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 area and dimensions of gilthead sea bream Sparus aurata L.

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

4种弹涂鱼鳃的形态度量学比较及其生态学意义

通过对背眼虎鱼亚科中薄氏大弹涂鱼(Boleophthalmus boddarti)、青弹涂鱼(Scartelaos histophorus)、新几内亚弹涂鱼(Periophthalmus novaeguineaensis)和点弹涂鱼(P.spilotus)3属4种弹涂鱼鳃参数的测定,比较了各种之间鳃的形态度量学差异。结果表明,4种弹涂鱼的鳃参数(Y)与其体重(W)均符合方程logY=log a+b logW,且各鳃参数与体重的相关性显著(R2=0.50～0.98,P0.05)。等体重的弹涂鱼相比较,青弹涂鱼的总鳃丝数、总鳃丝长(mm)、鳃丝一侧鳃小片数(/mm)、总鳃面积(mm2)和相对鳃面积(mm2/g)均最大,薄氏大弹涂鱼相应鳃参数次之,新几内亚弹涂鱼和点弹涂鱼相应鳃参数较小。弹涂鱼鳃结构的这种梯度退化,表明青弹涂鱼和薄氏大弹涂鱼水生性较强,而新几内亚弹涂鱼和点弹涂鱼陆生性较强。4种弹涂鱼的总鳃丝长和总鳃面积明显小于其他等体重水生鱼类,这与弹涂鱼的两栖生活特征相符。     

Allometry of gill dimensions in some British and American decapod crustacea

The gill areas and their component measurements of 16 species of North American crab and seven species of British decapod crustaceans have been analysed in relation to body mass using the method of logarithmic transformation.
A wide range of relationships was found, each of which is typical for a given species. The slope, b , of the log/log regression lines varied from 0·5 to 1·0, the lower values being most commonly found in the Macrura. For the North American species the average slope is about 0·8 whereas for British brachyurans the relationship was close to linear (b=0·97).
The analysis shows that the increase in gill surface body size is mainly due to the increasing area for individual platelets or gill lamellae.
Comparison of weight-specific gill areas for animals of the same body weight suggests that the most active species have larger gill areas. For some of these species the values (900mm²/g) approximate to those of active fish.
As plots for interspecific relationships derived from average values for many individual species have slopes which are not typical for any of the component species, it is concluded that caution must be exercized when interpreting such interspecific plots in Allometric studies.     

Phenotypic plasticity and the possible role of genetic assimilation: Hypoxia-induced trade-offs in the morphological traits of an African cichlid

In this study we investigate the possible role of phenotypic plasticity and genetic assimilation in the process of adaptation and evolutionary change in the cichlid Pseudocrenilabrus multicolor victoriae . In the field we compared a population of a stable hypoxic habitat with one of a stable well-oxygenated habitat. In the laboratory, we compared individuals from the same mother raised under hypoxic or well-oxygenated conditions to examine phenotypic plasticity. Morphological parameters of three categories were measured: (a) the gill apparatus, (b) the surrounding structural elements, and (c) the outer shape of the fish. Swamp-dwelling fish had a 29% greater total gill surface area than fish from the well-oxygenated habitat due to their larger gill filament length and greater lamellar area. In the plasticity experiment, total gill surface area was 18% greater in the hypoxia group due to a larger number of longer filaments. Surrounding elements and outer shape also differed between the field populations and between fish grown under hypoxic and well-oxygenated conditions, but there was disparity between the field results and the plasticity experiment. The disparity between field and experimental fish may be due to: (a) differences in selection pressures between populations, (b) different constraints for genetic and plasticity changes, or (c) selection against plastic responses to hypoxia. Our results suggest that both (a) and (c) are involved.     

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

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

Embryo developmental events and the egg case of the Aleutian skate Bathyraja aleutica (Gilbert) and the Alaska skate Bathyraja parmifera (Bean)

Embryo development events were correlated with egg-case changes for the Aleutian skate Bathyraja aleutica and the Alaska skate Bathyraja parmifera . Yolk absorption underwent two phases: that of steady absorption during early development and that of rapid yolk absorption during the final development stages. Total length ( L _T) for 50% of the pre-hatching embryos egg-case jelly disappearance was 92·04 mm (range 81–102 mm) and 99·36 mm (range 81–100 mm) for B. aleutica and B. parmifera , respectively, allowing the inner chamber to open to seawater flow. The tail filament underwent three phases of growth: rapid elongation during early development (<100 mm embryo L _T), stasis of tail filament length during the remainder of embryo development and rapid absorption soon after hatching. Complete tail filament development coincided with the disappearance of egg-case jelly. Clasper buds first developed at embryos >70 mm L _T for both species and the sex ratio was 1:1 well before hatching. Egg cases that were devoid of an ova or developing embryo were c. 5·0 and 6·5% of the egg cases examined for B. aleutica and B. parmifera , respectively. Measurements showed that egg cases containing only egg jelly were smaller in both width and length than those possessing an ova. Embryo stages were punctuated with distinct events that correlated with egg case changes controlling the internal environment of the developing embryo.     

The pattern of gill perfusion in two species of Corophium (Crustacea: Amphipoda) and its relation to environmental salinity

Total surface area of the ion-permeable lamellar gills of Corophium volutator and Corophium curvispinum is 0·81 mm²mg^-1 and 0·78 mm²mg^-1 (wet weight), respectively. In both species, haemolymph flow (as visualized by haemocyte movements) is rapid through the peripheral canal and central luminal lacunae of each gill, general flow being from posterior to anterior margin of the gill. There appears to be countercurrent flow of haemolymph and ventilatory current water over the gill integument, which may facilitate dissolved-gas exchange.
Rate of haemolymph flow (perfusion) through the gills of the euryhaline C. volutator is markedly reduced immediately following transfer to a considerably hyperosmotic salinity ( e.g. 15% S.W. to 85% S.W. transfer). No reduction in the rate of gill perfusion occurs following transfer of C. volutator to hypoosmotic salinity. The freshwater C. curvispinum does not tolerate hyperosmotic salinity transfers, but does exhibit a similar immediate gill perfusion restriction. The onset of gill perfusion restriction is dependent on a change in the magnitude of the ionic ([NaCl]), not the osmotic, gradient across the integument. In C. volutator only, normal rate of gill perfusion is eventually restored (within 24 hours of transfer), but can be immediately restored if the animal is transferred back to the acclimation salinity.
In C. volutator , branchial perfusion pattern is postulated to be regulated in relation to environmental salinity by a mechanism operating under neural control. The possible significance of gill perfusion restriction to C. volutator as a short-term adaptive osmoregulatory response is considered. Perfusion restriction in the gills of C. curvispinum is considered to be a relic of a recent estuarine ancestry.     

The linear cable theory as a model of gill blood flow

The vascular organization of the teleost gill suggests that blood flow distribution from the filamental artery to the respiratory lamellae is governed by relationships analogous to the cable conduction properties of a nerve axon. The space constant (λ) by definition is the distance along the gill filament at which the in-series resistance of the afferent filament artery equals the in-parallel resistance of the afferent lamellar arteriolar, lamellar, efferent lamellar arteriolar (ALA-L-ELA) segments. Constriction of the afferent filamental artery or uniform dilation of the ALA-L-ELA will decrease λ. As λ decreases, flow through the proximal (basal) lamellae greatly increases at the expense of distal lamellar perfusion. When λ increases in a system of finite length the flow profile must account for reflected pressures within the main vessel. The λ calculated from corrosion casts of gill vasculature is $\text{1}\text{4}$ to $\text{1}\text{2}$ the filament length. This favors blood flow through the proximal lamellae and when cardiac output increases, the proportion of cardiac output perfusing the proximal areas increases at the expense of distal lamellar blood flow. To offset these changes it is proposed that increased distal lamellar perfusion is achieved by simultaneous vasodilatation of distal and constriction of proximal ALA-L-ELA segments and dilation of the afferent filamental artery.     

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.     

Experimental vaccination of rainbow trout against Loma salmonae using a live low-virulence variant of L. salmonae

Prior exposure of rainbow trout Oncorhynchus mykiss juveniles to the low-virulence variant of Loma salmonae, L. salmonae SV, spores resulted in a xenoma intensity in the gill filaments fourteen times lower (0·044 v. 0·641 xenomas per filament; P=0·0001) than that observed in the naive controls, challenged with L. salmonae spores, as determined morphometrically by in situ hybridization at the peak of the disease (between 4 and 6 weeks post exposure). The marked degree of reduction in numbers of xenomas that formed after challenge suggests that use of the low-virulence variants should be further considered as a means to protect fish in regions where the parasite is endemic, to protect them during grow out periods.     

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.     

Extent of gill pathology in the toadfish Tetractenos hamiltoni caused by Naobranchia variabilis (Copepoda: Naobranchiidae)

Sanguinivorous Naobranchia variabilis prefer the first gill arch, external hemibranch and anterior end of the gill arch. The smallest N. variabilis observed attached to fish by a thin filament which connects fused tips of second maxillae to a 'plug' inserted into the gill tissue. Second maxillae enlarge to encircle and increasingly compress the gill filament, which results in a thin layer of epithelium and connective tissue overlying the cartilaginous supporting bar. Early juveniles cause little tissue proliferation, but the extent of proliferated epithelial and connective tissue (PR) adjacent to the maxillae increases from late juveniles to subadult and adult copepods. Most variation in length of gill filament damage (PL, proliferated and compressed tissue) among age classes is explained by maxilla length (ML, length of compressed gill filament); adult trunk width (TRW) explains an extra, small amount of variation, but not trunk length (TRL) or total fish length (TL). Most variation in ML is explained by TRW of adults, subadults and late juveniles, and TRL of early juveniles. PR is explained by TRW for adults, but by ML for other ages. These patterns are due to elongation of the juvenile trunk during growth and lateral expansion of adult egg pouches during maturation. Up to 38 N. variabilis, average (avg.) = 9.3, infected individual Tetractenos hamiltoni and damaged up to 3.4% (avg. 0.72%) of total filament length and 8.6% (avg. 2.1%) of gill filaments per fish.     

Chloride cell responses to ion challenge in two tropical freshwater fish,the erythrinids Hoplias malabaricus and Hoplerythrinus unitaeniatus

Chloride cell (CC) responses to ion challenge and plasma ion concentration were evaluated in two ecologically distinct erythrinids, Hoplias malabaricus, an exclusively water-breathing species, and Hoplerythrinus unitaeniatus, a facultative air-breathing fish, at one, two, seven, and 15 days of exposure to deionized water and to ion-rich water. H. malabaricus displayed high CC proliferation on filament and lamellar epithelium during exposure to deionized water and significant CC proliferation in the filament epithelium on the first day of exposure to water rich in NaCl and Ca2+ and in the lamellar epithelium on the first, second, and seventh day of exposure to such water. CC proliferation in H. unitaeniatus occurred only in the lamellar epithelium of fish exposed to deionized water. CC proliferation on both species was not accompanied by significant increase of CC density in contact with the external medium. The increase in the CC fractional area (CCFA) resulted from the increase of individual CC apical surface area on the first and second days of exposure to deionized water in H. malabaricus and only on the first day in H. unitaeniatus. Plasma ions in both erythrinid species showed transitory changes and, on the fifteenth day of exposure to the two types of experimental water, the plasma ion concentration was similar to the control fish. The CC responses of these erythrinid fish showed that CC proliferation depends on previous CC density in the gill and is not related solely to exposure to ion-poor water. Furthermore, CC proliferation in gill epithelium did not always involve an increase of CC density in contact with the external medium.     

Food resource partitioning and trophic morphology of Brevoortia gunteri and B. patronus

The menhadens Brevoortia gunteri and B. patronus are sympatric and morphologically similar. The two species are planktophagous and exhibited significant ( P < 0·0001) food resource partitioning, with phytoplankton predominating in B. patronus stomachs and zooplankton in B. gunteri. The branchial apparatus of both species is of the typical alosine form. Brevoortia patronus has significantly more branchiospinules per mm (=19·47) and significantly longer gill rakers (=13·35 mm) than B. gunteri (=14·11, =12·01 mm respectively). B. patronus is characterized by a gill raker system forming a fine-meshed filter capable of retaining smaller food items. The results support the hypothesis that food resource partitioning is related to different morphological features of the branchial apparatus.     

Morphological and mitochondrial DNA divergence validates blackmouth, Galeus melastomus, and Atlantic sawtail catsharks, Galeus atlanticus, as separate species

A total of 60 morphometric traits and nucleotide sequences of the entire mtDNA NADH dehydrogenase subunit 2 (ND2) gene [1047 base pair (bp)] in 23 individuals of blackmouth, Galeus melastomus , and 13 individuals of sawtail catsharks, Galeus atlanticus , caught in Southern Portugal, were examined to test the validity of these two taxa. These sharks closely resemble each other, have overlapping geographical ranges and are difficult to identify by morphological characters. Non-metric multidimensional scaling of morphometric variables indicates a clear separation between the two species, with 10 characters each contributing 2·12–2·45% of the total variability between species. Maximum likelihood, parsimony and neighbour-joining trees revealed two major mtDNA haplotype clades, corresponding to the two species, with an average corrected sequence divergence between them of 3·39 ± 0·56%. Within species divergences between haplotypes averaged 0·27 ± 0·18% in G. melastomus and 0·12 ± 0·08% in G. atlanticus . A total of 35 diagnostic nucleotide site differences and four restriction fragment length polymorphism recognition sites in the ND2 gene can be used to distinguish the two species.     

Reexamination of the Byczkowska-Smyk gill surface area data for European teleosts, with new measurements on the pikeperch, Sander lucioperca

This paper reexamines the gill morphometrics of 20 European teleosts first reported in the early gill literature by Byczkowska-Smyk and colleagues in attempt to clarify the long-recognized discrepancies between these data and those obtained in subsequent works. Determination of gill dimensions for the pikeperch, Sander lucioperca, in this study (a species for which Byczkowska-Smyk reported data), along with a literature review for other European teleosts, reveals inaccurate estimation of the total gill surface area by up to 18× for 19 of the 20 species reexamined. This error results primarily from imprecise determination of the bilateral surface area of individual gill lamellae and, to a lesser extent, the incorrect assumption that lamellar area and frequency are species-specific constants that do not vary with fish body mass. This review compiles gill morphometric data from various sources to be used in place of the inaccurate gill area estimates of Byczkowska-Smyk and colleagues and thereby clears the way for higher resolution in the comparative analysis of gill morphology and its correlation to fish habitat and life history characteristics.     

On the conservative nature of the gill filaments of sharks

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

Characteristics of egg and larval production in captive bluespotted gobies

Spawning of the Hawaiian coral-reef goby Asterropteryx semipunctata was diurnal, occurring at various times throughout the day. Mean length of eggs deposited in nests was 0·76 mm (range 0·67–0·84); mean egg width was 0·47 mm (range 0·41–0·52). Clutch size varied from 296 to 1552 eggs (mean=886±309), and was independent of standard length, total body weight, and body condition. Mean relative clutch size was 1·59 eggs mg^-1 total body weight (range 0·84–2·43). Clutches hatched 4–5 nights after being deposited in a nest. Mean notochord length of newly-hatched larvae was 1·88 mm (range 1·60–2·04). The minimum period of time that elapsed between egg deposition and subsequent growth of a new batch of oocytes to spawning size was 5–6 days, providing a reasonable estimate of minimum spawning interval. Compared with other gobiids, tropical species tend to have shorter incubation periods, smaller eggs and smaller larvae at hatching.     

Copepod ectoparasites of Merlangius merlangus and Platichthys flesus

Seasonal changes in the levels of copepod ectoparasitic infections from Merlangius merlangus and Platichthys flesus were examined and related to the annual migrations of young fish into an estuary. Lernaeocera branchialis (L.) was the only parasite common to both fish species; its life-cycle stages infected the branchial chambers of 96·7% flounders ( P. flesus ) and 40·4% whiting ( M. merlangus ). Infection in the two fish species exhibited similar seasonal fluctuations and a temporal relationship between the parasite's occurrence on its two hosts was apparent. Whiting were also parasitized by Clavella uncinata (Milller); 26·9 % fish were affected. The copepods' distribution was highly localized with the majority restricted to the long gill rakers of the first gill arch. Infection was related to size of whiting up to 12·5 cm; there was little increase beyond this length. In addition to L. branchialis , flounder was also host to Acanthochondria depressa (T. Scott) and Lepeophtheirus pectoralis (Müller). A. depressa showed a preference for the ocular side of the body with its developing stages attached mainly to the second gill arch and the adults located in the posterior pocket of the branchial chamber. L. pectoralis was associated with the paired fins. Factors which could result in such localized distributions are discussed.