Particle retention in suspension-feeding fish after removal of filtration structures

The suspension-feeding cichlids Oreochromis aureus (blue tilapia) and Oreochromis esculentus (ngege tilapia) are able to selectively retain small food particles. The gill rakers and microbranchiospines of these species have been assumed to function as filters. However, surgical removal of these oral structures, which also removed associated mucus, did not significantly affect the total number of 11–200 μm particles ingested by the fish. This result supports the hypothesis that the branchial arch surfaces themselves play an important role in crossflow filtration. Both species selectively retained microspheres greater than 50 μm with gill rakers and microbranchiospines intact as well as removed, demonstrating that neither these structures nor mucus are necessary for size selectivity to occur during biological crossflow filtration. After removal of the gill rakers and microbranchiospines, O. esculentus retained significantly more microspheres 51–70 μm in diameter and fewer 91–130 μm microspheres compared to retention with intact structures, but the particle size selectivity of O. aureus was not affected significantly. These results support conclusions from previous computational fluid dynamics simulations indicating that particle size can have marked effects on particle trajectory and retention inside the fish oropharyngeal cavity during crossflow filtration. The substantial inter-individual variability in particle retention by suspension-feeding fish is an unexplored area of research with the potential to increase our understanding of the factors influencing particle retention during biological filtration.     

Evidence for ram suspension feeding by the piscivore, Seriola dumerili (Carangidae)

Synopsis We have quantitatively analyzed a videotape of Seriola dumerili (Carangidae) displaying ram suspension-feeding behavior and ram ventilation in the field. This is the first report of facultative suspension feeding by a piscivorous carangid. The intraoral morphology of S. dumerili is not typical of ram suspension-feeding fishes in that closely-spaced, long gill rakers are lacking. While the mechanism of particle retention is not known for any ram suspension-feeding fish species, scanning electron microscopy revealed denticles on the branchial surfaces of S. dumerili that could play a role in particle entrapment.     

Computational fluid dynamics in the oral cavity of ram suspension-feeding fishes

We have modeled steady, three-dimensional flow with a no-slip boundary condition in cylindrical and conical oral cavities possessing vertical or slanted branchial slits. These numerical simulations illustrate the transport of food particles toward the esophagus, as well as the velocity profiles of water exiting the oral cavity via the branchial slits. The maximum and average velocities are highest for flow exiting the most posterior branchial slit. The highest volume flow rates also occur in the most posterior slit for the cylindrical simulations, but occur in the most anterior slit for the conical simulations. Along the midline, there is a pronounced bilaterally symmetrical vortex in the posterodorsal region of the cylindrical and conical oral cavities and a second bilaterally symmetrical vortex in the posteroventral region of the cylinder. Particles entrained in the vortices will recirculate in the posterior oral cavity, increasing the probability of encounter with sticky, mucus-covered surfaces such as the oral roof, gill arches, or gill rakers. The posterodorsal vortex could serve to concentrate particles near the entrances of the epibranchial organs. The ventral vortex could be involved in sequestering dense inorganic particles that sink toward the floor of the oral cavity. All vortices are absent in the conical simulation with vertical branchial slits, indicating that the slanted branchial slits between the gill arches are responsible for the formation of the vortex in the conical oral cavity. Experiments using in vivo flow visualization techniques are needed to determine whether ram suspension feeders, pump suspension feeders, and non-suspension-feeding fishes possess vortices in the posterior oral cavity that contribute to particle transport, food particle encounter with sticky surfaces, and inorganic particle rejection.     

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.     

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.     

Structure,development and function of the branchial sieve of the common bream,Abramis brama,white bream,Blicca bjoerkna and roach,Rutilus rutilus

Synopsis The filter feeding organ of cyprinid fishes is the branchial sieve, which consists of a mesh formed by gill rakers and tiny channels on the gill arches. In order to establish its possible role during growth we measured the following morphological gill raker parameters over a range of sizes in three cyprinid fishes, bream, white bream and roach: inter raker distance, bony raker length, raker width, cushion length and channel width. At any given standard length common bream has the largest inter raker distance, roach the lowest and white bream is intermediate. In the comb model of filter feeding the inter raker distance is considered to be a direct measure of the mesh size and retention ability (= minimal size of prey that can be retained) of a filter. For the three species under study there is a conflict between the comb model and experimental data on particle retention. Lammens et al. (1987) found that common bream has a large retention ability whereas roach and white bream have a much smaller one. A new model, the channel model (Hoogenboezem et al. 1991) has been developed for common bream; in this model the lateral gill rakers can regulate the mesh size of the medial channels on the other side of the gill slit. The present data indicate that this model is not appropriate for white bream and roach. At any given standard length white bream and roach only reach 70% of the raker length of common bream, which means that in this model the gill slits should to be very narrow during filter feeding. The gill rakers consist of a bony raker and a fleshy cushion. The bony rakers have a rather long needle-like part outside the cushion in bream, but not in white bream and roach which have blunt gill rakers. Blunt gill rakers are not suited to reduce the diameter of the medial channels. The comb model seems more appropriate for white bream and roach, but doubts about the validity of this simple model remain. The sum of the areas of the medial channels is an approximation of the area through which water flows in the filter. This channel area therefore gives an impression of the capacity or flow rate of the filter. With this capacity estimation and an estimation of energy consumption we calculated an energy ratio of filter feeding. The energy ratio decreases with increasing standard length with an exponent close to the expected exponent of -0.40. The energy ratio is highest in bream, intermediate in white bream and lowest in roach.     

Surface ultrastructure of gill arches and gill rakers in relation to feeding of an Indian major carp, Cirrhinus mrigala

The surface ultrastructure of the gill arches and the gill rakers of an herbivorous fish, Cirrhinus mrigala was investigated by scanning electron microscopy. These structures show significant adaptive modifications associated with the food and feeding ecology of the fish. Closely lying short gill rakers and narrow inter-raker channels on the gill arches are associated to filter and retain food particles. Prominent epithelial protuberances on the gill rakers and the gill arches enable the taste buds, located at their summit, to project well above the surface of the epithelium. This could increase the efficiency of the taste buds in selective sorting of palatable food. Surface specializations of the postlingual organ are recognized adaptive modifications for selecting, trapping or holding food particles. Prominent molariform teeth born on the lower pharyngeal jaw, and the chewing pad opposite it, are associated to work together as an efficient pharyngeal mill. Mucous goblet cells are considered to elaborate mucus secretions to trap, glue and lubricate food particles for their smooth transport for swallowing.     

Morphology of the pharyngeal cavity, especially the surface ultrastructure of gill arches and gill rakers in relation to the feeding ecology of the catfish Rita rita (Siluriformes, Bagridae)

Gill arches and the gill rakers of a sluggish, carnivorous catfish, Rita rita, show significant differences of their surface ultrastructure, which are recognized adaptive modifications in relation to food and feeding ecology of fish. Gill rakers on the first and second pairs of gill arches are borne on the oral side and are long and stout at the epi-ceratobranchial union. Gill rakers on the third and fourth pairs of gill arches, in contrast, are borne on the oral and aboral sides and are relatively delicate and short. Long and stout gill rakers on the first and second pairs of gill arches are considered primarily to prevent entry of undesirably large food items into the pharynx. Two types of taste buds, Type I and Type II, occur on the gill arches and the gill rakers. The raised taste buds, located at the apical ends of the gill rakers on the third, fourth, and the fifth pairs of gill arches could increase gustatory efficiency in the pharynx. Differences in the distribution of taste buds on the pharyngeal sides of different gill arches indicate that the posterior part of the pharynx plays a more crucial role in gustation than does the anterior part. Co-occurrence of teeth and taste buds on the epi- and hypopharyngeal bones denotes that food processing and gustation occur simultaneously in the pharynx. Villiform and caniform teeth on the epi- and hypopharyngeal bones are associated with a complex food-processing cycle. Mucous secretions, oozing through mucous cell openings, provide lubrication facilitating smooth passage of food through the pharynx. The angle of curvature at the epi-ceratobranchial union of the first to fourth pairs of gill arches could assist the ventral drag of ceratobranchials in lowering of the pharyngeal floor, thus resulting in a great expansion of the pharynx, as needed to accommodate the large quantities of food captured.     

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.     

Development, morphometry and particle retention capability of the gill rakers in the herring, Clupea harengus L.

The development of gill rakers in the herring, Clupea harengus L. was followed from the larva to the adult. The first rakers appear on the gill arches at a total length ( t.l .) of about 16 mm. Their number then increases rapidly until the fish are about 50 mm t.l . when the rate of addition becomes much slower. The length of individual rakers and the space between them continues to increase throughout life. The rakers on the first gill arch account for almost 60% of the whole filtering area. The observed particle retention capabilities of the fish when filter-feeding were lower than those expected on the basis of the estimated spaces between the rakers. Several reasons are suggested for the discrepancy.     

官亭水库黄尾鲴食性的初步研究

黄尾鲴仔幼鱼阶段的食性是随着鳃耙和肠管形态的变化而变化。体长11.8—12.3mm,鳃耙形状开始分化,肠呈1—2弯曲,仔鱼吞食小型枝角类,主要是裸腹溞;体长15.8—17.4mm,口端位,鳃耙成筛网,肠呈4—8弯曲,前肠膨大,主要食物是腐屑,摇蚊幼虫,“水华”型的裸藻与蓝绿藻。体长18mm的幼鱼,口下位,鳃耙与肠管进一步发育,幼鱼转入底栖,其前肠内含物主要为泥沙、腐屑、摇蚊幼虫,浮游动物与浮游植物。黄尾鲴成鱼的主要食物为大量的腐屑和极少数的着生硅藻、颤藻。成鱼食物营养价值很差,其总N含量为0.372%,有机质为4.8%,每克湿重的热值为146.35卡,成鱼周年摄食,摄食量大,这是黄尾鲴摄食的特点。       

A fish that uses its hydrodynamic tongue to feed on land

To capture and swallow food on land, a sticky tongue supported by the hyoid and gill arch skeleton has evolved in land vertebrates from aquatic ancestors that used mouth-cavity-expanding actions of the hyoid to suck food into the mouth. However, the evolutionary pathway bridging this drastic shift in feeding mechanism and associated hyoid motions remains unknown. Modern fish that feed on land may help to unravel the physical constraints and biomechanical solutions that led to terrestrialization of fish-feeding systems. Here, we show that the mudskipper emerges onto land with its mouth cavity filled with water, which it uses as a protruding and retracting ‘hydrodynamic tongue’ during the initial capture and subsequent intra-oral transport of food. Our analyses link this hydrodynamic action of the intra-oral water to a sequence of compressive and expansive cranial motions that diverge from the general pattern known for suction feeding in fishes. However, the hyoid motion pattern showed a remarkable resemblance to newts during tongue prehension. Consequently, although alternative scenarios cannot be excluded, hydrodynamic tongue usage may be a transitional step onto which the evolution of adhesive mucosa and intrinsic lingual muscles can be added to gain further independence from water for terrestrial foraging.     

Experimental evidence for trait utility of gill raker number in adaptive radiation of a north temperate fish

North temperate fish in post‐glacial lakes are textbook examples for rapid parallel adaptive radiation into multiple trophic specialists within individual lakes. Speciation repeatedly proceeded along the benthic–limnetic habitat axis, and benthic–limnetic sister species diverge in the number of gill rakers. Yet, the utility of different numbers of gill rakers for consuming benthic vs. limnetic food has only very rarely been experimentally demonstrated. We bred and raised families of a benthic–limnetic species pair of whitefish under common garden conditions to test whether these species (i) show heritable differentiation in feeding efficiency on zooplankton, and (ii) whether variation in feeding efficiency is predicted by variation in gill raker numbers. We used zooplankton of three different size classes to investigate prey size dependency of divergence in feeding efficiency and to investigate the effect strength of variation in the number of gill rakers. Our results show strong interspecific differences in feeding efficiency. These differences are largest when fish were tested with the smallest zooplankton. Importantly, feeding efficiency is significantly positively correlated with the number of gill rakers when using small zooplankton, also when species identity is statistically controlled for. Our results support the hypothesis that a larger number of gill rakers are of adaptive significance for feeding on zooplankton and provide one of the first experimental demonstrations of trait utility of gill raker number when fish feed on zooplankton. These results are consistent with the suggested importance of divergent selection driven feeding adaptation during adaptive radiation of fish in post‐glacial lakes.     

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.     

Adaptive divergence between lake and stream populations of an East African cichlid fish

Divergent natural selection acting in different habitats may build up barriers to gene flow and initiate speciation. This speciation continuum can range from weak or no divergence to strong genetic differentiation between populations. Here, we focus on the early phases of adaptive divergence in the East African cichlid fish Astatotilapia burtoni, which occurs in both Lake Tanganyika (LT) and inflowing rivers. We first assessed the population structure and morphological differences in A. burtoni from southern LT. We then focused on four lake–stream systems and quantified body shape, ecologically relevant traits (gill raker and lower pharyngeal jaw) as well as stomach contents. Our study revealed the presence of several divergent lake–stream populations that rest at different stages of the speciation continuum, but show the same morphological and ecological trajectories along the lake–stream gradient. Lake fish have higher bodies, a more superior mouth position, longer gill rakers and more slender pharyngeal jaws, and they show a plant/algae and zooplankton‐biased diet, whereas stream fish feed more on snails, insects and plant seeds. A test for reproductive isolation between closely related lake and stream populations did not detect population‐assortative mating. Analyses of F1 offspring reared under common garden conditions indicate that the detected differences in body shape and gill raker length do not constitute pure plastic responses to different environmental conditions, but also have a genetic basis. Taken together, the A. burtoni lake–stream system constitutes a new model to study the factors that enhance and constrain progress towards speciation in cichlid fishes.     

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.     

Permeability properties and occludin expression in a primary cultured model gill epithelium from the stenohaline freshwater goldfish

Techniques for the primary culture of fish gill epithelia on permeable supports have provided ‘reconstructed’ gill models appropriate for the study of gill permeability characteristics in vitro. Models developed thus far have been derived from euryhaline fish species that can tolerate a wide range of environmental salinity. This study reports on procedures for the primary culture of a model gill epithelium derived from goldfish, a stenohaline freshwater (FW) fish that cannot tolerate high environmental salt concentrations. The reconstructed goldfish gill epithelium was cultured on permeable filter inserts and using electron microscopy and immunocytochemical techniques, was determined to be composed exclusively of gill pavement cells. When cultured under symmetrical conditions (i.e. with culture medium bathing both apical and basolateral surfaces), epithelial preparations generated appreciable transepithelial resistance (TER) (e.g. 1,150 ± 46 Ωcm²) within 36–42 h post-seeding in inserts. When apical medium was replaced with FW (asymmetrical conditions to mimic conditions that occur in vivo), epithelia exhibited increased TER and elevated paracellular permeability. Changes in permeability occurred in association with altered occludin-immunoreactive band position by western blot and no change in occludin mRNA abundance. We contend that the goldfish gill model will provide a useful in vitro tool for examining the molecular components of a stenohaline fish gill epithelium that participate in the regulation of gill permeability. The model will allow molecular observations to be made together with assessment of changing physiological properties that relate to permeability. Together, this will allow further insight into mechanisms that regulate gill permeability in fishes.     

Branchial arches of suspension–feeding Oreochromis esculentus: sieve or sticky filter?

Only 4% of 600 particles slid on or adhered to buccopharyngeal surfaces of Oreochromis esculentus . Only a minute quantity of mucus was visible during feeding (0·6% of 68 224 video frames; 30 frames s^–1), and very few particles were retained in this mucus. Filtration by mucus entrapment on the branchial arches is rejected as a mechanism of particle retention in this species. Since particles contacted the branchial arches infrequently, and the inter–raker spaces are too large to retain particles less than approximately 50 μm, sieving by gill rakers as a particle retention mechanism is rejected also. Unlike the suspension–feeding congener O. niloticus, O. esculentus does not use branchial arches to retain food particles by sieving or by mucus entrapment.     

The absorption efficiency and respiration rate of the Florida Lancelet, Branchiostoma floridae

The present study investigates some aspects of the digestive biology and physiological energetics of the Florida lancelet, Branchiostoma floridae. Florida lancelets are able to remove 47.2–56.9% of the energy from a diet of mixed algae. The respiration rate is 0.100 mL O₂ (STPD) h^− 1 g^− 1 (wet), which estimates a metabolic rate of 0.248 J h^− 1, at an average body mass of 0.125 g (wet). Published values of the chlorophyll a concentration in its natural habitat indicate that a 125 mg lancelet would need to filter 0.018–0.031 L h^− 1 to remove sufficient food to support its resting metabolism. The filtration rate of lancelets has been reported as 0.138 L h^− 1, indicating that the actual filtration rate is 4–7 times greater than the filtration rate needed to meet resting metabolic demands. It appears that lancelets have the potential to be raised in aquaculture, because their absorption efficiency and respiration rate are comparable to suspension-feeding invertebrates that have been successfully aquacultured.     

Ecomorphological correlates in ten species of subtropical seagrass fishes: diet and microhabitat utilization

Synopsis Ecomorphological correlates were sought among ten species of distantly related subtropical seagrass fishes. Morphometric data associated with feeding and microhabitat utilization were compared by principal components analysis, cluster analysis, and canonical correspondence analysis to dietary data. Morphology was generally a poor predictor of diet except for a group of mid-water planktotrophic filter feeders. Separation of the species along morphological axes appears to be related more to microhabitat utilization resulting in three major groups: (1) a group of planktotrophic, mid-water fishes specialized for cruising and seeking out evasive prey characterized by a compressed fusiform body, forked caudal fin, long, closely spaced gill rakers, short to intermediate! length pectoral fin, pointed pectoral fin, large lateral eye, short head, and a terminal or subterminal mouth; (2) slow swimming, less maneuverable epibenthic fishes that pick or suck their prey off the substrate. They are united by more rounded caudal and pectoral fins, and short or no gill rakers; and (3) a group of more mobile and maneuverable epibenthic foragers characterized by a more compressed, sub-gibbose body, long, pointed pectoral fins, forked caudal fins, large lateral eyes, subterminal mouth, and greater jaw protrusibility. Cases of convergence in trophic and microhabitat utilization characters were apparent in some of the groups.