Brain function in antarctic fish: frequency response analysis of central vestibular units

Summary Extracellular single-unit recordings were made from central vestibular units responding to horizontal head rotation in antarctic fish (Pagothenia borchgrevinki) at temperatures below 0 °C. The frequency of head rotation was varied between 0.05–16 Hz and the results were analysed in terms of the phase and gain of the response with respect to the stimulus. The model of the peripheral vestibular system derived by Hartmann and Klinke (1980) was fitted to the data from antarctic fish in order to obtain a quantitative comparison of vestibular function at two different temperatures. Despite the 20 °C temperature difference, and the different recording sites (primary afferents in the goldfish, and central vestibular units in the antarctic fish) vestibular function in antarctic fish is comparable to that previously reported in goldfish.     

Ultrastructural observations and pH-measurements on red and white muscle from Antarctic fish

Summary Red and white muscle in the two Antarctic notothenioid fishes Dissostichus mawsoni and Pagothenia borchgrevinki show a rate of postmortem fall of 0.2 pH units per hour, which is close to the rate reported for mammalian muscle at 30°C, but the plateau value is reached several hours earlier in the Antarctic fish, indicating significantly lower stores of initial glycogen. A few particles, most likely representing glycogen, were seen in P. borchgrevinki white muscle and D. mawsoni red muscle, whereas predictably fewer glycogen still was evident in D. mawsoni white muscle. When large numbers of mitochondria and lipid stores were encountered in combination with a small amount of glycogen, we concluded that aerobic metabolism is dominant and that the two species examined would not use white trunk muscle for sustained or slow swimming. Rapid contractions of white trunk muscle as in prey capture or predator evasion are more likely.     

Exercise challenge in Antarctic fishes: do haematology and muscle metabolite levels limit swimming performance?

 Burst swimming increased haematocrit (partly from erythrocyte swelling) in the cryopelagic nototheniid Pagothenia borchgrevinki, but not in the benthic species Trematomus bernacchii. Erythrocyte nucleotides, which regulate haemoglobin-oxygen affinity, remained constant. Plasma cortisol was high in all captive fish and raised questions about the effects of chronic stress on metabolic measurements from Antarctic fish held in captivity. Glycogen was reduced in white trunk muscle, but not in the red pectoral muscle of exercised P. borchgrevinki. Red pectoral muscle glycogen was nearly 3 times higher in T. bernacchii than in P. borchgrevinki but post-exercise lactate rises were modest. Lactate values were, however, higher in exercised P. borchgrevinki white muscle than in T. bernacchii, and correlated with muscle-buffering capacity. Resting adenylate energy charge (AEC) was unexpectedly low in both species and reduced with exercise only for white muscle in P. borchgrevinki. While it appears that the capacity for burst swimming is limited by endogenous metabolic fuels, confirmation of low resting values of ATP and AEC in Antarctic fishes requires the development of methods that maintain high phosphocreatine levels in the muscle. Received: 12 February 1996/Accepted:1 May 1996     

Ultrastructure of microtubules in dermal melanophores and spinal nerve of the Antarctic teleost Pagothenia borchgrevinki

Summary The antarctic teleost, Pagothenia borchgrevinki inhabits the Antarctic Ocean where the water temperature remains around -1.9° C throughout the year. Dermal melanophores of this fish respond within minutes to epinephrine and theophylline with melanosome aggregation and dispersion, respectively. Numerous cytoplasmic microtubules are present in these cells despite the low environmental temperature. In longitudinal profiles, many microtubules are twisted, beaded and sometimes even branched. In cross sections, C-, U-, S-, 6- and other irregularly shaped tubules are observed. Nocodazole partially disrupts microtubules and inhibits epinephrine-induced pigment aggregation. Pigment movements are also prevented by erythro-9-[3-(2-hydroxynonyl)] adenine. Although the participation of these incomplete microtubules in cell motility remains uncertain, the results indicate that this fish has a cold-resistant microtubule system on which melanosome movements depend. Unlike those in melanophores, microtubules in the axons of spinal nerves are of uniform thickness and often contain an electron-dense core in the center.     

Effect of temperature on isotonic twitch of white muscle and predicted maximum swimming speeds of skipjack tuna,Katsuwonus pelamis

Synopsis Latent period, rise time, contraction time, and half relaxation time from isotonic contractions of isolated white muscle samples from skipjack tuna, Katsuwonus pelamis, were determined at 20°, 27°, and 34° C. These parameters were found to be inversely proportional to temperature (Q₁₀ = 1.47, 1.67, 1.62, and 1.72, respectively). The data show that contraction time and the effect of temperature on contraction time of skipjack tuna white muscle are not unique when compared to other equal-sized teleosts. Based on contraction time, maximum swimming speeds at each muscle temperature were calculated and found not significantly to exceed the maximum speeds of other equal-sized teleosts, when comparisons are made at the same white muscle temperatures     

Thermal sensitivity of heart rate and insensitivity of blood pressure in the Antarctic nototheniid fish <Emphasis Type="Italic">Pagothenia borchgrevinki</Emphasis>

The Antarctic notothenioids are among the most stenothermal of fishes, well adapted to their stable, cold and icy environment. The current study set out to investigate the thermal sensitivity/insensitivity of heart rate and ventral aortic blood pressure of the Antarctic nototheniid fish Pagothenia borchgrevinki over a range of temperatures. The heart rate increased rapidly from –1 to 6°C (Q₁₀=2.0–3.3), but was relatively insensitive to temperature above the ~6°C lethal limit of the species (Q₁₀=1.2). The increase in heart rate from –1 to 6°C was the result of a 45% increase in excitatory adrenergic tone, masking a 37% increase in inhibitory cholinergic tone. Ventral aortic pressure was regulated well above the lethal limit, up to at least 10°C. With the return of the fish to environmental temperatures, the heart rate rapidly decreased back to control levels, while ventral aortic pressure increased and remained elevated for over an hour following a 6°C exposure.     

Constancy and control of heart rate during an increase in temperature in the Antarctic fish Pagothenia borchgrevinki

The effect of an acute temperature increase on the control of the heart of the Antarctic teleost Pagothenia borchgrevinki was examined. Heart rate was thermally independent over the range −1.2°C to 3°C, although increasing the temperature from −1.2°C to 3°C elicited a decrease in ventral aortic pressure. Administration of the muscarinic receptor antagonist atropine and the β-adrenoreceptor antagonist sotalol abolished the thermal independence of heart rate, with heart rate increasing at Q₁₀=2. As temperature was increased from −1.2°C to 3°C, cholinergic tone on the heart also increased, from 44.6±4.2% to 70.0±8.4%. At the same time the adrenergic tone increased from 35.5±3.3% to 43.0±3.1%, but the effect on the heart was masked by the increase of cholinergic tone, leading to the thermal independence of heart rate.     

Recovery from exhausting exercise in an Antarctic fish,Pagothenia borchgrevinki

Summary Pagothenia borchgrevinki, an Antarctic teleost fish was swum to exhaustion and changes in lactic acid levels and blood haematocrit were monitored during recovery. The fish did not perform well at high swimming speeds due to an inability of the white myotomal muscle to produce ATP by anaerobic glycolysis. Consequently, low levels of lactic acid were produced which were fairly rapidly broken down. Haematocrit values were low in non-exercised fish, and these increased by over 100% during exercise, falling back to control levels over many hours. This is probably related to the increased oxygen demand during exercise.     

Brain function in antarctic fish: Activity of central vestibular neurons in relation to head rotation and eye movement

Summary Recordings were made from central vestibular neurons responding to horizontal head rotation in antarctic fish,Pagothenia borchgrevinki, at a temperature close to 0 °C. The spontaneous activity of these units varied between 0 and 56 Imp/s with a mean value of 20. Almost all units responded to horizontal rotation with a maximum firing rate that was approximately in phase with head velocity, either towards the recording side (type I units) or away from the recording side (type II), with no alteration of firing pattern during saccadic eye movements. The mean gain of these units was 2.6 Imp/s//s at 0.35 Hz which is higher than that reported for central vestibular neurons in other fish.     

Temperature dependency of miniature end plate currents from the extraocular muscle of Antarctic teleost fishes

The effects of temperature on the decay phase of post-synaptic currents were examined to determine the extent of temperature compensation in the inferior oblique extraocular muscles of four Antarctic fishes (Trematomus bernacchii, Trematomus pennellii, Trematomus hansoni, and Pagothenia borchgrevinki, Family Nototheniidae). At ambient temperatures, different fish produce miniature end plate currents (MEPCs), which vary in duration and rate of decay. Low temperatures normally prolong MEPCs, however, Antarctic fishes were found to produce MEPCs of significantly shorter duration than predicted (based on back-extrapolation of temperate fish data to sub-zero temperatures). Notothenioid decay time constants were approximately 500 μs faster than their temperate counterparts, extrapolated to −2°C, suggesting that the difference is consistent with temperature compensation in the neural-systems of Antarctic fish. Results presented here conform the hypothesis that post-synaptic MEPCs of Antarctic fish exhibit temperature compensation, an adaptive feature that has permitted the successful radiation throughout the Southern Ocean.     

Adaptation of intestinal cell membrane enzymes to low temperatures in the Antarctic teleost Pagothenia bernacchii

The enzymatic activity (expressed as milliunits per milligram total proteins) of three intestinal brush-border membrane enzymes, leucine aminopeptidase, alkaline phosphatase and maltase, measured over a range of temperatures between 1.5 and 37 °C, has been found to be much higher in the Antarctic fish Pagothenia bernacchii than in the temperate fish Anguilla anguilla. To explain this experimental observation the apparent Michaelis-Menten constant, the maximal velocity, the activation energy values and the thermal stability of these three enzymes were measured. The apparent Michaelis-Menten constant values of leucine amino peptidase and alkaline phosphatase were different in the intestine mucosal homogenate of the two fish at each measured temperature (from a minimum of 2.5 to a maximum of 37 °C). However, the values found at 2.5 °C for the Antarctic species and 15 °C for the eel where comparable. Furthermore, its value was unchanged in eel intestine apical membranes, both in the presence and without enzyme lipid microenvironment. While the maximal enzymatic activities of the leucine aminopeptidase and maltase did not decrease without their enzyme lipid microenvironment, produced by treatment with Triton X-100, the impairment of alkaline phosphatase maximal activity cannot be significantly differentiated from a non-specific inhibitory effect of the detergent. The activation energy values of leucine amino peptidase, alkaline phosphatase and maltase were lower in the Antarctic fish (11.7, 5.6 and 11.8 kcal·mol^-1, respectively) than in the eel (13.6, 7.6 and 13.1 kcal·mol^-1, respectively). The thermal stability of alkaline phosphatase and maltase is different in Pagothenia bernacchii and Anguilla anguilla intestinal homogenate.Abbreviations BBM brush border membrane - E _a activation energy - EGTA ethyleneglycol-bis-(-amino ethylether)N, N-tetraacetic acid - HEPES 2-[4-(2-hydroxyethyl)-1-piperazinyl]-ethane sulphonic acid - Km_app apparent Michaelis-Menten constant - PMSF phenylmethyl-sulphonyl fluoride - TRIS TRIS (hydroxymethyl)-aminomethane     

X-cell gill disease in Pagothenia borchgrevinki from McMurdo Sound, Antarctica

The Antarctic nototheniid fish Pagothenia borchgrevinki is a schooling, cryopelagic fish growing to about 280 mm maximum length. It is affected by X-cell disease, which causes gross swelling of gill filaments. Overall, 22% of the fish sampled had X-cell disease with individual schools ranging from 9.2 to 43.9%, which is a very high incidence compared to figures of other fish with the disease. In P. borchgrevinki, the disease caused a doubling of gill mass but had no effect on liver mass. Condition factor of affected fish was low. Received: 24 March 1997 / Accepted: 12 July 1997     

Lipid content and composition of three species of Antarctic fish in relation to buoyancy

Summary The lipip content and composition of various tissues from three species of nototheniid fish from McMurdo Sound, Antarctic have been examined in relation to their habitat and buoyancy. The pelagic midwater Dissostichus mawsoni is neutrally buoyant. It is rich in lipid which is located subcutaneously, as adipose tissue associated intimately with white muscle, and as lipid droplets within the cells of various tissues. White muscle, red muscle and liver are particularly lipid-rich, although the liver is not positively buoyant. The amount of lipid stored in the white muscle increases towards the centre of buoyancy of the fish. These deposits are documented at the anatomical, histological and ultrastructural levels. Tissues of Pagothenia borchgrevinki contain less lipid than D. mawsoni, but liver, red muscle and white muscle are still very rich in lipid. This species is cryopelagic, that is it spends most of the time in the water column just beneath the surface ice layer. It is not neutrally buoyant, but has a low weight in seawater. The tissues of the benthic Trematomus bernacchii contain only normal levels of lipid. The lipid class compositions of all three species are dominated by triacylglycerol, particularly when lipid contents are high. Serum lipids are an exception in containing high levels of the transport lipid sterol ester. The reason why Antarctic fish use triacylglycerols for buoyancy rather than was esters (as used by many myctophids) or squalene (as used by some sharks) is unclear.     

Temperature preferences and tolerances of three fish species inhabiting hyperthermal ponds on mangrove islands

The fish species Cyprinidon artifrons, Floridichthys carpio, and Gambusia yucatana inhabit shallow mangrove ponds off the coast of Belize. Portions of these ponds experience a diurnal temperature change from 26 °C at night to 40 °C and above during midday. Repeated field observations indicate Cyprinidon prefer the warmer (and much larger) portions of the ponds whereas the other two species stay in the cooler areas.The hypothesis that temperature is serving as a cue for partitioning within the ponds was supported by laboratory thermal gradient tests in which Cyprinidon preferred temperatures clearly higher than the other two species.The critical thermal maximum (CTM) was determined for the three species using members that had been acclimated to either a daily cycling temperature similar to that for the ponds, or to the mean of the 24-hour cycle (30 °C). Cyprinidon acclimated to the cycling temperature had a CTM of 45.5 °C, which apparently sets a new record for fish CTM. Acclimation to a constant 30 °C lowered the CTM to 43.7 °C. Floridichthys and Gambusia acclimated to the cycled temperature had CTMs of 43.9 and 43.3 °C respectively, and 42.5 and 42.6 °C for those acclimated to 30 °C.All three species appear to have the ability to tolerate the high temperatures throughout the ponds but only Cyprinidon utilize the whole pond during the day. This may help to explain the large populations of Cyprinodon found in these mangrove ponds compared to the other species.     

Timing of Recruitment Events, Residence Periods and Post-Settlement Growth of Juvenile Fish in a Seagrass Nursery Area, South-Eastern Australia

We sampled juvenile fish approximately fortnightly using a fine mesh beach seine net to determine the recruitment patterns of Sillago ciliata, Centropogon australis and Girella tricuspidata to seagrass, Zostera capricorni, habitats in Botany Bay, south-eastern Australia. We used trends in the length frequency distributions of juveniles to estimate the timing of recruitment events, rates of post-settlement growth and the residence time of each species in seagrass. We detected discrete pulses of recruitment by each species. The timing of recruitment events by S. ciliata reflected the timing of spawning events. Recruitment by G. tricuspidata reflected lunar or tidal cycles. The factors influencing the timing of recruitment by C. australis were unclear. The growth rate of S. ciliata length cohorts varied and was positively related to estuarine water temperature. The timing of emigration from seagrass of C. australis and G. tricuspidata juveniles appeared to be length-dependant.     

Characterization of proteases produced by newly isolated and identified proteolytic microorganisms from fermented fish (Budu)

Eight different strains ofBacillus were isolated from fermented fish (Budu) and their proteolytic enzyme activities were determined after 18 h cultivation at room temperature (35° C). Four isolates possessed high protease activities. Optimum pH for these enzymes was between 7.0 and 8.0 and the optimal temperature was 55° C. The proteases retained 40% of their original activity after 20 min at 55° C but lost all activity at 65° C. Three of the four isolates were identified asBacillus subtilis, the fourth asBacillus licheniformis.     

Ecological and behavioural correlates of intracellular buffering capacity in the muscles of antarctic fishes

Summary Five species of antarctic fishes can be arranged in order of increasing anaerobic capacity of the white muscles for burst swimming: Rhigophila dearborni (Zoarcidae), icefish (Channichthyidae), Dissostichus mawsoni, Trematomus centronotus, and Pagothenia borchgrevinki (Nototheniidae). This order reflects increasing dependence on anaerobic work done during short bursts of speed during prey capture or predator avoidance. Buffer capacity () for white muscle was lower than that of behaviourally equivalent fish from lower latitudes and is itself temperature-dependent.     

Thermal sensitivity of scope for activity in Pagothenia borchgrevinki, a cryopelagic Antarctic nototheniid fish

The thermal sensitivity of scope for activity was studied in the Antarctic nototheniid fish Pagothenia borchgrevinki. The scope for activity of P. borchgrevinki at 0°C was 189 mg O₂ kg⁻¹ h⁻¹ (factorial scope 6.8) which is similar to that of temperate and tropical species at their environmental temperatures, providing no evidence for metabolic cold adaptation of maximum activity. The scope for activity increased to a maximum value of 266 mg O₂ kg⁻¹ h⁻¹ (factorial scope 8.3) at 3°C and then decreased from 3 to 6°C. The thermal sensitivity of critical swimming speed was also investigated and followed a similar pattern to aerobic scope for activity, suggesting oxygen limitation of aerobic performance. Oxygen consumption rates and ventilation frequencies were monitored for 24 h after the swimming challenge and the recovery of both parameters to resting levels was rapid and independent of temperature.     

The Antarctic notothenioid fish <Emphasis Type="Italic">Pagothenia borchgrevinki</Emphasis> is thermally flexible: acclimation changes oxygen consumption

Antarctic marine organisms are considered to have extremely limited ability to respond to environmental temperature change. However, here we show that the Antarctic notothenioid fish Pagothenia borchgrevinki is an exception to this theory. P. borchgrevinki was able to acclimate its resting metabolic rate and resting ventilation frequency after a 5°C rise in temperature. Acute exposure to 4°C resulted in an elevation in metabolic rate (57.8 ± 4.79 mg O₂ kg⁻¹ h⁻¹) and resting ventilation rate (40.38 ± 1.61 breaths min⁻¹) compared with fish at −1°C (metabolic rate 34.45 ± 3.12 mg O₂ kg⁻¹ h⁻¹; ventilation rate 29.88 ± 3.72 breaths min⁻¹). However, after a 1-month acclimation period, there was no significant difference in the metabolic rate (cold fish 29.52 ± 3.01; warm fish 31.13 ± 2.30 mg O₂ kg⁻¹ h⁻¹), or the resting ventilation rate (cold fish 28.75 ± 0.98; warm fish 34.25 ± 2.28 breaths min⁻¹) of cold and warm acclimated fish. Acclimation changes to the rate of oxygen consumption following exhaustive exercise were complex. The pattern of oxygen consumption during recovery from exhaustive exercise was not significantly different in either cold or warm acclimated fish.