Ontogenetic changes in the daily rhythms of ...

Ontogenetic changes in the daily rhythms of swimming activity and of vertical distribution in juvenile pink salmon (Oncorhynchusgorbuscha Walbaum)' JEAN-GUY J. GODIN*

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Department ofZoology, University ofBritish Columbia, Vancouver, B.C., Canada V6T2A9 Received September 4, 1979

GODIN,J.-G. J . 1980. Ontogenetic changes in the daily rhythms of swimming activity and of vertical distribution in juvenile pink salmon (Oncorhynchus gorbuscha Walbaum). Can. J. Zool. 58: 745-753. Pink salmon fry exhibited, on the average, an irregular daily pattern of swimming activity, and swam near the water surface at night (nocturnal rhythm of vertical distribution) during the 1st week after gravel emergence. The nocturnal rhythm of vertical distribution indicated a relative negative response of the fry to high light intensities. A shift from an irregular pattern t o a diurnal rhythm of swimming activity occurred 7 to 13 days after emergence. Coincident with this shift was an increasing tendency of the fry to swim in the upper half of the water column during daylight. This suggested a gradual weakening of the fry's negative phototactic response during the 2nd week. Thereafter, daily rhythms of swimming activity were diurnal, whereas rhythms of vertical distribution remained nocturnal. Periodogram analysis revealed that these behavioural rhythms were synchronized strongly with the artificial, daily light-dark cycle. The onset of light appeared to synchronize the diurnal swimming activity rhythms, whereas the onset of darkness synchronized the nocturnal patterns of fish rising toward the water surface. GODIN,J.-G. J. 1980. Ontogenetic changes in the daily rhythms of swimming activity and of vertical distribution in juvenile pink salmon (Oncorhynchus gorbuscha Walbaum). Can. J . Z001.58: 745-753. Dcs alevins de saurnons roses ant une activitd locomotrice sans pattern difini el ils nagent prks de la surface de I'eaw la nuir (rythrne nocturne de distribution venicale) duranl la premitre semaine qui suit leur sortie du gravier. Le rythrne nocturne de distribution venicale indique que les alevins ont une rkaction ntgative ila lurnitrc d'intensite elevee. S e p a 13 jours aprirs I'ernergence. le cycle irrigulier de I'activiti est rernplack par une rythrne diurne d'activite de naEe. On peut observer en mOme temps que Ics atevinsont de plus en plus tendance a nagerdans la rnuitic sup&riturede la colunne d'cau durant te jour. Ce phenomkne s'cxplique sans doute par I'inhibi~iongraduelle de la riaction negative a la lurnikredurao t la deuxikme sernaine. Par la suite, les ryrhrnes d'aetiviti son1 diurnes. alurs que leu rythrnes de distriburion verticale derneurent nocturnes. L'analyse de periodogrammes a revile que ces rythmes dans le comportement sont etro~tementlies au cycle artificiel quotidien de lumitre et d'obscurite. L'apparition de la lumikre semble synchroniser le rythme diurne d'activite. alors que I'apparition de I'obscurite semble synchroniser les patterns nocturnes de distribution verticale au cours desquels les poissons nagent vers la surface. [Traduit par le journal]

Introduction Emergence of pink salmon (Oncorhvnchiis gorhuschn Walbaum) fry from gravel nests and their subsequent seaward migration are mainly nocturnal (Godin 1980). Migrant fry may reach the estuary during the same night of their gravel emergence in relatively small coastal rivers (McDonald 1964); Neave 1966; Bakshtanskii 1970). However, the duration of this downstream migration is likely proportional to the distance of riverine grave1 nests from the estuary. In general. the majority of mi-

grant fry enter estuaries in British Columbia from March until May (Neave 1966; Vernon 1966). They remain in nearshore areas of estuaries and adjacent coastal waters through their first spring and part of that summer before migrating further offshore into the open ocean (Parker 1962; Neave 1966). During this coastal phase the fry school and feed during daylight hours (Neave 1966; Healey 1967; Godin 1979). Little is known about the daily pattern of swimming activity of pink salmon fry in seawater. The schooling and feeding of wild fry during the day ' T h i s paper is dedicated to Dr. William S, Hoar on the occasuggest that they have a corresponding diurnal sion of his official retirement Dom the Department of Zootogy at rhythm of swimming activity. Therefore, I the University of Brit~shColumbia. Vancouver. 'Resent address: Depm-tmenr of Zoulogy, The Univcrsity of hypothesized that the fry shift their nocturnal acWestern Onrario. h d o n , Ont.. Canada N6A -m7. tivity rhythm, characteristic of downstream mi0008-4301/80/050745-09$01.W/O a 1 9 8 0 National Research Council of CanadaIConseil national de recherches du Canada

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CAN. J . ZOOL. VOL. 58. 1980

False bottom

/

FIG. 1. Oblique view of the experimental tank showing the observation section, delimited by a baftle and a screen at opposite ends. Dotted lines were drawn with a grease pencil on the front viewing glass and the back wall as aids in recording behaviour. See text for further details.

grants, to a diurnal rhythm in their new marine against which the small fry could be easily seen under dim (21x) habitat. This hypothesis was tested by examining night illumination. The tank had a false, perforated, Plexiglas bottom. No substrate shelter was provided in this tank because ontogenetic changes in the daily (diel) rhythms of pink salmon fry are pelagic schooling fish, and they are not swimming activity and of vertical distribution in a known to commonly seek shelter when undisturbed in estuaries water column in newly emerged pink salmon fry and adjacent coastal waters. Seawater, filtered to 5 pm, entered the tank through a manifold, located at one end of the tank, at a under laboratory conditions.

rate of about 1L min-I. A perforated sheet of Plexiglas, acting as a baftle, reduced any water current at the surface. At the other end of the tank, a standpipe, isolated from the rest of the tank by Fish and holding conditions a plastic screen, regulated the water level at 42cm. The top of Fry used in this study emerged from simulated redd No. 3 in the tank was covered with clear nylon mesh screening to prevent Godin (1980) during the night of 15-16 February 1977. One fish from escaping. The observation compartment of the tank hundred and thirty eight (half) sibling fry emerged that night. was divided vertically into three equal sections by lines drawn at Except for six individuals, the fish were placed in an enclosed intervals of 26cm on the front viewing glass and on the back 484-L fiberglass holding tank as they emerged. This tank had wall, and was also divided horizontally by a line into halves of running seawater of ambient temperature. Seawater was 19cm in height each. pumped from a depth of 21 m in nearby Departure Bay, and The tank was exposed to a 12 h L: 12 h D (430:2 ix) cycle withpassed through the sand filters before entering the tank. Water out twilight periods. Lights-on and lights-off occurred at 0800 temperature did not vary more than +_ 1°C from experimental and 2000 hours, respectively. Overhead illumination was incantemperatures (see below). An interval timer regulated a Light- descent. Water temperature was recorded continuously at the -dark (LD) cycle of 12h of light (6001x, measured at the water inlet with a thennograph. Experimental temperatures were regsurface) alternating with 12h of dark (llx) without twilight ulated near 9 . f C (Table 1) by mixing water of different temperperiods. "Lights-on" and "lights-off' occurred at OsOOand 2000 atures. Differences between daily maximum and minimum temhours, respectively. Overhead illumination was incandescent. peratures never exceeded TC, and usually were less than 1°C. Fish were fed ad libitum with a mixture of small pieces of frozen Water salinity rangedfrom 25.8 to 26.Wm, anddissolved oxygen zooplankton, liver, and Oregon Moist Pellets, a prepared fish in the water always exceeded 91% of air saturation. The experifood, five to eight times daily. Feeding times were randomized mental illumination cycle and temperatures used are commonly every day. experienced by wild fry inhabiting coastal waters in British Columbia. Experimental tank The experimental tank was a 190-L glass aquarium (Fig. 1) Experimental procedure Six different groups of six sibling fry each were removed with a slate bottom, and lined on three sides with white polyethylene plastic. This plastic served as a background sequentially without known bias from the holding tank, intro-

Materials and methods

TABLE 1. Experiments conducted sequentially o n six groups of six pink salmon fry each a t different times after emergence from gravel. Water temperature, total length, and wet weight of fish are given for each experiment

Group number

Dates of experiments (1977)

Days after emergence

1 2 3 4 5 6

Feb. 16-21 Feb. 22-27 Feb. 28-Mar. 5 Mar. 6-1 1 Mar. 14-19 Mar. 20-25

1-5 7-1 1 13-17 19-23 27-3 1 33-37

+

"C

Mean k S D total length, mm

Mean SD wet weight, mg

9.6k0.7 9.5k0.4 9.6k0.5 9.4k0.6 9.5k0.4 9.650.4

36.2k0.2 36.0k1.3 38.5k0.5 36.4k0.7 42.7k0.9 44.0k1.7

253+5 246k 16 301 k 20 362k33 435 f 34 456k47

Mean f S D temperature,

-

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duced separately in the experimental tank. and observed in tendem over $-day ~ r i o d sduring the first 37 days after emergence (Table 3). Each of the six experimental groups was comprised of different Fry which ware discarded at the end of t h e ~ rrespective 5day observatian period. Group I was introduced in the experimental tank at 0630 hours on the night of emergence IFeb. 161. Observation of this gmup began 2 b later and continued for 5 days (Days 1-5, Table 1). Group 1 had not k e n Fcd previously. However, the other five 6sh groups were Fed in the holding tank prior to experimentation, Except for group t at1 fish groups were acclimated to the experimental tank for a! least 24 h before observation. The fish were not fed dunng the experimentai period since preliminary observarions showed that feeding enhanced swimming activity. and feeding is known to synchronize fish swimming activity [Davis and Bardach I965; Byrne 19623). Swimming activity and vertical distribution of the fish were recorded simultaneously with the aid of a Sanyo silicon diode video camera, equipped with a wide-angle lens (1 : 1.8110), locatedabout 1mfromthe front ofthe tank. Manualadjustments of the lens aperture permitted filming of the fish in the light and dark of the LD cycle. A timer activated the camera and a video tape recorder for a 10-min period every alternate hour. Al! observations were stored on video tapes Grlater analysis. Swimming activity was recorded as the number of venical lines on rhc viewing glass traversed per fish per I0min. This value was convened to mean sntinrtning s p e d by multiplying the number orlines traversed per fish per 10 min by 26crn. Mean swimming speed was expressed i n metres travelled per frsh per lQmin, and in fish body length per second IBLS-~I.Vertical distribution of fish in the 38-cm warer column wm recorded as the tendency of the fish to swim in the upper half of the water column (i.c. top 39crn).This tendency was estimated by noting the instantaneous (ca. 2s) numher of fish in the upper half ofthe warer column at 1-min intervals during the IWmin observation period. Therefore, a maximum score of 60 (6 fish x 10 instantaneous scans) is obtained for a 10-rnin observation period if all six Rsh are swimming in thc top 19cm of warer on each of the 10 instantaneous scans of the tank. For each IO-rnin period, the total number offish observed instantaneously in the upper hair ofthe watercoIumn was divided by the maximum possible score of60. This ratio then was mutriplied by 100 to yield the "instantaneous percentage of the fish in the upper half of the water column per 10 min." which henceforth is referred toas the index qfwrtical disrribarion. This index is considered a relative measure of the photoractic response of the fish to overhead illuminatian. Average daily rhythms of swimming activity and of venical distribution were obtained for each fish group by platting, at 2-h intervals, mean lo-min score5 of these mO behavi~uralprocesses recorded over 5 consecutive days.

.

Estimation ofrhythm parameters ( I ) Daily diurnal+octurnal(D/N) ratio The daily DIN ratio was calculated as the mean of the 10-min scores recorded during the day divided by the mean of the 10-min scores recorded during the succeeding night of a 24-h L D cycle. This ratio provided a relative index of the degree of diurnalism or nocturnalisin of the recorded daily behavioural rhythms. ( 2 ) Period Period is defined as the duration of one recunine oscillation or cycle in a rhythmic function. Period lengths o f the daily behavioural rhythms and their probability of being significantly different from random fluctuations or "noise" in the data record were determined using the periodogram analysis of Dorrscheidt and Beck (1975). The significance level was set at 5%; periodogram values above this level were considered to represent periodicities significantly different from random noise. Time-series data records, used in the periodogram analysis, contained 60 sample points each (i.e. 5 days of observation for each fish group).

Results General behauiour offish In general, the fish swam continuously day and night along the length of the aquarium. Individual fish infrequently held a stationary position in the water column for short periods of time (< 5 min). Fish were never observed to rest on the false bottom of the aquarium. On Day 1, the fish swam about the aquarium as individuals during day and night. A schooling tendency was not apparent. Swimming fish formed small temporary aggregations of two to three individuals on Day 2. These aggregations were nonpolarized. Beginning on Day 3, fish formed polarized schools of four to six individuals during the day. From Days 3 to 37 (end of study), schooling fish generally swam in the lower half of the water column during the day. At night the school broke up, and the fish swam as individuals near the water sirface. ~~~~~~~i~~behaviour among fish was not observed. During the day, fish occasionally "snapped" at what appeared to be small particles or air

CAN. J.

ZOOL. VOL.

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Days

I

bubbles in the water column or at the water surface. Sometimes individual fish exhibited short bouts of "fluttering" behaviour; that is, up and down vertical swimming along the walls of an aquarium. This occurred too infrequently to be recorded.

1-5

Swimming activity Pink salmon fry exhibited, on the average. a bimodal daily activity pattern during the first 5 days after emergence (Fig. 2). Activity peaks occurred shortly after theonsets oflight and dark. Swimming speeds during other times of the die1 cycle did not vary significantly from each other. The DIN ratio was near 1.0 during the I st week. except on Days 1 and 4 (Fig. 3). This indicates that the daily activity pattern was irregular in that it was not consistently either diurnal or nocturnal. However, the daily activity rhythm appeared diurnal, but remained bimodal, during the 2nd week. This pattern resulted from the shift of the second activity peak from early evening to just before the onset of dark. The increasing degree o f diurnalism of the activity rhythm during the second week is reflected by the corresponding increase in the DIN ratio (Fig. 3). The fry continued to display diurnal rhythms of swimming activity. which were either unirnodal or bimodal. during Days 13 to 37 (Fig. 2). Comespondingly. the DIN ratio was continually above 1 .O during this period, but the degree of diurnalism varied with fish age (Fig. 3). The synchrony between the morning peak ofactivity and the lights-on stimulus on the majority of days after the 1st week suggests that the abrupt dark to light ID-L) transition synchronized the die1 rhythms of swimming activity. Period lengths of the daily rhythms of swimming activity for each of the six fish groups were significantly different from random noise (Table 2). These period lengths also were within 5% of 24.0 h, except for group 4. Figure 4 illustrates the periodograms from which these periods were ob-

D a y s 7-11

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t

12

58, 1980

D a y s 13-17

I-+-+-+-+

+\

m

a

Days 19-23

D a y s 27-31

6 4

12

D a y s 33-37

4 2

08

12

16

20

24

04

08

Time o f d a y th) fit. 2. Average daily patterns of mean swimming speed re-

corded for six different groups of sibling pink salmon fry at different times after emergence. Each graph represents the avApe l d e y a poatarnergoncel erage daily rhythm for one of the six groups of fish. Each mean value is based on five data points obtained on five consecutive FIG.3. Relationship between daily DIN ratio for swimming days. Vertical lines about the means are 95% confidence limits. speed of pink salmon fry and age after emergence. Arrows Light and dark horizontal bars indicate day (L) and night (D), indicate the times when one group of six fish was replaced by respectively. another group of six fish in the experimental tank.

TABLE2. Period lengths of the daily rhythms of swimming activity and of vertical distribution for six groups of pink saIrnon fry tested at different times after emergence. Period Iength of the cycle of water tempemture for each expetiment is also given. All period lengths are significantly different (P < 0.05) from nndom noise, except where indicated otherwise by an asterisk Period length, h Group Days after No. emergence

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1

2 3 4 5 6

1-5 7-1 1 13-17 19-23 27-3 1 33-37

Swimming Vertical Temperature activity distribution cycle 23.8 23.7 23.3 22.5 23.7 23.7

23.7 23.7 23.7 23.7 23.6 23.7

30.7* 24.7 22.9 21.8* 25.1 23.4

tained. Period length did not change significantly with fish age. These period lengths (Table 2, Fig. 4) indicate that the daily rhythms of swimming activity were synchronized with the 24-h LD cycle during the first 37 days after emergence. The period of 22.5 h for group 4 suggests that the degree of synchrony of the die1 activity rhythm for this group with the LD cycIe was weaker compared with that for the other five groups. The significant periodic component near 12 h, a submultiple of 24 h, in the periodograms for the activity rhythms during the first 11 days after emergence results from the general bimodality of the daily rhythms during this period (Fig. 2). Cycles of water temperature occurred inadvertently during each experiment (Table 2), despite attempts at keeping temperature constant. Water temperature affected swimming speed, as evidenced by the positive correlation between water temperature and swimming speed scores for three of the six fish goups (Table 31. However, the period length of the temperature cycle (Table 2), recorded during each 5-day experiment, did not correlate significantly ( r = 0.63, P > 0.05) with the corresponding period Iength for the swimming activity rhythm of each fish group (Table 2). This indicates that temperature cycles did not synchronize the daily rhythms of swimming activity. The periods of four of the six temperature cycles were significantly different from random noise. but only two were between 23 and 25 h.

Vertical distribution During the 1st week after emergence the majority of the fry were observed swimming in the upper half of the water column during the night, and almost exclusively in the lower half of the water column during the day (Fig. 5). This die1 pattern is referred to as a nocturnal rhythm of vertical distribution.

The tendency of the fish to swim, on the average, nearer the water surface at night than during the day during the 1st week suggests that they had a negative response to light during this period. Although the daily rhythm of vel-tical distribution remained nocturnal during the 2nd week. the fry showed an increased tendency to swim in the upper half of the water column during the day (Fig. 5). This latter tendency became more pronounced during Days 13 to 17. These observations suggest that the negative phototactic response of the fry weakened progressively on Days 7 to 17. Thereafter until the end of the study, the fry showed a stable negative phototactic response, as their die1 rhythms of vertical distribution remained nocturnal. unimodal. and relatively stable in form {Fig, 5). The abrupt L-D transition appeared to time the rising of the fish toward the water surface at night. The daily DIN ratio was always less than 1.0, indicating the predominance of a nocturnal rhythm of verticaldistribution throughout the experimental perjod (Fig. 6). However, this ratio varied significantly with fish age. The lowest ratio values occurred on Days 2 to 5, reflecting the strongest degree of nocturnalism in the die1 rhythm of vertical distribution. The daily DIN ratio increased rapidly between Days 7 and 17. This period corresponds to the phase wherein the fry showed a gradually increasing tendency to swim in the upper half of the water column during the day. The ratio declined slightly after Day 17, but showed a weak increasing trend from Day 27 to the end of the experimental period. Daily changes in this ratio were relatively small from Days 13 to 37 compared with the first 2 weeks of observation. The relative stability of the daily DIN ratio during Days 13 to 37 reflects the low day-to-day variability in the nocturnal rhythm of vertical distribution during this period. Nocturnal rhythms of vertical distribution for each fish group had significant period lengths approximating 24.0 h (Table 2, Fig. 4). These period lengths indicate that the nocturnal rhythms were synchronized strongly with the 24-h LD cycle during the first 37 days after emergence. Short-term fluctuations in water temperature did not affect the vertical distribution of the fish (Table 3). Further, temperature cycles did not synchronize the daily rhythms of vertical distribution. This is indicated by the weak correlation ( r = -0.05, P > 0.05) between the period of the temperature cycle in each experiment and the corresponding period of the rhythm of vertical distribution (Table 2). Relationship between swimming activity and uertical distribution Daily rhythms of swimming activity and of verti-

CAN. J . ZOOL. VOL. 58. 1980

Swimming

distribution

Days

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activity

Vertical

Period

(h)

FIG.4. Periodograms of rhythms of swimming activity and of vertical distribution recorded simultaneously in LD 12: 12 for each of six groups of sibling pink salmon fry on Days 1 to 37 after emergence. Each periodogram is based on five consecutive days of observation on each fish group. P is the major periodic component (in hours) in the time-series data record. AU P values are significantly different (P < 0.05) from random noise.

GODIN: I1

75 1

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cal distribution were diurnal and nocturnal, respectively, on Days 13 to 37 (Figs. 2 and 5). This difference in phase is reflected in significant negative correlations between the 10-min scores of swimming speed and the 10-min scores of the index of vertical distribution during this period (Table 3). Daily rhythms of swimming activity and of vertical distribution were synchronized strongly with the 24-h LD cycle. Corresponding periods for the rhythms of swimming activity and of vertical distribution for the same group of fish frequently were similar, but did not correlate with one another (r, = -0.06, P > 0.05). This suggests that the degree of synchrony of these two behavioural processes with the LD cycle differed in some instances (Table 2, Fig. 4). Diurnal swimming activity rhythms appeared to be synchronized with the lights-on stimulus of the LD cycle, whereas nocturnal patterns of rising toward the water surface appeared to be synchronized with the daily lights-off stimulus. Discussion The data showed that pink salmon fry exhibited, on the average, an irregular daily pattern of swimming activity and a nocturnal rhythm of vertical distribution during the 1st week after emergence. However, a shift from an irregular pattern to a diurnal rhythm of swimming activity occurred 7 to 13 days after emergence. Coincident with this ontogenetic shift was an increasing tendency of the fry to swim in the upper half of the water column during the day. Thereafter until the end of the study (Day 37), the fry displayed diurnal rhythms of swimming activity and nocturnal rhythms of vertical distribution. These observations support the hypothesis that pink salmon fry shift their nocturnal activity rhythm, characteristic of downstream migrants, to a diurnal rhythm shortly after emergence and after entering seawater. Field and laboratory observations indicate that emergence and seaward migration of pink salmon fry are mainly nocturnal (Godin 1980). However, the observations of Mason (1976) and Godin (1980), as well as some field observations (McCart 1967; Bakshtanskii 1970), indicate an increasing tendency of the fry of pink, coho (Oncorhynchus kisutch), and sockeye salmon ( 0 . nerka) to emerge and migrate downstream during light as the emergence period progresses. This tendency may relate to a gradual weakening of the fry's negative 201 0

I'

08 12 16 20 2 4 0 4 08

Time of day (h)

FIG.5. Average daily patterns of the index of vertical distribution in a water column recorded for six groups of sibling pink salmon fry at different times after emergence. Each graph represents the average daily rhythm for one of the six groups of fish. Each mean value is based on five data points obtained on five consecutive days. Vertical lines about the means and horizontal bars are as in Fig. 2.

CAN. J. ZOOL. VOL. 58, 1980

TABLE 3. Spearman rank correlation coefficients (r,) for comparisons between values of (1) water temperature and swimming speed, (2) water temperature and the index of vertical distribution, and (3) swimming speed and the index of vertical distribution. Swimming speed, vertical distribution, and water temperature were recorded simultaneously every 2 h for each of six groups of pink salmon fry. The different groups were observed at different times after emergence Temperature and swimming speed Group No.

rr

P

r.

0.19 NS 0.03 0.21 NS -0.03 0.40 *+* -0.04 0.37 *+ -0.12 -0.04 NS -0.17 0.36 ** -0.17 Nan: NS. not significant: *, P c 0.05; **, P c 0.01: ***, P < 0.001.

1 2 3 4 5 6

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Days after emergence

Temperature and vertical distribution

1-5 7-1 1 13-17 19-23 27-31 33-37

FIG.6. Relationship between daily DIN ratio for the index of vertical distribution in a water column for pink salmon fry and age after emergence. Arrows are as in Fig. 3.

phototactic response with age and (or) size, as demonstrated in the data of Mason (1976) for coho salmon. Noakes (1978) reviewed the behavioural development of salmonid fishes during the period from hatching until a few days after emergence. In general, there is a progressive development of motor patterns leading to emergence from gravel. Concurrently, the alevins show a progressive development of visual capability such that, at the time of emergence, fry are positively phototactic (change from negative phototaxis), show marked photomechanical changes in the retina, and possess full visual acuity necessary for feeding and other behaviours . My data indicate that the progressive weakening of the negative phototactic response of pink salmon fry continues after emergence. This is evidenced by the gradual appearance of a diurnal rhythm of swimming activity, and by the increasing tendency of the fry to swim closer to the water surface by day following the 1st week after emergence. These lab-

P NS NS NS NS NS NS

Swimming speed and vertical distribution r.

0.18 -0.06 -0.40 -0.32 -0.28 -0.65

P NS NS

** * *

z**

oratory findings confirm those of Hoar and coworkers (Hoar 1958,1976;Hoar et al. 1957) on pink salmon fry. Collectively, these observations indicate that pink salmon fry are nocturnally active, exhibit negative phototaxis, and rise toward the water surface at night during the period of downstream migration. While residing in estuaries and adjacent coastal waters, the fry school by day, gradually become ''day-active." and their negative phototactic response weakens somewhat. However, the fry retain their negative phototaxis and their tendency to rise toward the water surface at night and to descend in the water column by day. No field data are available to confirm these laboratory findings, except for the daytime schooling of pink salmon fry in marine waters (Neave 1966; Healey 1967). Juvenile pink saImon are diurnal feeders in nature (Godin 1979). This fact correlates well with the diurnal rhythm of swimming activity exhibited by fry in the current study. Sincejuvenile pink salmon are schooling, visual feeders, a diurnal rhythm of swimming activity is considered adaptive for feeding on small planktonic invertebrates in nearshore habitats of estuaries and adjacent coastal waters. A diurnal activity rhythm could increase the fry's prey-encounter rate during daylight hours available for feeding, and could reduce the fry's energy demands at night when little or no feeding occurs. Schooling during the day may reduce the fry's susceptibility to predation (Neil1 and Cullen 1974; Major 1978). Recent ontogenetic studies of the locomotor activity of some fish species (Darnel1 and Meierotto 1965; Dill 1970; Byrne 1971 ; Westin 197 1 ; Solem 1973; Gibson pt al. 1978; Staples 1978) provide additional support for the hypothesis that the photobehaviour and daily rhythms of locomotor activity in fishes are adapted to their environment. These studies indicate that ontogenetic changes in

GODIN: 11

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the phase of daily rhythms of swimming activity frequently are associated with changes in habitat. Periodogram analysis showed that the daily rhythms of swimming activity and of vertical distribution in pink salmon fry were synchronized closely with the 24-h LD cycle during the 1st month after emergence. The daily D-L and L-D transitions appeared to have synchronized the die1 rhythms of swimming activity and of vertical distribution, respectively. Daily cycles of temperature did not exert significant synchronizing effects on either of these two types of behavioural rhythms. The daily cycle of illumination, the most predictable and consistent environmental cycle, is generally recognized as the most important synchronizer of biological rhythms for a wide spectrum of organisms in nature (Aschoff 1963; Biinning 1973). Acknowledgements This paper is based on a thesis submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy at the University of British Columbia. The study was conducted at the Pacific Biological Station, Nanaimo, British Columbia. I thank its Director for permission to work there, and Dr. C. Groot for making research facilities available to me and providing helpful criticism during the study. Members of my supervisory committee and two anonymous referees commented constructively on the manuscript. This research was supported by the Federal Department of Fisheries and Oceans, an NRCC grant-in-aid to my supervisor, Dr. W. S. Hoar, and scholarships from the National Research Council of Canada, the Killam Foundation, and the Salmon Research Society of British Columbia.

ASCHOFF,J. 1963. Comparative physiology: diurnal rhythms. Annu. Rev. Physiol. 25: 581-600. BAKSHTANSKII, E. L. 1970. Downstream migrations of pink and red salmon and causes of their delay in streams of the Kola Peninsula. In "Fish culture in nature waters." Tr. Vses. Nauchno-Issled Inst. Morsk. Rybn. Khoz. Okeanogr. 74: 129-143. (Fish. Res. Board Can. Trans]. Ser. No. 1765,1971). B~~NNIN E.G1973. , The physiological clock. Revised 3rd ed. Springer-Verlag, Inc., New York. BYRNE, J. E. 1968. The effects of photoperiod and temperature on the daily pattern of locomotor activity in juvenile sockeye salmon, Oncorhynchus nerka (Walbaum). Ph.D. Thesis, University of British Columbia, Vancouver, British Columbia. 1971. Photoperiodic activity changes in juvenile sockeye salmon (Oncorhynchus nerka). Can. J. Zool. 49: 1155-1158. DARNELL,R. M., and R. R. MEIEROTTO.1965. Diurnal periodicity in the black bullhead, Ictalurus melas (Rafinesque). Trans. Am. Fish. Soc. 94: 1-7. DAVIS,R. E., and J. BARDACH.1965. Time-co-ordinated Frefeeding activity in fish. Anim. Behav. 13: 154-162. DILL,P. A. 1970. On the development of die] activity rhythms in Atlantic salmon and rainbow trout. Ph.D. Thesis, University of Western Ontario, London, Ontario.

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