within the filaments connect with afferent branchial arteries. No shunts between afferent and efferent filament arteries were found.Data from this study and previous physiological and histopathological studies suggest a mechanism for the control of blood flow to suit the respiratory requirements of the fish. This mechanism involves a system of recruitment of additional respiratory units and changes in overall blood flow patterns.This work formed part of a thesis submitted for the degree of Doctor of Philosophy in 1971 and for which M. M. was in receipt of a studentship from the Natural Environmental Research Council. The authors are grateful for the support given by research grants from the M.R.C (P.T.) and the N.E.R.C. (M.M.), and to Prof. G. M. Hughes in whose department the work was carried out.     

Morphogenesis in hatchery-reared larvae of the black rockfish,Sebastes schlegeli,and its relationship to the development of swimming and feeding functions

The developmental sequence of morphological characteristics related to swimming and feeding functions was investigated in hatchery-reared larvae and juveniles ofSebastes schlegeli, a viviparous scorpaenid. The fish were extruded at an early larval stage, when the mean body size was 6.23 mm TL. Fin-ray rudiments became visible at 9.0 mm TL in the dorsal and anal fins, at 8.0 mm TL in the pectoral and pelvic fins and 6.0 mm TL (size at extrusion) in the caudal fin. Completion of segmentation of soft rays in the dorsal and anal fins was attained by 14 mm TL and in all fins by 17 mm TL. Branching of soft rays in the respective fins started and was completed considerably later than the completion of segmentation, as well as ossification of the fin-supports. Morphological transformation from larva to juvenile was apparently completed by about 17 mm TL. Although the completion of basic juvenile structures was attained by transformation at that body size, succeeding morphological changes occurred between 17 mm and 32 mm TL. Newly-extruded larvae possessed one or two teeth on the lower pharyngeal and pharyngobranchials 3 and 4, but lacked premaxillary, dentary, palatine and prevomer teeth. The fish attained full development of gill rakers and gill teeth by 15 mm TL, the upper and lower pharyngeal teeth subsequently developing into a toothplate. Development of the premaxillary, dentary and palatine teeth was completed at about 30 mm TL, by which time loop formation of the digestive canal and the number of pyloric caeca had attained the adult condition. The developmental sequence of swimming and feeding functions during larval and early juvenile periods appeared to proceed from primitive functions to advanced or complex ones, from the ability to produce propulsive force to that of swimming with high maneuverability and from development of the irreducible minimum function of passing food into the stomach to the ability to actively capture prey via passive food acquisition with the gill rakers and gill teeth. The relationship of morphological development to the behavior and feeding activity of artificially-produced hatchlings is also discussed.     

Interspecific variations in the surface ultrastructure of the gills of freshwater mullets

SEM studies were made on the gills of freshwater mullets,Rhinomugil corsula andSicamugil cascasia, to correlate surface ultrastructure of various gill units with their probable functions. Two types of lamellated gill rakers of the former fish are suited for plankton feeding and the short, stumpy and transversely beaded gill rakers of the latter reflect the varied food and feeding habit of the fish.R. corsula has numerous mucous glands on the epithelium covering the gill arch and gill filaments,S. cascasia has fewer. In accordance with the differences in the density and distribution of the mucous glands, the microridged epithelial cells also show variations in their architectural plan. In both species the epithelium of the secondary lamellae is smooth, probably an adaptation for better gaseous exchange.     

Osteology,myology and feeding mechanism of Astronotus ocellatus (Pisces,Perciformes)

Summary Astronotus ocellatus captures its prey by creating a negative pressure in the buccal cavity which is caused by its quick expansion. Once the prey has been accommodated, the buccal cavity undergoes a compression which may propel the prey towards the pharyngeal jaws for mastication. The motion picture recordings indicate retracted premaxillae at the beginning of food intake followed by a maximum attainment of mouth gape and then mastication. During the maximum opening of the mouth the premaxillae are protruded and dentaries are at maximum depression. These events are followed by activities such as buccopharyngeal cavity expansion, bulging on the ventral surface of the head, and prominent curvature on the ventral surface anterior to the urohyal, caused by the upward movement of the glossohyal. Based on the cinematographic results, it may be inferred that the maximum mouth gape is caused by the sternohyoid-hyoid-interopercular-mandible coupling, and not by the opercular apparatus-mandible coupling, as the latter acts after the full descent of the lower jaw. Impression of the expanded buccopharyngeal cavity has been made by a paraffin mold technique, which confirms the displacement of the buccopharyngeal elements during expansion of the cavity.     

Confocal microscopy as a useful approach to describe gill rakers of Asian species of carp and native filter‐feeding fishes of the upper Mississippi River system

To better understand potential diet overlap among exotic Asian species of carp and native species of filter‐feeding fishes of the upper Mississippi River system, microscopy was used to document morphological differences in the gill rakers. Analysing samples first with light microscopy and subsequently with confocal microscopy, the three‐dimensional structure of gill rakers in Hypophthalmichthys molitrix, Hypophthalmichthys nobilis and Dorosoma cepedianum was more thoroughly described and illustrated than previous work with traditional microscopy techniques. The three‐dimensional structure of gill rakers in Ictiobus cyprinellus was described and illustrated for the first time.