Gill Surface Area Research Articles

Ecology of ontogenetic body-mass scaling of gill surface area in a freshwater crustacean

Several studies have documented ecological effects on intraspecific and interspecific body-size scaling of metabolic rate. However, little is known about how various ecological factors may affect the scaling of respiratory structures supporting oxygen uptake for metabolism. To our knowledge, our study is the first to provide evidence for ecological effects on the scaling of a respiratory structure among conspecific populations of any animal. We compared the body-mass scaling of gill surface area (SA) among eight spring-dwelling populations of the amphipod crustacean Gammarus minus Although gill SA scaling was not related to water temperature, conductivity or G. minus population density, it was significantly related to predation regime (and secondarily to pH). Body-mass scaling slopes for gill SA were significantly lower in four populations inhabiting springs with fish predators than for four populations in springs without fish (based on comparing means of the population slopes, or slopes calculated from pooled raw data for each comparison group). As a result, gill SA was proportionately smaller in adult amphipods from springs with versus without fish. This scaling difference paralleled similar differences in the scaling exponents for the rates of growth and resting metabolic rate. We hypothesized that gill SA scaling is shallower in fish-containing versus fishless spring populations of G. minus because of effects of size-selective predation on size-specific growth and activity that in turn affect the scaling of oxygen demand and concomitantly the gill capacity (SA) for oxygen uptake. Although influential theory claims that metabolic scaling is constrained by internal body design, our study builds on previous work to show that the scaling of both metabolism and the respiratory structures supporting it may be ecologically sensitive and evolutionarily malleable.

Climatic variability in combination with eutrophication drives adaptive responses in the gills of Lake Victoria cichlids.

Textbook examples of adaptive radiation often show rapid morphological changes in response to environmental perturbations. East Africa's Lake Victoria, famous for its stunning adaptive radiation of cichlids, has suffered from human-induced eutrophication over the past decades. This cultural eutrophication is thought to be partly responsible for the dramatically reduced cichlid biodiversity, but climatic variability in itself might also have contributed to the eutrophication which resulted in low oxygen levels and decreased water transparency. To determine how recent environmental changes have influenced the lake and its cichlids over the past 50years, we gathered environmental and meteorological variables and compared these with gill surface area of four cichlid species. We found that during the period of severe eutrophication and temperature increase (1980s), reduced wind speeds coincided with a reduction in oxygen levels and a decrease in both water temperature and transparency. The gill surface area in three out of the four cichlid species increased during this period which is consistent with adaptive change in response to increased hypoxia. During the 2000s, wind speeds, oxygen levels, water transparency and water temperature increased again, while cichlid gill surface area decreased. Our results imply that climatic changes and especially wind speed and direction might play a crucial role in tropical lake dynamics. The changes in Lake Victoria's water quality coincide with fluctuations in cichlid gill surface area, suggesting that these fish can respond rapidly to environmental perturbations, but also that climatic variability, together with continued eutrophication, might be detrimental to the lake's cichlid biodiversity.

Interspecific and environment-induced variation in hypoxia tolerance in sunfish

Hypoxia tolerance is a plastic trait, and can vary between species. We compared hypoxia tolerance (hypoxic loss of equilibrium, LOE, and critical O2 tension, Pcrit) and traits that dictate O2 transport and metabolism in pumpkinseed (Lepomis gibbosus), bluegill (L. macrochirus), and the naturally occurring hybrid in different acclimation environments (wild versus lab-acclimated fish) and at different temperatures. Wild fish generally had lower Pcrit and lower PO2 at LOE in progressive hypoxia than lab-acclimated fish, but time to LOE in sustained hypoxia (PO2 of 2kPa) did not vary between environments. Wild fish also had greater gill surface area and higher haematocrit, suggesting that increased O2 transport capacity underlies the environmental variation in Pcrit. Metabolic (lactate dehydrogenase, LDH; pyruvate kinase, PK; citrate synthase; cytochrome c oxidase) and antioxidant (catalase and superoxide dismutase) enzyme activities varied appreciably between environments. Wild fish had higher protein contents across tissues and higher activities of LDH in heart, PK in brain, and catalase in brain, liver, and skeletal muscle. Otherwise, wild fish had lower activities for most enzymes. Warming temperature from 15 to 25°C increased O2 consumption rate, Pcrit, PO2 at LOE, and haemoglobin-O2 affinity, and decreased time to LOE, but pumpkinseed had ≥2-fold longer time to LOE than bluegill and hybrids across this temperature range. This was associated with higher LDH activities in the heart and muscle, and lower or similar antioxidant enzyme activities in several tissues. However, the greater hypoxia tolerance of pumpkinseed collapsed at 28°C, demonstrating that the interactive effects of hypoxia and warming temperature can differ between species. Overall, distinct mechanisms appear to underpin interspecific and environment-induced variation in hypoxia tolerance in sunfish.

Estimating Symbiont Abundances and Gill Surface Areas in Specimens of the Hydrothermal Vent Mussel Bathymodiolus puteoserpentis Maintained in Pressure Vessels

The hydrothermal vent mussel Bathymodiolus puteoserpentis hosts gill-associated sulfur- and methane-oxidizing bacteria which sustain host nutrition and allow it to reach high densities at various sites along the northern Mid-Atlantic Ridge. Previous studies have demonstrated that in similar dual symbioses, relative abundances of each bacterial type could change following variations in symbiont substrate availabilities. In this study, pressurized recovery and incubations in pressure vessels were used to test whether B. puteoserpentis symbionts displayed similar behavior in the presence of symbiont substrates. The relative abundances of both types of symbionts were analyzed using fluorescence in situ hybridization (FISH) and group-specific gene copy numbers were assessed using qPCR. Specimens sampled using isobaric and non-isobaric recovery contained similar relative proportions (in surface coverage) of sulfur- and methane-oxidizing bacteria indicating that recovery type did not have impact on measured relative areas. Similarly, pressurized incubations with different substrates did lead to significant differences in the relative surface coverage of the two types of bacteria, although slight variations were measured with qPCR, suggesting changes in relative abundances of gene copy numbers but not in relative areas covered. Total gill surface areas and total bacterial numbers in specimens were estimated for the first time. Symbiont bearing-mussels display exchange surfaces about 20-fold higher than those found in similar-sized coastal mussels, and mean bacterial numbers of 2.5*1012 per specimen were estimated. This emphasizes that symbiotic mussels are a major reservoir of bacteria in vent ecosystems.

Differences in feeding adaptations in intertidal and subtidal suspension-feeding gastropods: studies on Crepidula fornicata and Crepipatella peruviana

Suspension-feeding organisms living in the intertidal zone experience reduced feeding times associated with periodic aerial exposure. The potential morphological and physiological adaptations to this reduced feeding time were investigated for two closely related gastropods, Crepidula fornicata and Crepipatella peruviana. Intertidal C. fornicata had heavier gills than subtidal conspecifics, a difference mediated by larger gill surface areas and greater numbers of gill filaments among intertidal individuals of a given size. In contrast, the gills of intertidal and subtidal C. peruviana were morphologically indistinguishable. Despite relatively larger food-collecting organs, individuals of C. fornicata from the intertidal zone had clearance rates (CR) that were not significantly different from those of subtidal conspecifics. In contrast, the CR of intertidal C. peruviana were significantly lower than those of subtidal conspecifics. The low CR of intertidal C. peruviana may be partially explained by significantly lower measured particle transport velocities across their gills. In the context of feeding, intertidal individuals of C. fornicata performed at least as well as subtidal conspecifics, resulting in a population whose adults were as large as those found subtidally. This suggests that C. fornicata has had a long interaction with the environmental heterogeneity associated with intertidal life. In contrast, intertidal individuals of C. peruviana were on average smaller than subtidal individuals and may be stressed in the intertidal.

Gill dimensions in near-term embryos of Amazonian freshwater stingrays (Elasmobranchii: Potamotrygonidae) and their relationship to the lifestyle and habitat of neonatal pups

This comparative study of gill morphometrics in near-term embryos of freshwater stingray potamotrygonids examines gill dimensions in relation to neonatal lifestyle and habitat. In embryos of the potamotrygonids Paratrygon aiereba, Plesiotrygon iwamae, Potamotrygon motoro, Potamotrygon orbignyi, and cururu ray Potamotrygon sp. the number and length of filaments, total gill surface area, mass-specific surface area, water-blood diffusion distance, and anatomical diffusion factor were analysed. In all potamotrygonids, the 3rd branchial arch possessed a larger respiratory surface than the other gill arches. Larger embryos had more gill surface area and large spiracles, which are necessary to maintain the high oxygen uptake needed due to their larger body size. However, the higher mass-specific gill surface area observed in near-term embryos may be advantageous because neonates can use hypoxic environments as refuges against predators, as well as catch small prey that inhabit the same environment. As expected from their benthic mode of life, freshwater stingrays are sluggish animals compared to pelagic fishes. However, based on gill respiratory morphometry (such as gill area, mass-specific gill area, the water-blood diffusion barrier, anatomical diffusion factor, and relative opening of the spiracle), subtypes of lifestyles can be observed corresponding to: active, intermediate, and sluggish species according to Gray's scale.

Gill morphometrics of the thresher sharks (Genus Alopias): Correlation of gill dimensions with aerobic demand and environmental oxygen.

Gill morphometrics of the three thresher shark species (genus Alopias) were determined to examine how metabolism and habitat correlate with respiratory specialization for increased gas exchange. Thresher sharks have large gill surface areas, short water-blood barrier distances, and thin lamellae. Their large gill areas are derived from long total filament lengths and large lamellae, a morphometric configuration documented for other active elasmobranchs (i.e., lamnid sharks, Lamnidae) that augments respiratory surface area while limiting increases in branchial resistance to ventilatory flow. The bigeye thresher, Alopias superciliosus, which can experience prolonged exposure to hypoxia during diel vertical migrations, has the largest gill surface area documented for any elasmobranch species studied to date. The pelagic thresher shark, A. pelagicus, a warm-water epi-pelagic species, has a gill surface area comparable to that of the common thresher shark, A. vulpinus, despite the latter's expected higher aerobic requirements associated with regional endothermy. In addition, A. vulpinus has a significantly longer water-blood barrier distance than A. pelagicus and A. superciliosus, which likely reflects its cold, well-oxygenated habitat relative to the two other Alopias species. In fast-swimming fishes (such as A. vulpinus and A. pelagicus) cranial streamlining may impose morphological constraints on gill size. However, such constraints may be relaxed in hypoxia-dwelling species (such as A. superciliosus) that are likely less dependent on streamlining and can therefore accommodate larger branchial chambers and gills.

Exposure to acute severe hypoxia leads to increased urea loss and disruptions in acid-base and ionoregulatory balance in dogfish sharks (Squalus acanthias).

The effects of acute moderate (20% air O2 saturation; 6-h exposure) and severe (5% air O2 saturation; 4-h exposure) hypoxia on N-waste, acid-base, and ion balance in dogfish sharks (Squalus acanthias suckleyi) were evaluated. We predicted that the synthesis and/or retention of urea, which are active processes, would be inhibited by hypoxia. Exposure to moderate hypoxia had negligible effects on N-waste fluxes or systemic physiology, except for a modest rise in plasma lactate. Exposure to severe hypoxia led to a significant increase in urea excretion (Jurea), while plasma, liver, and muscle urea concentrations were unchanged, suggesting a loss of urea retention. Ammonia excretion (Jamm) was elevated during normoxic recovery. Moreover, severe hypoxia led to disruptions in acid-base balance, indicated by a large increase in plasma [lactate] and substantial decreases in arterial pHa and plasma [Formula: see text], as well as loss of ionic homeostasis, indicated by increases in plasma [Mg(2+)], [Ca(2+)], and [Na(+)]. We suggest that severe hypoxia in dogfish sharks leads to a reduction in active gill homeostatic processes, such as urea retention, acid-base regulation and ionoregulation, and/or an osmoregulatory compromise due to increased functional gill surface area. Overall, the results provide a comprehensive picture of the physiological responses to a severe degree of hypoxia in an ancient fish species.

Hypoxia effects on gill surface area and blood oxygen-carrying capacity of the Atlantic stingray, Dasyatis sabina

Atlantic stingrays, Dasyatis sabina, are common residents of shallow-water seagrass habitats that experience natural cycles of severe hypoxia during summer months. We hypothesized that stingrays exposed to hypoxic episodes would improve their hypoxia tolerance by increasing branchial surface area and altering blood oxygen-carrying capacity. To this end, we compared critical oxygen minimum, gill morphology, and hemoglobin/hematocrit levels in a control group of Atlantic stingrays held at continuous oxygen saturations of 80-90% (≥5.5 mg/l), to treatment groups exposed to a 7-h hypoxic interval at 55% (~4.0 mg/l), or 30% oxygen saturation (~2.0 mg/l). Stingrays in hypoxic treatment groups significantly improved their hypoxia tolerance. Critical oxygen minimum values fell from 0.7 ± 0.11 mg/l in control fish to 0.4 ± 0.05 and 0.4 ± 0.06 mg/l in the 55 and 30% saturation treatment groups, respectively. Mass-specific gill surface area between control fish and the 30% saturation treatment group increased by 1.7-fold, from 85 to 142 mm(2)/g. Although stingrays did not show an increase in hematocrit or hemoglobin levels, production of more efficient hemoglobin isoforms could not be ruled out. An increase in hypoxia tolerance allows Atlantic stingrays to forage for longer times and across a wide range of hypoxic habitats that are less accessible to predators and competitors.

Theme and variations: amphibious air‐breathing intertidal fishes

Over 70 species of intertidal fishes from 12 families breathe air while emerging from water. Amphibious intertidal fishes generally have no specialized air-breathing organ but rely on vascularized mucosae and cutaneous surfaces in air to exchange both oxygen and carbon dioxide. They differ from air-breathing freshwater fishes in morphology, physiology, ecology and behaviour. Air breathing and terrestrial activity are present to varying degrees in intertidal fish species, correlated with the tidal height of their habitat. The gradient of amphibious lifestyle includes passive remainers that stay in the intertidal zone as tides ebb, active emergers that deliberately leave water in response to poor aquatic conditions and highly mobile amphibious skipper fishes that may spend more time out of water than in it. Normal terrestrial activity is usually aerobic and metabolic rates in air and water are similar. Anaerobic metabolism may be employed during forced exercise or when exposed to aquatic hypoxia. Adaptations for amphibious life include reductions in gill surface area, increased reliance on the skin for respiration and ion exchange, high affinity of haemoglobin for oxygen and adjustments to ventilation and metabolism while in air. Intertidal fishes remain close to water and do not travel far terrestrially, and are unlikely to migrate or colonize new habitats at present, although in the past this may have happened. Many fish species spawn in the intertidal zone, including some that do not breathe air, as eggs and embryos that develop in the intertidal zone benefit from tidal air emergence. With air breathing, amphibious intertidal fishes survive in a variable habitat with minimal adjustments to existing structures. Closely related species in different microhabitats provide unique opportunities for comparative studies.

Interspecific Differences in Hypoxia-Induced Gill Remodeling in Carp

The gills of many fish, but in particular those of crucian carp (Carassius carassius) and goldfish (Carassius auratus), are capable of extensive remodeling in response to changes in oxygen (O2), temperature, and exercise. In this study, we investigated the interspecific variation in hypoxia-induced gill modeling and hypoxia tolerance in 10 closely related groups of cyprinids (nine species, with two strains of Cyprinus carpio). There was significant variation in hypoxia tolerance, measured as the O2 tension (P(O2)) at which fish lost equilibrium (LOEcrit), among the 10 groups of carp. In normoxia, there was a significant, phylogenetically independent relationship between mass-specific gill surface area and LOEcrit, with the more hypoxia-tolerant carp having smaller gills than their less hypoxia-tolerant relatives. All groups of carp, except the Chinese bream (Megalobrama pellegrini), increased mass-specific gill surface area in response to 48 h of exposure to hypoxia (0.7 kPa) through reductions in the interlamellar cell mass (ILCM) volume. The magnitude of the hypoxia-induced reduction in the ILCM was negatively correlated with LOEcrit (and thus positively correlated with hypoxia tolerance), independent of phylogeny. The hypoxia-induced changes in gill morphology resulted in reduced variation in mass-specific gill surface area among species and eliminated the relationship between LOEcrit and mass-specific gill surface area. While behavioral responses to hypoxia differed among the carp groups, there were no significant relationships between hypoxia tolerance and the Po2 at which aquatic surface respiration (ASR) was initiated or the total number of ASR events observed during progressive hypoxia. Our results are the first to show that the extent of gill remodeling in cyprinids is associated with hypoxia tolerance in a phylogenetically independent fashion.

Respiratory function in common carp with different stress coping styles: a hidden cost of personality traits?

The purpose of this study was to compare investment in structures for gas exchange in common carp, Cyprinus carpio, with different stress coping styles, which are known to differ in resting metabolic rate. Common carp were classified as proactive or reactive on the basis of rate of emergence from cover into a novel, potentially dangerous environment in three successive tests. The fish were then killed and their gill arches removed. Length-independent estimates of the size of the respiratory structures were derived by multivariate analysis of arch length and the number and length of gill filaments and lamellae for all gill arches. Overall gill area was also estimated. Filaments from the second gill arch were sampled for histological estimation of the extent to which the respiratory surface is covered by epithelial cells (hyperplasia). Proactive carp had longer gill filaments and more, longer lamellae, and consequently a larger gill surface area, than reactive carp. In contrast, the extent of hyperplasia was higher in reactive than proactive carp. Thus, compared to reactive fish, proactive carp had a larger respiratory surface, more of which was exposed to the surrounding water rather than being covered by epithelial cells. We suggest that the higher metabolic rate of proactive fish requires greater investment in, and greater exposure of, the respiratory structures. This is likely to make oxygen uptake more effective, but may also impose hidden costs of a proactive, aggressive lifestyle.

Physical gills in diving insects and spiders: theory and experiment

Insects and spiders rely on gas-filled airways for respiration in air. However, some diving species take a tiny air-store bubble from the surface that acts as a primary O(2) source and also as a physical gill to obtain dissolved O(2) from the water. After a long history of modelling, recent work with O(2)-sensitive optodes has tested the models and extended our understanding of physical gill function. Models predict that compressible gas gills can extend dives up to more than eightfold, but this is never reached, because the animals surface long before the bubble is exhausted. Incompressible gas gills are theoretically permanent. However, neither compressible nor incompressible gas gills can support even resting metabolic rate unless the animal is very small, has a low metabolic rate or ventilates the bubble's surface, because the volume of gas required to produce an adequate surface area is too large to permit diving. Diving-bell spiders appear to be the only large aquatic arthropods that can have gas gill surface areas large enough to supply resting metabolic demands in stagnant, oxygenated water, because they suspend a large bubble in a submerged web.

Balancing the competing requirements of air-breathing and display behaviour during male–male interactions in Siamese fighting fish Betta splendens

Air-breathing fish of the Anabantoidei group meet their metabolic requirements for oxygen through both aerial and aquatic gas exchange. Siamese fighting fish Betta splendens are anabantoids that frequently engage in aggressive male–male interactions which cause significant increases in metabolic rate and oxygen requirements. These interactions involve opercular flaring behaviour that is thought to limit aquatic oxygen uptake, and combines with the increase in metabolic rate to cause an increase in air-breathing behaviour. Air-breathing events interrupt display behaviour and increase risk of predation, raising the question of how Siamese fighting fish manage their oxygen requirements during agonistic encounters. Using open-flow respirometry, we measured rate of oxygen consumption in displaying fish to determine if males increase oxygen uptake per breath to minimise visits to the surface, or increase their reliance on aquatic oxygen uptake. We found that the increased oxygen requirements of Siamese fighting fish during display behaviour were met by increased oxygen uptake from the air with no significant changes in aquatic oxygen uptake. The increased aerial oxygen uptake was achieved almost entirely by an increase in air-breathing frequency. We conclude that limitations imposed by the reduced gill surface area of air-breathing fish restrict the ability of Siamese fighting fish to increase aquatic uptake, and limitations of the air-breathing organ of anabantoids largely restrict their capacity to increase oxygen uptake per breath. The resulting need to increase surfacing frequency during metabolically demanding agonistic encounters has presumably contributed to the evolution of the stereotyped surfacing behaviour seen during male–male interactions, during which one of the fish will lead the other to the surface, and each will take a breath of air.

Gill surface area and metabolic enzyme activities of demersal fishes associated with the oxygen minimum zone off California

Metabolic enzyme activities and gill surface areas were measured across 10 species of demersal fishes from Monterey Canyon, California, which features a prominent oxygen minimum zone (OMZ). Comparisons were made between species living both within and outside of the OMZ. Enzyme activities showed no significant trend toward aerobic suppression or heightened reliance on anaerobic metabolism in response to the OMZ. While flatfish species living both within and outside of the OMZ had similarly low enzyme activities, the OMZ‐dwelling Microstomus pacificus had 1.8–3 times larger gill surface area than comparably sized flatfishes from higher‐oxygen waters, suggesting a morphological adaptation to low oxygen. In scorpaeniform fishes, high aerobic metabolism was accompanied by large gill surface areas in two routine‐swimming OMZ‐dwelling species (Anoplopoma fimbria and Careproctus melanurus). Low aerobic activities and small gills were found in two Sebastolobus species, suggesting a low oxygen demand resulting from a more sedentary behavior compared to other Scorpaeniformes. In gadiform fishes, no differences were measured in enzyme activity levels, but larger gill surface areas were measured in OMZ‐dwelling Nezumia liolepis. These results indicate adaptation to low oxygen in a variety of ways that balance oxygen demand with supply, with no indication that these species rely on enhanced anaerobic metabolism. With both flatfishes and rattails, adaptation to OMZs is demonstrated through increased gill surface area.

Analysis of cutaneous and internal gill gas exchange morphology in early larval amphibians, Pseudophryne bibronii and Crinia georgiana

This study uses stereological techniques to examine body, internal gill and cardiovascular morphology of two larval amphibians, Pseudophryne bibronii and Crinia georgiana, to evaluate the roles of diffusive and convective gas exchange. Gosner stage 27 specimens were prepared for light microscopy and six parallel sections of equal distance taken through the body as well as a further six through the heart and internal gills. Body, internal gill and heart volume as well as body and internal gill surface areas were determined. The harmonic mean distance across the internal gills was also measured and used to estimate oxygen diffusive conductance, DO₂. The species were of similar body size and surface area, but the heart and internal gills were larger in P. bibronii, which may represent precursors for greater growth of the species beyond stage 27. The much larger surface area of the skin compared to the internal gills in both species suggests it is the main site for gas exchange, with the gills supplementing oxygen uptake. The sparse cutaneous capillary network suggests diffusion is the main oxygen transport mechanism across the skin and directly into deeper tissues. A numerical model that simplifies larval shape, and has an internal (axial vessels) and external oxygen source, confirms that diffusion is able to maintain tissue oxygen with limited convective input.

Differences in activity level between cownose rays (Rhinoptera bonasus) and Atlantic stingrays (Dasyatis sabina) are related to differences in heart mass, hemoglobin concentration, and gill surface area

Aquatic animals are faced with the challenge of extracting oxygen from water, a medium that is metabolically expensive to ventilate and that contains just a fraction of the oxygen concentration relative to air, yet the physiologies of fishes have evolved to support a wide range of activity levels in nature. Oxygen delivery components, including gill surface area (oxygen uptake), blood chemistry (oxygen transport), and the heart (system pump), have been positively correlated to activity level in teleost fishes, yet relatively little is known about how these components are related to activity in elasmobranches. The current study addresses this question by examining heart mass, hemoglobin concentration, hematocrit level, and gill surface area in wild-caught representatives of the benthic Atlantic stingray (Dasyatis sabina) and active cownose ray (Rhinoptera bonasus). Allometric scaling exponents are similar for all four measures between the study species. Heart mass, gill surfaces areas, and hemoglobin concentrations were 2.1 times, approximately 7.1 times, and 2.0 times higher, respectively, in active cownose rays, when compared to benthic Atlantic stingrays, after correcting for differences in body mass. When considered in the context of functional plasticity within the oxygen delivery systems of benthic and active species, data from the current study indicate that higher activity levels in cownose rays are supported by modifications that, at least in part, are likely to enhance oxygen uptake.

Mechanisms underlying parallel reductions in aerobic capacity in non-migratory threespine stickleback (Gasterosteus aculeatus) populations

Non-migratory, stream-resident populations of threespine stickleback, Gasterosteus aculeatus, have a lower maximum oxygen consumption ((O(2),max)) than ancestral migratory marine populations. Here, we examined laboratory-bred stream-resident and marine crosses from two locations (West and Bonsall Creeks) to determine which steps in the oxygen transport and utilization cascade evolved in conjunction with, and thus have the potential to contribute to, these differences in (O(2),max). We found that West Creek stream-resident fish have larger muscle fibres (not measured in Bonsall fish), Bonsall Creek stream-resident fish have smaller ventricles, and both stream-resident populations have evolved smaller pectoral adductor and abductor muscles. However, many steps of the oxygen cascade did not evolve in stream-resident populations (gill surface area, hematocrit, mean cellular hemoglobin content and the activities of mitochondrial enzymes per gram ventricle and pectoral muscle), arguing against symmorphosis. We also studied F1 hybrids to determine which traits in the oxygen cascade have a genetic architecture similar to that of (O(2),max). In West Creek, (O(2),max), abductor and adductor size all showed dominance of marine alleles, whereas in Bonsall Creek, (O(2),max) and ventricle mass showed dominance of stream-resident alleles. We also found genetically based differences among marine populations in hematocrit, ventricle mass, pectoral muscle mass and pectoral muscle pyruvate kinase activity. Overall, reductions in pectoral muscle mass evolved in conjunction with reductions in (O(2),max) in both stream-resident populations, but the specific steps in the oxygen cascade that have a genetic basis similar to that of (O(2),max), and are thus predicted to have the largest impact on (O(2),max), differ among populations.

Gill remodelling during terrestrial acclimation reduces aquatic respiratory function of the amphibious fishKryptolebias marmoratus

The skin-breathing amphibious fish Kryptolebias marmoratus experiences rapid environmental changes when moving between water- and air-breathing, but remodelling of respiratory morphology is slower (~1 week). We tested the hypotheses that (1) there is a trade-off in respiratory function of gills displaying aquatic versus terrestrial morphologies and (2) rapidly increased gill ventilation is a mechanism to compensate for reduced aquatic respiratory function. Gill surface area, which varied inversely to the height of the interlamellar cell mass, was increased by acclimating fish for 1 week to air or low ion water, or decreased by acclimating fish for 1 week to hypoxia (~20% dissolved oxygen saturation). Fish were subsequently challenged with acute hypoxia, and gill ventilation or oxygen uptake was measured. Fish with reduced gill surface area increased ventilation at higher dissolved oxygen levels, showed an increased critical partial pressure of oxygen and suffered impaired recovery compared with brackish water control fish. These results indicate that hyperventilation, a rapid compensatory mechanism, was only able to maintain oxygen uptake during moderate hypoxia in fish that had remodelled their gills for land. Thus, fish moving between aquatic and terrestrial habitats may benefit from cutaneously breathing oxygen-rich air, but upon return to water must compensate for a less efficient branchial morphology (mild hypoxia) or suffer impaired respiratory function (severe hypoxia).

Oxygen utilization and the branchial pressure gradient during ram ventilation of the shortfin mako,Isurus oxyrinchus: is lamnid shark–tuna convergence constrained by elasmobranch gill morphology?

Ram ventilation and gill function in a lamnid shark, the shortfin mako, Isurus oxyrinchus, were studied to assess how gill structure may affect the lamnid-tuna convergence for high-performance swimming. Despite differences in mako and tuna gill morphology, mouth gape and basal swimming speeds, measurements of mako O(2) utilization at the gills (53.4±4.2%) and the pressure gradient driving branchial flow (96.8±26.1 Pa at a mean swimming speed of 38.8±5.8 cm s(-1)) are similar to values reported for tunas. Also comparable to tunas are estimates of the velocity (0.22±0.03 cm s(-1)) and residence time (0.79±0.14 s) of water though the interlamellar channels of the mako gill. However, mako and tuna gills differ in the sites of primary branchial resistance. In the mako, approximately 80% of the total branchial resistance resides in the septal channels, structures inherent to the elasmobranch gill that are not present in tunas. The added resistance at this location is compensated by a correspondingly lower resistance at the gill lamellae accomplished through wider interlamellar channels. Although greater interlamellar spacing minimizes branchial resistance, it also limits lamellar number and results in a lower total gill surface area for the mako relative to tunas. The morphology of the elasmobranch gill thus appears to constrain gill area and, consequently, limit mako aerobic performance to less than that of tunas.