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1.
Article in English | MEDLINE | ID: mdl-36049728

ABSTRACT

High CO2 (hypercapnia) can impose significant physiological challenges associated with acid-base regulation in fishes, impairing whole animal performance and survival. Unlike other environmental conditions such as temperature and O2, the acute CO2 tolerance thresholds of fishes are not understood. While some fish species are highly tolerant, the extent of acute CO2 tolerance and the associated physiological and ecological traits remain largely unknown. To investigate this, we used a recently developed ramping assay, termed the Carbon Dioxide maximum (CDmax), that increases CO2 exposure until loss of equilibrium (LOE) is observed. We investigated if there was a relationship between CO2 tolerance and the Root effect, ß-adrenergic sodium proton exchanger (ßNHE), air-breathing, and fish habitat in 17 species. We hypothesized that CO2 tolerance would be higher in fishes that lack both a Root effect and ßNHE, breathe air, and reside in tropical habitats. Our results showed that CDmax ranged from 2.7 to 26.7 kPa, while LOE was never reached in four species at the maximum PCO2 we could measure (26.7 kPa); CO2 tolerance was only associated with air-breathing, but not the presence of a Root effect or a red blood cell (RBC) ßNHE, or fish habitat. This study demonstrates that the diverse group of fishes investigated here are incredibly tolerant of CO2 and that although this tolerance is associated with air-breathing, further investigations are required to understand the basis for CO2 tolerance.


Subject(s)
Carbon Dioxide , Protons , Adrenergic Agents , Animals , Ecosystem , Erythrocytes/physiology , Fishes/physiology , Sodium
2.
J Exp Biol ; 223(Pt 7)2020 04 01.
Article in English | MEDLINE | ID: mdl-32127382

ABSTRACT

Acute (<96 h) exposure to elevated environmental CO2 (hypercarbia) induces a pH disturbance in fishes that is often compensated by concurrent recovery of intracellular and extracellular pH (pHi and pHe, respectively; coupled pH regulation). However, coupled pH regulation may be limited at CO2 partial pressure (PCO2 ) tensions far below levels that some fishes naturally encounter. Previously, four hypercarbia-tolerant fishes had been shown to completely and rapidly regulate heart, brain, liver and white muscle pHi during acute exposure to >4 kPa PCO2  (preferential pHi regulation) before pHe compensation was observed. Here, we test the hypothesis that preferential pHi regulation is a widespread strategy of acid-base regulation among fish by measuring pHi regulation in 10 different fish species that are broadly phylogenetically separated, spanning six orders, eight families and 10 genera. Contrary to previous views, we show that preferential pHi regulation is the most common strategy for acid-base regulation within these fishes during exposure to severe acute hypercarbia and that this strategy is associated with increased hypercarbia tolerance. This suggests that preferential pHi regulation may confer tolerance to the respiratory acidosis associated with hypercarbia, and we propose that it is an exaptation that facilitated key evolutionary transitions in vertebrate evolution, such as the evolution of air breathing.


Subject(s)
Acidosis, Respiratory , Carbon Dioxide , Acid-Base Equilibrium , Animals , Fishes , Humans , Hydrogen-Ion Concentration
3.
Proc Biol Sci ; 286(1903): 20190339, 2019 05 29.
Article in English | MEDLINE | ID: mdl-31138074

ABSTRACT

A successful spawning migration in salmon depends on their athletic ability, and thus on efficient cardiovascular oxygen (O2) transport. Most teleost fishes have highly pH-sensitive haemoglobins (Hb) that can release large amounts of O2 when the blood is acidified at the tissues. We hypothesized that plasma-accessible carbonic anhydrase (paCA; the enzyme that catalyses proton production from CO2) is required to acidify the blood at the tissues and promote tissue O2 extraction. Previous studies have reported an elevated tissue O2 extraction in hypoxia-acclimated teleosts that may also be facilitated by paCA. Thus, to create experimental contrasts in tissue O2 extraction, Atlantic salmon were acclimated to normoxia or hypoxia (40% air saturation for more than six weeks), and the role of paCA in enhancing tissue O2 extraction was tested by inhibiting paCA at rest and during submaximal exercise. Our results show that: (i) in both acclimation groups, the inhibition of paCA increased cardiac output by one-third, indicating a role of paCA in promoting tissue O2 extraction during exercise, recovery and at rest; (ii) the recruitment of paCA was plastic and increased following hypoxic acclimation; and (iii) maximal exercise performance in salmon, and thus a successful spawning migration, may not be possible without paCA.


Subject(s)
Carbonic Anhydrases/metabolism , Oxygen Consumption , Oxygen/blood , Salmo salar/metabolism , Acclimatization , Anaerobiosis , Animals , Biological Transport
4.
J Fish Biol ; 92(6): 1731-1746, 2018 Jun.
Article in English | MEDLINE | ID: mdl-29691861

ABSTRACT

The effect of substratum on growth and metabolic rate was assessed in larval white sturgeon Acipenser transmontanus. Yolk-sac larvae (YSL) were reared in bare tanks or tanks with gravel as substratum from hatch until approximately 16 days post hatch (dph). The effect of an artificial substratum was also evaluated on growth alone. Substratum had a significant effect on mass, with larvae reared in gravel and artificial substrata being larger than those reared without substratum. Routine metabolic rates were significantly lower and relative aerobic scope (the difference between maximum and routine metabolic rate) was significantly higher for YSL and feeding larvae (FL) reared in gravel relative to those reared in bare tanks, particularly before fish started feeding exogenously. Furthermore, gravel-reared larvae had higher whole-body glycogen concentrations relative to bare-tank-reared larvae. Routine factorial scope (maximum metabolic rate divided by routine metabolic rate) was relatively low in all treatments (< 1·7) indicating a limited ability to elevate metabolic rate above routine early in development and mass exponents for metabolic rate exceeded 1. Taken together, these data indicate that YSL reared without substratum may divert more of their energy to non-growth related processes impairing growth. This finding underscores the importance of adequate rearing substratum for growth of A. transmontanus and may provide support for habitat restoration and alternative hatchery rearing methods associated with sturgeon conservation.


Subject(s)
Aquaculture/instrumentation , Fishes/growth & development , Animals , Fishes/metabolism , Glycogen/metabolism , Larva/growth & development , Larva/metabolism , Oxygen Consumption
5.
Sci Rep ; 7(1): 16238, 2017 11 24.
Article in English | MEDLINE | ID: mdl-29176558

ABSTRACT

Mitochondrial function has been suggested to underlie constraints on whole-organism aerobic performance and associated hypoxia and thermal tolerance limits, but most studies have focused on measures of maximum mitochondrial capacity. Here we investigated whether variation in mitochondrial oxygen kinetics could contribute to local adaptation and plasticity in response to temperature using two subspecies of the Atlantic killifish (Fundulus heteroclitus) acclimated to a range of temperatures (5, 15, and 33 °C). The southern subspecies of F. heteroclitus, which has superior thermal and hypoxia tolerances compared to the northern subspecies, exhibited lower mitochondrial O2 P50 (higher O2 affinity). Acclimation to thermal extremes (5 or 33 °C) altered mitochondrial O2 P50 in both subspecies consistent with the effects of thermal acclimation on whole-organism thermal tolerance limits. We also examined differences between subspecies and thermal acclimation effects on whole-blood Hb O2-P50 to assess whether variation in oxygen delivery is involved in these responses. In contrast to the clear differences between subspecies in mitochondrial O2-P50 there were no differences in whole-blood Hb-O2 P50 between subspecies. Taken together these findings support a general role for mitochondrial oxygen kinetics in differentiating whole-organism aerobic performance and thus in influencing species responses to environmental change.


Subject(s)
Biological Variation, Population , Fundulidae/metabolism , Mitochondria/metabolism , Oxygen/metabolism , Thermotolerance , Animals , Fundulidae/genetics , Hemoglobins/metabolism
6.
Conserv Physiol ; 3(1): cov002, 2015.
Article in English | MEDLINE | ID: mdl-27293687

ABSTRACT

Accurate measurements of blood gases and acid-base status require an array of sophisticated laboratory equipment that is typically not available during field research; such is the case for many studies on the stress physiology, ecology and conservation of elasmobranch fish species. Consequently, researchers have adopted portable clinical analysers that were developed for the analysis of human blood characteristics, but often without thoroughly validating these systems for their use on fish. The aim of our study was to test the suitability of the i-STAT system, the most commonly used portable clinical analyser in studies on fish, for analysing blood gases and acid-base status in elasmobranchs, over a broad range of conditions and using the sandbar shark (Carcharhinus plumbeus) as a model organism. Our results indicate that the i-STAT system can generate useful measurements of whole blood pH, and the use of appropriate correction factors may increase the accuracy of results. The i-STAT system was, however, unable to generate reliable results for measurements of partial pressure of oxygen (PO2) and the derived parameter of haemoglobin O2 saturation. This is probably due to the effect of a closed-system temperature change on PO2 within the i-STAT cartridge and the fact that the temperature correction algorithms used by i-STAT assume a human temperature dependency of haemoglobin-O2 binding; in many ectotherms, this assumption will lead to equivocal i-STAT PO2 results. The in vivo partial pressure of CO2 (PCO2) in resting sandbar sharks is probably below the detection limit for PCO2 in the i-STAT system, and the measurement of higher PCO2 tensions was associated with a large measurement error. In agreement with previous work, our results indicate that the i-STAT system can generate useful data on whole blood pH in fishes, but not blood gases.

7.
Conserv Physiol ; 3(1): cov021, 2015.
Article in English | MEDLINE | ID: mdl-27293706

ABSTRACT

Every year, bar-headed geese (Anser indicus) perform some of the most remarkable trans-Himalayan migrations, and researchers are increasingly interested in understanding the physiology underlying their high-altitude flight performance. A major challenge is generating reliable measurements of blood parameters on wild birds in the field, where established analytical techniques are often not available. Therefore, we validated two commonly used portable clinical analysers (PCAs), the i-STAT and the HemoCue systems, for the analysis of blood parameters in bar-headed geese. The pH, partial pressures of O2 and CO2 (PO2 and PCO2), haemoglobin O2 saturation (sO2), haematocrit (Hct) and haemoglobin concentration [Hb] were simultaneously measured with the two PCA systems (i-STAT for all parameters; HemoCue for [Hb]) and with conventional laboratory techniques over a physiological range of PO2, PCO2 and Hct. Our results indicate that the i-STAT system can generate reliable values on bar-headed goose whole blood pH, PO2, PCO2 and Hct, but we recommend correcting the obtained values using the linear equations determined here for higher accuracy. The i-STAT is probably not able to produce meaningful measurements of sO2 and [Hb] over a range of physiologically relevant environmental conditions. However, we can recommend the use of the HemoCue to measure [Hb] in the bar-headed goose, if results are corrected. We emphasize that the equations that we provide to correct PCA results are applicable only to bar-headed goose whole blood under the conditions that we tested. We encourage researchers to validate i-STAT or HemoCue results thoroughly for their specific study conditions and species in order to yield accurate results.

8.
J Comp Physiol B ; 184(7): 865-76, 2014 Oct.
Article in English | MEDLINE | ID: mdl-25160040

ABSTRACT

Marine teleost fish secrete bicarbonate (HCO3 (-)) into the intestine to aid osmoregulation and limit Ca(2+) uptake by carbonate precipitation. Intestinal HCO3 (-) secretion is associated with an equimolar transport of protons (H(+)) into the blood, both being proportional to environmental salinity. We hypothesized that the H(+)-sensitive haemoglobin (Hb) system of seawater teleosts could be exploited via the Bohr and/or Root effects (reduced Hb-O2 affinity and/or capacity with decreasing pH) to improve O2 delivery to intestinal cells during high metabolic demand associated with osmoregulation. To test this, we characterized H(+) equilibria and gas exchange properties of European flounder (Platichthys flesus) haemoglobin and constructed a model incorporating these values, intestinal blood flow rates and arterial-venous acidification at three different environmental salinities (33, 60 and 90). The model suggested red blood cell pH (pHi) during passage through intestinal capillaries could be reduced by 0.14-0.33 units (depending on external salinity) which is sufficient to activate the Bohr effect (Bohr coefficient of -0.63), and perhaps even the Root effect, and enhance tissue O2 delivery by up to 42 % without changing blood flow. In vivo measurements of intestinal venous blood pH were not possible in flounder but were in seawater-acclimated rainbow trout which confirmed a blood acidification of no less than 0.2 units (equivalent to -0.12 for pHi). When using trout-specific values for the model variables, predicted values were consistent with measured in vivo values, further supporting the model. Thus this system is an elegant example of autoregulation: as the need for costly osmoregulatory processes (including HCO3 (-) secretion) increases at higher environmental salinity, so does the enhancement of O2 delivery to the intestine via a localized acidosis and the Bohr (and possibly Root) effect.


Subject(s)
Bicarbonates/metabolism , Flounder/metabolism , Intestinal Mucosa/metabolism , Oncorhynchus mykiss/metabolism , Oxygen/metabolism , Acidosis , Animals , Fresh Water , Hemoglobins/metabolism , Hydrogen , Osmoregulation , Salinity , Seawater
9.
J Comp Physiol B ; 184(6): 709-18, 2014 Aug.
Article in English | MEDLINE | ID: mdl-24973965

ABSTRACT

Preferential intracellular pH (pHi) regulation, where pHi is tightly regulated in the face of a blood acidosis, has been observed in a few species of fish, but only during elevated blood PCO2. To determine whether preferential pHi regulation may represent a general pattern for acid-base regulation during other pH disturbances we challenged the armoured catfish, Pterygoplichthys pardalis, with anoxia and exhaustive exercise, to induce a metabolic acidosis, and bicarbonate injections to induce a metabolic alkalosis. Fish were terminally sampled 2-3 h following the respective treatments and extracellular blood pH, pHi of red blood cells (RBC), brain, heart, liver and white muscle, and plasma lactate and total CO2 were measured. All treatments resulted in significant changes in extracellular pH and RBC pHi that likely cover a large portion of the pH tolerance limits of this species (pH 7.15-7.86). In all tissues other than RBC, pHi remained tightly regulated and did not differ significantly from control values, with the exception of a decrease in white muscle pHi after anoxia and an increase in liver pHi following a metabolic alkalosis. Thus preferential pHi regulation appears to be a general pattern for acid-base homeostasis in the armoured catfish and may be a common response in Amazonian fishes.


Subject(s)
Acid-Base Equilibrium/physiology , Acidosis/metabolism , Catfishes/physiology , Homeostasis/physiology , Animals , Bicarbonates/administration & dosage , Carbon Dioxide/analysis , Cell Hypoxia/physiology , Hematocrit , Hydrogen-Ion Concentration , Liver/metabolism , Muscle, Skeletal/metabolism , Physical Exertion/physiology
10.
J Exp Biol ; 217(Pt 8): 1205-14, 2014 Apr 15.
Article in English | MEDLINE | ID: mdl-24744420

ABSTRACT

Teleost fishes constitute 95% of extant aquatic vertebrates, and we suggest that this is related in part to their unique mode of tissue oxygenation. We propose the following sequence of events in the evolution of their oxygen delivery system. First, loss of plasma-accessible carbonic anhydrase (CA) in the gill and venous circulations slowed the Jacobs-Stewart cycle and the transfer of acid between the plasma and the red blood cells (RBCs). This ameliorated the effects of a generalised acidosis (associated with an increased capacity for burst swimming) on haemoglobin (Hb)-O2 binding. Because RBC pH was uncoupled from plasma pH, the importance of Hb as a buffer was reduced. The decrease in buffering was mediated by a reduction in the number of histidine residues on the Hb molecule and resulted in enhanced coupling of O2 and CO2 transfer through the RBCs. In the absence of plasma CA, nearly all plasma bicarbonate ultimately dehydrated to CO2 occurred via the RBCs, and chloride/bicarbonate exchange was the rate-limiting step in CO2 excretion. This pattern of CO2 excretion across the gills resulted in disequilibrium states for CO2 hydration/dehydration reactions and thus elevated arterial and venous plasma bicarbonate levels. Plasma-accessible CA embedded in arterial endothelia was retained, which eliminated the localized bicarbonate disequilibrium forming CO2 that then moved into the RBCs. Consequently, RBC pH decreased which, in conjunction with pH-sensitive Bohr/Root Hbs, elevated arterial oxygen tensions and thus enhanced tissue oxygenation. Counter-current arrangement of capillaries (retia) at the eye and later the swim bladder evolved along with the gas gland at the swim bladder. Both arrangements enhanced and magnified CO2 and acid production and, therefore, oxygen secretion to those specialised tissues. The evolution of ß-adrenergically stimulated RBC Na(+)/H(+) exchange protected gill O2 uptake during stress and further augmented plasma disequilibrium states for CO2 hydration/dehydration. Finally, RBC organophosphates (e.g. NTP) could be reduced during hypoxia to further increase Hb-O2 affinity without compromising tissue O2 delivery because high-affinity Hbs could still adequately deliver O2 to the tissues via Bohr/Root shifts. We suggest that the evolution of this unique mode of tissue O2 transfer evolved in the Triassic/Jurassic Period, when O2 levels were low, ultimately giving rise to the most extensive adaptive radiation of extant vertebrates, the teleost fishes.


Subject(s)
Biological Evolution , Fishes/physiology , Oxygen/metabolism , Anaerobiosis , Animals , Biological Transport , Feeding Behavior , Swimming
11.
J Fish Biol ; 84(3): 682-704, 2014 Mar.
Article in English | MEDLINE | ID: mdl-24502749

ABSTRACT

The evolution of air breathing during the Devonian provided early fishes with bimodal respiration with a stable O2 supply from air. This was, however, probably associated with challenges and trade-offs in terms of acid-base balance and ionoregulation due to reduced gill:water interaction and changes in gill morphology associated with air breathing. While many aspects of acid-base and ionoregulation in air-breathing fishes are similar to water breathers, the specific cellular and molecular mechanisms involved remain largely unstudied. In general, reduced ionic permeability appears to be an important adaptation in the few bimodal fishes investigated but it is not known if this is a general characteristic. The kidney appears to play an important role in minimizing ion loss to the freshwater environment in the few species investigated, and while ion uptake across the gut is probably important, it has been largely unexplored. In general, air breathing in facultative air-breathing fishes is associated with an acid-base disturbance, resulting in an increased partial pressure of arterial CO2 and a reduction in extracellular pH (pHE ); however, several fishes appear to be capable of tightly regulating tissue intracellular pH (pHI ), despite a large sustained reduction in pHE , a trait termed preferential pHI regulation. Further studies are needed to determine whether preferential pHI regulation is a general trait among bimodal fishes and if this confers reduced sensitivity to acid-base disturbances, including those induced by hypercarbia, exhaustive exercise and hypoxia or anoxia. Additionally, elucidating the cellular and molecular mechanisms may yield insight into whether preferential pHI regulation is a trait ultimately associated with the early evolution of air breathing in vertebrates.


Subject(s)
Acid-Base Equilibrium/physiology , Fishes/physiology , Respiration , Adaptation, Physiological , Air , Animals , Biological Evolution , Gills/physiology , Hydrogen-Ion Concentration , Hypoxia
12.
Conserv Physiol ; 2(1): cou037, 2014.
Article in English | MEDLINE | ID: mdl-27293658

ABSTRACT

Portable clinical analysers, such as the i-STAT system, are increasingly being used for blood analysis in animal ecology and physiology because of their portability and easy operation. Although originally conceived for clinical application and to replace robust but lengthy techniques, researchers have extended the use of the i-STAT system outside of humans and even to poikilothermic fish, with only limited validation. The present study analysed a range of blood parameters [pH, haematocrit (Hct), haemoglobin (Hb), HCO3 (-), partial pressure of CO2 (PCO2), partial pressure of O2 (PO2), Hb saturation (sO2) and Na(+) concentration] in a model teleost fish (rainbow trout, Oncorhynchus mykiss) using the i-STAT system (CG8+ cartridges) and established laboratory techniques. This methodological comparison was performed at two temperatures (10 and 20°C), two haematocrits (low and high) and three PCO2 levels (0.5, 1.0 and 1.5%). Our results indicate that pH was measured accurately with the i-STAT system over a physiological pH range and using the i-STAT temperature correction. Haematocrit was consistently underestimated by the i-STAT, while the measurements of Na(+), PCO2, HCO3 (-) and PO2 were variably inaccurate over the range of values typically found in fish. The algorithm that the i-STAT uses to calculate sO2 did not yield meaningful results on rainbow trout blood. Application of conversion factors to correct i-STAT measurements is not recommended, due to significant effects of temperature, Hct and PCO2 on the measurement errors and complex interactions may exist. In conclusion, the i-STAT system can easily generate fast results from rainbow trout whole blood, but many are inaccurate values.

13.
Philos Trans R Soc Lond B Biol Sci ; 367(1596): 1770-9, 2012 Jun 19.
Article in English | MEDLINE | ID: mdl-22566682

ABSTRACT

Pink salmon, Oncorhynchus gorbuscha, are the most abundant wild salmon species and are thought of as an indicator of ecosystem health. The salmon louse, Lepeophtheirus salmonis, is endemic to pink salmon habitat but these ectoparasites have been implicated in reducing local pink salmon populations in the Broughton Archipelago, British Columbia. This allegation arose largely because juvenile pink salmon migrate past commercial open net salmon farms, which are known to incubate the salmon louse. Juvenile pink salmon are thought to be especially sensitive to this ectoparasite because they enter the sea at such a small size (approx. 0.2 g). Here, we describe how 'no effect' thresholds for salmon louse sublethal impacts on juvenile pink salmon were determined using physiological principles. These data were accepted by environmental managers and are being used to minimize the impact of salmon aquaculture on wild pink salmon populations.


Subject(s)
Aquaculture/methods , Copepoda/pathogenicity , Ecosystem , Salmon/parasitology , Animal Migration/physiology , Animals , Body Size/physiology , British Columbia/epidemiology , Conservation of Natural Resources/methods , Copepoda/physiology , Fish Diseases/epidemiology , Fish Diseases/parasitology , Homeostasis , Salmon/physiology , Seawater , Swimming/physiology , Water-Electrolyte Balance
14.
J Comp Physiol B ; 182(6): 781-92, 2012 Aug.
Article in English | MEDLINE | ID: mdl-22466615

ABSTRACT

Smolting salmonids typically require weeks to months of physiological preparation in freshwater (FW) before entering seawater (SW). Remarkably, pink salmon (Oncorhynchus gorbuscha) enter SW directly following yolk absorption and gravel emergence at a size of 0.2 g. To survive this exceptional SW migration, pink salmon were hypothesized to develop hypo-osmoregulatory abilities prior to yolk absorption and emergence. To test this, alevins (pre-yolk absorption) and fry (post-yolk absorption) were transferred from FW in darkness to SW under simulated natural photoperiod (SNP). Ionoregulatory status was assessed at 0, 1 and 5 days post-transfer. SW alevins showed no evidence of hypo-osmoregulation, marked by significant water loss and no increase in gill Na⁺/K⁺-ATPase (NKA) activity or Na⁺:K⁺:2Cl⁻ cotransporter (NKCC) immunoreactive (IR) cell frequency. Conversely, fry maintained water balance, upregulated gill NKA activity by 50 %, increased the NKA α1b/α1a mRNA expression ratio by sixfold and increased NKCC IR cell frequency. We also provide the first evidence of photoperiod-triggered smoltification in pink salmon, as fry exposed to SNP in FW exhibited preparatory changes in gill NKA activity and α1 subunit expression similar to fry exposed to SNP in SW. Interestingly, fry incurred larger increases in whole body Na⁺ than alevins following both SW and FW + SNP exposure (40 and 20 % in fry vs. 0 % in alevins). The ability to incur and tolerate large ion loads may underlie a novel mechanism for maintaining water balance in SW prior to completing hypo-osmoregulatory development. We propose that pink salmon represent a new form of anadromy termed "precocious anadromy".


Subject(s)
Adaptation, Physiological/physiology , Salmon/physiology , Sodium-Potassium-Chloride Symporters/metabolism , Sodium-Potassium-Exchanging ATPase/metabolism , Water-Electrolyte Balance/physiology , Animals , Fresh Water , Gills/metabolism , Larva/physiology , Salmon/growth & development , Seawater , Sodium-Potassium-Chloride Symporters/genetics , Sodium-Potassium-Exchanging ATPase/genetics
15.
Physiol Biochem Zool ; 84(6): 535-42, 2011.
Article in English | MEDLINE | ID: mdl-22030846

ABSTRACT

Gill remodeling can be extensive in crucian carp, where up to a 7.5-fold increase in gill surface area has been observed during exposure to hypoxia through a reduction in the interlamellar cell mass (ILCM) and increased lamellar protrusion that has been hypothesized to be signaled by the need to maximize oxygen uptake under a given condition. Sustained aerobic exercise may have the greatest influence on oxygen demand in fish; however, its effect on gill remodeling in crucian carp has not been investigated. The specific objectives of this study were to determine (i) whether sustained aerobic exercise induces gill remodeling in the crucian carp, (ii) whether gill remodeling following sustained exercise affects the maximum critical swimming speed (U(crit)) and maximal oxygen consumption rate ([Formula: see text]), and (iii) whether gill remodeling following sustained exercise is associated with trade-offs related to ionoregulation. We measured [Formula: see text] in crucian carp at each step during an initial U(crit) test (U(crit1)), forced them to swim at 70% of U(crit) for 40 h, and then conducted a second U(crit) test (U(crit2)). From rest to U(crit1) (7-8 h), we observed a significant increase in protruding lamella height and area of the gills and a reduction in ILCM height and volume, likely associated with partial shedding of the ILCM, indicating that gill remodeling during exercise is rapid. Further changes were observed between U(crit1) and U(crit2), with statistically significant increases in protruding lamellar height, basal length and area, and a statistically significant reduction in protruding lamellar thickness and ILCM height and volume. Interestingly, there was no significant difference between U(crit1) and U(crit2) values, nor in maximal [Formula: see text] measured at U(crit1) and U(crit2). Furthermore, there was no significant difference in plasma osmolarity, [Na(+)], or [Cl(-)] in fish at rest, following U(crit1) or U(crit2). Thus, while these data support the hypothesis that the need to maximize oxygen uptake is an important signal for gill remodeling, which can occur quite rapidly (within 7 h at 15°C), the physiological implications of remodeling during exercise are less clear.


Subject(s)
Airway Remodeling/physiology , Carps/physiology , Gills/anatomy & histology , Physical Conditioning, Animal/physiology , Swimming/physiology , Animals , Carps/blood , Gills/physiology , Osmolar Concentration , Oxygen Consumption , Task Performance and Analysis
16.
J Fish Biol ; 77(9): 2072-92, 2010 Dec.
Article in English | MEDLINE | ID: mdl-21133917

ABSTRACT

The objective of this study was to examine the spatial genetic relationships of the Lake Qinghai scaleless carp Gymnocypris przewalskii within the Lake Qinghai system, determining whether genetic evidence supports the current taxonomy of Gymnocypris przewalskii przewalskii and Gymnocypris przewalskii ganzihonensis and whether Gymnocypris przewalskii przewalskii are returning to their natal rivers to spawn. Comparison of mitochondrial (control region) variation (42 haplotypes in 203 fish) of G. przewalskii with the postulated ancestral species found in the Yellow River, Gymnocypris eckloni (10 haplotypes in 23 fish), indicated no haplotype sharing, but incomplete lineage sorting. Consistent with the sub-species status, an AMOVA indicated that the Ganzi River population was significantly different from all other river populations (F(ST) = 0·1671, P < 0·001). No genetic structure was found among the other rivers in the Lake Qinghai catchment. An AMOVA of amplified fragment length polymorphism (AFLP) loci, however, revealed significant genetic differences between most spawning populations (F(ST) = 0·0721, P < 0·001). Both mitochondrial and AFLP data found significant differences among G. p. przewalskii, G. p. ganzihonensis and G. eckloni (F(ST) values of 0·1959 and 0·1431, respectively, P < 0·001). Consistent with the incomplete lineage sorting, Structure analysis of AFLP loci showed evidence of five clusters. One cluster is shared among all sample locations, one is unique to G. p. ganzihonensis and G. eckloni, and the others are mostly found in G. p. przewalskii. Genetic evidence therefore supports the current taxonomy, including the sub-species status of G. p. ganzihonensis, and is consistent with natal homing of most Lake Qinghai populations. These findings have significant implications for the conservation and management of this unique and threatened species. The evidence suggests that G. p. przewalskii should be treated as a single population for conservation purposes. Exchangeability of the populations, however, should not be used to promote homogenization of fish spawning in the different rivers. As some degree of genetic divergence was detected in this study, it is recommended that the spawning groups be treated as separate management units.


Subject(s)
Carps/genetics , Phylogeny , Amplified Fragment Length Polymorphism Analysis , Animals , Carps/physiology , Conservation of Natural Resources , DNA, Mitochondrial/chemistry , Haplotypes , Homing Behavior , Likelihood Functions , Phylogeography , Polymorphism, Genetic , Rivers , Sexual Behavior, Animal
17.
J Fish Biol ; 77(6): 1282-92, 2010 Oct.
Article in English | MEDLINE | ID: mdl-21039505

ABSTRACT

Salinity tolerance in wild (Glendale) and hatchery (Quinsam) pink salmon Oncorhynchus gorbuscha (average mass 0·2 g) was assessed by measuring whole body [Na(+)] and [Cl⁻] after 24 or 72 h exposures to fresh water (FW) and 33, 66 or 100% sea water (SW). Gill Na(+), K(+)-ATPase activity was measured following exposure to FW and 100% SW and increased significantly in both populations after a 24 h exposure to 100% SW. Whole body [Na(+)] and whole body [Cl⁻] increased significantly in both populations after 24 h in 33, 66 and 100% SW, where whole body [Cl⁻] differed significantly between Quinsam and Glendale populations. Extending the seawater exposure to 72 h resulted in no further increases in whole body [Na(+)] and whole body [Cl⁻] at any salinity, but there was more variability among the responses of the two populations. Per cent whole body water (c. 81%) was maintained in all groups of fish regardless of salinity exposure or population, indicating that the increase in whole body ion levels may have been related to maintaining water balance as no mortality was observed in this study. Thus, both wild and hatchery juvenile O. gorbuscha tolerated abrupt salinity changes, which triggered an increase in gill Na(+), K(+)-ATPase within 24 h. These results are discussed in terms of the preparedness of emerging O. gorbuscha for the marine phase of their life cycle.


Subject(s)
Adaptation, Physiological , Salinity , Salmon/physiology , Water-Electrolyte Balance/physiology , Animals , Chlorides/analysis , Fresh Water , Gills/physiology , Seawater , Sodium/analysis , Sodium-Potassium-Exchanging ATPase/metabolism
18.
Physiol Biochem Zool ; 83(2): 322-32, 2010.
Article in English | MEDLINE | ID: mdl-20100089

ABSTRACT

Soon after hatching, the osteoglossid fish Arapaima gigas undergoes a rapid transition from a water breather to an obligate air breather. This is followed by a gradual disappearance of gill lamellae, which leaves smooth filaments with a reduced branchial diffusion capacity due to loss of surface area, and a fourfold increase in diffusion distance. This study evaluated the effects these changes have on gill function by examining two size classes of fish that differ in gill morphology. In comparison to smaller fish (approximately 67.5 g), which still have lamellae, larger fish (approximately 724.2 g) without lamellae took up a slightly greater percentage of O2 across the gills (30.1% vs. 23.9%), which indicates that the morphological changes do not place limitations on O2 uptake in larger fish. Both size groups excreted similar percentages of CO2 across the gills (85%-90%). However, larger fish had higher blood PCO2 (26.51.9 vs. 16.51.5 mmHg) and HCO3(-) (40.2 +/- 2.9 vs. 33.6 +/- 4.5 mmol L(-1)) concentrations and lower blood pH (7.58 +/- 0.01 vs. 7.70 +/- 0.04) than did smaller fish, despite having lower mass-specific metabolisms, suggesting a possible diffusion limitation for CO2 excretion in larger fish. With regard to ion regulation, rates of diffusive Na+ loss were about 3.5 times higher in larger fish than they were in smaller fish, despite the lowered branchial diffusion capacity, and rates of Na+ uptake were higher by about the same amount despite 40% lower activity of branchial Na+/K+-ATPase. Kinetic analysis of Na uptake revealed an extremely low-affinity (K(m) = 587.9 +/- 169.5 micromol L(-1)), low-capacity (J(max) = 265.7 +/- 56.8 nmol g(-1) h(-1)) transport system. These data may reflect a general reduction in the role of the gills in ion balance. Renal Na+/K+-ATPase activity was 5-10 times higher than Na+/K+-ATPase activity in the gills, and urine: plasma ratios for Na+ and Cl(-) were very low (0.001-0.005) relative to that of other fish, which suggested an increased role for dietary salt intake and renal salt retention and which was representative of a more "terrestrial" mode of ion regulation. Such de-emphasis of branchial ion regulation confers greatly reduced sensitivity of diffusive ion loss to low water pH. Ammonia excretion also appeared to be impacted by gill changes. Rates of ammonia excretion in larger fish were one third less than that in smaller fish, despite larger fish having blood ammonia concentrations that were twice as high.


Subject(s)
Fishes/physiology , Gills/anatomy & histology , Animals , Biological Transport/physiology , Carbon Dioxide/physiology , Fishes/anatomy & histology , Fishes/growth & development , Gills/growth & development , Gills/physiology , Oxygen Consumption/physiology , Respiration , Respiratory Transport/physiology , Sodium/metabolism , Sodium-Potassium-Exchanging ATPase/physiology
19.
J Comp Physiol B ; 180(1): 73-82, 2010 Jan.
Article in English | MEDLINE | ID: mdl-19590877

ABSTRACT

Tunas (family Scombridae) are exceptional among most teleost fishes in that they possess vascular heat exchangers which allow heat retention in specific regions of the body (termed 'regional heterothermy'). Seemingly exclusive to heterothermic fishes is a markedly reduced temperature dependence of blood-oxygen (blood-O(2)) binding, or even a reversed temperature dependence where increasing temperature increases blood-O(2) affinity. These unusual binding properties have been documented in whole blood and in haemoglobin (Hb) solutions, and they are hypothesised to prevent oxygen loss from arteries to veins within the vascular heat exchangers and/or to prevent excessive oxygen unloading to the warm tissues and ensure an adequate supply of oxygen to tissues positioned efferent to the heat exchangers. The temperature sensitivity of blood-O(2) binding has not been characterised in an ectothermic scombrid (mackerels and bonitos), but the existence of the unusual binding properties in these fishes would have clear implications for their proposed association with regional heterothermy. Accordingly, the present study examined oxygenation of whole blood of the chub mackerel (Scomber japonicus) at 10, 20 and 30 degrees C and at 0.5, 1 and 2% CO(2). Oxygen affinity was generally highest at 20 degrees C for all levels of CO(2). Temperature-independent binding was observed at low (0.5%) CO(2), where the PO(2) at 50% blood-O(2) saturation (P (50)) was not statistically different at 10 and 30 degrees C (2.58 vs. 2.78 kPa, respectively) with an apparent heat of oxygenation (H degrees ) close to zero (-6 kJ mol(-1)). The most significant temperature-mediated difference occurred at high (2%) CO(2), where the P (50) at 10 degrees C was twofold higher than that at 20 degrees C with a corresponding H degrees of +43 kJ mol(-1). These results provide clear evidence of independent and reversed open-system temperature effects on blood oxygenation in S. japonicus, and it is therefore speculated that these unusual blood-O(2) binding characteristics may have preceded the evolution of vascular heat exchangers and regional heterothermy in fishes.


Subject(s)
Biological Evolution , Body Temperature , Oxygen/blood , Perciformes/physiology , Adaptation, Biological , Animals , California , Carbon Dioxide/blood , Hemoglobins/metabolism , Kinetics , Pacific Ocean , Perciformes/anatomy & histology , Perciformes/blood , Phylogeny , Temperature
20.
Am J Physiol Regul Integr Comp Physiol ; 296(6): R1868-80, 2009 Jun.
Article in English | MEDLINE | ID: mdl-19339675

ABSTRACT

Sturgeons are among the most CO2 tolerant of fishes investigated to date. However, the basis of this exceptional CO2 tolerance is unknown. Here, white sturgeon, Acipenser transmontanus, were exposed to elevated CO2 to investigate the mechanisms associated with short-term hypercarbia tolerance. During exposure to 1.5 kPa Pco2, transient blood pH [extracellular pH (pHe)] depression was compensated within 24 h and associated with net plasma HCO3- accumulation and equimolar Cl- loss, and changes in gill morphology, such as a decrease in apical surface area of mitochondrial-rich cells. These findings indicate that pHe recovery at this level of hypercarbia is accomplished in a manner similar to most freshwater teleost species studied to date, although branchial mechanisms involved may differ. White sturgeon exposed to more severe hypercarbia (3 and 6 kPa Pco2) for 48 h exhibited incomplete pH compensation in blood and red blood cells. Despite pHe depression, intracellular pH (pHi) of white muscle, heart, brain, and liver did not decrease during a transient (6 h of 1.5 kPa Pco2) or prolonged (48 h at 3 and 6 kPa Pco2 blood acidosis. This pHi protection was not due to high intrinsic buffering in tissues. Such tight active cellular regulation of pHi in the absence of pHe compensation represents a unique pattern for non-air-breathing fishes, and we hypothesize that it is the basis for the exceptional CO2 tolerance of white sturgeon and, likely, other CO2 tolerant fishes. Further research to elucidate the specific mechanisms responsible for this tremendous pH regulatory capacity in tissues of white sturgeon is warranted.


Subject(s)
Acid-Base Equilibrium , Acidosis, Respiratory/metabolism , Carbon Dioxide/metabolism , Gills/metabolism , Hypercapnia/metabolism , Acidosis, Respiratory/pathology , Acidosis, Respiratory/physiopathology , Adaptation, Physiological , Animals , Bicarbonates/metabolism , Brain/metabolism , Carbon Dioxide/blood , Chlorides/metabolism , Fishes , Gills/physiopathology , Gills/ultrastructure , Hydrogen-Ion Concentration , Hypercapnia/pathology , Hypercapnia/physiopathology , Liver/metabolism , Muscle Fibers, Fast-Twitch/metabolism , Myocardium/metabolism , Proton-Translocating ATPases/metabolism , Sodium-Potassium-Exchanging ATPase/metabolism , Time Factors
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