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DIEL RHYTHMS of BEHAVIOR in JUVENILE PINK SALMON (Oncorhynchus Gorbuscha Walbaum)

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DIEL RHYTHMS of BEHAVIOR in JUVENILE PINK SALMON (Oncorhynchus Gorbuscha Walbaum) DIEL RHYTHMS OF BEHAVIOR IN JUVENILE PINK SALMON (Oncorhynchus gorbuscha Walbaum) by JEAN-GUY JOSEPH GODIN B.Sc. (Honors), St. Francis Xavier University, 1973 A THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY in THE FACULTY OF GRADUATE STUDIES (Department of Zoology) We accept this thesis as conforming to the required standard THE UNIVERSITY OF BRITISH COLUMBIA June, 1979 cj Jean-Guy Joseph Godin, 1979 In presenting this thesis in partial fulfilment of the requirements for an advanced degree at the University of British Columbia, I agree that the Library shall make it freely available for reference and study. I further agree that permission for extensive copying of this thesis for scholarly purposes may be granted by the Head of my Department or by his representatives. It is understood that copying or publication of this thesis for financial gain shall not be allowed without my written permission. Department of Zoology The University of British Columbia 2075 Wesbrook Place Vancouver, Canada V6T 1W5 Date ii ABSTRACT Anadromous pink salmon undergo several migratory movements between different habitats during their life history. These migrations are accurately timed on a seasonal basis. Annual rhythms or seasonally-timed events may result from interactions between daily rhythms and annual changes in environmental factors. Therefore, knowledge of daily behavioral rhythms in pink salmon may improve our current poor understanding of the seasonal timing of its migrations. Hence, the objective of this study was to investigate, in a seasonal context and mainly under laboratory conditions, diel rhythms of ecologically-relevant behavior in juvenile pink salmon, and their timing mechanisms. Fry emergence from a simulated gravel redd in fresh water was mainly nocturnal below 13°C. Diel emergence timing was synchronized with the onset of night, but was affected by temperature in a non-linear manner. Temperature affected negatively the duration of the intra-gravel alevin stage and the rate of emergence. Nocturnal emergence was considered an anti-predator adaptation. Fry exhibited mainly nocturnal rhythms of swimming activity and of vertical distribution during the first week after emergence. However, a gradual shift from a nocturnal to a diurnal swimming activity rhythm occurred 7 to 13 days after emergence, when wild fish are residing in estuaries and adjacent coastal waters. Coincident with this shift was an increasing tendency of the fry to swimnnear the water surface during iii the day. This suggested a weakening of their negative phototactic response during this period. Thereafter, the fish usually displayed diurnal rhythms of swimming activity and nocturnal rhythms of vertical distribution. The ontogenetic shift in the phase of the activity rhythm and in photobehavior was considered adaptive for schooling and feeding during the day. Wild fry fed mainly during daylight hours in littoral areas of two marine bays. However, their feeding rhythms varied among study sites. Laboratory experiments showed that hunger level affected fish feeding rate and ration consumed positively. Fish fed continuously on live copepods under idealized laboratory conditions. During a 12-h session they rapidly (< 30 min) filled their stomachs with prey; thereafter, they maintained their stomachs full by feeding at a rate that balanced the rate of evacuation of prey from the stomach. Hence, I concluded that pink salmon have flexible feeding activity rhythms, which may permit opportunistic exploitation of prey, and feed at a relatively low hunger threshold. This feeding strategy may explain in part their relatively high growth rates in nature. During the periods corresponding to their juvenile coastal and pelagic ocean phases, the fish exhibited generally diurnal rhythms of swimming activity and of aggression, and nocturnal rhythms of vertical distribution in response to simulated seasonal photoperiodic and temperature changes. These rhythms were synchronized with the artificial light-dark (LD) cycle throughout most of the year. Some parameters of these rhythms varied on a seasonal basis, but not according to the iv Aschoff-Wever model. Mean swimming speed, the degree of diurnalism of the swimming activity rhythm, and the timing of the daily peak of the rhythms were affected by daylength. Hence, photoperiod might be an important proximate factor that pink salmon use to time their oceanic migration on a seasonal basis. Some data suggested the existence of an endogenous, circadian activity rhythm, and thus a daily "clock", in pink salmon. However, this remains uncertain. The free-running period of their activity rhythm was not related negatively to constant light intensity, as predicted by the Circadian Rule. The LD cycle affected directly swimming activity (masking), rather than entraining an endogenous circadian system. Since the activity rhythm of pink salmon does not possess a strong endogenous component, it is doubtful that the seasonal timing of its migrations results from interactions between a circadian clock and seasonal changes in environmental factors. However, the flexibility and inter-individual variability of their behavioral rhythms may be adaptive responses to the instability and heterogeneity of the marine environment. V TABLE OF CONTENTS Title Page ABSTRACT ii TABLE OF CONTENTS v LIST OF TABLES viii LIST OF FIGURES xi ACKNOWLEDGEMENTS . xix CHAPTER I. GENERAL INTRODUCTION 1 CHAPTER II. GENERAL MATERIALS AND METHODS A. Fish and incubation procedures 5 B. Holding conditions 6 C. Experimental conditions 6 D. Statistical procedures 7 CHAPTER III. EMERGENCE FROM A SIMULATED REDD INTRODUCTION 8 MATERIALS AND METHODS 9 RESULTS A. Temporal pattern of emergence 16 B. Diel timing of emergence 23 DISCUSSION 30 CHAPTER IV. ONTOGENY OF DIEL RHYTHMS OF SWIMMING ACTIVITY AND OF VERTICAL DISTRIBUTION INTRODUCTION 37 MATERIALS AND METHODS A. Fish 38 B. Experimental tank 38 C. Experimental procedure 40 D. Estimation of rhythm parameters 43 RESULTS A. General behavior of fish 44 B. Swimming activity 45 C. Vertical distribution 54 D. Relationship between swimming activity and 58 vertical distribution DISCUSSION 59 vi TABLE OF CONTENTS (cont'd) Page CHAPTER V. TEMPORAL PATTERNS OF FEEDING BEHAVIOR INTRODUCTION 64 MATERIALS AND METHODS A. Pattern of feeding behavior in the field 66 B. Pattern of feeding behavior in the laboratory 69 1. Experimental apparatus 69 2. Feeding experiments 71 3. Prey-capture success and prey 73 biomass consumed, 4. Gastric evacuation rate 75 RESULTS A. Pattern of feeding behavior in the field 76 B. Pattern of feeding behavior in the laboratory 83 DISCUSSION 92 CHAPTER VI. ANNUAL CHANGES IN THE DIEL PATTERNS OF SWIMMING ACTIVITY, AGGRESSION, AND VERTICAL DISTRIBUTION INTRODUCTION 102 MATERIALS AND METHODS A. Fish 104 B. Experimental tank 105 C. Experimental procedure 106 D. Estimation of rhythm parameters 107 RESULTS A. General behavior of fish 110 B. Swimming activity 110 C. Aggressive behavior 127 D. Vertical distribution 134 E. Relationship between swimming activity, 142 aggression, and vertical distribution DISCUSSION 148 CHAPTER VII. TIMING OF THE DIEL SWIMMING ACTIVITY RHYTHM OF INDIVIDUAL FISH INTRODUCTION 164 vii TABLE OF CONTENTS (cont'd) Page MATERIALS AND METHODS A. Fish and holding conditions 167 B. Description of the activity channels 167 and activity monitors 1. Activity channels 167 2. Activity monitors 170 3. Evaluation of activity monitors 172 C. Experimental procedures 173 1. Experiment 1, Circadian Rule 173 2. Experiment 2, Catching the 174 free-running rhythm 3. Experiment 3, Phase-shifting of 174 the endogenous rhythm D. Statistical procedures 176 RESULTS A. Experiment 1, Circadian Rule 176 B. Experiment 2, Catching the free-running 184 rhythm C. Experiment 3, Phase-shifting of the 186 endogenous rhythm DISCUSSION 189 CHAPTER VIII. GENERAL DISCUSSION AND CONCLUSIONS 200 REFERENCES 214 APPENDICES 243 viii LIST OF TABLES Mean ± SD daily water temperature experienced by sibling alevins in gravel from median hatching time to the time of 50% emergence for each of six simulated redds. Regression coefficients (b) and their 95% confidence limits (CL) for Probit Y = a + b logjg ^, where Y is theecumulative percentage of fry emerging from a simulated redd at different mean temperatures, and X the number of days elapsed since median hatching time (Day 0). Geometric mean (95% confidence limits) age at emergence (days after median hatching time = mean duration of the alevin stage in gravel) for pink salmon fry at different mean redd temperatures. Geometric mean ages at emergence for sibling fry emerging during light and dark of the experimental LD cycle are also shown for each redd, and are compared using the t-test. Period lengths of the diel rhythms of swimming activity and of vertical distribution for six groups of fry tested at different times after emergence. Period length of the cycle of water temperature for each experiment is also given. All period lengths are significantly different (P < 0.05) from random "noise", except where indicated specifically by an asterisk. Spearman rank correlation coefficients (rs) 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 two hours for each of six groups of fish. The fish were observed at different
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