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J. exp. Biol. 129, 165-178 (1987) 165Printed in Great Britain © The Company of Biologists Limited 1987

LUNAR CYCLES OF COHO SALMON, ONCORHYNCHUSKISUTCH

I. GROWTH AND FEEDING

BY K. J. FARBRIDGE AND J. F. LEATHERLAND

Department of Zoology, Group for the Advancement of Fish Studies,University ofGuelph, Guelph, Ontario, Canada, N1G2W1

Accepted 6 January 1987

SUMMARY

Coho salmon (Oncorhynchus kisutch Walbaum) parrs and smolts, maintained in alaboratory under a fixed artificial 12h light: 12h dark photoperiod from the time ofhatching, exhibited a pattern of alternating periods of rapid and slow growth inbody mass; the peaks and troughs in growth rate were significantly different fromone another. The alternating growth rate changes were rhythmic in nature, ofapproximately 14 to 15 days in length.

Evidence for cyclic patterns of growth in relative length and in food consumptionwas also found in coho salmon parr. Peak food intake appeared to occur 2-4 daysafter each peak of growth in relative mass. Although the pattern of growth in relativelength was less clear, there was evidence to suggest that growth in length might beout of phase with growth in mass.

There was no pattern of cycling growth rates in coho salmon parr subsampledfrom a common stock. The significance of this is discussed.

The data suggest that the lunar cycle acts as a Zeitgeber for synchronization of thegrowth rate rhythms.

INTRODUCTION

Biological rhythmicity, the periodicity of which is correlated with major events inthe fluctuating physical (abiotic) environment, is a widespread phenomenon in theliving world. The general properties of the observed rhythms in a variety of life formsare remarkably similar, suggesting that they are fundamental and ancient phenomena(see reviews by Brown, 1973; Saunders, 1977) which permit organisms to makecontinuous and frequent adjustments in advance of changing environmental or socialconditions. They also allow for the coordination of behavioural, physiological andreproductive activities within a species and between the species of an integratedecosystem.

Circadian (Leatherland, McKeown & John, 1974; de Vlaming, Sage & Tiegs,1975; Leatherland & Nuti, 1982) and annual (Shul'man, 1974; Saunders &Henderson, 1970; de Vlaming, 1972) rhythms have been well documented in teleostfishes. Also, in teleosts there are several documented cases of a correlation between

Key words: teleost fish, Zeitgeber, growth, lunar cycles.

166 K. J. FARBRIDGE AND J. F. LEATHERLAND

lunar cycles in association with annual rhythms and the timing and synchronizationof physiological and metabolic events (Walker, 1949, cited by Grau et al. 1981;Mason, 1975; Grau et al. 1981).

Observations in our laboratory and anecdotal reports from several local hatcheriessuggested a rhythmic pattern of food intake in salmonid fish; the fish showed markedcyclic variation in their feeding activity with apparent peaks and troughs in foodintake. Since growth patterns are closely correlated with food intake, it is likely thatalterations in food intake in the short term are reflected in short-term changes ingrowth. Such growth patterns would not necessarily be identified in the conventionallong-term growth rate studies, particularly those involved in growth modelling (e.g.Corey, Leith & English, 1983), but have been found in brown trout, Salmo trutta(Brown, 1946), and rainbow trout, Salmo gairdneri (Wagner & McKeown, 1985;Farbridge, 1985). This study examines the short-term cyclical growth patterns incoho salmon, Oncorhynchus kisutch, during the parr and smolt stages of develop-ment, and evaluates the possible interrelationship between the cycles of growth, thecycles of food intake and lunar cycles.

MATERIALS AND METHODS

Source and maintenance of animals

The coho salmon, Oncorhynchus kisutch, used in the study were hatched andraised in the laboratory. Gametes were obtained in 1982, from salmon at the PlatteRiver Hatchery, Michigan, and in 1983 from salmon taken from the Credit River,Streetsville, Ontario. The eggs of 15-20 females were fertilized with sperm from 2-3males. After water hardening on site for approximately 2 h, the eggs were returned tothe laboratory where they were maintained in horizontal hatchery trays in constantlyrunning well water at 10 ± 1 °C.

In all experiments the fish were maintained in constantly running and aerated wellwater (the seasonal water temperature range was 9—11°C) under a 12h:12h L:Dartificial photoperiod (L = 08.00 h to 20.00 h) unless otherwise indicated. They werefed with either a commercial salmonid diet (Martin Feed Mill, Elmira, Ontario) or adiet formulated by Dr J. Hilton, Department of Nutritional Science, University ofGuelph. The composition of the two diets was as follows: Martin's diet — herringmeal 35 %, wheat middlings 35 %, soybean meal 20%, soybean oil 6%, linseed oil1%, vitamin mix 2%, mineral mix 1%; Hilton's diet - fish meal 40%, wheatmiddlings 13%, soybean meal 10%, gelatin 10%, poultry by-product meal 7%,shrimp meal 5 %, brewer's yeast 5 %, fish oil 7 %, vitamin mix 2 %, mineral mix 1 %.

Fish body masses (±0-05 g) were measured by placing groups of fish (the numberdepended on the size of the animals) into a tared water-filled container.

Experimental design

Experiment 1: growth and feeding patterns in coho salmon parr

To examine possible relationships between growth in mass (and/or length) andfeeding of coho salmon parr, 450 6-month-old fish [means 12-9 ± 1 -27 (s.D.)g,

Lunar cycles of salmon I 167

9-78 ± l-64cm] were randomly distributed between nine aquaria (801, SOfish/aquaria); water temperature throughout the experiment was 11-5 ± 1-5°C. Fish werefed to satiety three times a day with Hilton's diet; the feeding order of tanks wasrandomized daily and records of food consumption were kept. Food consumptionwas expressed as a fraction of the mean fish mass at the beginning of each 4-dayinterval (see below).

The aquaria were divided into three study groups, each consisting of threereplicates (three aquaria/group). The study groups were weighed in sequence at4-day intervals (i.e. day 0 — group 1, day 4 — group 2, day 8 - group 3, day 12 —group 1, etc.), in lieu of the morning feeding, from June 23 to September 19, 1983.Thus, masses were obtained at 4-day intervals but fish in any one group were onlyweighed at 12-day intervals; this design was chosen to eliminate the possibility ofstress-related effects on growth rate. The fish in any group were weighed in groups of10. The standard lengths (±0-05 cm) of 30 fish from each group (10 from eachreplicate) were measured on the appropriate mornings.

Experiment 2: growth patterns in coho salmon parr sampled from a common stock

To determine whether sampling from a common stock would reveal the samegrowth pattern as that seen in the experimental design above, approximately 1100coho salmon parr were distributed between two circular aquaria (5001); watertemperature throughout the experiment was 11-5 ± 1*5°C. The fish were fed tosatiety three times a day with Hilton's diet.

Fifty fish from each aquarium were weighed in groups of 10, at 4-day intervalsin lieu of the morning feeding from June 23 to July 1, 1983. Thereafter 100 fish fromeach tank were weighed at 4-day intervals until August 22, 1983.

Experiment 3: growth patterns in coho salmon smolts

Two hundred and forty 1-year-old coho salmon smolts (mean mass 80-8 ±8-76g) were distributed randomly between 12 compartments of four circular aquaria(5001; 20 fish/compartment); water temperature throughout the experiment was10-0 ± 1-5°C. Differences in total mass between compartments were adjusted to10-0g or less at the beginning of the study. The fish were fed to satiety three times aday with the commercial diet.

The compartments were allocated randomly to three study groups, each consistingof three replicates. In addition, three 'reference' groups were maintained; these wereweighed only at the beginning and the end of the study in order to evaluate whetherthe weighing procedure itself affected overall growth. The study groups wereweighed in sequence at 4-day intervals, in lieu of the morning feeding (seeexperiment 1), from March8 to May 15, 1984. All groups were weighed on May 19,1984.


Calculations and statistical analysis

The growth of fish, assessed by the increase in wet body mass, was expressed asrelative growth rate calculated with the following equation from Ricker (1979):

W - w 100Relative growth rate = T-t w

where W and w represent final and initial mass (g), respectively, and T—t representsthe change in time. In this paper 'growth rate' is equated with 'relative growth rate'.Relative growth in length was calculated in the same manner.

In experiment 3, the total mass of fish in each aquarium at all times of samplingwas expressed as a fraction of the total mass of the fish in the aquarium at the end ofthe study. These were termed 'corrected' masses in that they were corrected for anydifferences in the mass of fish in a given aquarium at the end of the study. Thesemasses represented the fraction of the final mass achieved by the time of samplingand were used to calculate a 'corrected' growth rate. 'Corrected' growth rates couldnot be calculated for experiment 1 because fish were removed periodically fromaquaria at the end of the experiment to analyse various tissue constituents.

In experiments 1 and 3, replicates were randomly allocated a subgroup desig-nation; aquaria with the same subgroup designation were compared to obtain agrowth rate for a given interval. Growth rates for each interval were expressed as amean ± S.D. In experiment 2, growth rates were calculated for each aquarium andexpressed as mean ± S.D.

In order to test for significant differences between apparent peaks and troughs andto test for the presence of a semi-lunar periodicity, growth rates (means ± S.E.M.) formass were plotted on a common semi-lunar scale (Astronomical Almanac 1983, 1984,1985) and means were compared using one-way analysis of variance. Wheresignificance is indicated (P< 0-05), differences between peaks and troughs in growthwere compared with the least significant means procedure (Steele & Torrie, I960);the critical level of significance for testing hypotheses was P ^ 0-05.

RESULTS

Experiment 1: growth and feeding patterns in coho salmon parr

Between June 27 and September 18, 1983, the coho salmon parr showed cyclicalpatterns of growth in mass (Fig. 1A). When a sine curve with semi-lunar periodicitywas superimposed over the data for growth in mass it was observed that the growthrate pattern was in phase with the sine curve from June 27 to July 25, then fell out ofphase with the semi-lunar sine curve after July 25 but was in phase from August 26 toSeptember 19.

When the data were plotted on a semi-lunar scale, growth was lowest at the time ofnew and full moons and increased thereafter (Fig. 2).

The cyclical pattern of growth in relative length was not as pronounced as that forgrowth in mass (Fig. IB). From June27 to July 25 the apparent cycle of growth inlength was out of phase with that of growth in mass. Any obvious cycling was lost

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Fig. 1. (A) Relative growth rates (% day ') and a sine curve with semi-lunar periodicity(broken line); (B) relative increases in standard length (%day~'); and (C) foodconsumption (expressed as the food consumed per average fish mass) for coho salmonparr weighed at 4-day intervals from June 23 to September 18, 1983. Variation expressedas ±s.D. (Ar = 3). Occurrences of full moons (open circles) and new moons (filled circles)are indicated. Experimental group 1, A ; experimental group 2, • ; experimental group 3,

after July 25 when growth in mass fell out of phase with a semi-lunar sine curve, butappeared to be re-established after August 26, although it was then in phase with thatof growth in mass.

The observed peaks in the amount of food consumed/mean fish mass occurredapproximately 2—4days after the peak for growth rate (Fig. 1C). Again, the patternwas less distinct for a period after July 25 but became clearer towards the end of thestudy.

Experiment 2: growth patterns in coho salmon parr sampled from a common stock

There was no consistent pattern of cycling of growth rates in coho salmon parrsubsampled from a common stock (Fig. 3).

Experiment 3: growth patterns in coho salmon smolts

The coho salmon smolts showed a cyclical pattern of growth similar to thatobserved in the parrs, whether or not masses were corrected for the final massachieved by each aquarium at the end of the study (Fig. 4). The largest 'corrected'growth rate was recorded on March 8, 1984, 12 days before the spring equinox(March 20, 1984). The 'corrected' growth rate pattern after the spring equinox,


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Fig. 2. Relative growth rates (%day-1 ± S.E.M., Ar = 3 or 6) for coho salmon parrweighed at 4-day intervals from June 23 to September 18, 1983 plotted on a single semi-lunar scale. Same lower-case letter indicates no significant difference between means.

although not in complete synchrony, kept in phase with that of a semi-lunar sinecurve.

A cyclical pattern was also evident with 'uncorrected' growth rates (Fig. 4B)although it was slightly different from that seen with 'corrected' growth rates.

When 'corrected' and 'uncorrected' growth rates after the spring equinox wereplotted on a semi-lunar scale both showed a similar cyclical pattern (Fig. 5).Although the curves of 'corrected' and 'uncorrected' growth rates appeared to beslightly out of phase, lower growth rates tended to be associated with the times ofnew and full moons or slightly thereafter.

The mass gain of fish in the 'reference' aquarium was not significantly differentfrom that of fish in the study aquaria.

DISCUSSION

Both parr and smolt stages of coho salmon displayed rhythmical patterns ofgrowth, with the fish alternating between periods (approximately 1 week in length)of rapid and slow growth in mass.

Growth rhythms have also been reported in brown trout (Brown, 1946) andrainbow trout (Wagner & McKeown, 1985; Farbridge, 1985). Other evidence for


short-term growth rhythms in teleosts is derived from daily, bimonthly and monthlypatterns of otolith growth (Pannella, 1971, 1974; Campana, 1984), which are charac-terized by a period of increasing daily increment width followed by a period of

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Fig. 4. (A) 'Corrected' and (B) relative growth rates (%day ') for coho salmon smoltsweighed at 4-day intervals from March 8 to May 15, 1984. Variability expressed as ±S.D.(N = 3). Occurrences of full moons (open circles) and new moons (filled circles) areindicated. Experimental group 1, • ; experimental group 2, O; experimental group 3, A.

decreasing daily increment width (Campana, 1984), a pattern identical to that shownin this study.

Growth in length also showed evidence of a similar rhythmical pattern as growth inmass in coho salmon parr, although the pattern was not as distinct. At the beginningof the study the periods of rapid growth in length corresponded with the periods ofslow growth in mass; this relationship was lost after July 25. A similar relationshipbetween growth in mass and length was observed in brown trout (Brown, 1946).Swift (1955), while studying annual changes in growth rate in brown trout, noted


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that monthly averages of growth rates for mass and length always varied in the sameway but that the cycle for mass preceded that for length. Wagner & McKeown (1985)suggest that the periods of reduced growth in rainbow trout might be analogous tothe anabolic refractory periods seen in rats when tissues are unresponsive to growthhormone. However, if this relationship between growth in length and mass does existit would suggest that the phenomenon is more complicated than a simple reduction ingrowth. Instead, there may be a switch in processing resources. One possibleexplanation is that the fish are partitioning the processes involved with growth inmass from those involved with growth in length. Presumably, the fish enter a periodof 'assimilation' followed by a period of 'lengthening' during which some of the bodymass laid down during the 'assimilation' period is converted into an increase inlength. Indeed, brown trout with a condition factor (ratio of mass:length3) of less


than 1 -08 grew relatively faster in mass than length, while fish with a condition factorof more than 1-08 grew relatively faster in length (Brown, 1957). The biologicalvalue of partitioning the two processes is not clear. It may be that the two events aretoo metabolically demanding to occur simultaneously or that the controlling factors(endocrine system, etc.) would be in conflict if the two processes were to occursimultaneously. Higgs et al. (1977) observed that the administration of bovinegrowth hormone and \l-a methyltestosterone resulted in greater growth in lengththan in mass in coho salmon, while the administration of L-thyroxine (T4) had theopposite effect.

Negative growth rates for both mass and length were recorded on a few occasions,although their significance is unknown since they could be a result of the exper-imental design.

Food consumption showed a similar rhythmical pattern to growth in mass. Brown(1946) also reported biweekly fluctuations in appetite of brown trout. The periodsfor increased feeding activity were observed to occur slightly after those for growth inmass; the apparent independence of food intake and growth when food is notrestricted suggests that both food intake and body mass gain, or growth, areregulated. Indeed, Brown (1946) observed an increase in the efficiency of foodutilization before periods of maximum growth in mass and food consumption.

Fish are stressed by handling and this can result in reduced growth (Schreck,1982). The stress of the weighing protocol was minimized by rapid handling butcould not be completely eliminated, particularly since short intervals betweenweighings were desired. Consequently, the experimental design attempted tobalance these considerations. In studies of growth cycles of rainbow trout, severalaquaria were sampled at 4-day intervals (Farbridge, 1985). Because this was likely tobe stressful, the studies were kept short. Such an experimental design, whilstappropriate for the rainbow trout, is less useful in a species such as coho salmonwhich is more susceptible to handling stress. However, studies of a longer time serieswere necessary, especially if possible Zeitgeber were to be considered.

Consequently, the masses of fish in different groups on different dates werecompared to obtain a growth rate for a given interval. Thus, the time betweenweighings for any particular group was increased without having to increase thegrowth rate interval. In doing this, the assumption was made that when aquaria arerandomly allocated an equal biomass of fish, they also possess the same growthpotential over time. In other words, at any given point in the time series, all groupsweigh approximately the same.

A possible criticism of this experimental design is that this assumption cannot bemade and that the masses of different aquaria cannot be compared to calculate agrowth rate for a given interval. Any apparent rhythm may simply reflect differencesin masses between groups. However, several points argue against that assertion.First, the rhythmic patterns in experiments 1 and 3 followed over several cycles arenot easily explained by the above argument given the random block design of theexperiments. Moreover, the experimental design has been used on three separate


occasions, two presented here and one presented elsewhere (Farbridge, 1985) withthe same results. Furthermore, if certain groups had exhibited consistently highergrowth rates throughout the study period, one might expect to find significantdifferences in mass between the groups at the end of the study. This was not found inany of the studies. Moreover, expression of the masses as a fraction of the final bodymass achieved by an individual group supports this conclusion, since, if cyclingpatterns were a result of different growth rates in different groups, 'corrected' growthrates calculated on the basis of final mass should eliminate the cycling patterns; thisdid not happen. Also, the phase shifting of growth in mass, food consumption andpossibly growth in length in experiment 1 argues against a chance observation; onewould expect that the group exhibiting the greatest growth and, hence, occupyingthe peak position for growth in mass would simultaneously occupy the peak positionsfor growth in length and food consumption. The pattern observed when growth ratesfrom experiments 1 and 3 were plotted on a semi-lunar scale specifically supports asemi-lunar rhythm. Lower growth rates appear to be associated with the time of newand full moons. If the observed growth rhythm had been a result of a 12-dayweighing cycle, then one would expect it gradually to become out of phase with asemi-lunar cycle at an approximate rate of 2 days/cycle. This was not observed evenin experiment 1 where a semi-lunar rhythm is more tenuous. Finally, the cyclicalpattern of amino acid uptake by scales, liver and muscle RNA:DNA ratios, carcasswater content, haematocrit, and plasma thyroxine, triglyceride, glucose and choles-terol levels during the semi-lunar period strongly suggest the existence of a semi-lunar cycle in physiology and thus, indirectly, growth (Farbridge & Leatherland,1987). These results were based on measurements taken over several different lunarcycles and thus do not suffer the same problems of experimental design as thosereported in this paper.

The fish were started on the experimental feeding regime several weeks before thebeginning of the weighing schedule. This should have precluded the possibility of aninitial increased feeding rate initiating the growth rate pattern which may have beenmaintained simply by digestion rates and degree of stomach fullness. Given thecombined length of the pre-experimental and experimental periods one wouldotherwise have expected to see a slow loss of synchronicity between fish.

It is not possible to assign precise dates to the times of peaks and troughs ofgrowth, because there is no information on the growth of the fish during the weighinginterval itself. The growth may actually peak some time during the interval.Consequently, the observed peaks only represent the approximate positions ofperiods of rapid growth. This fact is most pertinent when speculating on possibleZeitgeber.

The lunar cycle is the most obvious environmental factor that might be serving as aZeitgeber for the synchronization of the observed growth rhythm. A biologicalrhythm may be defined as having a lunar periodicity if the peaks and troughs of therhythmical process appear once or twice in every lunar month at the same time, thatis at the time of a certain lunar phase (Hauenschild, 1961). Periods of rapid growth


were correlated with lunar phases. New and full moons appear to be associated withperiods of lower growth while more rapid growth appears to occur some time midwaybetween new and full moons. The precise phase relationship between growth andlunar phenomenon is difficult to determine from these data, primarily because of therelatively long time between weighings (4 days).

Rounds (1983) reported a 10- to 14-day rhythm of acetylcholine receptor escapefrom atropine blocking in cockroach hearts. This rhythm could not be explainedsimply by the lunar phase cycle. The 10- to 14-day cycle seemed to be the product oftwo pulses, 12 h apart, progressing across successive days. The times of pulseprogression did not correspond to SOminday"1 which could indicate upper andlower transits of the moon (tidal variations) but instead to the rate of change ofmoonset across successive days (30-80 minday"1). Perhaps these fish are also using asimilar lunar cue of moonrise and/or moonset. If so, it is important to consider thatcoho salmon feed primarily by sight and, consequently, depend on illumination forfeeding. If their growth is influenced by lunar phenomena, the resulting rhythm islikely to be a result of an interaction between lunar day (24-8 h) and solar day (24-0 h)phenomena. It is important to remember that these fish have been maintained undera constant photoperiod from the time of their emergence from the egg. The patternof growth may take on a different appearance in the natural environment.

The mechanism which allows these fish to respond to lunar and perhaps solar cues(see below) is not known. In marine organisms, the daily changes in tides maydirectly determine physiology and behaviour. Yet marine teleosts that depend ontides for feeding exhibit lunar and semi-lunar checks (discontinuities) in otolithgrowth. Check formation is normally associated with a stressful incident in the lifehistory of the fish (Pannella, 1980); stresses reduce branchial uptake of calcium,resulting in a calcium-poor structure which is usually prominent relative to thesurrounding daily increments (Campana, 1983). However, an analogous mechanismdoes not appear to exist during the formation of lunar checks (Campana, 1984).These observations suggest that it is not simply tidal variation which determines thepattern of growth. Certainly, one can envisage the advantages of anticipating tidallydetermined feeding behaviour.

The unusually high growth rate followed by a rapid trough in growth just beforethe spring equinox was observed in rainbow trout in 1984 (Farbridge, 1985) and incoho salmon parr in 1985 (Farbridge & Leatherland, 1987). Observations suggestthat the spring equinox is an important event for these fish.

The poor documentation of the growth rhythms in these salmonid species is at firstperplexing. However, in most studies on growth, fish are weighed at intervals of1 week or longer. Obviously, the growth rhythm described in this study would havebeen difficult to detect if a similar weighing regime had been employed. Also, thegrowth rhythm was lost when fish were sampled from a common stock. Numerousstudies have obtained growth data by subsampling. However, because of theinherent variation in size of these fish, this method may not be suitable for detectingshort-term changes in growth.


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pp. 429-456. Philadelphia: Saunders.BROWN, M. E. (1946). The growth of brown trout (Salmo trutta Linn.). II. The growth of two-

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coho salmon, Oncorhynchus kisutch. Comp. Biochetn. Physiol. 75A, 215-220.CAMPANA, S. E. (1984). Lunar cycles of otolith growth in the juvenile starry flounder, Platichthys

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PANNELLA, G. (1980). Growth patterns in fish sagittae. In Skeletal Growth of Aquatic Organisms(ed. D. C. Rhoads & R. A. Lutz), pp. 519-560. New York: Plenum Press.

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