ADAPTIVE SIGNIFICANCE OF VERTICAL MIGRATION BEHAVIOUR OF SKISTODIAPTOMUS OREGONENSIS by DAVID GHAN B.Sc, McGill University, 1987 M.Sc, The University of Toronto, 1991 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 March 1997 David Ghan, 1997 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. 1 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 or her representatives. It is understood that copying or publication of this thesis for financial gain shall not be allowed without my written permission. Department of piD J\ Uy — zru~ The University of British Columbia Vancouver, Canada Date lm/7srA .7 I'/fl"? DE-6 (2/88) 11 Abstract I have studied the adaptive significance of vertical migration of zooplankton in 2 populations of the copepod Skistodiaptomus oregonensis that migrate and 2 populations that do not migrate. Vertical migration of the copepods is associated with the presence of pelagic sticklebacks. This observation is consistent with the hypothesis that the adaptive benefit of vertical migration by S. oregonensis is to avoid stickleback predators. The alternative hypotheses including avoidance of juvenile sockeye predators, foraging efficiency, bioenergetic efficiency, or combined foraging/bioenergetic efficiency are not supported by the comparisons of migratory behaviour of S. oregonensis in the 4 lakes. Both the depth and timing of S. oregonensis migration are consistent with the hypothesis that copepods are avoiding predation by sticklebacks. Light intensities at the depth at which S. oregonensis reside during the day are sufficiently low to.reduce predation risk from visual foraging stickleback and the timing of ascent at dusk and descent at dawn are such that S. oregonensis remain at light intensities that reduce risk from stickleback. S. oregonensis are at the surface at dusk and dawn at the time that juvenile sockeye feed in the surface habitat. Vertical migration appears to be a trade-off with resource acquisition. Phytoplankton are less concentrated in the deep habitat where S. oregonensis reside during the day. Furthermore, migrating copepods contain less phytoplankton as food in their guts than do non-migrating individuals. Ill In vertical columns in the laboratory, the presence or absence of sticklebacks does not influence the vertical distributions of S. oregonensis collected from lakes with either migratory or non-migratory populations. This indicates that the migration phenotype is fixed rather than being a flexible behaviour induced by environmental cues. I developed a dynamic optimization model to predict the optimal depth decisions for S. oregonensis based on depth dependent lake food and temperature conditions, fish abundance and predation rates, and S. oregonensis bioenergetics. The model predicts that vertical migration should occur to avoid sticklebacks under a broad range of modelled conditions, but with a fitness cost due to feeding opportunity costs. This demonstrates quantitatively that it is tenable to hypothesize that vertical migration involves a trade• off between stickleback avoidance and feeding opportunity. Taken together, these results are consistent with the view that different migration behaviours in these populations are a result of divergent evolution driven by environmental variation affecting the optimal solution to the predation risk/resource acquisition trade-off. iv Table of Contents Abstract ii Table of Contents iv List of Tables v List of Figures vi Acknowledgements xii Chapter 1: General Introduction 1 Chapter 2: Testing hypotheses on the benefits and costs of vertical migration by Skistodiaptomus oregonensis by comparing populations 9 Introduction . 9 Methods 10 Results 19 Discussion 48 Chapter 3: The Timing and extent of vertical migration by Skistodiaptomus oregonensis relative to the temporal- spatial distribution of predation risk 58 Introduction 58 Methods 59 Results 63 Discussion . 98 Chapter 4: Vertical migration behavior of Skistodiaptomus oregonensis: constitutive or induced? . 103 Introduction 103 Methods 104 Results 108 Discussion 120 Chapter 5: A dynamic optimization model of Skistodiaptomus oregonensis vertical migration 128 Introduction 128 Model Description 129 Model Results 140 Summary 151 Chapter 6: Thesis Summary 153 References 158 V List of Tables Table 2.1: Physical conditions in the four study lakes. ... 37 Table 2.2: Biological conditions in the four study lakes. 3 8 Table 3.1: ANOVA results testing H0 that initial zooplankton densities in experimental feeding tanks did not differ among light intensity treatments 64 Table 3.2: ANOVA results for each prey type testing Ho that initial densities of the prey types did not differ among treatments 65 Table 3.3: ANOVA results testing Ho that initial zooplankton densities in experimental feeding tanks did not differ among days 69 Table 3.4: Regression results for the effect of light (X) on four Y variables where In(Y+l)=a*ln(X)+b, except for the capture/strike ratio where arcsin(sqrt (Y+l) ) =a*ln(X) +b 78 Table 4.1: Experiment 1 - univariate repeated measures analyses of variance for A) the effect of fishwater [+/-] treatments on the proportion of S. oregonensis below 100 cm during the day and B) the effect of fishwater [+/-] treatments on the change in the proportion of S. oregonensis below 100 cm from night to day 112 Table 4.2: Experiment 1 - nested analyses of variance for depths of individual S. oregonensis: tests of significance for fishwater [+/-] treatment effects and tube within treatment effects 114 Table 4.3: Experiment 2 - univariate repeated measures analyses of variance for A) the effect of fishwater [+/-] treatments on the proportion of S. oregonensis below 100 cm during the day and B) the effect of fishwater [+/-] treatments on the change in the proportion of S. oregonensis below 100 cm from night to day 118 Table 4.4: Experiment 2 - nested analyses of variance for depths of individual S. oregonensis: tests of significance for fishwater (+/-) treatment effects and tube within treatment effects 119 Table 4.5: Experiment 3 - nested analyses of variance for depths of individual S. oregonensis: tests of significance for fish (+/-) treatment effects and tube within treatment effects 123 vi List of Figures Fig. 2.1: Location of the four study lakes in southwestern British Columbia 11 Fig. 2.2: Map of Great Central Lake showing sample location (X) and lake contours in meters. Depth contours taken from Rutherford et al. (1986) 12 Fig. 2.3: Map of Hobiton Lake showing location of sample site (X) and lake contours in meters 13 Fig. 2.4: Map of Kennedy Lake showing location of sample site (X) and depth contours in meters 14 Fig. 2.5: Map of Paxton Lake showing location of sample site (X) and depth contours in meters 15 Fig. 2.6: Day (hatched bars) and night (solid bars) vertical distribution for 5 metasome length classes of S. oregonensis in Kennedy Lake on August 25, 1993 20 Fig. 2.7: Day (hatched bars) and night (solid bars) vertical distribution for 5 metasome length classes of S. oregonensis in Kennedy Lake on November 12, 1992. ... 21 Fig. 2.8: A) Mean day and night depth of 750-850 um metasome length S. oregonensis in Kennedy Lake on 13 sample dates from 1992-1994. B) Mean day and night depth of 3-50 um size fraction of phytoplankton in Kennedy Lake from 13 sample dates from 1992 to 1994. C) Data in part A and B redrawn to compare mean day and night depth of S. oregonensis with mean day and night depth of 3-50 um size fraction of phytoplankton 22 Fig. 2.9: Vertical distribution of chlorophyll a from the 3-50 um size fraction of phytoplankton on 12 sample dates in Kennedy Lake 23 Fig. 2.10: Depth distribution of temperature (open circles) and of chlorophyll a from the 3-50 um size fraction of phytoplankton day (open squares) and night (solid squares) on six sample dates 25 Fig. 2.11: Changes in density of S. oregonensis in three depth strata of Paxton Lake during dawn of August 19, 1994. 26 Fig. 2.12: Changes in density of S. oregonensis in three depth strata of Paxton Lake during dusk of August 19, 1994 27 Fig. 2.13: Day and night vertical distribution of chlorophyll a from the 3-50 um size fraction of phytoplankton in Paxton Lake, August, 1994 28 vii Fig. 2.14: Day (hatched bars) and night (solid bars) vertical distribution for 5 metasome length classes of S. oregonensis in Great Central Lake on July 7, 1992. 30 Fig. 2.15: Day (hatched bars) and night (solid bars) vertical distribution for 5 metasome length classes of S. oregonensis in Great Central Lake on August 18, 1992. • 31 Fig. 2.16: A) Mean day and night depth of 750-850 um metasome length S. oregonensis in Great Central Lake on 7 sample dates in 1992 and 1993. B) Mean day and night depth of 3-50 um size fraction of phytoplankton in Great Central Lake from 7 sample dates from 1992 and 1993. C) Data in part A and B redrawn to compare mean day and night depth of S. oregonensis with mean day and night depth of 3-50 um phytoplankton 32 Fig. 2.17: Day (hatched bars) and night (solid bars) vertical distribution for 5 metasome length classes of S. oregonensis in Hobiton Lake on August 5, 1992. ... 33 Fig. 2.18: Day (hatched bars) and night (solid bars) vertical distribution for 5 metasome length classes of S.