Behavioural studies on the lesser sandeel Ammodytes marinus (Raitt) III. The effect of temperature on activity and the environmental control of the annual cycle of activity

The behaviour of the lesser sandeel, Ammodytes marinus (Raitt), has been investigated at 5, 10 and 15° C, using a photographic method of recording activity. The activity patterns at 10 and 15° C were very similar, there being a high level of swimming activity during the light period, which fell to a low level at 5° C. It was also lower at 10° C at the end of the experiment than at the beginning and it is suggested that this might have been due to an increase in the fat contents of the fish. The feeding rate of the fish was measured and showed a Q ₁₀ of 2.08 for the temperature range 5–15° C. The annual cycle of activity of A. marinus is discussed in relation to seasonal changes in food availability, light and temperature, and in the fat content of the fish. It is concluded that after spawning in the December–January period the fish remain buried in the sand until April, because of the limiting effect on swimming and feeding activity of the environmental factors in the intervening period. The proportion of fish available for capture at the start of the fishery in April is related mainly to temperature, but food (as measured by numbers of copepods) light intensity and photoperiod are by then increasing rapidly. After July the fishery ceases and it is thought that this is because the fish have entered an overwintering stage, during which they remain buried in the sand. This phase is also thought to be associated with the maturation of the gonads in readiness for the winter spawning. The factors causing the fish to enter this stage are as yet undetermined but may be related to the attainment of a certain level of fat content.     

Observations on the Nocturnal Activity and Feeding Behavior of Anguilla japonica Glass Eels Under Laboratory Conditions

Glass eels of the temperate anguillid species, Anguilla japonica, clearly showed a nocturnal activity rhythm under laboratory conditions. Light–dark cycle was a determinant factor affecting their photonegative behavior, nocturnal locomotor activity, and feeding behavior. Under natural light conditions, glass eels remained in shelters with little daytime feeding, but came out to forage during darkness. They moved and foraged actively in the following dark, and then their activity gradually declined possibly because of food satiation. They finally buried in the sand or stayed in tubes immediately after the lights came on. Under constant light, glass eels often came out of the shelters to forage in the lights but spent little time moving outside the shelters (e.g. swimming or crawling on the sand). Glass eels took shelter to avoid light and preferred tubes to sand for shelter possibly because tubes were much easier for them to take refuge in than sand. Feeding and locomotor activities of the glass eels were nocturnal and well synchronized. They appeared to depend on olfaction rather than vision to detect and capture prey in darkness. Feeding was the driving force for glass eels to come out of sand under constant light. However, in the dark, some glass eels swam or crept actively on sand even when they were fully fed. The lunar cycles of activity rhythms of glass eels that have been observed in some estuarine areas were not detected under these laboratory conditions.     

Diel activity pattern and food search behaviour in cod, Gadus morhua

Food search behaviour in cod, Gadus morhua, was studied by means of a stationary positioning system. Six fish in a fjord in northern Norway were tagged in situ by allowing them to shallow bait-wrapped acoustic tags, and their swimming behaviour was continuously recorded. The fish exhibited a diel activity rhythm, with higher swimming speeds and a larger range during the day than at night. Chemically mediated food search was studied in periods of both high and low activity by setting a string of baits in the morning and at night. During the period of high activity, more fish localized the baits (70 versus 45% of the observations) and the time to localization was 50% shorter, indicating that high swimming activity increased the probability of encountering the odour plume and the odour source. No diel variations in the response threshold to olfactory stimuli were found, as the proportion of fish in the odour plume that responded rheotactically, and their response distances were similar in the two periods (240 and 227 m respectively). Cod performed area-restricted searches on encountering the string of baits during the day. The probability of cod detecting prey by taste receptors, encountering the odour plume of prey or localizing a stationary food source after olfactory stimulation should be relatively independent of light, and this could explain why cod were active throughout the 24 h cycle. On the other hand, the visual detection distance and the ability to capture active prey are influenced by the light level, resulting in higher activity during the day.     

Diurnal changes in intestinal apolipoprotein A-IV and its relation to food intake and corticosterone in rats

To further investigate the role of intestinal aplipoprotein A-IV (apo A-IV) in the management of daily food intake, we examined the diurnal patterns in apo A-IV gene and protein expression in freely feeding (FF) and food-restricted (FR; food provided 4 h daily for 4 wk) rats that were killed at 3-h intervals throughout the 24-h diurnal cycle. In FF rats, the intestinal apo A-IV mRNA and protein levels showed a circadian rhythm concomitant with the feeding pattern. The daily pattern of fluctuation of apo A-IV, however, was altered in FR rats, which had a marked increase in intestinal apo A-IV levels during the 4-h feeding period of light phase. In both FF and FR rats, increased plasma corticosterone (Cort) levels temporally coincided with the increasing phase of intestinal apo A-IV mRNA and protein expression. Depletion of Cort by adrenalectomy abolished the diurnal rhythm by decreasing the apo A-IV expression during the dark period but did not change the feeding rhythm. Exposure of adrenalectomized rats to consistent Cort level (50-mg continuous release Cort pellet) resulted in fixed apo A-IV levels throughout the day. These results indicate that intestinal apo A-IV exhibits a diurnal rhythm, which can be regulated by endogenous Cort independently of the light-dark cue. The fact that intestinal apo A-IV levels were consistent with the food intake during the normal diurnal cycle as well as during the cycle of 4-h feeding each day suggests that intestinal apo A-IV is involved in the regulation of daily food intake.     

Ontogeny of an endogenous rhythm in Eurydice pulchra

Field catches of Eurydice pulchra (Leach) from an Isle of Man beach indicated that adult animals were active in the water column solely during spring tide periods, whereas juvenile animals swam abundantly at high tide irrespective of lunar phase. Under constant conditions in the laboratory, animals kept in actographs with sand showed a circa-tidal rhythm of spontaneous emergence and swimming activity. In adults, the activity was greatest during “expected” night-time high-waters and was expressed solely after collection during spring tide periods. The rhythm was independent of sex, season or reproductive status. Juveniles showed no such diurnal modulation of the rhythm and the pattern was expressed throughout the semi-lunar cycle. These ontogenetic differences in behaviour are discussed in the light of previous work on the rhythm, and in terms of the differing habits of the mature and immature animals.     

Adult emergence rhythm of the egg-parasitoid Telenomus busseolae

The adult emergence rhythm of Telenomus busseolae, an egg parasitoid of Sesamia nonagrioides, was examined when parasitoids were exposed to different light-dark regimes. Most of the adult parasitoids emerged throughout the whole period of the photoperiodic cycle. Peak male emergence occurred 2–5 hours earlier than that of females. Adult emergence was asynchronous in continuous darkness or light. However, regimes of alternative light and dark phases such as L4:D20, L8:D16, L12:D12, L16:D8 and L20:D4 h generated a population rhythm with a period length of 24 hours. The peak of the emergence activity moves from the scotophase to the middle of the photophase with an increase of the photophase from 4 to 20 h. Rhythmical activity of adults was synchronised within 2 cycles when immature stages of parasitoid grow under continuous light conditions (LL) and then transferred to L12:D12. Moreover, emergence rhythm persisted and continued in a free-run with a period length of less than 24 hours by transferring a rhythmic culture from L12:D12 h to LL or RR (continuous red light) conditions, indicating the existence of a circadian rhythm. The ecological implications of the expression rhythm relate to better survival of the parasitoids.     

Effects of temperature on allocation of metabolic energy in perch (Perca fluviatilis) fed submaximal rations

Growth and long-term trends of oxygen consumption were monitored at 15 and 20° C in spontaneously swimming juvenile perch fed a fixed daily submaximal ration. The average rate as well as the efficiency of assimilation were the same at the two temperatures but a much higher proportion of food energy was allocated to activity and maintenance, and a correspondingly lower proportion to growth, at 20 than at 15° C. By computing average specific rates of oxygen consumption separately for all light and dark periods, it was found that at 20, but not at 15° C, the' scope for spontaneous activity' of two consecutive (dark and light) phases of a diurnal cycle was indirectly proportional to the average rate of oxygen consumption in the dark phase. This indicates that at 20° C the perch displayed partial compensation for a high metabolic rate in the dark by reducing swimming activity in the following light phase. However, the overall effect of this behaviour was probably too small to make a noticeable impact on the low conversion efficiency in the juvenile perch at 20 as compared to 15° C.     

Evidence for time-of-day dependent effect of neurotoxic dorsomedial hypothalamic lesions on food anticipatory circadian rhythms in rats

The dorsomedial hypothalamus (DMH) is a site of circadian clock gene and immediate early gene expression inducible by daytime restricted feeding schedules that entrain food anticipatory circadian rhythms in rats and mice. The role of the DMH in the expression of anticipatory rhythms has been evaluated using different lesion methods. Partial lesions created with the neurotoxin ibotenic acid (IBO) have been reported to attenuate food anticipatory rhythms, while complete lesions made with radiofrequency current leave anticipatory rhythms largely intact. We tested a hypothesis that the DMH and fibers of passage spared by IBO lesions play a time-of-day dependent role in the expression of food anticipatory rhythms. Rats received intra-DMH microinjections of IBO and activity and body temperature (T(b)) rhythms were recorded by telemetry during ad-lib food access, total food deprivation and scheduled feeding, with food provided for 4-h/day for 20 days in the middle of the light period and then for 20 days late in the dark period. During ad-lib food access, rats with DMH lesions exhibited a lower amplitude and mean level of light-dark entrained activity and T(b) rhythms. During the daytime feeding schedule, all rats exhibited food anticipatory activity and T(b) rhythms that persisted during 2 days without food in constant dark. In some rats with partial or total DMH ablation, the magnitude of the anticipatory rhythm was weak relative to most intact rats. When mealtime was shifted to the late night, the magnitude of the food anticipatory activity rhythms in these cases was restored to levels characteristic of intact rats. These results confirm that rats can anticipate scheduled daytime or nighttime meals without the DMH. Improved anticipation at night suggests a modulatory role for the DMH in the expression of food anticipatory activity rhythms during the daily light period, when nocturnal rodents normally sleep.     

The effect of antidepressant drugs on the ultradian rhythms of the locomotor activity in rats

Abstract

The effect of two antidepressant drugs (+)‐ and (‐)‐oxaprotiline hydrochloride (Ciba‐Geigy, OXA) on the exploration and the basal activity of rats in the light and dark phases of the diurnal cycle was investigated. (+)‐OXA is a selective noradrenaline (NA) uptake inhibitor, while its (‐)‐enantiomer is devoid of such an activity. Male Wistar rats housed individually on a 12:12 h light‐dark schedule (light on: 07.00 h) were treated with (+)‐ or (‐)‐OXA in a dose of 10 mg/kg twice daily, for 14 days. The rats received the last dose at the beginning of the light or dark phase and their movements were registered using Animex actometers for 12 h. The first 30 min of activity was regarded as the exploratory and the further period as the basal activity. In the light phase both (+)‐ and (‐)‐OXA decreased the exploration (80% and 70% of control, resp., p < 0.05) and potentiated it (180% and 190% of control, resp., p < 0.01) in the dark phase. The effect on the ultradian rhythm of the basal activity was phase‐dependent also. (+)‐OXA prolonged the period and did not change mesor, amplitude or acrophase of the rhythm in the light phase, and diminished mesor and amplitude, shifted acrophase and did not change period in the dark phase. (‐)‐OXA did not change parameters of the rhythm in the light phase and shortened period, diminished mesor and shifted acrophase of the rhythm in the dark phase. The results show that both (+)‐ and (‐)‐OXA given in the same dose change the same activity in opposite ways in the light and dark phases of the diurnal cycle. The NA uptake inhibition seems not to be a requisite of the light/dark phase differences.     

The relationship between locomotor activity rhythm and burying behavior in the wrasse,Suezichthys gracilis

The wrasse,Suezichthys gracilis, is a diurnal fish which buries itself in sand during the night-time. The present paper deals with the locomotor activity rhythms ofS. gracilis, examined by using an actograph with infra-red photo-electric switches in a dark room. The fish were kept in eight experimental tanks (each 30l in capacity), with three different bottom conditions: sand (grain size about 1 mm in diameter and 5 cm deep); 1 or 2 stones (about 10cm in diameter) without sand; and transparent acrylic pellets (2 × 2 × 3 mm in size, 5 cm deep). The light intensities were 550–700 lux just above the water surface, decreasing to 21.3% under the acrylic pellets at a water depth of 20cm. The water temperatures were kept at 22.0–25.0°C during the experiments for 7 to 14 days. In the aquarium with bottom sand, diel activity rhythms ofS. gracilis were mostly synchronized to LD (LD12:12; 06:00–18:00 light, 18:00–06:00 dark), free-running activity rhythms continued distinctly under LL (constant illumination), and locomotor activity was greatly suppressed, with disappearance of the activity rhythm, under DD (constant darkness). In the aquarium without sand, locomotor activity ofS. gracilis could be summarized as follows. The fish moved throughout almost the entire period under LD, though more frequent movements were observed in light conditions than in dark ones. Under LL they showed continuous locomotor activity during the experiment, with no obvious periodicity. Under DD the activity of the species was somewhat suppressed, but irregular movement or indistinct periodicity was observed. In the aquarium with transparent acrylic pellets, locomotor activity under LD and DD, respectively, bore a close resemblance to activity patterns under the same light conditions with sand, whilst activity under LL was identical to that under LL without sand. Accordingly, it seems that maintenance of normal activity rhythms in the wrasse was due not only to the darkness, but also to the presence of bottom sand. It therefore seems that the biological clock inS. gracilis is not related to locomotor activity, but to burying behavior.     

Synchronization of motor activity in young pigs to a non-circadian rhythm without affecting food intake and growth

The influence of length of light:dark cycle on motor activity, food intake and growth has been investigated in young pigs subject to either 12 hr light:12 hr dark, or 9 hr light:9 hr dark. Motor activity was positively correlated with the light phase in both groups. No differences were found in growth rate or in the average amount of food eaten in a 72 hr period between the two treatments. Body conformation and composition were also similar. Thus, unlike many other mammals the young pig can synchronize its activity to a non-circadian rhythm. Moreover, this does not affect growth.     

Behavioural studies on the lesser sandeel Ammodytes marinus (Raitt) II. The effect of light intensity on activity

The behaviour of the lesser sandeel, Ammodytes marinus (Raitt), has been investigated at light intensities of 1, 10, 100 and 1000 lux, using a photographic method of recording activity. The level of swimming activity was high at 1000 and 100 lux, declining to a very low level at 1 lux. It was concluded that this was due to the limiting effect of light on feeding. The threshold light intensity for swimming activity in the tank was estimated as being approximately 20 lux but it was considered that in the area of the sandeel fishing grounds the threshold might be higher than this, in the region of 100 lux. The number of hours light per day above 20 and 100 lux at a depth of 15 m in the area of the Outer Dowsing sandbank (53°30'N, 01°00'E) was estimated for the various months of the year. It was shown that during the winter the light intensity does not normally reach 100 lux and only exceeds 20 lux for a few hours each day. It is suggested that this could limit swimming activity and accessibility at this time of year. Measurements were made of the penetration of light into sand and it was concluded that fish which are buried might be able to detect light, possibly via the pineal gland.     

Entrainment of Circadian Wheel-Running Rhythms of the Northern Brown Bandicoot, Isoodon macrourus, by Daily Restricted Feeding Schedules

Northern brown bandicoots (Isoodon macrourus) were subjected to restricted feeding for 3 h in the middle of the light period of a 14: 10 light/dark cycle and immediately following this in constant dark. When feeding was restricted to the middle of the light period of the light/dark cycle, all bandicoots maintained a nocturnal activity rhythm. In addition to the nocturnal rhythm, a few bandicoots showed meal-anticipatory activity during the light period. In bandicoots that did not show meal-anticipatory activity, diurnal activity was sometimes evident either during or shortly after the daily meal time. The observation of meal-anticipatory activity in some bandicoots suggests that this species may have a mechanism separate from the light-entrainable mechanism that allows the daily anticipation of periodically available food sources. In the next stage of the experiment, which was in constant dark, the meal was presented at the same time of day as it had been in the previous stage. In all bandicoots, the previously light-entrained component of activity free-ran and was eventually affected by the restricted feeding schedule to some degree. Bandicoots showed weak entrainment and relative coordination, suggesting that restricted feeding is a weak zeitgeber in this species. Evidence also suggesting that two separate but coupled pacemakers control the activity rhythms of the bandicoot was that (a) bandicoots simultaneously showed free-running light-entrainable rhythms and meal-entrained anticipatory rhythms; (b) in several bandicoots, the light-entrainable rhythm was phase advanced when it free-ran through the meal time; and (c) in one bandicoot, meal-entrained anticipatory activity was forced away from the meal time when the previously light-entrained component of activity free-ran through it.     

Eyeless Mexican Cavefish Save Energy by Eliminating the Circadian Rhythm in Metabolism

The eyed surface form and eyeless cave form of the Mexican tetra Astyanax mexicanus experience stark differences in the daily periodicities of light, food and predation, factors which are likely to have a profound influence on metabolism. We measured the metabolic rate of Pachón cave and surface fish at a fixed swimming speed under light/dark and constant dark photoperiods. In constant darkness surface forms exhibited a circadian rhythm in metabolism with an increase in oxygen demand during the subjective daytime, whereas cave forms did not. The lack of circadian rhythm in metabolism leads to a 27% energy savings for Pachón cave fish compared to surface fish when comparing both forms in their natural photoperiods. When surface forms were tested under constant dark conditions they expended 38% more energy than cave forms under equivalent conditions. Elimination of the circadian rhythm in metabolism may be a general feature of animals that live in perpetually dark food-limited environments such as caves or the deep sea.     

Diurnal rhythm of rat liver mRNAs encoding 3-hydroxy-3-methylglutaryl coenzyme A reductase. Correlation of functional and total mRNA levels with enzyme activity and protein

Rat liver 3-hydroxy-3-methylglutaryl coenzyme A reductase exhibits a diurnal rhythm of activity which coincides with a diurnal rhythm of reductase protein and reductase mRNA levels. This diurnal rhythm of reductase activity, polypeptide mass, and mRNA exists in rats fed a normal diet (unsupplemented rat chow) and in rats fed a diet supplemented with cholestyramine plus or minus mevinolin. Levels of reductase protein were determined by 8 M urea/sodium dodecyl sulfate-polyacrylamide gel electrophoresis and immunoblotting. Reductase mRNA was measured by in vitro translation or blot hybridization of liver RNA. Functional reductase mRNA levels in rats fed a normal diet were approximately 10-fold higher during the middle of the dark cycle than during the middle of the light cycle. Maximum induction of functional reductase mRNA was observed in rats fed cholestyramine and mevinolin. This latter level was 157-fold higher than the level measured at the diurnal low point in rats fed a normal diet. Blot hybridization of liver RNA showed two predominant mRNAs of 4.6 and 4.2 kilobase pairs and a minor species at 6.9 kilobase pairs. These mRNAs exhibited a diurnal rhythm for rats on all three diets and reached peak levels during the 12-h dark period. These data indicate that the diurnal rhythm of reductase mass and activity is closely paralleled by the level of its mRNA.     

The influence of diurnal rhythms of carbohydrate metabolism in adult rat liver on the metabolic characteristics of isolated liver parenchymal cells.

Rats trained to the "8 + 16" controlled feeding cycle where food is only available for the first 8 h of the 12 h dark period exhibit a pronounced diurnal rhythm of hepatic glycogen metabolism. Glycogen is stored within the liver parenchymal cells during the dark period and subsequently mobilized for energy production during the light period. Hepatocytes, isolated by collagenase perfusion, from livers of such animals have differing capacities for glycogen synthesis when incubated with glucose. Cells prepared at the end of the 16 h period without food have very little capacity for synthesis compared with much higher rates obtained in cells obtained during the feeding period. Cells obtained from liver containing a large glycogen concentration produce a net breakdown of glycogen during incubations with glucose, however experiments using radioactively labelled glucose indicate that synthesis does occur in these cells. The changes in the capacity of the cells for glycogen synthesis appear to be due, in part, to changes in the percentage of the cell population involved in synthesis and in the activity of glycogen synthetase a. Attempts of influence the rate of glycogen synthesis at any time of day with insulin or dexamethasone were unsuccessful.     

Effects of endogenous rhythms and light conditions on foraging and predator-avoidance in juvenile plaice

The influences of a light: dark cycle and a persistent endogenous rhythm of activity on foraging (on the bivalve Donax vittatus ) and avoiding a predator (juvenile cod, Gadus morhua ) were investigated in freshly-caught juvenile plaice, Pleuronectes plalessa . Time lapse video recordings were made of fish in the presence and absence of prey and predators in laboratory tanks over 24-hour periods between the times of successive daytime low waters. Endogenous rhythms of activity were seen in all experimental treatments. Swimming both close to the bottom and in the water column showed a strong circatidal rhythm, with most activity 2 to 3 h after the predicted time of high water. Swimming in the water column was more frequent at night than by day. In the presence of a population of Donax , whose siphon tips could be eaten as food, swimming close to the bottom became more frequent. This increase in benthic swimming was independent of the endogenous cycle of activity and was correlated with the frequency of attacks on siphons. The presence of the cod predator delayed the onset of foraging activity, producing a foraging/predator avoidance trade-off. The independence of foraging from light and endogenous rhythms suggests that this trade-off may be similarly independent. The cod also greatly reduced swimming in the water column in darkness, behaviour apparently unrelated to foraging.     

Energetics and metabolic correlates of starvation in juvenile perch (Perca fluviatilis)

Long-term measurements of the diurnal pattern of oxygen consumption were conducted in fasting juvenile perch at 15 and at 20° C. In addition, dry body mass, protein and glycogen concentrations and the activity of two key enzymes of energy metabolism, phosphofructokinase and glutamate pyruvate transaminase, were monitored during the period of food deprivation. The average rate of oxygen consumption decreased during the starvation period, but the regular diurnal pattern of low rates in the dark and high rates in the light was upset by a break around days 7 to 8 at both temperatures. This break coincided with the exhaustion of the glycogen reserves in the muscles and in the liver, indicating that switching to a new energetic fuel was accompanied by a change in the pattern of swimming activity. Choice of the major energy source after exhaustion of the carbohydrate store was substantially influenced by water temperature. A negative correlation was found between the scope for spontaneous activity and the specific rate of oxygen consumption in the dark phase suggesting that the resting rate of metabolism responded more strongly to food deprivation than the rate of spontaneous activity in the light phase.     

Temperature and light effects on the circadian rhythm and locomotory activity of the plains garter snake (Thamnophis radix hayendi)

Abstract

The Locomotory activity of the Plains Garter snake was determined under L/D: 12/12 conditions at five constant temperatures and three light intensities during the light period. The snakes were diurnal at low temperatures with nocturnal activity increasing in various amounts at higher temperatures. The different light intensities had relatively small effects on the activity rhythm.

Activity was recorded under four constant light conditions at five constant temperatures and the characteristics of the free‐running rhythm measured. A comparison of the characteristics of the free‐running rhythm to Aschoff's circadian rule indicates that this snake is an exception to this rule.

Increase light intensity decreased total activity under all conditions. Under a L/D: 12/12 cycle the decrease in activity was more pronounced during the dark period than the light period.

It is suggested that crepuscular or nocturnal activity shown by snakes at high temperatures may be an effect the temperature level has on the biological clock and activity controlling mechanisms rather than temperature selection by the snake.     

Diel patterns in the habitat utilisation of sandeels revealed using integrated acoustic surveys

Tracking the movements of sandeels in relation to their habitat will provide an improved understanding of sandeel ecology, including their interrelationships with predators and fishing activity. We examined spatial and temporal changes in the behaviour and distribution of the lesser sandeel Ammodytes marinus by integrating the acoustic ground discrimination system QTC VIEW with a Simrad EK500 fisheries scientific echosounder. QTC VIEW was used to identify acoustic changes in the properties of the seabed in the presence of buried sandeels, whilst the EK500 simultaneously recorded temporal changes in their distribution throughout the water column. Our results suggest that high densities of sandeels buried in sediment give a different acoustic signal to that of its surroundings. This integrated approach showed that sandeels had a diurnal activity pattern that was strongly, although not exclusively, associated with day length. Using this integrated survey method will enable large-scale cost-effective surveys of sandeel behaviour, distribution and abundance to be conducted.