Rapp. P.-v. Réun. Cons. int. Explor. Mer, 191: 400-408. 1989 The role of barosensitivity in the control of migrations of larval and juvenile sole (Solea solea L.): influence of pressure variations on swimming activity and orientation

C. Macquart-Moulin, C. Castelbon, G. Champalbert, D. Chikhi, L. Le Direach-Boursier, and G. Patriti

Macquart-Moulin, C., Castlebon, C., Champalbert, G., Chikhi, D., Le Direach- Boursier, L., and Patriti, G. 1989. The role of barosensitivity in the control of migrations of larval and juvenile sole (Solea solea (L.)): influence of pressure variations on swimming activity and orientation. - Rapp. P.-v. Réun. Cons. int. Explor. Mer, 191: 400-408.

Pressure variations from 0.5 to 50% of the reference pressure (0-1500 mb) were applied in total darkness suddenly or in cycles varying in period from 4 sec to more than 12 h. In juveniles, swimming activity and the amount of upward swimming increased during pressure decreases (sudden or progressive), during cyclic pressure variations simulating tide effects, and also during cyclic variations of low amplitude and very short period simulating wave effects in shallow areas. Larvae and juveniles reacted in the opposite sense from juveniles when they were subjected to sudden pressure variations, but reacted in the same sense when they were subjected to cyclic variations simulating waves.

C. Macquart-Moulin, C. Castelbon, G. Champalbert, D. Chikhi, L. Le Direach- Boursier, and G. Patriti: Centre d’Océanologies de Marseille, Faculté des Sciences de Luminy, Case 901, F-13288 Marseille Cédex 9, France.

Introduction In benthic or hyperbenthic animals whose behaviour is not very different from that of the sole after meta­ This paper summarizes the first results of a study sup­ morphosis, barosensitivity may be involved in the con­ ported by a French national programme on the recruit­ trol of several kind of movements, especially in the ment of some marine species including the sole, Solea intertidal zone and in estuaries. These are: solea (L.). In the sea, young sole are subjected to different kinds of hydrostatic pressure changes: (1) cyc­ 1. Movements due to waves if animals are sensitive to lic and progressive pressure changes caused by the tidal small and sudden pressure changes. Waves at the sea cycle, during which the amplitude does not exceed one surface induce pressure variations on the bottom. bar; (2) cyclic pressure changes of short period and The depth range influenced by these variations small amplitude caused by waves in shallow waters; (3) depends on wave amplitude and wave length. sudden changes related to vertical migration during 2. Ebb transport when a pressure decrease induces pelagic swimming and (4) changes caused by animal increased swimming activity. movements. 3. Flood transport when a pressure increase induces During the last decades, several studies have shown active swimming. the great sensitivity of several species of aquatic animals 4. Tidal swimming in all directions for species stimu­ to small hydrostatic pressure variations (Hardy and lated during pressure increase or decrease. Bainbridge, 1951; Enright, 1962; Qasim et al., 1963; Rice, 1964; Morgan, 1972; Blaxter, 1978). The most Many authors such as Dijkgraaf (1942), Qasim et al. frequent reaction in planktonic animals, including soleid (1963), Rice (1964), McCutcheon (1966), Blaxter and larvae, is an upward movement when the pressure is Tytler (1972), Gibson (1982) have studied pressure sen­ increasing and a downward movement (active or not) sitivity of fish including pleuronectiforms (especially when the pressure is decreasing. These two reactions plaice and dab). Adults or larvae with a swimbladder may regulate the depth at which the animals swim. can be particularly barosensitive: thus, a pressure

400 increase of 5-10 mb induces upward swimming in Blen- Material and methods nius pholis larvae (Qasim et al., 1963) and different behavioural or physiological responses were observed In order to determine changes in behaviour occurring for variations of similar amplitude (0.5-1%) in several during development, experiments were carried out on fishes such as cod, haddock, minnow, trout, and gold­ 3-5 mm larvae and juveniles of different stages (1- fish. The barosensitivity of adults or larvae without a 4 cm). Most animals came from a hatchery on the French swimbladder (most pleuronectiforms) is known to be Atlantic coast at Brest, but a few were caught at night smaller, nevertheless Pholis gunnelus larvae react to in the Mediterranean plankton. They were maintained pressure increase of 25 mb and the dab exhibits a cardiac in the laboratory at constant temperature (14°C) under response for a A p/p less than 1%; that means a sen­ atmospheric pressure and exposed to a natural light sitivity similar to the sensitivity of fish with swimbladders cycle. Each day, but at different times, they were fed (Blaxter and Tytler, 1972). on Artemia nauplii. For each experimental set, 80 larvae This study is an attempt to establish the effects of or 10-15 juveniles were used. Animals were not fed these different kinds of pressure changes on swimming during the experiments. activity, orientation, and migratory processes of larval Special actographs were built for this study. Each and juvenile sole. Most experiments deal with pressure consisted of a dark temperature-controlled chamber cycles whose amplitude and period are within the range inside which was a cylindrical tank (50 cm in height, normally encountered in the sea, such as variations 14 cm in diameter) fitted with two sets of three photo­ induced by waves or tides, but some experiments with electric infra-red barriers mounted on a circular frame sudden pressure changes were carried out. (Fig. 1). The bottom of the tank was covered with a 2- 4 cm layer of sand.

relating arm

experimental chamber

Mercury Reservoir

14 cm — insulating wa

W a t e r

Membrane

Figure 1. Actograph and pressure device: cyclic pressure changes inside the experimental tank are produced by monitoring a mercury reservoir attached to a rotating-arm set in action by a motor.

401 The device producing pressure variations was adapted fidence interval (at 95 or 99%) of the regression line from Morgan’s (Morgan et al., 1964) and Gibson’s calculated with the points of a new spectrum set with a (1982) apparatus. It consisted of a mercury reservoir similar method after randomization of these same data. connected to the experimental tank by means of a silicon pipe and a device with a membrane insulating the tank Results water from the water in contact with the mercury. The mercury reservoir was attached to a rotating arm driven In total darkness, larvae and juveniles exhibit an by an electric motor that was completely isolated from endogenous circadian rhythm of swimming activity, the actograph chamber. The amplitude of the pressure maximum activity occurring in the evening and mini­ changes could be adjusted by changing the position of mum in the morning (Champalbert and Castelbon, the attachment point on the rotating arm. 1989). Two kinds of motor were used: a variable fast speed motor giving periodic variations similar to those of Sudden variations waves (from 2 to 15 sec), and a constant speed motor giving 12 h periodic cycles, equivalent to tidal cycles. Larvae Movements of fish broke the light beams and the num­ Since light had little effect on the vertical movements ber of interruptions was recorded per unit time on a of the young sole under experimentation, direct obser­ printing counter. These counts were used as a measure vation of behaviour was made. When pressure was of swimming activity. Movements were recorded in increased to 100 mb in larvae 3, 9, and 13-d-old (i.e. 3- total darkness in order to eliminate possible interactions 5 mm) an immediate increase in the amount of upward between reactions to pressure and light. Some experi­ swimming was observed. This effect stopped as soon ments were carried out in total darkness and without as the pressure change ceased. After every pressure pressure variations in order to determine the circadian decrease there was a passive sinking toward the bottom. rhythm and the timing of peaks of activity. The acto­ These short-term responses were visible to the naked graph only records activity near the surface and bottom eye but were not obvious on the actograms. of the tanks. The analysis of rhythmic movements and the deter­ Juveniles mination of the period of the oscillatory components After metamorphosis, direct observation becomes dif­ was that adapted by Williams and Naylor (1978) and ficult because light influences juvenile behaviour Macquart-Moulin and Castelbon (1983) from Enright’s (Champalbert and Castelbon, 1989). Nevertheless, in periodogram method (1965). The periodogram rep­ the youngest stages subjected to sudden pressure resents the amplitude spectrum of relative variability or changes, a few brief reactions were sometimes observed, “variation coefficient” (standard deviation divided by because their duration was long enough to appear on the mean) of the means calculated on data arranged the actograms. In very young juvenile stages, (about according to the Buys-Ballot table. The periodogram 10 mm), both increase and decrease of pressure induced significance was tested with the upper limit of the con­ intense swimming activity (Fig. 2). The threshold of this

mb 2000-n

1500_

1000-

T i m e of d a y

Figure 2. Juveniles 10 mm long: activity (interruptions of infra-red beam as a function of time) at the surface of 8 animals subjected to successive pressure increases and decreases. Reference pressure = 1 atm + 500 mb; Ap = 100 mb.

402 mb 210«-.

1500 -

1 0 0 0 -

2 0 0 - Figure 3. Juveniles 14 mm long: activity (interruptions of infra-red beam as a function of time) at the surface of 10 animals subjected to successive pressure 0- increases and decreases. Reference pressure = 1 atm; Ap = 250 mb, 500 mb, 1000 mb, 1500 mb. Time ol day reaction was about 7% of the reference pressure. Later in older juveniles (15 mm) upward swimming occurred mainly after a pressure decrease and lasted during the low pressure periods. Conversely, activity was very low 12 18 0 6 12 h during the high pressure periods (Fig. 3). M ' HI ! 1 $ Cyclic variations of short period and low R am plitude ITT" " ~ H " ~ T* 7 r In most of our experiments, the period of cyclic changes r i* i 1 was 6 sec and the amplitude (Ap/2) 30 mb for a ref­ i j 1 i erence pressure of 1500 mb (1 atm + 500 mb). Never­ n; --pr s theless, different periods and amplitudes were also -r 1 T~K HIT‘ S tested. S sI n 1 i i i i 1 I 1 1 1 Larvae 1 1 Two experiments were carried out on 9- and 14-d-old d a sole, 4 and 6 mm respectively; ±25 mb variations were 1 T r ï ï ï t applied over a 6 sec period, for 2 h, 3 times every 24 h. i 1 1 1 In both experiments, increased swimming activity at the 1 surface was observed during most periods of pressure variation (Fig. 4). i h ! s 1 m f i r Juveniles Time sf day Seven experiments lasting about 7 d each were per­ Figure 4. Sole larvae 4 mm long (9-d-old): activity (inter­ formed. In each experiment, pressure cycles were ruptions of infra-red beam as a function of time) at the surface applied twice a day: once during the activity phase of of 80 larvae subjected to cyclic pressure changes during 4 d. the circadian rhythm, between 2300 h and 0100 h, and Top: frames indicate pressure changes (period: 6 sec; ampli­ once during the rest phase (between 1100 h and 1300 h). tude: ±25 mb) applied for 2h , three times a day (1500 to 1700 h, 2300 to 0100 h, 0700 to 0900 h). Reference pressure = Regardless of the origin and the age of the animals and 1 atm. + 500 mb. R = Ac/A v where Ac: Hourly activity during the time of the day, the activity at the surface increased the 2 h preceding the cyclic variations. A v: Hourly activity during the pressure cycles. Upward swimming often during the 2 h of cyclic variations. occurred as soon as the pressure was applied but often R = Day 1:0.54 a maximum response took place after 20-30 min (Fig. = Day 2:0.62 5). Sometimes the aggregation of animals near the sur­ = Day 3:0.74 face was more progressive and maximum density was = Day 4:0.71

403 1500 1500 ±35111 1 5 0 0

4 5 0

12 13 14 hours Time of day

Figure 5. Juvenile sole 14 mm long: activity (interruption of infra-red beam as a function of time) at the surface of 8 juveniles subjected during 2 h (top frame) to cyclic pressure variations (period: 6 sec; amplitude: 35 mb). Reference press­ ure = 1 atm + 500 mb. reached more than one hour after the pressure changes had started and even after they had stopped. Generally, pressure variation cycles induced periodic phases of increased activity re-occurring always at the same time. Sometimes the phase of the endogenous rhythm shifted slightly (Fig. 6). When animals were subjected to press­ ure cycles much longer than 2 h, the response decreased 3 or 4 h after the onset of the pressure changes and the activity level returned to the value determined by the 0 * circadian rhythm. Y S The amplitude change necessary to induce an increase Time ef day in activity varied according to time. During the activity phase, the extent of variation may be particularly low Figure 6. Juvenile sole 11 mm long: activity at the surface of 10 juveniles subjected for 6 consecutive d to cyclic pressure (amplitude of 10 mb, about 1% of the reference press­ changes whose period was 6 sec and amplitude 25 mb. Pressure ure) (Fig. 7). At the end of the experiment, the reduced variations were applied for 2h, twice a day (from 1100 to effectiveness of lower amplitude variations could 1300 h and from 2300 to 0100 h). (In contrast to the activity depend on the effect of previous treatment. Whatever peaks induced by pressure cycles, the peak occurring in the the time, juveniles always reacted to variations up to late afternoon, which is controlled by the circadian rhythm, shifts to the evening during the experiment.) Reference press­ 4%. Up to the present, different periods have been ure = 1 atm + 500 mb. top: Frames indicate the hours of cyclic tried (between 4 and 12 sec) and in all cases, for a 3% pressure changes. variation, typical reactions have been observed. R (see legend to Fig. 4) = 0.21 (whole experiment) = 0.33 (23.00-01.00 h variations) = 0.07 (11.00-13.00 h variations) Cyclic variations of large period and high am plitude The effects of pressure cycles whose period was 12 h Ap/2 = 300 mb and Fig. 9: Ap/2 = 400 mb). For an (about tidal period) and whose amplitude ranged from amplitude of 160 mb, the effect of pressure change only 160 to 500 mb above atmospheric pressure were appeared during the activity phase. Smaller changes in observed in 15 experiments carried out on juveniles. amplitude were not tried. One or two cycles a day were applied to the animals. Experiments with one variation cycle a day (Fig. 10) Experiments with two pressure cycles each day Four experiments were carried out with a single daily The experiments showed that the increase in the amount pressure cycle: two with maxima at noon and two with of upward swimming was always much greater when the maxima at midnight. Note that a peak of activity was pressure was decreased during the hours of maximum observed without any pressure change 12 h after the activity between 1500-2100 h and 2100-0300 h than vice- peak induced by the pressure decrease. The peri­ versa between 0300-0900 h and 0900-1500 (see Fig. 8: odogram analysis (Fig. 10) clearly shows that the peak

404 Discussion

1 50 0 ± 3 0 mb [ 9 0 0 Very little information on the barosensitivity of juvenile or adult sole was available before this study, but several reports describe the behaviour of another flatfish, the plaice Pleuronectes platessa (Qasim et al., 1963; Rice, 1964; Gibson, 1982). When plaice larvae are subjected to sudden pressure changes of about one bar they exhibit reactions to gravity very similar to those observed in sole T L H tiZ hz larvae; nevertheless, after metamorphosis, the juveniles do not swim up after a pressure increase. In addition, the influence of progressive and cyclic TfKTTÏÏI variations whose period varied from 2 to 12.6 h was studied by Gibson (1982) in young plaice about 5-8 cm long (in horizontal tanks). For a pressure range of 100 mb or more, activity increased when pressure was IhlT jl: decreased; for a smaller range (25 mb) the increase of activity was obvious only when the period was short, i.e. the speed of pressure change was high. Roper (1979, cited by Gibson, 1982) found similar results in two Rhombosoleidae Peltorhampus latus and Rhombosolea tapirina for cyclic variations whose period was 10 h and amplitude 1.35 m. The finding of similar behaviour in juvenile sole show that responses to cyclic pressure variations may be wide­ ± 5 spread in pleuronectiforms. We did not measure accurately the threshold for i É-^j-LjTTfrLd-rT^rh^lrb upward swimming reactions. Nevertheless, for a 12 h Ii -Tv. D ili l I' period of pressure cycles, an amplitude smaller than I r 160 mb (reference pressure 1500 mb) seems to be suf­ ficient to induce the reaction. Thus, tides, especially 8 y^K m rrrB III fk lK l near the coast of Brittany seem to be great enough to Time o I day induce a general increase in activity near the bottom during the ebb and an increase in upward swimming. Figure 7. Juvenile sole 15 mm long: activity at the surface of 7 juveniles subjected for 8 days to cyclic pressure variations, The surface cannot be reached during the day because period: 6 sec; amplitude variable. The stimulus of variations of light effects (unpublished data). was applied twice a day from 1100 to 1300 h and 2300 to 0100 h . According to our results, one can assume that an Reference pressure = 1 atm + 500 mb. Top: Frames indicate endogenous circatidal rhythm could maintain this swim­ the hours of cyclic pressure changes. ming activity. Such a rhythm has been shown to exist R (see legend to Fig. 4) = 0.29 (Ap = ±30 mb) = 0.43 (Ap = ±20 mb) in several intertidal fish, including pleuronectiforms = 0.94 (Ap = ±10 mb) (Gibson, 1976). In plaice this rhythm is very probably = 0.91 (Ap = ±5 mb) synchronized by pressure variations related to tides (Gibson, 1973, 1982, 1984). of activity observed without any pressure change Whatever its origin, either a response to pressure appears 12 h after the peak induced by the pressure decrease or a circatidal rhythm, or a combination of the change and the timing of this activity is different from two, the increased swimming of juveniles is always the timing of the endogenous circadian rhythm.. This strongly controlled by the circadian rhythm. Experi­ peak indicates the probable existence of an endogenous ments carried out on the effects of cyclic variations of rhythm with a spontaneous circatidal period. This large period and high amplitude, imposed twice a day, rhythm may be synchronized by a single tidal cycle and show that barosensitivity decreases during the rest phase may remain unexpressed in juveniles coming from the of the circadian rhythm. In the sea, behavioural changes hatchery or Mediterranean Sea where tidal changes are related to pressure decreases during the ebb would vary negligible. greatly in intensity according to the time of the day. Experiments in constant conditions on animals pre­ The main purpose of our study is to emphasize the viously subjected to cyclic pressure variations should influence of pressure cycles of short period and small be carried out to confirm the existence of a circatidal amplitude on larval and juvenile sole. Quite a few rhythm. published investigations have been carried out in order

405 m b 200 0 mb 2 0 0 0 P = I a i m 1 4 0 0 1 5 0 0

f f l Time of day Time ol day Time o I day a b C Figure 8. Juvenile sole 15 mm long: three simultaneous experiments, a and c: Activity at the surface of 7 juveniles subjected to hydrostatic pressure cycle with a period of 12 h. b: Activity at the surface of juveniles subjected to a constant pressure. to assess the possible effect of pressure changes similar According to theoretical calculations (Draper, 1957; to those induced by waves in shallow areas. The exist­ Draper and Maxted, 1966) the pressure changes we ence of a short geonegative reaction was observed in an imposed on juvenile sole were within the normal range amphipod (Synchelidium sp.) by Enright (1962) for of those occurring 10 m down when waves are present rapid variations of very low amplitude. The pycnogonid at the surface. An amplitude of ±20 mb is experienced Nymphon gracile starts a geonegative reaction every 5 m down for waves of 60 cm height when the period time pressure is increased during cycles whose period is is 6 sec; when the period is higher (8 sec), the same 6 sec and amplitude 2 5 ^ 0 mb (Morgan et al., 1964). amplitude is experienced 10 m down. The possible effect of pressure variations induced by It is difficult to consider the stimulating and orien­ waves in benthic fishes was discussed by Blaxter and tating effect of the pressure variations, without taking Tytler (1972). Because of the sensitivity of some fish to into account the effect of other external factors such sudden changes in pressure, these authors assumed that as light, current and salinity. It has been emphasized waves of large period could have an effect in shallow (Gibson, 1975, 1976, 1984) that the increase in swim­ waters. Our results seem to reinforce such a hypothesis ming intensity during the ebb has an adaptive value in strongly since the increase in swimming activity was preventing bottom-living animals becoming stranded. obtained for a range of variations of 1% of the reference In an estuary, if this activity is accompanied by a positive pressure applied cyclically and gradually. rheotaxis the result may be an upstream movement

1400 1 4 0 0 0 0 « 800 C T I V 1 T y

T i m e ol d a y T i m e of d a y T i m e ol d a y

Figure 9. Juvenile sole 30 mm long: three simultaneous experiments, a and c: Activity at the surface of 7 juveniles subjected to hydrostatic pressure cycle with a period of 12 h. b: Activity at the surface of juveniles subjected to a constant pressure.

406 .1 2 12 h i ni 20 50 m b 205 0

1450 1450 i p4o{ 1 i 360 L T I I i f k L n h _TI r t H fh m-H- - T U r, J " i i i Ttrfl' JVrlTh r T Thi 1 1 1

Figure 10. Juvenile sole 11 mm j h t JI J" K fl i "h h irfh j r r il i 1 long. Top a. b: Activity at the 1 surface of two groups of 7 1 juveniles daily submitted to a S 4 A i l . j i >i M L ' r f^ r T rLrr-rTl single pressure cycle (period: Time ol day Time of day 12 h; amplitude: (Ap/2 300 mb). a Bottom: CV: variation coefficient; circle: periodogram CV CV derived from original data; cross: periodogram derived after randomization of the data; A: ..A regression line calculated with randomized data; B: upper confidence limit at 95 and 99% of this regression line. The 12 h peak indicates circatidal rhythm: the 24 h peak shows the persistence of the circadian rhythm of activity.

instead of a downstream movement. On the bottom, Enright, J. T. 1965. The search for rhythmicity in biological if a pressure decrease induces increased activity and, time series. J. Theor. Biol., 9: 426-468. conversely, if a pressure increase inhibits activity, move­ Gibson, R. N. 1973. Tidal and circadian activity rhythms in juvenile plaice, Pleuronectes platessa. Mar. Biol., 22: 379- ment toward shallow water will be enhanced and move­ 386. ment toward deep water will be reduced. Nocturnal Gibson, R. N. 1975. A comparison of fields and laboratory swimming activity of young benthic stages should activity patterns of juvenile plaice. In Ninth European Mar­ increase during the ebb and decrease during the flow. ine Biology Symposium, pp. 13-28. Ed. by H. Barnes. Aberdeen University Press, Aberdeen, Scotland. Thus, according to the time of the ebbs, the daily Gibson, R. N. 1976. Comparative studies on the rhythms number of pelagic phases will change regularly. The of juvenile flatfish. In Biological rhythms in the marine stimulating effect of pressure variations induced by environment. Ed. by J. De Coursey. University of South waves should result in the accumulation of larvae and Carolina Press, Columbia. juveniles in calm and sheltered waters. Gibson, R. N. 1982. The effect of hydrostatic pressure cycles on the activity of young plaice Pleuronectes platessa. J. Mar. Biol. Ass. UK, 62: 621-635. References Gibson, R. N. 1984. Hydrostatic pressure and the rhythmic behaviour of intertidal marine fishes. Trans. Am. Fish. Soc., Blaxter, J. H. S. 1978. Baroreception. In Sensory ecology, pp. 113: 479-483. 375-409. Ed. by M. A. Ali. Plenum Press, New York. Hardy, A. C., and Bainbridge, R. 1951. Effects of pressure on Blaxter, J. H. S., and Tytler, P. 1972. Pressure discrimination the behaviour of decapod larvae. Nature, 168: 327-328. in teleost fish. Symposia Soc. Exper. Biol., 26: 417-443. Knight Jones, E. W., and Morgan, E. 1966. Responses of Champalbert, G., and Castelbon, C. 1989. Swimming activity marine animals to changes in hydrostatic pressure. Oce­ in Solea vulgaris (Q) juveniles. Mar. Behav. Physiol., 14: anogr. Mar. Biol. Ann. Rev., 4: 267-299. 201-209. Macquart-Moulin, C., and Castelbon, C. 1983. Périodicité Dijkgraaf, S. 1942. Über Druckwahrnehmung bei Fishen. Z. circadienne spontanée chez les jeunes Nebalia bipes (Fabri- vergl. Physiol., 30: 39-66. cius) (Crustacea:Phyllocarida). Induction et synchronisation Draper. L. 1957. L’atténuation de la houle en fonction de la intiale du rythme endogène d’activité. J. Exp. Mar. Biol. profondeur. La Houille Blanche, 6: 1-6. Ecol., 70: 1-20. Draper, L., and Maxted, A. V. 1966. Graphs of attenuation McCutcheon, F. H. 1966. Pressure sensitivity reflexes and of waves with depth. Natl. Inst. Oceanogr. Rep., pp. 1-2, buoyancy responses of teleosts. Anim. Behav., 14: 204-217. 12 graphs. Morgan, E. 1972. The pressure sensitivity of marine invert­ Enright, J. T. 1962. Responses of an amphipod to pressure ebrate - a resumé after 25 years. Proc. Roy. Soc. Edin. B., changes. Comp. Biochem. Physiol., 7: 131-145. 73: 287-299.

407 Morgan, E.. Nelson Smith A., and Knight Jones, E. W. 1964. Rice, A. L. 1964. Observations on the effects of changes Responses of Nymphon gracile (Pycnogonida) to pressure of hydrostatic pressure on the behaviour of some marine cycles of tidal frequency. J. Exp. Biol., 41: 825-836. animals. J. Mar. Biol. Ass. UK, 44: 163-175. Qasim, S. Z., Rice, A. L., and Knight Jones, E. W. 1963. Williams, B. G., and Naylor, E. 1978. A procedure for the Sensitivity to pressure changes in teleost lacking swim- assessment of significance of rhythmicity in time-series data. bladders. J. Mar. Biol. Ass. India, 5: 289-293. Int. J. Chronobiol., 5: 435-444.

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