Response of heart rate and cloacal ventilation in the bimodally respiring freshwater turtle, Rheodytes leukops to experimental changes in aquatic PO2

Changes in heart rate (f(H)) and cloacal ventilation frequency (f(C)) were investigated in the Fitzroy turtle, Rheodytes leukops, under normoxic (17.85 kPa) and hypoxic (3.79 kPa) conditions at 25 degrees C. Given R. leukops' high reliance on aquatic respiration via the cloacal bursae, the objective Of this Study was to examine the effect of varying aquatic PO2 levels upon the expression of a bradycardia in a freely diving, bimodally respiring turtle. In normoxia, mean diving f(H) and f(C) for R. leukops remained constant with increasing submergence length, indicating that a bradycardia failed to develop during extended dives of up to 3 days. Alternatively, exposure to aquatic hypoxia resulted in the expression of a bradycardia as recorded by a decreasing mean diving f(H) with increasing dive duration. The observed bradycardia is attributed to a hypoxic-induced metabolic depression, possibly facilitated by a concurrent decrease in f(C). Results suggest that R. leukops alters its strategy from aquatic O-2 extraction via cloacal respiration in normoxia to O-2 conservation when exposed to aquatic hypoxia for the purpose of extending dive duration. Upon surfacing, a significant tachycardia was observed for R. leukops regardless of aquatic PO2, presumably functioning to rapidly equilibrate blood and tissue gas tensions with alveolar gas to reduce surfacing duration.

Blood-respiratory and acid-base changes during extended diving in the bimodally respiring freshwater turtle Rheodytes leukops

Changes in blood-gas, acid-base, and plasma-ion status were investigated in the bimodally respiring turtle, Rheodytes leukops, during prolonged dives of up to 12 h. Given that R. leukops routinely submerges for several hours, the objective of this study was to determine whether voluntarily diving turtles remain aerobic and simultaneously avoid hypercapnic conditions over increasing dive lengths. Blood PO2, PCO2, and pH, as well as plasma concentrations of lactate, glucose, Na+, K+, Cl-, total Ca, and total Mg were determined in venous blood collected from the occipital sinus. Blood PO2 declined significantly with dive length; however, oxy-haemoglobin saturation remained greater than 30% for all R. leukops sampled. No changes were observed in blood PCO2, pH, [HCO3-], or plasma glucose, with increasing dive length. Despite repeated dives lasting more than 2 h, plasma lactate remained less than 3 mmol l(-1) for all R. leukops sampled, indicating the absence of anaerobiosis. Compensatory acid-base adjustments associated with anaerobiosis (e.g. declining [Cl-], increasing total [Ca] and [Mg]) were likewise absent, with plasma-ion concentrations remaining stable with increasing dive length. Results indicate that R. leukops utilises aquatic respiration to remain aerobic during prolonged dives, thus effectively avoiding the development of a metabolic and respiratory acidosis.

Effect of water depth and water velocity upon the surfacing frequency of the bimodally respiring freshwater turtle, Rheodytes leukops

This study examines the effect of increasing water depth and water velocity upon the surfacing behaviour of the bimodally respiring turtle, Rheodytes leukops. Surfacing frequency was recorded for R. leukops at varying water depths (50, 100, 150 cm) and water velocities (5, 15, 30 cm s(-1)) during independent trials to provide an indirect cost-benefit analysis of aquatic versus pulmonary respiration. With increasing water velocity, R. leukops decreased its surfacing frequency twentyfold, thus suggesting a heightened reliance upon aquatic gas exchange. An elevated reliance upon aquatic respiration, which presumably translates into a decreased air-breathing frequency, may be metabolically more efficient for R. leukops compared to the expenditure (i.e. time and energy) associated with air-breathing within fast-flowing riffle zones. Additionally, R. leukops at higher water velocities preferentially selected low-velocity microhabitats, presumably to avoid the metabolic expenditure associated with high water flow. Alternatively, increasing water depth had no effect upon the surfacing frequency of R. leukops, suggesting little to no change in the respiratory partitioning of the species across treatment settings. Routinely long dives (>90 min) recorded for R. leukops indicate a high reliance upon aquatic O-2 uptake regardless of water depth. Moreover, metabolic and temporal costs attributed to pulmonary gas exchange within a pool-like environment were likely minimal for R. leukops, irrespective of water depth.

The influence of body size on the diving behaviour and physiology of the bimodally respiring turtle, Elseya albagula

In aquatic vertebrates that acquire oxygen aerially dive duration scales positively with body mass, i.e. larger animals can dive for longer periods, however in bimodally respiring animals the relationship between dive duration and body mass is unclear. In this study we investigated the relationships between body size, aquatic respiration, and dive duration in the bimodally respiring turtle, Elseya albagula. Under normoxic conditions, dive duration was found to be independent of body mass. The dive durations of smaller turtles were equivalent to that of larger individuals despite their relatively smaller oxygen stores and higher mass specific metabolic rates. Smaller turtles were able to increase their dive duration through the use of aquatic respiration. Smaller turtles had a relatively higher cloacal bursae surface area than larger turtles, which allowed them to extract a relatively larger amount of oxygen from the water. By removing the ability to respire aquatically (hypoxic conditions), the dive duration of the smaller turtles significantly decreased restoring the normal positive relationship between body size and dive duration that is seen in other air-breathing vertebrates.

The role of branchial and orobranchial O-2 chemoreceptors in the control of aquatic surface respiration in the neotropical fish tambaqui (Colossoma macropomum): progressive responses to prolonged hypoxia

The present study examined the role of branchial and orobranchial O-2 chemoreceptors in the cardiorespiratory responses, aquatic surface respiration (ASR), and the development of inferior lip swelling in tambaqui during prolonged (6 h) exposure to hypoxia. Intact fish (control) and three groups of denervated fish (bilateral denervation of cranial nerves IX+X (to the gills), of cranial nerves V+VII (to the orobranchial cavity) or of cranial nerves V alone), were exposed to severe hypoxia (Pw(O2) = 10 mmHg) for 360 min. Respiratory frequency (fR) and heart rate (fH) were recorded simultaneously with ASR. Intact (control) fish increased fR, ventilation amplitude (V-AMP) and developed hypoxic bradycardia in the first 60 min of hypoxia. The bradycardia, however, abated progressively and had returned to normoxic levels by the last hour of exposure to hypoxia. The changes in respiratory frequency and the hypoxic bradycardia were eliminated by denervation of cranial nerves IX and X but were not affected by denervation of cranial nerves V or V+VII. The VAMP was not abolished by the various denervation protocols. The fH in fish with denervation of cranial nerves V or V+VII, however, did not recover to control values as in intact fish. After 360 min of exposure to hypoxia only the intact and IX+X denervated fish performed ASR. Denervation of cranial nerve V abolished the ASR behavior. However, all (control and denervated (IX+X, V and V+VII) fish developed inferior lip swelling. These results indicate that ASR is triggered by O-2 chemoreceptors innervated by cranial nerve V but that other mechanisms, such as a direct effect of hypoxia on the lip tissue, trigger lip swelling.

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 (Po-2 = 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.

Light history-dependent respiration explains the hysteresis in the daily ecosystem metabolism of seagrass

Oxygen flux between aquatic ecosystems and the water column is a measure of ecosystem metabolism. However, the oxygen flux varies during the day in a “hysteretic” pattern: there is higher net oxygen production at a given irradiance in the morning than in the afternoon. In this study, we investigated the mechanism responsible for the hysteresis in oxygen flux by measuring the daily pattern of oxygen flux, light, and temperature in a seagrass ecosystem (Zostera muelleri in Swansea Shoals, Australia) at three depths. We hypothesised that the oxygen flux pattern could be due to diel variations in either gross primary production or respiration in response to light history or temperature. Hysteresis in oxygen flux was clearly observed at all three depths. We compared this data to mathematical models, and found that the modification of ecosystem respiration by light history is the best explanation for the hysteresis in oxygen flux. Light history-dependent respiration might be due to diel variations in seagrass respiration or the dependence of bacterial production on dissolved organic carbon exudates. Our results indicate that the daily variation in respiration rate may be as important as the daily changes of photosynthetic characteristics in determining the metabolic status of aquatic ecosystems.

Control of respiration in fish, amphibians and reptiles

Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)

The breathing pattern and the ventilatory response to aquatic and aerial hypoxia and hypercarbia in the frog Pipa carvalhoi

Anuran amphibians are known to exhibit an intermittent pattern of pulmonary ventilation and to exhibit an increased ventilatory response to hypoxia and hypercarbia. However, only a few species have been studied to date. The aquatic frog Pipa carvalhoi inhabits lakes, ponds and marshes that are rich in nutrients but low in O-2. There are no studies of the respiratory pattern of this species and its ventilation during hypoxia or hypercarbia. Accordingly, the aim of the present study was to characterize the breathing pattern and the ventilatory response to aquatic and aerial hypoxia and hypercarbia in this species. With this purpose, pulmonary ventilation (V-1) was directly measured by the pneumotachograph method during normocapnic normoxia to determine the basal respiratory pattern and during aerial and aquatic hypercarbia (5% CO2) and hypoxia (5% O-2). Our data demonstrate that P. carvalhoi exhibits a periodic breathing pattern composed of single events (single breaths) of pulmonary ventilation separated by periods of apnea. The animals had an enhanced V-1 during aerial hypoxia, but not during aquatic hypoxia. This increase was strictly the result of an increase in the breathing frequency. A pronounced increase in V-1 was observed if the animals were simultaneously exposed to aerial and aquatic hypercarbia, whereas small or no ventilatory responses were observed during separately administered aerial or aquatic hypercarbia. P. carvalhoi primarily inhabits an aquatic environment. Nevertheless, it does not respond to low O-2 levels in water, although it does so in air. The observed ventilatory responses to hypercarbia may indicate that this species is similar to other anurans in possessing central chemoreceptors. (C) 2012 Elsevier Inc. All rights reserved.

Tidal and spatial variations of DI13C and aquatic chemistry in a temperate tidal basin during winter time

Here, the pelagic carbonate system and the ?13C signature of dissolved inorganic carbonate (DIC) were investigated in a tidal basin of the southern North Sea, the Jade Bay, with respect to tidal cycles and a transect towards the North Sea in winter time (January and November, 2010). Physical parameters, major and trace elements, and nutrient concentrations were considered, too. Primary production and pelagic organic matter respiration were negligible during winter time. Both, the compositional variations on the transects as well as during the tidal cycles indicate the mixing of North Sea with fresh water. The combined spatial co-variations of different parameters indicate an introduction of fresh water that was enriched in DI12C, metabolites (e.g., ammonia), protons, and dissolved redox-sensitive elements (e.g., Mn2+). During the January campaign, the discharge via the flood gates was limited due to ice cover of the hinterland drainage ditches, allowing for an observation of tidal variations without significant mixing contributions from surface water discharges. Considering a binary mixing model with North Sea and fresh water as end-members, the extrapolated fresh water end-member composition for this campaign is estimated to contain about 3.8 mmol/kg DIC , and enhanced concentrations of NH4+, Mn2+, and protons compared to North Sea water. The fast temporal response of dissolved geochemical tracers on tidal variations in the Jade Bay indicates a continuous supply of a fresh water component. The measured composition of fresh waters entering the Jade Bay via flood gates (end of October, 2010) did not match the values estimated by the binary mixing model. Therefore, the overall fresh water component likely is a mixture between sources originating from flood gates and (in January) dominating submarine groundwater discharge entering the Jade Bay. This model is consistent with the results obtained during the November campaign, when a more important contribution from flood gates is expected and a more variable fresh water end-member is estimated. The co-variations of the concentrations and the stable carbon isotope composition of DIC are applied to evaluate possible superimposed sink-source-transformation processes in the coastal waters and a general co-variation scheme is suggested.