The scaling and potential importance of cutaneous and branchial surfaces in respiratory gas exchange in larval and juvenile walleye

Measurements were made of the surface areas (As) of the skin and gills of larval and juvenile walleye Stizostedion vitreum with a body mass (M) of between 2mg (1 day post hatch) and 2.3g (98 days post hatch). The skin, with a relative surface area (As/M) of approximately 8500mm2g-1, accounted for more than 99.9% of the total surface area (skin + gills) at 1 day post hatch. The relative area of the skin decreased as fish grew at an allometric rate of b-1=-0.32±0.01 (mean ± s.e.m., where b-1 is the specific-mass exponent in the allometric equation YxM-1=aMb-1, in which Y is surface area and a is a constant). The relative surface area of the gills (filaments + lamellae) increased in a hyperbolic fashion from very low levels (approximately 5mm2g-1) at 1 day post hatch to reach a maximum of approximately 1100mm2g-1 at a body mass of approximately 200mg. Thereafter, relative gill area declined at an allometric rate of b-1=-0.19±0.10 (mean ± s.e.m.). Gill area, because it declined at a slower relative rate, finally exceeded skin area at a body mass of approximately 700mg. The relative surface area of the skin and gills combined (total surface area) decreased at a more-or-less constant allometric rate of b-1=-0.21±0.01 (mean ± s.e.m.) throughout the experimental period. On the basis of the allometric rates of expansion, the structural capacity to supply oxygen (b-1=-0.19; total gill area, this study) and metabolic demand for oxygen (b-1~-0.13; mean literature value for routine and resting metabolism) appear to remain fairly closely matched in postlarval walleye (>300mg). The two parameters do not display the same degree of concordance during larval development. In larvae, total respiratory surface area declines on a mass-specific basis at roughly the same rate (b-1=-0.21) as gill area does in older fish but, unlike in older fish, metabolic demand for oxygen does not change (b-1~0.0). This results in a progressive decline in effective respiratory surface area (As/M.O2) but does not affect O2 uptake, probably because larvae are so small that surface area is not the limiting factor in gas exchange. Analysis of data from the literature suggests that surface area typically becomes limiting at a body mass of approximately 100mg. The major function of gills in smaller larvae (<100mg) appears to involve ionoregulation or related aspects of acidbase balance rather than respiratory gas exchange.

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The scaling and potential importance of cutaneous and branchial surfaces in respiratory gas exchange in young chinook salmon (oncorhynchus tshawytscha)

Journal of Experimental Biology ◽

10.1242/jeb.154.1.1 ◽

1990 ◽

Vol 154 (1) ◽

pp. 1-12 ◽

Cited By ~ 1

Author(s):

PETER J. ROMBOUGH ◽

BRENDA M. MOROZ

Keyword(s):

Gas Exchange ◽

Metabolic Rate ◽

Surface Area ◽

Chinook Salmon ◽

Oncorhynchus Tshawytscha ◽

Total Surface Area ◽

Tissue Mass ◽

Respiratory Gas Exchange ◽

Yolk Absorption ◽

Gill Lamellae

Measurements were made of the surface areas of the yolk sac, the fins, the head and trunk, the gill filaments and the gill lamellae of chinook salmon (Oncorhynchus tshawytscha Walbaum) weighing between 0.045 g (3.7 days posthatch) and 13.4g (180 days posthatch). Cutaneous surfaces initially accounted for the vast majority (approx. 96%) of the total area available for respiratory gas exchange. As fish grew, total branchial surface area expanded at a more rapid rate than cutaneous surface area and, thus, came to represent a progressively larger fraction of total surface area. The transition was relatively slow, however, and it was not until fish reached 2.5-4.0 g that branchial area exceeded cutaneous area. Although some individual surfaces (e.g. the gill lamellae) followed rather complex patterns of expansion, the overall increase in respiratory surface area with tissue mass could be described reasonably well using only two equations; one for the period prior to complete yolk absorption (<0.4 g) and one for the period following complete yolk absorption (>0.4 g). Mass exponents for total surface area (b = 0.85) and metabolic rate (b = 0.8-0.9) were not significantly different for the larger fish. In contrast, the mass exponent for total surface area (b = 0.39) was significantly less than that for metabolic rate (b ≈ 0.9-1.0) for fish weighing less than 0.4 g. Changes in the relative efficiencies of the various exchange surfaces during the course of larval development probably account for this discrepancy.

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Gas exchange and metabolism in the sirenidae (Amphibia: Caudata)—I. Oxygen consumption of submerged sirenids as a function of body size and respiratory surface area

Comparative Biochemistry and Physiology Part A Physiology ◽

10.1016/0300-9629(74)90012-7 ◽

1974 ◽

Vol 47 (2) ◽

pp. 485-498 ◽

Cited By ~ 34

Author(s):

Gordon R Ultsch

Keyword(s):

Oxygen Consumption ◽

Body Size ◽

Gas Exchange ◽

Surface Area ◽

Respiratory Surface

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The respiratory development of Atlantic salmon. I. Morphometry of gills, yolk sac and body surface

Journal of Experimental Biology ◽

10.1242/jeb.199.12.2725 ◽

1996 ◽

Vol 199 (12) ◽

pp. 2725-2736 ◽

Cited By ~ 3

Author(s):

P Wells ◽

A Pinder

Keyword(s):

Atlantic Salmon ◽

Surface Area ◽

Early Development ◽

Body Mass ◽

Body Surface ◽

Yolk Sac ◽

High Mass ◽

Skin Area ◽

Diffusion Distance ◽

Yolk Absorption

During development from larva to juvenile in Atlantic salmon, Salmo salar, there is a change in the anatomical potential for gas exchange among gills, body skin and yolk sac as the larvae resorb yolk, grow and develop gills. Newly hatched Atlantic salmon have poorly developed gills but do have a high skin area to mass ratio and a large well-vascularized yolk sac. Cutaneous surfaces accounted for over 95 % of the total area available for respiration in newly hatched Atlantic salmon (body mass 0.0320.060 g). The branchial contribution to total area increased rapidly, however, so that by the end of yolk absorption (body mass 0.190.23 g) it constituted 22 % of the total area and overtook cutaneous surface area between 5 and 6 g wet body mass. Harmonic mean diffusion distance across the skin increased through development from 20 µm at hatch (14 µm across the yolk sac) to 70 µm in an 11 g fish. Diffusion distances across both the filaments and lamellae of the gills decreased through development, from 3.7 to 2.4 µm for lamellae and from 14.5 to 10.8 µm for filaments. The total anatomical diffusion factor (ADF, mass-specific surface area per unit diffusion distance) remained constant over early development and appeared to be higher than in adult fish. The distribution of ADF changed over early development from 50 % yolk sac, 42 % body surface and 8 % branchial in newly hatched fish to 68 % branchial and 32 % cutaneous at the end of yolk resorption. Generally, early post-hatch development of gills, ADF and some cutaneous surfaces showed high mass exponents. After yolk resorption (body mass 0.2 g), however, these coefficients were lower and closer to unity. The change in scaling at the end of yolk resorption in this study may reflect the completion of larva to juvenile metamorphosis in Atlantic salmon. Comparison between our data and values in the literature suggests that the timing of gill development is related more to developmental stage than to body size.

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Size, shape, and surface area of beaver, Castor canadensis, a semiaquatic mammal

Canadian Journal of Zoology ◽

10.1139/z93-114 ◽

1993 ◽

Vol 71 (5) ◽

pp. 876-882 ◽

Cited By ~ 7

Author(s):

P. S. Reynolds

Keyword(s):

Surface Area ◽

Body Mass ◽

Marine Mammal ◽

Body Shape ◽

Castor Canadensis ◽

Total Surface Area ◽

Energetic Efficiency ◽

Terrestrial Mammals ◽

Surface Areas ◽

Average Surface Area

The beaver, Castor canadensis, is a large, herbivorous, semiaquatic rodent. Beaver forage on land as well as in water; thus functional compromise between competing activities should result in a less streamlined body shape than expected for a similarly sized marine mammal. Standard morphometrics and surface areas of 70 Wisconsin beaver ranging in size from 5 to 35 kg were measured. Geometric similarity of surface area was maintained during growth (i.e., area was proportional to body mass raised to the 2/3 power). Scaly-tail area was positively allometric with body mass; hind foot web area was weakly negatively allometric. The surface area of the unfurred extremities (hind feet and scaly tail) comprised 30% of the total surface area of adults and over 50% for younger beaver. The average surface area of 21 adult beaver (mean body mass = 20 kg) was 0.52 m2. This value was significantly lower (P < 0.001) than predicted from the Meeh equation for terrestrial mammals, but similar to that expected for a marine mammal of equivalent mass. Body shape was described by the fineness ratio (a hydrodynamic index of streamlining). The fineness ratio for beaver was 4.8, a value similar to that for phocid seals. Therefore, in spite of expected constraints on body shape imposed by herbivory and the competing demands of terrestrial and aquatic foraging, beaver do not differ significantly in overall shape from other, more aquatic, species. However, shape alone is not a reliable indicator of either hydrodynamic or energetic efficiency. Future comparative studies should incorporate both phylogeny and biomechanical data into evaluations of mammalian morphology.

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A stereological comparison of villous and microvillous surfaces in small intestines of frugivorous and entomophagous bats: species, inter-individual and craniocaudal differences.

Journal of Experimental Biology ◽

10.1242/jeb.200.18.2415 ◽

1997 ◽

Vol 200 (18) ◽

pp. 2415-2423 ◽

Cited By ~ 1

Author(s):

A N Makanya ◽

J N Maina ◽

T M Mayhew ◽

S A Tschanz ◽

P H Burri

Keyword(s):

Surface Area ◽

Body Mass ◽

Membrane Surface ◽

Total Surface Area ◽

Membrane Surface Area ◽

Intestinal Tube ◽

Surface Areas ◽

Intestinal Length ◽

Mass Coefficient ◽

Extensive Surface

The extents of functional surfaces (villi, microvilli) have been estimated at different longitudinal sites, and in the entire small intestine, for three species of bats belonging to two feeding groups: insect- and fruit-eaters. In all species, surface areas and other structural quantities tended to be greatest at more cranial sites and to decline caudally. The entomophagous bat (Miniopterus inflatus) had a mean body mass (coefficient of variation) of 8.9 g (5%) and a mean intestinal length of 20 cm (6%). The surface area of the basic intestinal tube (primary mucosa) was 9.1 cm2 (10%) but this was amplified to 48 cm2 (13%) by villi and to 0.13 m2 (20%) by microvilli. The total number of microvilli per intestine was 4 x 10(11) (20%). The average microvillus had a diameter of 8 nm (10%), a length of 1.1 microns (22%) and a membrane surface area of 0.32 micron 2 (31%). In two species of fruit bats (Epomophorus wahlbergi and Lisonycteris angolensis), body masses were greater and intestines longer, the values being 76.0 g (18%) and 76.9 g (4%), and 73 cm (16%) and 72 cm (7%), respectively. Surface areas were also greater, amounting to 76 cm2 (26%) and 45 cm2 (8%) for the primary mucosa, 547 cm2 (29%) and 314 cm2 (16%) for villi and 2.7 m2 (23%) and 1.5 m2 (18%) for microvilli. An increase in the number of microvilli, 33 x 10(11) (19%) and 15 x 10(11) (24%) per intestine, contributed to the more extensive surface area but there were concomitant changes in the dimensions of microvilli. Mean diameters were 94 nm (8%) and 111 nm (4%), and mean lengths were 2.8 microns (12%) and 2.9 microns (10%), respectively. Thus, an increase in the surface area of the average microvillus to 0.83 micron 2 (12%) and 1.02 microns 2 (11%) also contributed to the greater total surface area of microvilli. The lifestyle-related differences in total microvillous surface areas persisted when structural quantities were normalised for the differences in body masses. The values for total microvillous surface area were 148 cm2g-1 (20%) in the entomophagous bat, 355 cm2g-1 (20%) in E. wahlbergi and 192 cm2g-1 (17%) in L. angolensis. This was true despite the fact that the insecteater possessed a greater length of intestine per unit of body mass: 22 mm g-1 (8%) versus 9-10 mm g-1 (9-10%) for the fruit-eaters.

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Comparative study of gill dimensions of three erythrinid species in relation to their respiratory function

Canadian Journal of Zoology ◽

10.1139/z94-020 ◽

1994 ◽

Vol 72 (1) ◽

pp. 160-165 ◽

Cited By ~ 34

Author(s):

Marisa Narciso Fernandes ◽

Franscisco Tadeu Rantin ◽

Ana Lúcia Kalinin ◽

Sandro EsteVAN Moron

Keyword(s):

Surface Area ◽

Body Mass ◽

Respiratory Function ◽

Ecological Factors ◽

Specific Area ◽

Filament Length ◽

Respiratory Surface ◽

Secondary Lamellae ◽

Increase Surface Area ◽

Hoplerythrinus Unitaeniatus

Gill dimensions were analysed in relation to body mass in three erythrinid fish, an air-breathing species, Hoplerythrinus unitaeniatus, and two ecologically distinct water-breathing species, Hoplias malabaricus and Hoplias lacerdae. Evidence was obtained of remarkable differences in patterns of increase in filament length, number of secondary lamellae, bilateral area of the secondary lamellae, total area of the secondary lamellae, and mass-specific area of the secondary lamellae among these three species. The analysis showed a large increase in respiratory surface area relative to body mass in H. malabaricus (b = 1.14) compared with Hoplias lacerdae (b = 0.81) and H. unitaeniatus (b = 0.66). This difference is mainly attributed to an increase surface area of individual secondary lamellae together with an increase in filament length and total number of secondary lamellae. The results indicate that the increased respiratory surface area of the H. malabaricus gill facilitates oxygen uptake in hypoxic environments as the fish grows and this suggests that gill dimensions may reflect ecological factors and not only respiratory requirements.

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An analysis of respiratory surface area as a limit to activity metabolism in anurans

Canadian Journal of Zoology ◽

10.1139/z79-277 ◽

1979 ◽

Vol 57 (11) ◽

pp. 2100-2105 ◽

Cited By ~ 26

Author(s):

Stanley S. Hillman ◽

Philip C. Withers

Keyword(s):

Oxygen Consumption ◽

Gas Exchange ◽

Surface Area ◽

Interspecific Difference ◽

Capillary Length ◽

Anuran Amphibians ◽

Interspecific Differences ◽

Respiratory Surface ◽

Consumption Rates ◽

Maximum Limit

Maximal [Formula: see text] and resting [Formula: see text] oxygen consumption rates of a variety of anuran amphibians were measured to evaluate the proportionality between [Formula: see text], [Formula: see text], and mass. Interspecific differences in the slope of the function relating [Formula: see text] and body mass were not correlated with differences in respiratory capillary length. Interspecific differences in absolute [Formula: see text] were not matched by any interspecific difference in respiratory capillary length. Unilaterally pneumonectomized Xenopus laevis did not show a decline in [Formula: see text] proportional to the amount of respiratory surface area removed. The data indicate that respiratory surface area does not impose a maximum limit on gas exchange in anuran amphibians.

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Postnatal treatment with retinoic acid increases the number of pulmonary alveoli in rats

AJP Lung Cellular and Molecular Physiology ◽

10.1152/ajplung.1996.270.2.l305 ◽

1996 ◽

Vol 270 (2) ◽

pp. L305-L310 ◽

Cited By ~ 65

Author(s):

G. D. Massaro ◽

D. Massaro

Keyword(s):

Retinoic Acid ◽

Gas Exchange ◽

Surface Area ◽

Body Mass ◽

Regulatory Mechanism ◽

Pulmonary Alveoli ◽

Experimental Support ◽

Postnatal Treatment ◽

Exchange Surface ◽

Postnatal Rats

Dexamethasone, a glucocorticosteroid hormone, inhibits the formation of alveoli; retinoids and glucocorticosteroid hormones can be mutually antagonistic. These observations led us to test the hypothesis that the administration of retinoic acid to postnatal rats would prevent the low alveolar number and the low body mass-specific gas-exchange surface area (Sa) produced by treatment with dexamethasone. We used serial lung sections to distinguish alveoli from alveolar ducts and stereological procedures that allow quantitation of alveoli uninfluenced by their size, shape, or distribution. Treatment with retinoic acid prevented the low number of alveoli and the low body mass-specific Sa caused by treatment with dexamethasone. In otherwise untreated rats, retinoic acid caused a 50% increase in the number of alveoli, but without an increase in Sa, suggesting the action of a regulatory mechanism to prevent unneeded Sa. These findings provide the first experimental support for the possibility that, in individuals with too few alveoli for adequate gas exchange, treatment with a pharmacological agent may provide preventative or remedial therapy.

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