Partitioning of respiration between the gills and air-breathing organ in response to aquatic hypoxia and exercise in the pacific tarpon, Megalops cyprinoides

The evolution of air-breathing organs (ABOs) is associated not only with hypoxic environments but also with activity. This investigation examines the effects of hypoxia and exercise on the partitioning of aquatic and aerial oxygen uptake in the Pacific tarpon. The two-species cosmopolitan genus Megalops is unique among teleosts in using swim bladder ABOs in the pelagic marine environment. Small fish (58-620 g) were swum at two sustainable speeds in a circulating flume respirometer in which dissolved oxygen was controlled. For fish swimming at 0.11 m s(-1) in normoxia (Po2 = 21 kPa), there was practically no air breathing, and gill oxygen uptake was 1.53 mL kg(-0.67) min(-1). Air breathing occurred at 0.5 breaths min(-1) in hypoxia (8 kPa) at this speed, when the gills and ABOs accounted for 0.71 and 0.57 mL kg(-0.67) min(-1), respectively. At 0.22 m s(-1) in normoxia, breathing occurred at 0.1 breaths min(-1), and gill and ABO oxygen uptake were 2.08 and 0.08 mL kg(-0.67) min(-1), respectively. In hypoxia and 0.22 m s(-1), breathing increased to 0.6 breaths min(-1), and gill and ABO oxygen uptake were 1.39 and 1.28 mL kg(-0.67) min(-1), respectively. Aquatic hypoxia was therefore the primary stimulus for air breathing under the limited conditions of this study, but exercise augmented oxygen uptake by the ABOs, particularly in hypoxic water.     

Continuous measurement of oxygen tensions in the air-breathing organ of Pacific tarpon (Megalops cyprinoides) in relation to aquatic hypoxia and exercise

The Pacific tarpon is an elopomorph teleost fish with an air-breathing organ (ABO) derived from a physostomous gas bladder. Oxygen partial pressure (PO₂) in the ABO was measured on juveniles (238 g) with fiber-optic sensors during exposure to selected aquatic PO₂ and swimming speeds. At slow speed (0.65 BL s⁻¹), progressive aquatic hypoxia triggered the first breath at a mean PO₂ of 8.3 kPa. Below this, opercular movements declined sharply and visibly ceased in most fish below 6 kPa. At aquatic PO₂ of 6.1 kPa and swimming slowly, mean air-breathing frequency was 0.73 min⁻¹, ABO PO₂ was 10.9 kPa, breath volume was 23.8 ml kg⁻¹, rate of oxygen uptake from the ABO was 1.19 ml kg⁻¹ min⁻¹, and oxygen uptake per breath was 2.32 ml kg⁻¹. At the fastest experimental speed (2.4 BL s⁻¹) at 6.1 kPa, ABO oxygen uptake increased to about 1.90 ml kg⁻¹ min⁻¹, through a variable combination of breathing frequency and oxygen uptake per breath. In normoxic water, tarpon rarely breathed air and apparently closed down ABO perfusion, indicated by a drop in ABO oxygen uptake rate to about 1% of that in hypoxic water. This occurred at a wide range of ABO PO₂ (1.7–26.4 kPa), suggesting that oxygen level in the ABO was not regulated by intrinsic receptors.     

Growth during the early life history of the Pacific tarpon,Megalops cyprinoides

The early growth of the Pacific tarpon,Megalops cyprinoides, was studied by larval otolith analysis and rearing of larvae and juveniles in the laboratory. Morphology of the sagitta, validation of sagittal daily increments, age at the start of metamorphosis, decrement of standard length in early metamorphosis, and growth under rearing conditions are described. The sagitta of fully-grown Pacific tarpon leptocephali were transparent and circular, with regular intervals between the neighboring rings becoming wider at the onset of metamorphosis. Alizarin complexone treatment of larvae confirmed the daily formation of the sagittal rings. Metamorphosis was estimated to start about one month after hatching. After drastic shrinkage during the first several days of metamorphosis, the body length more or less stabilized for one month and then resumed rapid growth. The early growth of Pacific tarpon was divided into four phases as follows: A) leptocephalus positive growth phase; B) leptocephalus negative growth phase; C) sluggish growth phase; and D) juvenile growth phase.     

Oxygen uptake capacity of gills and skin in relation to body weight of the air-breathing siluroid fish, Clarias batrachus (Linn.).

Oxygen consumption through gills and skin in relation to body weight was estimated in the air-breathing catfish, Clarias batrachus, under two experimental conditions, viz., (i) when access to air was allowed and (ii) when air-breathing was prevented. There was a positive correlation between VO2 (ml/hr) and body weight in both experimental conditions. Oxygen consumption (ml/hr) increased by a power of 0.869 when access to air was allowed whereas the power was slightly less (b = 0.841) when air-breathing was prevented. As the values for exponent (b) were less than 1.0, the weight specific VO2 (ml/kg/hr) decreased with increasing body weight. The decrease was more marked (b = - 0.180) in fishes which were not allowed air than in those where access to air was allowed (b = - 0.148). Under normal conditions of water and air-breathing the rate of VO2 (ml/kg/hr) via gills and skin from water ranged from 39.7 +/- 3.21 to 76.7 +/- 9.01 and this increased to 42.17 +/- 6.2 to 105.9 +/- 8.33 when air-breathing was prevented. The increase in the rate of VO2 was perhaps associated with the increase in the volume of water irrigating the gills per unit time.     

Toxicity of mercury: A comparative study in air-breathing and non air-breathing fish

Annual primary production was estimated from two years data. The results indicate a high primary productivity and a short turn over time for nitrogen.

     

A bioenergetics model for an air-breathing fish, Channa striatus

Food consumption, standard metabolism, and growth of juvenile snakehead, Channa striatus, a cannibalistic and air-breathing fish were measured at 24–26 °C under controlled laboratory condition. Snakehead weighing 3.2–29.5 g were evaluated, and were fed smaller snakehead. Based on our observations, we determined bioenergetics relationships between specific food consumption, metabolic rates, and body weight. These values, along with other published parameter values allowed us to construct a bioenergetics model for snakehead. We then verified our model with growth and food consumption measurements from an independent feeding trial. Predicted fish growth closely matched observed growth. Our model underestimated cumulative food consumption when a constant activity value was used, but consumption estimates improved when we used non-constant activity values (1-5 times of standard metabolism). Predicted fish maintenance ration was 1.7% of body weight per day. Food conversion efficiency was greatest (0.59) when fed 2% body weight daily, but declined when daily consumption exceeded 6% body weight. This model provides a useful approach for assessing food requirements of snakehead under controlled condition. This revised version was published online in July 2006 with corrections to the Cover Date.     

Air breathing minimizes post-exercise lactate load in the tropical Pacific tarpon, Megalops cyprinoides Broussonet 1782 but oxygen debt is repaid by aquatic breathing

Swimming in a flume at reduced water pO₂ resulted in muscle and blood lactate levels in Pacific tarpon Megalops cyprinoides that were significantly higher when fish did not have access to air. Blood glucose and haematological variables were unchanged throughout the regimes of exercise at two swimming speeds and hypoxia. Strenuous exercise with bouts of burst swimming, however, resulted in both high blood lactate and glucose, and perturbed haematological status with elevated haemoglobin and reduced mean cell-haemoglobin concentration. Post-exercise recovery was achieved through aquatic breathing rather than by air breathing. The air-breathing organ in Pacific tarpon therefore prolonged aerobic activity, but gill breathing was used to repay oxygen debt.     

Oxygen transport during steady-state submaximal exercise in chronic hypoxia

Arterial O2 delivery during short-term submaximal exercise falls on arrival at high altitude but thereafter remains constant. As arterial O2 content increases with acclimatization, blood flow falls. We evaluated several factors that could influence O2 delivery during more prolonged submaximal exercise after acclimatization at 4,300 m. Seven men (23 +/- 2 yr) performed 45 min of steady-state submaximal exercise at sea level (barometric pressure 751 Torr), on acute ascent to 4,300 m (barometric pressure 463 Torr), and after 21 days of residence at altitude. The O2 uptake (VO2) was constant during exercise, 51 +/- 1% of maximal VO2 at sea level, and 65 +/- 2% VO2 at 4,300 m. After acclimatization, exercise cardiac output decreased 25 +/- 3% compared with arrival and leg blood flow decreased 18 +/- 3% (P less than 0.05), with no change in the percentage of cardiac output to the leg. Hemoglobin concentration and arterial O2 saturation increased, but total body and leg O2 delivery remained unchanged. After acclimatization, a reduction in plasma volume was offset by an increase in erythrocyte volume, and total blood volume did not change. Mean systemic arterial pressure, systemic vascular resistance, and leg vascular resistance were all greater after acclimatization (P less than 0.05). Mean plasma norepinephrine levels also increased during exercise in a parallel fashion with increased vascular resistance. Thus we conclude that both total body and leg O2 delivery decrease after arrival at 4,300 m and remain unchanged with acclimatization as a result of a parallel fall in both cardiac output and leg blood flow and an increase in arterial O2 content.(ABSTRACT TRUNCATED AT 250 WORDS)     

The source of lamellar mitochondria-rich cells in the air-breathing fish, Trichogaster leeri

Pavement cells and the mitochondria-rich cells (MRCs) are two of the main types of cells in fish gill epithelia. The pavement cells are generally responsible for gas exchange and MRCs for ion regulation. MRCs are found especially in the trailing edge and the interlamellar region of gill filament. In some species, MRCs are also observed in the gill lamellae. A previous study reported the likelihood of having lamellar MRCs in air-breathing fishes. Nevertheless, the source of lamellar MRCs is unclear. We used the air-breathing fish, Trichogaster leeri, to investigate the source of proliferated cells on the lamellae when 5-bromo-2-deoxyuridine (BrdU) was injected at different times before fish were sampled from deionized water. There were two major findings in this study. First, undifferentiated cells were found in the lamellae, as well as in the filaments. And, within 12-24 hr, a proliferated cell, identified as BrdU cell, could differentiate to an MRC in the gill lamellae. Second, the filaments and the lamellae in T. leeri responded to ionic stress differently but the proportion of the proliferated MRCs to the BrdU cells remained constant. Our results suggested that the lamellar MRCs were mainly differentiated from the cells that proliferated earlier from the lamellae.     

Bimodal oxygen uptake in a freshwater air-breathing fish,Notopterus chitala

Measurements of bimodal oxygen uptake have been made in a freshwater air-breathing fish,Notopterus chitala at 29.0±1(S.D.)°C. xhe mean oxygen uptake from continuously flowing water without any access to air, was found to be 3.58±0.37 (S.E.) ml O₂ · h^?1 and 56.84+4.29 (S.E.) ml O₂ · kg^?1 · h^?1 for a fish weighing 66.92 + 11.27 (S.E.) g body weight. In still water with access to air, the mean oxygen uptake through the gills were recorded to be 2.49 ± 0.31 (S.E.) ml O₂ · h^?1 and 38.78 ± 1.92 (S.E.) ml O₂ · kg^?1 · h^?1 and through the accessory respiratory organs (swim-bladder) 6.04±0.87 (S.E.) ml O₂ · h^?1 and 92.32±2.91 (S.E.) ml O₂ · kg^?1 · h^?1 for a fish averaging 66.92±11.27 (S.E.) g. Out of the total oxygen uptake (131.10 ml O₂ · kg^?1 · h^?1), about 70% was obtained through the aerial route and the remainder 30% through the gills.     

Oxygen uptake through gills and skin in relation to body weight of an air-breathing siluroid fish, Saccobranchus (=Heteropneustes) fossilis

Oxygen uptake through gills and skin has been measured in juvenile and adult Saccobranchus fossilis and its relationship represented by the equation Vo₂= aW^b. When air-breathing is allowed the O₂ uptake via the gills and skin together increases by powers of 1 -084, 0–986 and 1–328 in juvenile, adult and juvenile+adult respectively. When air-breathing is prevented the slope (b) for O₂ uptake via the gills appear to be less in juveniles (0–765) than in adults (0–784) and juveniles+adults together (0–814). Under the same experimental condition, the slope for O₂ uptake via the gills+skin is also less in juveniles (0–478) than in adults (0–799) and juveniles+adults (0–755). Further decrease in the exponent value is found for the oxygen uptake of skin in relation to body weight under surfacing-prevented conditions ( b = 0–542). Different exponent values for juvenile and adult fishes may be due to their different growth pattern and physiology.     

Oxygen transport during exercise in large mammals. II. Oxygen uptake by the pulmonary gas exchanger

Because the maximal rate of O2 consumption (VO2max) of the horse is 2.6 times larger than that of steers of equal size, we wondered whether their pulmonary gas exchanger is proportionately larger. Three Standardbred racehorses [body mass (Mb) = 447 kg] and three domestic steers (Mb = 474 kg) whose cardiovascular function at VO2max had been thoroughly studied (Jones et al. J. Appl. Physiol. 67: 862-870, 1989) were used to study their lungs by morphometry. The basic morphometric parameters were similar in both species. The nearly 2 times larger lung volumes of the horses caused the gas exchange surfaces and capillary blood volume to be 1.6 to 1.8 times larger. Morphometric pulmonary diffusing capacity was 2 times larger in the horse than in the steer; the 2.6-fold greater rate of O2 uptake thus required the alveolar-capillary PO2 difference to be 1.3 times larger in the horse than in the steer. Combining physiological and morphometric data, we calculated capillary transit time at VO2max to be 0.4-0.5 s. Bohr integration showed capillary blood to be equilibrated with alveolar air after 75 and 58% of transit time in horses and steers, respectively; horses maintain a smaller degree of redundancy in their pulmonary gas exchanger.     

Seasonal variations in the blood constituents of an air-breathing fish, Channa punctatus Bloch

A year long study based on monthly observations on the haematology of female Channa punctatus with respect to haemoglobin, haematocrit values, total erythrocyte and leucocyte numbers together with a differential enumeration of various leucocytes viz. thrombocytes small and large lymphocytes, monocytes, neutrophils, eosinophils and basophils is recorded. The study showed that the total erythrocytic number, haemoglobin and haematocrit values decrease during the breeding time i.e. July to September. The thrombocyte number significantly increased while the neutrophilic number showed a decrease. The physiological significance of these changes is discussed with reference to the available literature.     

Retinopetal neuronal system in the brain of an air-breathing teleost fish,Channa punctata

Summary Retinopetal neurons were visualised in the telencephalon and diencephalon of an air-breathing teleost fish, Channa punctata, following administration of cobaltous lysine to the optic nerve. The labelled perikarya (n=45–50) were always located on the side contralateral to the optic nerve that had received the neuronal tracer. The rostral-most back-filled cell bodies were located in the nucleus olfactoretinalis at the junction between the olfactory bulb and the telencephalon. In the area ventralis telencephali, two groups of telencephaloretinopetal neurons were identified near the ventral margin of the telencephalon. The rostral hypothalamus exhibited retrogradely labelled cells in three discrete areas of the lateral preoptic area, which was bordered medially by the nucleus praeopticus periventricularis and nucleus praeopticus, and laterally by the lateral forebrain bundle. In addition to a dorsal and a ventral group, a third population of neurons was located ventral to the lateral forebrain bundle adjacent to the optic tract. The dorsal group of neurons exhibited extensive collaterals; a few extended laterally towards the lateral forebrain bundle, whereas others ran into the dorsocentral area of the area dorsalis telencephali. A few processes extended via the anterior commissure into the telencephalon ipsilateral to the optic nerve that had been exposed to cobaltous lysine. However, the ventral cell group did not possess collaterals. In the diencephalon, retinopetal cells were visualised in the nucleus opticus dorsolateralis located in the pretectal area; these were the largest retinopetal perikarya of the brain. The caudal-most nucleus that possessed labelled somata was the retinothalamic nucleus; it contained the largest number of retinopetal cells. The limited number of widely distributed neurons in the forebrain, some with extensive collaterals, might participate in functional integration of different brain areas involved in feeding, which in this species is influenced largely by taste, not solely by vision.