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Foraging behaviour and perceived predation risk of juvenile chinook salmon (Oncorhynchus tshawytscha)… Gregory, Robert S. 1991

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FORAGING BEHAVIOUR AND PERCEIVED PREDATION RISK OF JUVENILE CHINOOK SALMON (ONCORHYNCHUS TSHAWYTSCHA) IN TURBID WATERS. by ROBERT S. GREGORY BSc(Honours Biology) Acadia University 1980 MSc(Biology) Trent University 1984 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 February 1991 ©  Robert S. Gregory  1991  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. copying  of this thesis for scholarly  department  or  by  his  or  her  I further agree that permission for  purposes  may be granted  representatives.  It  is  by the head of my  understood  that  publication of this thesis for financial gain shall not be allowed without permission.  Department of  Zoology  The University of British Columbia Vancouver, Canada Date  DE-6 (2/88)  A p r i l 22, 1991  extensive  copying  or  my written  ii  ABSTRACT  I investigated the e f f e c t of  juvenile  I examined a  and "perceived"  behavioural  to  Chinook  log-linear  tshawytscha)  "tradeoff"  by measuring the  planktonic Artemia prey.  decline  in reaction  To determine the e f f e c t s rate,  on the foraging behaviour in the  between  laboratory.  visual  ability  risk.  I assessed visual ability a  turbidity  Chinook salmon (Oncorhynchus  Specifically,  juvenile  of  I conducted separate  distance  reaction  with increasing  experiments f o r  surface  prey  (Drosophila),  turbidity  25, 50, 100, 200, 400, 800 mg-L ).  were reduced at  turbidity.  of turbidity and microhabitat on foraging  and benthic (Tubifex)  (0,  of  I found Chinook exhibited  planktonic (Artemia), levels  distance  across a range of Foraging rates  -1  higher turbidity  conditions f o r  all three  prey.  However, f o r surface and benthic prey, foraging rates were also low in clear levels  water; highest rates (50-200  mg-L ).  were attained  The  -1  degree  at  intermediate  turbidity  to which intermediate  turbidities  were associated with higher foraging rates was size-dependent. individuals clear  (150-57  conditions  mm FL) than  did larger  foraging rates  by juveniles  regardless  fish size.  In  of  experiments  exhibited relatively individuals.  were consistently  manipulating light  level  higher However,  foraging rates in planktonic  high in clear independent  water,  of  I allowed salmon to forage under conditions which were either clear  but  with light  intensity  correspondingly reduced.  Smaller  turbidity, turbid, or  Foraging  rates  were similar between the two treatments f o r planktonic prey, but differed f o r benthic and surface prey. exhibited by of  visual  juvenile  ability  Generally, foraging rates  Chinook salmon could not be explained on the  alone.  I suggest  that  basis  young salmon also exhibited  iii foraging  behaviour  consistent  with t h e i r  perception  of  risk  to  predation. In  arena  randomly  in  turbid  the bottom. altered of  experiments,  juvenile  conditions;  Chinook  in c l e a r  conditions  When bird and f i s h p r e d a t o r  their  spatial distribution,  turbidity.  However,  their  occupying  response time.  the  predation  in juvenile  of  of  turbidity  either  prey  quality  microhabitats apparent  on or  foraging perceived  (surface,  water  behaviours.  Perceived  risk  of  of  conditions  a  non-visual  perceived  less  I conclude behaviour ability  "fixed-risk" risk that  as  stimulus  turbidity in  turbid  in a manner c o n s i s t e n t  and  perceived  risk.  was  less  mitigated  to  the  model r e s o l v e d  and o t h e r predation  (sound),  salmon  general in  three the  foraging was  d i f f e r e n t between s u r f a c e and w a t e r column microhabitats. to  regardless  Assuming d i f f e r e n c e s  p r e d a t i o n in  planktonic Chinook  with  Chinook.  column, bottom),  dissimilarities between  regions  model t h a t p r e d i c t e d t h e  behaviour. risk  associated  Turbidity a p p a r e n t l y  I developed a conceptual t r a d e o f f effect  deeper  in t u r b i d  a shorter  risk  they  themselves  models were i n t r o d u c e d t h e f i s h  m a r k e d and l a s t e d f o r perceived  distributed  significantly When e x p o s e d  apparently  increased. waters  juvenile  with a t r a d e o f f  salmon exhibit between t h e i r  foraging visual  iv TABLE  OF CONTENTS Page  ABSTRACT LIST OF TABLES  ii .  vii  LIST OF FIGURES  viii  ACKNOWLEDGEMENTS  xiii  Chapter  1. G E N E R A L I N T R O D U C T I O N  C h a p t e r 2. B A C K G R O U N D A N D H Y P O T H E S E S 2.1 Turbidity and Vision 2.2 Turbidity and Foraging Ability 2.3 Turbidity and Predation Risk 2.4 Foraging Under Risk of Predation 2.5 Hypotheses and Experiments Conducted - Visual Ability - Alteration o f Search Behaviour - Enhancement o f Visual C o n t r a s t - Predation Risk - The Ability-Risk T r a d e o f f C h a p t e r 3. G E N E R A L M E T H O D S 3.1 The Study Animal 3.2 Turbidity 3.3 Experiments on Foraging Rate - Prey - Pre-Experimental Conditioning - Experimental Apparatus - Experimental P r o t o c o l 3.4 Spatial Distribution and P r e d a t o r Models - Experimental Apparatus - Pre-Experimental Conditioning 3.5 S t a t i s t i c s C h a p t e r 4. V I S U A L A B I L I T Y A N D F O R A G I N G B E H A V I O U R 4.1 Reaction Distance - Visual Ability - Introduction - Methods experimental apparatus conditioning and observation p r o t o c o l - Results - Discussion  1  ;....  4 4 5 7 8 10 10 11 11 12 12 14 14 15 16 16 19 20 22 23 23 26 28 29 29 29 30 30 32 33 35  V  4.2 Foraging Rates f o r S u r f a c e , Planktonic, and Benthic Prey - Introduction - Methods the e f f e c t of turbidity on foraging r a t e the e f f e c t s o f ontogeny on foraging r a t e in turbid conditions - Results s u r f a c e foraging planktonic foraging benthic foraging the e f f e c t of ontogeny and turbidity on foraging behaviour - Discussion e f f e c t o f turbidity on foraging r a t e e f f e c t s o f ontogeny 4.3 The E f f e c t of Turbidity and Light on Foraging Behaviour - Introduction - Methods - Results s u r f a c e foraging planktonic foraging benthic foraging - Discussion  Page  C h a p t e r 5. M I C R O H A B I T A T S H I F T S A N D R E S P O N S E S T O PREDATORS 5.1 Spatial Distribution - Introduction - Methods - Results - Discussion 5.2 Responses to Model P r e d a t o r s - Introduction - Methods the magnitude o f the e f f e c t the duration of the e f f e c t - r e c o v e r y f r o m p r e d a t o r disturbance - Results the magnitude of the e f f e c t the duration o f the e f f e c t - Discussion C h a p t e r 6. A C O N C E P T U A L M O D E L O F F O R A G I N G B E H A V I O U R UNDER VISUAL C O N S T R A I N T 6.1 Introduction 6.2 The E f f e c t o f Visual Ability on Foraging Rate 6.3 The E f f e c t o f Perceived Risk of Predation on Foraging Rate 6.4 The T r a d e o f f  35 35 37 37 38 38 38 41 43 45 47 47 49 53 53 54 55 55 56 56 60 62 62 62 63 64 65 71 71 73 73 75 76 76 78 85 91 91 92 95 99  vi Page 6.5 Predictions o f the Model and Re-Interpretation Foraging Rates - The E f f e c t of Prey Quality and Microhabitat - The E f f e c t o f Enhanced Risk 6.6 Synopsis  of  C h a p t e r 7. T E S T S OF T H E V I S U A L A B I L I T Y - P E R C E I V E D RISK T R A D E O F F 7.1 The E f f e c t of Microhabitat and Prey Quality on Foraging Decisions - Introduction - Methods - Results - Discussion 7.2 The E f f e c t of Enhanced Risk on Foraging Rate in Turbid Water - Introduction - Methods - Results - Discussion  103 103 106 108 110 110 110 112 113 115 118 118 120 122 127  C h a p t e r 8. G E N E R A L D I S C U S S I O N A N D C O N C L U S I O N S 8.1 General Discussion - Vision as a C o n s t r a i n t - Turbidity and the Risk o f Predation - T r a d e o f f s Between Visual Ability and Perceived Risk in Fish Foraging Behaviour - Turbid Water Foraging in Fishes - Salmonid Life Histories - Perceived Risk in Behaviour Studies 8.2 Conclusions  132 133 134 135 137  LITERATURE  140  APPENDICES Appendix  CITED  131 131 131 131  152 1. Individual Feeding Trials f o r Drosophila, Listed by Experiment 152 Appendix 2. Individual Feeding Trials f o r A r t e m i a , Listed by Experiment 157 Appendix 3. Individual Feeding Trials f o r T u b i f e x , Listed by Experiment 162 Appendix 4. Godin ,T .1. and R . S . G r e g o r y , (in p r e p . ) abstract 166  vii  LIST OF  Table  3.1.  Physical foraging  Table  Table  4.1.  5.1.  Table  5.2.  5.3.  visual  rate  characteristics  of  prey  used  in  determinations  17  Analysis o f variance o f the e f f e c t o f turbidity and y e a r o f experiment on t h e f o r a g i n g r a t e o f juvenile Chinook salmon t o A . S u r f a c e p r e y (Drosophila), B. Planktonic prey (Artemia), a n d C . Benthic prey (Tubifex) The effect juvenile  Table  and  TABLES  of  Chinook  turbidity salmon  on the by  spatial  distribution  39  of  region  66  T h e e f f e c t o f t u r b i d i t y o n A . T h e l a t e r a l a n d B. T h e v e r t i c a l d i s t r i b u t i o n o f j u v e n i l e Chinook s a l m o n b y pooled region  67  T h e e f f e c t of Chinook s a l m o n The surface  69  t u r b i d i t y on p e r c e n t a g e o f juvenile a s s o c i a t e d with A . T h e b o t t o m a n d B.  Table  5.4.  Analysis o f variance o f the e f f e c t s o f turbidity, c o v e r , and e x p o s u r e t o p r e d a t o r models on p r o p o r t i o n s o f j u v e n i l e C h i n o o k s a l m o n l o c a t e d in A . D e e p e r w a t e r ; a n d B. S h a l l o w e r w a t e r o f an e x p e r i m e n t a l a r e n a . .. 79  Table  5.5.  Analysis o f variance o f the e f f e c t s o f turbidity, c o v e r , a n d p r e d a t o r t y p e on r e c o v e r y time f r o m e x p o s u r e t o mode) p r e d a t o r s  87  viii LIST OF FIGURES Figure 3.1. Aquarium a r r a y used f o r determinations o f foraging rate.  Figure 3.2.  Figure 3.3.  Figure 3.4.  A . Schematic r e p r e s e n t a t i o n .  B. P h o t o g r a p h .  21  The relationship o f turbidity concentration used in foraging r a t e experiments with measures o f light transmission . A . Nephelometric Turbidity Units . B . Light e n e r g y .  24  Arena used during experiments on spatial distribution and predation risK manipulation . Schematic r e p r e s e n t a t i o n . B . Photograph  25  The e f f e c t  A .  o f depth and turbidity concentration on  light, within the experimental arena  (Fig. 3.3).  ..  Figure 4 . 1 . Schematic r e p r e s e n t a t i o n o f the experimental apparatus used f o r the determination o f reaction distances Figure 4.2. The e f f e c t  o f turbidity on the reaction distance o f  juvenile Chinook salmon f o r Artemia p r e y .  Figure 4 . 3 . The e f f e c t s o f turbidity on mean foraging r a t e o f juvenile Chinook salmon feeding on s u r f a c e prey and the percentage o f salmon foraging in 70-L aquaria. A . 1987 - 5 t r i a l s . B. 1988 - 3 trials  27  31 34  40  Figure 4.4. The e f f e c t s o f turbidity on mean foraging r a t e o f juvenile Chinook salmon feeding on planktonic prey and the percentage o f salmon foraging in 70-L aquaria. A . 1987 - 5 t r i a l s . B. 1988 - 3 trials 42 Figure 4 . 5 . The e f f e c t s o f turbidity on mean foraging r a t e o f juvenile Chinook salmon feeding on benthic prey and the p e r c e n t a g e o f salmon foraging in 70-L aquaria. A . 1987 - 5 t r i a l s . B. 1988 - 3 trials  44  Figure 4.6. E f f e c t o f size o f juvenile Chinook salmon on the slope o f the ascending limb (0-100 mg*L~ ) o f the relationship between foraging r a t e and turbidity . A. S u r f a c e p r e y - Drosophila. B. Planktonic p r e y Artemia . C . Benthic p r e y - Tubif ex 46 1  Figure 4 . 7 . Hypothetical e f f e c t s on foraging r a t e o f variables differentially a f f e c t e d by turbidity and ontogeny. A . Matched e f f e c t s . B . O f f s e t e f f e c t s  52  ix Figure 4.8.  The e f f e c t on juvenile Chinook salmon o f turbidity and light level on foraging r a t e f o r s u r f a c e prey (Drosophila ). A . Mean foraging r a t e . 8 . Composite trial ~ T 57  Figure 4.9.  The e f f e c t on juvenile Chinook salmon o f turbidity and light level on foraging r a t e f o r planktonic p r e y (Artemia). A. Mean foraging r a t e . B. Composite trial.  Figure 4.10. The e f f e c t on juvenile Chinook salmon of turbidity and light level on foraging r a t e f o r benthic prey (Tubifex). A. Mean foraging r a t e . B. Composite trial 7 Figure 5.1.  Figure 5.2.  Figure 5.3.  58  59  The e f f e c t o f turbidity on the p r o p o r t i o n o f juvenile Chinook salmon in the lower 20 cm o f a 40 cm deep experimental arena  68  The immediate spatial r e s p o n s e o f juvenile Chinook salmon to exposure to p r e d a t o r models in clear and turbid conditions; p r o p o r t i o n o f f i s h in the deepest region of an experimental arena in, A . The absence and B. The p r e s e n c e o f additional cover in two replicates  77  The immediate spatial r e s p o n s e o f juvenile salmon to exposure to p r e d a t o r models in turbid conditions; p r o p o r t i o n of f i s h near s u r f a c e in deep water o f an experimental A. The absence and B . The p r e s e n c e o f cover in two replicates  80  Chinook clear and the arena i n , additional  Figure 5.4.  Changes in microhabitat distribution in juvenile chinook salmon, b e f o r e and a f t e r exposure to a model bird p r e d a t o r , in clear (A. and B.) and turbid (C. and D.) water with additional cover 81  Figure 5.5.  Changes in microhabitat distribution in juvenile chinook salmon, b e f o r e and a f t e r exposure to a model bird p r e d a t o r , in clear (A . and B.) and turbid (C . and D.) water without additional cover 82  Figure 5.6.  Changes in microhabitat distribution in juvenile chinook salmon, b e f o r e and a f t e r exposure to a model f i s h p r e d a t o r , in clear (A. and B.) and turbid (C. and D .) water with additional cover 83  X  Figure  Figure  5.7.  5.8.  Figure  6.1.  Figure  6.2.  C h a n g e s in m i c r o h a b i t a t d i s t r i b u t i o n in j u v e n i l e chinooK salmon, b e f o r e and a f t e r e x p o s u r e to f i s h p r e d a t o r , in c l e a r ( A . a n d B.) and turbid a n d D .) w a t e r w i t h o u t a d d i t i o n a l c o v e r  T h e e f f e c t o f turbidity and additional c o v e r on r e c o v e r y time o f juvenile c h i n o o k salmon after e x p o s u r e t o model p r e d a t o r s The  effect  of  turbidity  T h e e f f e c t o f visual foraging, P(F A)I H o l l i n g ' s (1959) " d i s c " rate a  V  Figure  6.3.  Figure  6.4.  Figure  Figure  6.5.  6.6.  6.7.  n  d  on  visual  ability  effect  of  turbidity  The  effect  of  perceived  on  perceived  86  (VA).  risk  of  risk  ...  (PR).  predation  on  84  the  ability o n : A . P r o b a b i l i t y of §• F o r a g i n g r a t e using equation solved f o r search  The  94  96 ..  98  A.  p r o b a b i l i t y o f f o r a g i n g P ( F p R ) , a n d B. f o r a g i n g r a t e u s i n g H o l l i n g ' s (1959) " d i s c " e q u a t i o n , s o l v e d f o r h y p o t h e t i c a l e f f e c t s o f p e r c e i v e d r i s k on s e a r c h rate  100  A c o n c e p t u a l model o f the e f f e c t o f a behavioural t r a d e o f f b e t w e e n visual ability and p e r c e i v e d r i s k o n r e l a t i v e f o r a g i n g r a t e in t u r b i d w a t e r s  102  Predicted perceived  Figure  a model (C.  relative  foraging  rates  at  two  levels  of  risk  104  H y p o t h e t i c a l e f f e c t o f enhancing r i s k stimuli on foraging r a t e f o r planktonic p r e y . A . Assuming d e c r e a s e in p e r c e i v e d r i s k a s a f u n c t i o n o f turbidity. B . A s s u m i n g a d e c r e a s e in f i x e d - r i s k as a function of turbidity  107  Figure  6.8.  H y p o t h e t i c a l e f f e c t o f e n h a n c i n g r i s k stimuli on f o r a g i n g r a t e f o r s u r f a c e and benthic p r e y . A. A s s u m i n g d e c r e a s e in p e r c e i v e d r i s k a s a f u n c t i o n o f turbidity. B . A s s u m i n g a d e c r e a s e in f i x e d - r i s k as a function of turbidity 109  Figure  7.1.  T h e e f f e c t o f t u r b i d i t y on f o r a g i n g r a t e chinook salmon. A . Surface foraging f o r  in j u v e n i l e Drosophila  and dried Artemia p r e y . B. P l a n k t o n i c foraging Artemia and P o l y s o r b a t e - 8 0 t r e a t e d D r o s o p h i l a .  ..  114  xi Figure 7.2.  Figure 7.3.  Figure 7.4. Figure 7.5. Figure 7.6.  The e f f e c t of turbidity and microhabitat on the c o e f f i c i e n t of variation (/.) in foraging r a t e by juvenile chinook salmon in individual t r i a l s . A. Artemia . B. Drosophila  116  Apparatus modifications to accommodate " r i s k enhancement" experiments . A . Schematic representation. B. Photograph  121  The e f f e c t  o f turbidity and risk on mean foraging  The e f f e c t  of turbidity and risk on mean foraging  The e f f e c t  o f turbidity and risk on mean foraging  r a t e on s u r f a c e p r e y by juvenile chinook salmon. . . r a t e on planktonic prey by juvenile chinook salmon. r a t e on benthic prey by juvenile chinook salmon. . .  123 125 126  Figure 7.7  The e f f e c t o f turbidity on the d i f f e r e n c e between c o n t r o l and enhanced risk foraging r a t e s by juvenile chinook salmon . A . S u r f a c e foraging - Drosophila . B. Planktonic foraging - Artemia. C . Benthic foraging - Tubifex 128  Figure A l .  Effect  o f turbidity on the foraging r a t e of  juvenile  Figure A2.  Effect  of turbidity on the foraging r a t e o f  juvenile  Effect  of A . Light and B.  Figure A3.  chinook salmon f o r Drosophila p r e y ,  chinook salmon f o r Drosophila p r e y ,  1987  1988  Turbidity on the foraging  r a t e o f juvenile chinook salmon f o r Drosophila p r e y .  152 153 154  Figure A4.  E f f e c t o f turbidity on the foraging r a t e of juvenile chinook salmon f o r A . S u r f a c e Drosophila and B. Planktonic Drosophila 155  Figure A5.  E f f e c t of turbidity on the foraging r a t e o f juvenile chinook salmon f o r Drosophila prey in A . "Normal" and B. "Enhanced" r i s k . 156  Figure A 6 .  Effect  of turbidity on the foraging r a t e o f  juvenile  Figure A7.  Effect  o f turbidity on the foraging r a t e o f  juvenile  Figure A8.  Effect  of A . Light and B.  chinook salmon f o r Artemia p r e y ,  chinook salmon f o r Artemia p r e y ,  1987  1988  Turbidity on the foraging  r a t e of juvenile chinook salmon f o r Artemia p r e y .  157 158 159  xii Figure A 9 .  Figure A10.  Figure A l l . Figure A12. Figure A13.  E f f e c t of turbidity on the foraging r a t e o f juvenile chinook salmon f o r A . S u r f a c e Artemia and B. Planktonic Artemia  160  E f f e c t of turbidity on the foraging r a t e of juvenile chinook salmon f o r Artemia prey in A . "Normal" and B. "Enhanced" risk 161 Effect  of turbidity on the foraging r a t e o f  juvenile  Effect  of turbidity on the foraging r a t e o f  juvenile  Effect  o f A . Light and B.  chinook salmon f o r Tubifex p r e y ,  chinook salmon f o r Tubif ex p r e y ,  1987  1988  Turbidity on the foraging  r a t e o f juvenile chinook salmon f o r Tubif ex p r e y .  162 163 164  Figure A14.  E f f e c t of turbidity on the foraging r a t e of juvenile chinook salmon f o r Tubif ex p r e y in A . "Normal" and B . "Enhanced" risk 165  Figure A15.  E f f e c t o f A . Prey c o l o u r , B. Background t u r b i d i t y , and C . Both f o r e g r o u n d and background turbidity, on the reaction time of juvenile chinook salmon f o r Artemia prey (Godin and G r e g o r y in p r e p . ) 167  xiii  ACKNOWLEDGEMENTS  Financial support f o r these studies was provided by a Natural Sciences  and Engineering Council (NSERC) operating grant  (#5-83454  to  T.G. Northcote), and a Fisheries and Oceans Canada, Subvention Grant (#5-56574).  Personal support was provided by NSERC Postgraduate  Scholarships,  a University  Graduate  Fellowship (UBC), UBC Teaching  Assistantships, and the above operating grant to T.G. Northcote.  I am  grateful f o r these sources of funds. Juvenile chinook were obtained through the cooperation of Chehalis hatchery  River  Fish  Hatchery.  manager, f o r  I particularly  expediting requests.  wish to  thank  the  Larry  Kahl,  Additional equipment was  provided by Cultus Lake Laboratory (Department of Fisheries and Oceans); I especially  thank  Dennis Martens.  The many hours of laboratory analysis were conducted by Theresa Godin, Melanie Tom Suzuki.  Johnston,  Ira  Leroy,  Regina Schiffer,  Lisa Sennewald, and  Many of the potential pitfalls often encountered when  maintaining fish at the South Campus Fisheries Compound were avoided with the advice and assistance of Rick Taylor. investigations  added much valuable  I have presented. without  the help of  Daniel, Theresa  Field and other  supporting information to  the  efforts  These investigations could not have been conducted Dana Atagi, Jim Berkson, AndrS Breault, Colin  Godin, Lois  Hollett,  Ira  Leroy,  Trish MacEachern, Carin  Magnhagen, Lana Mah, Tom Northcote, Regina Schiffer, Tom Suzuki, and Peter  Watts.  My sincere  I wish to McPhail, W.E.  thank  gratitude  my research  Neill, T.G. Northcote,  is extended to  all these individuals.  committee: Dr.'s K.D. Hyatt, and D.J.  Randall  for  their  J.D. support,  advice, and encouragement throughout the course of my investigations. My supervisor, Tom Northcote, is especially thanked f o r his support and  xiv uncanny ability to find funds f o r me to hire summer students each year. I owe a special debt of occasions took a great  gratitude  to Bill Neill, who on numerous  deal of time to critically review my research  plans and generally kept me on track. of  Dr.'s  J.  Gosline, M.C. Healey,  T.G. Northcote,  K.M.J. McErlane performing as chairman. G. Power (University  of  The defense committee consisted D.J.  Randall, with  The external examiners were Dr.  Waterloo) and Dr. J.D. Hall (Oregon State  University). The various  seminars in "the  Institute" provided a comprehensive  appraisal of the do's and don'ts of research.  Nancy Butler, Moira  Greaven, Glyph and the gang, Wes Hochachka, Dave Levy, Barbara McGregor, Debbie McLennan, and Peter Watts provided an endless supply of constructive  criticism, advice, amusement or  stages of my research.  encouragement  during all  In addition to my research committee, Lana Mah  and Peter Watts proofread d r a f t s of various chapters, greatly improving the manuscript.  Wes Hochachka painstakingly reviewed  anticipation of the defense.  the manuscript in  My many thanks are extended to these  individuals. My family and friends were a constant source of support. you made the  tribulations  bearable.  Lana,  1 CHAPTER 1  GENERAL  INTRODUCTION  No single topic in animal ecology receives feeding.  The  acquisition and assimilation of  linKed to f a c t o r s  such as growth, size at  survival, resistance few.  to  than  food has been variously  maturity, reproductive output,  disease, and social dominance, to  name but a  Placed at the same level of importance are behavioural and  morphological f a c t o r s perhaps every or  more attention  inevitable  associated with the  that  these  factors  animal is the prey of another.  avoidance of  predators.  will eventually  conflict.  It  Almost  Often, the very act of obtaining  searching f o r food places a foraging animal at risk to predators.  such instances, foragers must "trade o f f " the benefits of foraging against experimentally  the  costs  of  potentially  examined such a tradeoff  (Oncorhynchus  is  being, eaten  for  In  further  while doing so.  juvenile chinook salmon  tshawytscha).  A rich literature has developed over the past decade regarding behavioural t r a d e o f f s Lima and Dill 1990). investigations  of It  foraging and risk of predation (for  has been amply demonstrated in these  that animals respond to increased risk of  predation by  altering their foraging behaviour, often at the expense of intake. (for  Much of  this literature  review: Dill 1983 and  1986).  My work  review:  has been directed at  1987; Werner  and  Gilliam  lies within the general framework  energy  fish behaviour 1984; Milinski  of these studies.  However, the investigations I have conducted focus on an aspect of foraging  ecology  "perceived" risk between its  visual  effect  of  of  little  predation.  ability  on the  Underwater degree  receiving  attention  - visual  ability  I examined a behavioural  and perceived risk  foraging decisions of  of  tradeoff  predation and  juvenile  and investigated  chinook salmon.  images are generally poor in quality, due to the high  light attenuation  in most aquatic  systems  (Duntley  1963).  I  2 This attenuation particulate  is attributed  material  interference  by  to  the  presence  of  light-scattering  (e.g. plankton and suspended sediment), and to  water  molecules themselves.  Despite this  characteristic, most fish species depend on vision f o r sensory  input  elevated  turbidity,  acute.  (Hyatt  the  Visual range  concentration  1979; Miller  foraging ability  dissemination  declines  (Duntley  1979; Guthrie of  light  precipitously  much of  1986). signals  as  subsequent behaviour  is  especially  a function of of  their  In conditions of  1943; DiToro 1978) and must a f f e c t  and the  environmental  particle  visual  fish.  Chinook salmon have been demonstrated to occupy turbid estuaries for  a significant  Simenstad et  portion of  al. 1982).  its  susceptibility  to  1986). the  ability  (Levy  and Northcote 1982;  an unique opportunity  detection by its  1  to locate prey and  The hunting  salmonids predominantly involve the  the detection of and the  predators.  their prey (Hobson 1979; Guthrie may act  perceived risk  of  to  simultaneously  al. 1978; Gardner species rear  and foraging rate 1981), juveniles  in estuarine  of  (Vinyard  of  turbidity  and O'Brien 1976; Confer  et  many marine and anadromous fish  nurseries having high concentrations  suspended sediment (Blaber and Blaber Simenstad et  reduce  foraging chinook.  Despite evidence demonstrating the negative e f f e c t s on visual ability  to  environment  both the ability of a f o r a g e r  Therefore, increased turbidity  visual  life  in conditions where the  techniques of most predators of visual sense f o r  early  Turbidity presents  examine foraging behaviour simultaneously a f f e c t s  their  of  1980; Levy and Northcote 1982;  al. 1982; Cyrus and Blaber  1987a).  Juveniles of  several  species of fish have been shown to actively p r e f e r turbid over clear water (Cyrus and Blaber 1987b).  The presence of these fish in such  ^ I use the term "forager" when referencing juvenile salmon or any animal in a similar trophic position. "Prey" are food items consumed by foragers. A "predator" is an animal which consumes foragers. "Predation" occurs between predators and foragers; "foraging" occurs between foragers and prey.  3 waters has most commonly been attributed to the large prey densities in these  productive To  habitats.  investigate  perceived risk  potential tradeoff  between visual ability  in turbid conditions, I examined key  foraging  behaviour  effects  of  of  the  related  turbidity  to  visual constraints.  on reaction  predation, and their  of  fish  These included the  distance, light levels, perceived  subsequent e f f e c t s  Juvenile chinook salmon are  aspects  and  risk  on foraging behaviour.  generalist  foragers  (Keast 1979)  feeding on a variety of prey species from several microhabitats (Levy et al. 1979; Northcote  et  al. 1979; Healey  1982).  I investigated  the  e f f e c t of turbidity on the foraging rate of chinook f o r prey from each of  three generalized microhabitats frequented by these fish: surface,  water column, and bottom. levels  is  microhabitat  The e f f e c t  specific.  T h e r e f o r e , I also conducted  experiments to compare the e f f e c t s foraging behaviour  of  these  of turbidity on ambient light  of turbidity and light level on the  fish.  It has been suggested that turbidity provides a form of cover  for  foraging fish, especially  1980; Simenstad et concerning the  al. 1982; Bruton  juvenile forms (Blaber and Blaber 1985).  perceived predation risk  conditions, using both model p r e d a t o r s Using this information and that  protective  I tested of  several  hypotheses  juvenile chinook in turbid  and non-visual risk stimuli.  from experiments on visual ability  and  foraging rates, I constructed a conceptual tradeoff model to describe the  foraging behaviour  of  juvenile chinook salmon in turbid conditions.  I also tested assumptions made by this model regarding the e f f e c t s of turbidity  on the  risk  perceived by  juveniles  in turbid waters.  4 CHAPTER 2  Chapter  BACKGROUND AND  2.1  TURBIDITY  AND  HYPOTHESES  VISION  The teleost eye conforms to the general vertebrate plan, having an approximately outwardly 1986).  spherical  chamber  containing an inverted  facing receptors, and a focusable lens (for  Acclimation to  different  light  intensities  is  retina, with review: Guthrie  accomplished by  the movement of the outer segments of the receptors relative to the pigment of  layer  (Brett  and Ali 1958; Guthrie  fish visual pigments is largely  the  ambient wavelengths  McFarland 1977). different  of  Individual  1986).  The sensitivity  range  species specific and dependent upon  light particular  to the habitat  (Munz and  species have been shown to possess  pigments in different  habitats  (Munz 1958; Levine  MacNichol 1979) and individuals may modify pigments over  and  a period of  weeKs to new habitat  conditions (Muntz and Wainwright 1978).  However,  most  fish  exhibit their  ambient  light  conditions  apparently of  Visual ability  their in fish  natal  highest  habitat  sensitivity  to  the  (Guthrie 1986).  is commonly measured behaviourally  as  the  reaction distance - the distance at which a foraging fish reacts to a prey  item.  Visual ability  however,  is a function of  both the  visual  acuity of the forager and the scattering properties of the medium. Visual acuity is expressed as the minimum detectable angle subtended by a target on the retina of the subject (Tamura 1957).  The scattering  properties of media are defined by the scattering or  attenuation  coefficient  (a)  absorbed or effect  the proportion of  scattered  a collimated light beam that is  within one meter  (Duntley  1963).  The principal  of scatter is to reduce the visual contrast of a target with its  background. (Tamura  as  Much work has been done on the visual acuity of fish  1957; Hairston et  al. 1982; Li et  al. 1985) or  on emphasizing  5 its  relevance  to  foraging  (O'Brien et  Little research on the e f f e c t been performed (Hester contrast  is  as  as  al. 1984).  of contrast on fish visual perception has  1968).  influential  al. 1976; Mills et  However, it is widely recognized that acuity  on visual perception (Duntley 1963;  Hemmings 1966 and 1975; Lythgoe 1966 and 1980; Munz and McFarland 1977; McFarland  1986), especially  Turbidity  Chapter  primarily  2.2  affects  TURBIDITY  Evolutionary include: sensory sensory (Miller  in turbid the  AND  water  resolution of  FORAGING  adaptations  (Duntley  of  visual  1943; DiToro 1978). contrast.  ABILITY  fish species living in turbid waters  barbels, cutaneous  sense  organs, extensive cephalic-  networks, and electric, olfactory, and acoustic  1979; Bruton  1985).  Chinook  salmon exhibit no evidence  these, although the use of olfactory documented (Northcote  1984).  receptors of  cues in migration has been well  Although juvenile  sockeye salmon  (Oncorhynchus nerka) have been demonstrated to respond to food extracts by  initiating  could only  search  behaviour  (McBride et  be " accomplished visually.  al. 1963), effective  Juvenile chinook  1  foraging rates 300 times lower in near-dark lit  conditions (Gregory  (Brett and Groot primarily  sense  unpublished data). visually.  I apply  salmon exhibited  conditions as those in well-  Data f o r  1963) suggest similar e f f e c t s  prey  feeding  of  juvenile  light.  sockeye  Chinook salmon  this observation as  a working  principle. Of the various components of feeding strategy (for review: Hyatt 1979), prey  encounter  rate is likely  to be the most directly  influenced  by turbidity, although prey capture rate may also be affected.  Reduced  reaction distance in turbid conditions has been demonstrated  repeatedly  (Vinyard  and O'Brien 1976; Confer  Also,  on prey  avoidance responses (Drenner  et  al. 1981; Crowl 1989).  work  et al. 1978; Vinyard 1980; Eggers  6 1982) suggests that higher probabilities of prey escape may be associated  with turbid water, potentially  The e f f e c t  of turbidity on these rates is likely to have a negative  impact on foraging ability. ability, fish must alter are  to  maintain their  with their  In order of  demonstrate behaviour  their  food intake.  1982; Simenstad et  the  required  behavioural  and feed effectively  foraging behaviour  chinook  exhibit three  planktonic, or  surface  foraging.  Feeding at  to  1979; Levy  alter  their  will possess  affected  by turbidity.  specific  light  contrast benthic  the  these involves  surface  highest  different  All may be modified in  will result  in the  illumination, possibly the  Here,  the  in turbid conditions are  increasing  visual  Near-surface least  dynamics imposed by  particularly  will become progressively  turbidity,  taking of  Feeding on plankton will be affected by depth  conditions.  organisms  foraging  feeding: benthic,  predominantly insect prey trapped on the surface tension. waters  et  pers. obs.), may  general modes of  Each of  the  they  waters.  risks, and required search behaviour.  conditions.  if  Juvenile chinook salmon,  flexibility  in turbid  rate.  this decrease in  al. 1982; Gregory  Juvenile  turbid  of  capture  generalized feeding habits (Dunford 1975; Keast  al. 1979; Healey  rewards,  to o f f s e t  some aspect rate  decreasing the  due  to  the  reduction  relevant.  Foraging on  more difficult with in light  intensity.  All  three general modes of foraging are dissimilarly affected by the presence  of  turbidity.  Changes in foraging behaviour level have been demonstrated f o r  commensurate with turbidity  fish in several studies.  or  light  Threadfin  shad (Dorosoma petenense) change foraging strategy from particulate feeding  to  Benthically clear  filter feeding  water strike  movement  pattern  feeding at  low light levels  largemouth only at  bass  prey  (Crowl 1989).  of  (Holanov  (Micropterus particular  and Tash 1978).  salmoides) foraging in  shape, orientation, and  In turbid conditions, this  largely abandoned; bass may respond simply to target  size.  strategy  is  It has been  7 suggested that rainbow smelt (Osmerus mordax) in Lake Superior respond to an increase in turbidity by moving to the surface, although they may have been following zooplankton which were rising to the (Swenson 1978). rates  and Morgan (1985) demonstrated higher feeding  in turbid conditions f o r  pallasi).  They  silhouetting their  2.3  For  that  rotifer  prey  Pacific  herring larvae (Clupea  turbidity against  enhanced visual  harengus  contrast,  a uniformly illuminated  These studies all suggest that foraging fish may alter  feeding  Chapter  suggested  the  background.  fish  Boehlert  surface  strategy  as  TURBIDITY  turbidity  AND  increases.  PREDATION  RISK  juvenile salmonids, predators are of  piscivores.  gulls, herons,  The  most  notable  of  these  squawfish, sculpins, and other  two main types, avian and include: diving birds, salmonids (Scott  and  Crossman 1973; Ginetz and Larkin 1976; Simenstad et  al. 1982; Mace  1983).  (e.g. sculpins,  With the  herons),  all  are  exception of "active"  the  ambush predators  hunters.  Primarily, most predators on fish use vision to detect prey  (Hobson 1979).  abilities of  Any environmental condition that  a foraging fish is also likely  to a f f e c t  and attack  affects  those of  the  visual  one or  more of its predators. Juvenile salmon have been shown to be sensitive to predation risk (Dill 1983; Dill and Fraser  1984; Magnhagen 1988).  Fry  move  shorter  distances from cover on foraging bouts as this risk increases (Dill and Fraser  1984) or  as their  hunger  level declines (Magnhagen 1988).  susceptible to predation often occupy more structurally (Aggus and Elliott near  complex habitats  1975; Werner 1977; Cooper and Crowder 1979; Savino  and Stein 1982; Werner et within or  Fish  cover.  al. 1983; Gotceitas  and Colgan 1989) foraging  Fish so positioned may easily be able to flee  to  8 safety  should the need arise. Reduced light levels  (Woodhead  1956; Girsa  salmonids indicates patterns  Kwain 1966). of  cover  resident  1973; Cerri  there  in various  have been linked to reduced predation risk 1983).  is a risk  The behaviour  avoidance  light conditions (Hoar et  of  juvenile  component to  activity  al. 1957; McCrimmon and  Low light levels have also been implied to act  in explanations of juvenile  sockeye  vertical  migration behaviour  salmon (Levy  1987).  Levy  in lake  (1989) also suggests  that vertical migrants may be tracking food resources. reef  as a form  Work on coral  communities has suggested that light itself may not be a  universally species  good indicator of  specific  McFarland By  risk  in fishes, whose responses  and highly variable  (McFarland  are  and Munz 1975; Munz and  1977). acting as cover, elevated  turbidity  levels  may reduce predation  pressure on adult (Bruton 1979) and young fish (White 1936; Blaber Blaber 1982; or  1980; Gradall and Swenson Bruton 1985).  1982; Healey  1982; Simenstad et  Fish in turbid water may be able to evade  capture by a predator more effectively  than in clear water.  and al.  detection It has  been suggested that salmonids are able to assess predation risk in clear visibility  (Dill 1983 and  1987; Dill and  Fraser  1984; Magnhagen 1988).  They may also modify their behaviour in turbid waters to reflect a reduction in their  Chapter  perception of  2.4 FORAGING  The importance of over-emphasized.  UNDER  risk  RISK  to predators.  OF  PREDATION  avoiding predation while foraging cannot be  Fish have evolved many, often complex, mechanisms to  avoid being eaten (Cooper and Crowder 1979; Hobson 1979; Larkin 1979; Dill 1983 and  1987; Werner  and Chesson 1987).  and  Gilliam  1984; Milinski  1986; Mittelbach  Two basic predation avoiding strategies  exist.  The  9 f i r s t is to grow as quickly as possible beyond the size ranges most susceptible  to  predation  (Werner  and Gilliam 1984; Miller  the second is to adopt one feeding strategy change 1987).  this  with ontogeny  Salmonids of  the  (Werner  et  al. 1988);  or habitat early in life and  and Gilliam 1984; Gilliam and  genus Oncorhynchus follow both.  Fraser  During their  downstream migration, subyearling smolt and f r y  remain f o r  amounts of  al. 1979; Healey 1982;  Levy  time in estuarine  and Northcote  smolt generally duration of  habitats  1982; Simenstad  (Levy  et  et  al. 1982), while the  pass through the inner estuary  estuarine  residency  variable yearling  (Healey 1982).  is species and stock  The  specific, ranging  from days (pink salmon - O. gorbuscha) to months or years (chinook salmon).  In the turbid Fraser  Estuary,  chinook migrants may quadruple  their weight before they leave the tidal marshes a f t e r two months (Levy et  al. 1979; Levy  and Northcote  1982).  Juvenile chinook salmon clearly  achieve impressive growth rates in the Fraser Estuary. achieve  these  rates  in turbid conditions is  of  That chinook  ecological significance  f o r a species commonly associated with more pristine clear water environments (Scott and Crossman 1973).  The role of predation risk in  determining these growth rates has not been elucidated. The problem of predator avoidance is universal among foraging animals. very  Almost every  animal is the potential prey  of  another.  As the  act of foraging potentially attracts the attention of a predator  (Donnelly and Dill 1984), there may exist a tradeoff and benefits of  foraging (for  between the  review: Lima and Dill 1990).  The  costs costs  can often be expressed as the energetic e f f o r t of sequestering a food item and the risk to predators while doing so.  The benefits can be  expressed as the reward (usually expressed in energetic terms) of obtaining the instances  food.  Clearly, it may benefit  simply to not  forage  at  all (at  a foraging animal in some least  temporarily)  costs are too high in terms of risk of predation. tradeoffs  have been well described in the  if  the  For fish, these  literature  (Dill 1983 and  10 1987; Werner  and Gilliam 1984).  But  a vast  literature  also exists  for  other animals of a wide number of taxa representing both vertebrates and invertebrates  (for  review: Lima and Dill 1990).  Chapter 2.5 HYPOTHESES AND EXPERIMENTS CONDUCTED  Visual  Ability It has been often stated or implied that turbidity reduces  visual  foraging  Confer  et  ability  of  al. 1978; Gardner  on all  prey  1989).  I have broken the  into  two  prey,  types  foraging rate of microhabitats: light level.  of  (Vinyard  microhabitat  and O'Brien 1976;  (Minello et  al. 1987; Crowl  above hypothesis concerning foraging ability  a behaviourally  distance  fish  Furthermore, these reductions occur  components: visual ability  - reaction  further  1981).  regardless  I investigated  ability  searching  the  - as  and foraging rate.  For  manifested surrogate  a function of  turbidity.  column (plankton),  of  visual  I assessed  juvenile chinook salmon on prey in three  surface, water  planktonic  generalized  and bottom.  In a  series of experiments, I investigated the e f f e c t of reduced  intensity  expressed concurrently  The e f f e c t  of  with increases  in turbidity  light on foraging rates and reaction distances is  well established (Harden Jones 1956; Brett and Groot 1963; Vinyard and O'Brien 1976; Confer turbidity,  its  effect  et  al. 1978).  In any  on light level cannot  are reported in Chapter 4.3.  such investigation be ignored.  These  involving studies  11 Alteration of  Search  Behaviour  The search behaviour of fish may be altered in the presence of elevated  turbidity.  microhabitats  In  turbid conditions, fish may move into .  sparsely  occupied in clear  conditions (Bruton 1979;  Swenson and Matson 1982) or adopt different foraging patterns (Holanov and  Tash  1978; Crowl  1989).  rates may be insufficient  Simple alterations  to  Changes in microhabitat use may  occur. I have not addressed this hypothesis directly.  experiments required to altered  fully  The type of  describe all the potential forms of  search behaviour would involve studies well beyond the scope of  this thesis.  However,  horizontal  spatial  laboratory  over  5.1)  foraging  explain any exhibited changes in foraging  behaviour by fish in turbid waters. also  in various  provide  I have conducted observations on the vertical and  distribution of  a range of  juvenile chinook  turbidity conditions.  information on microscale  salmon in the  These experiments (Ch.  distributions  of  juvenile salmon.  Enhancement of Visual Contrast To explain increased feeding rates by turbid conditions, Boehlert prey  were contrasted  Pacific herring larvae in  and Morgan (1985) hypothesized that  against  rotifer  a uniformly illuminated background.  This  hypothesis was examined in a study by Godin and Gregory (in prep.). reaction time of various  juvenile chinook salmon f o r  manipulations of  contrast.  prey  planktonic prey  colour and turbidity  changed in  induced background  Boehlert and Morgan's hypothesis cannot be rejected  planktonic prey.  However,  contrast  The  for  will not be modified by increases in  turbidity f o r surface prey and only f o r benthic prey if the colour of the bottom itself is altered.  Although this phenomenon may be deemed  12 important  for  planktonic prey, it  consideration f o r  Predation  surface  can be effectively  eliminated from  and benthic prey.  Risk  Little increasing  hard  evidence  turbidity.  exists  Gradall  that  predation risk  and Swenson  declines with  (1982) show that salmonids  reduce their use of overhead cover in elevated turbidity and Bruton (1979)  correlates  with the  tilapia  presence  of  (Oreochromis  turbidity.  mossambicus) survival  and  No controlled investigation of  growth fish  response to predator exposure has been documented f o r turbid and clear waters. I explore two hypotheses on predation risk in turbid water. First, does turbidity a f f e c t presence of a predator? of  the response of juvenile chinook to  I assess this question with the use of models  two general salmonid predators: a bird and a fish.  turbidity - a f f e c t  the  Second, does  the post-exposure duration of the previous response?  These questions are addressed in Chapter 5.  The  Ability-Risk  Tradeoff  Documented evidence of behavioural t r a d e o f f s between the costs and benefits of foraging in the presence of varying degrees of predation risk  has been growing in recent  Turbidity  represents  years (for  an environmental  review: Lima and Dill 1990).  variable  which simultaneously  alters the costs (predation risk) and the benefits (food rewards) of foraging behaviour.  The existence of a tradeoff  cannot easily be  dismissed. In Chapter 6, I construct a conceptual model describing a tradeoff  13 between visual "explain" the ability  ability  risk of  increasing  risk.  I use  foraging rates observed in Chapter  and perceived  inherent  and perceived  risk  risk.  1 then  this  model to  4.2, in terms  of  make predictions concerning  the  foraging in various microhabitats and the e f f e c t stimuli  on foraging rate.  By  testing  these  model.  of  predictions  in Chapter 7, I attempt to support the assumptions concerning risk perception made by the conceptual tradeoff  visual  14 CHAPTER 3  Chapter  GENERAL  3.1  THE  STUDY  METHODS  ANIMAL  The study animals used were juveniles of chinook salmon (Oncorhynchus tshawytscha the  lower Fraser  type", et  River.  beginning their  al. 1986).  [Walbaum]) from Harrison River, a tributary Harrison chinook are predominantly "ocean-  seaward  migration as  underyearling f r y  the Fraser  Estuary  after  leaving their  natal stream.  As juveniles, these fish must traverse »100 km of the lower where  (Shepherd  They are suspected of spending several months rearing in  tidal channels of River,  of  I have measured turbidity  levels  Fraser  as high as 400 mg-L . -1  Therefore, the fish stock I used throughout my work probably has a well established  prior  Individuals  history  of  exposure to  turbid conditions.  were obtained as 0.8 g f r y  from the Chehalis River  Hatchery (on a tributary of the Harrison River) and transferred to holding facilities  at  the  were held in one of fish  densities  University  of  British  two 1000-L holding tanks  were 2.5-L . -1  Columbia. at  Densities declined as  Chinook  6.0 - 10.5°C. fry  fry Initial  were used in  experiments and were within accepted guidelines f o r  salmon culture.  The  light  automatic  the  regime  of  14:10 (light:dark  hours)  lights were turned on at 0800 h. treated with 5 - 2 0 free  chlorine.  Fry  was  set  by  timer;  The water supply to the facility  was  mg*L~ sodium thiosulphate concentrations to absorb 1  were fed "Oregon Moist Pellets"  (OMP)  twice daily  at  1000 and 2000 h, at a rate of 38X of the ration required to achieve maximum growth comm.).  rate  in hatcheries  (Kahl, Chehalis River Hatchery,  Growth rate was maintained at  pers.  approximately 10'/.  (weight-week ). -1  The  individual fish  used  in experiments varied  in size largely  as  a function of their growth throughout the duration of the experimental  15 "season". (FL).  Chinook generally ranged in size from 40 to 75 mm fork length  During any particular  experimental run and f o r  experiments, fish size was kept  reasonably  most whole  similar (+3 mm SD).  Sizes of  juveniles in the Fraser Estuary ranged from 35 - 75 mm FL (Levy and Northcote 1982; Gregory pers. obs.).  The seasonal range of fish size  created  during data  some analytical  difficulties  interpretation.  However, the opportunity to examine some behavioural changes with ontogeny was also presented.  Chapter  3.2  These have been described in Chapter 4.2.  TURBIDITY  Sediment f o r  all laboratory  procedures in this study was obtained  from a tidal marsh in the south arm of the Fraser River Estuary, at Ladner, British Columbia.  Approximately 10 L  of  this  sediment  was  sieved through a 0.40 mm sieve, to remove larger detritus, then suspended in 125 L of freshwater settle f o r a period of 2 h.  in a plastic bucket and allowed to  A f t e r this time, the supernatant (75 L) was  t r a n s f e r r e d to another bucket and allowed to settle f o r a further 48 h. The excess water was then poured o f f , and the remaining sediment slurry was autoclaved f o r required quantity The  slurry  Muller (1975).  (s90X <5 pm).  I repeated this procedure until the  was obtained.  individual particles  criterion of diameter  of  30 minutes.  were  classified as  subrounded, using the  Particle sizes ranged from <2 to 25 pm  16 Chapter 3.3 EXPERIMENTS ON  FORAGING  RATE  Prey Three types of prey were used in experiments investigating chinook foraging in three  generalized microhabitats.  These were broadly  categorized as surface, planktonic, and benthic prey. each of easily  the three  obtainable,  similar  in size  variance  types was selected to fit easily  to  the  maintained other  prey  under  laboratory  in size, similar in colour, and representative  criteria:  conditions, of  intraspecific the  type  of  The three prey chosen were:  - adult Drosophila melanogaster, planktonic - adult Artemia  salina, and benthic - Tubif ex sp. of  animal of  several subjective  used, non-evasive, low  prey encountered by chinook in the field. surface  A prey  The general characteristics  these prey animals may be found in Table 3.1.  behaviour relative to turbidity treatment,  of  each  No changes in  were noted f o r  these  prey.  Artemia and Tubifex were obtained from a local retail outlet, and winged, wild-strain Preliminary  Drosophila were  comparisons between  easily  cultured in the  laboratory.  living and frozen Drosophila indicated  no preferences by f r y f o r either of the two forms, therefore the frozen form was used as they could be easily stored f o r later use. Both Drosophila and Tubifex were readily of chinook f r y , with the latter diet  of  acceptable selection of  pers. obs.).  been found in the  because surface  chinook prey.  tend to  diet  of  the  Drosophila have not  wild caught  be relatively  fish, but  was  indiscriminant in their  Drosophila are within the size range of  surface prey taken by wild f r y . zooplanktonic prey.  types  being a demonstrated constituent of  wild individuals (Gregory  characteristically  identifiable prey  Artemia were intended to represent  Although they are much larger than the zooplankton  encountered by f r y in freshwater, they are not much larger than those encountered by  slightly  larger  conspecifics in the  marine  environment  17 Table  3.1  Prey  Physical and visual rate determinations. Length Weight mm mg(wet) 3  characteristics  of  prey  used  in  foraging  Other  D  Character i st i cs  Drosoph i1 a 2.5+0.3  0.9  black & white with red eyes; winged; previously frozen  Artemi a  6.7+1.1  5.3  white to pink with red/black eyes; weak swirrmers (no developed escape response)  Tubifex  14.8+7.0  1.9  dark red/black; burrowing; weakly evasive (no e f f e c t i v e escape - but longer handling time than other two prey)  a  D  mean+SD (minimum N=300)  batch weighings; mean weight/individual  only  18 and were much smaller, and less evasive, than Neomysis mercedis a mysid shrimp periodically (Northcote I prey  et  taken  by  al. 1979; Gregory  established prey  type  juvenile  Artemia density  of  and trial  Estuary  pers. obs.).  densities  in a series  chinook in the Fraser  and feeding trial  preliminary  durations  investigations.  for  A "working"  duration was identified by feeding f r y  satiation with an overabundance of prey to minimize the e f f e c t s search  time  satiation  (Holling 1959).  time  (i.e.  I set  1.0 minute).  the  trial  I then  duration to  set  the  each  trial  to of  be half prey  the  density  to  be double the number of prey consumed-min times 10 (10 fish used in a -1  trial)  in 64 Liters.  The  resulting  Artemia'L" , not outside the  range  1  fish  would encounter For  in the  was  s 3.5  densities  these  as  for  and trial duration were  Artemia.  However,  maximum feeding  this prey species occurred at elevated turbidity levels where feeding  incidents  observed satiation in clear  could not  of  As  a  Therefore, I  duration from a number of  differing duration at level.  be observed.  water to obtain subsequent trial  densities and estimated trial turbidity  density  planktonic prey  Tubifex, both working density  rates f o r  trials  of  prey  field.  identified in a similar manner individual  initial  result  this prey of  these  density  at  1  trials,  prey density and trial duration f o r Tubifex at s 5600TTT Although availability  difficult  field  area  prey, the  in both  and  laboratory  continues  fry  in the  2  to  I set  initial  and 5.0 be  a  studies dealing with benthic  densities used were well within natural levels  species of  preliminary  100 mg*L~  preliminary  minutes, respectively.  prey  field (Dunford 1975; Kistritz  of  many  prey  1978; Gregory  pers.  obs.). I set  the  trial density  similar to that f o r preliminary  trials  Artemia. occurred  and duration f o r As f o r at  Drosophila in a manner  Tubifex prey, maximum feeding in  elevated  turbidity  levels,  but  individual  feeding incidents were visible because the prey were taken from the  19 surface.  Consequently, setting trial  prey  comparatively easy; these were set minutes, respectively. instantaneous  prey  The prey densities  at  density  1300 Drosophila-m^ and 10.0  density f o r  likely  and duration was  to  Drosophila f a r  exceed  be encountered in the  field, but  they seemed reasonable given the densities of surface prey I have observed in the 1979) covered  field (a 6870'm~ d~ ). 2,  by  cruising chinook  m [2 x reaction distance in clear prey  densities in the  experimentally  were  field, I felt  Given the  1  search path (Keast  (8.8t2.1 rrrmin  -1  [pers.  obs.) x 0.656  water, from Fig. 4.2] x 10 min) and the  prey  densities  presented  reasonable.  The above prey densities have been expressed as individuals per unit area or volume.  I measured prey by weight, to expedite  experimental handling. Artemia [wet  weight],  These weights were predetermined to be 1.25 g 2.45 g Tubifex [wet  weight],  and 0.25 g Drosophila  f o r each treatment aquarium and were found to be accurate within «3'/. of the  actual numbers desired.  Pre-Experimental  Conditioning  Three days prior to any given experimental trial, I t r a n s f e r r e d appropriate numbers of chinook (usually to one of  72) from the main holding tanks  eight compartments in several 200-L "conditioning" tanks.  In  these tanks, fish were fed 30/. of the usual amount of "OMP"; feeding was augmented with approximately equal numerical amounts of types. any  given  Chinook were allowed to evacuate  experimental  In preliminary  trials, I exposed chinook to 1  experimentation. significant  The e f f e c t  guts 18 hours prior  trial.  turbidity (0, 50, and 200 mg-L" ) f o r not  prey  Test fish were fed this altered diet f o r three days before  experimentation. to  all three  one of  three  levels  of  a period of 7 days prior to n  of prior exposure to turbid conditions was  (ANOVA; df=2,18; p»0.25), regardless  of  prey  type.  20 Therefore, chinook were not exposed to turbidity as part of the , conditioning  procedure.  Experimental  Apparatus  The  experimental array  (Fig. 3.1) consisted of  7, 70-L, glass  aquaria enclosed and separated from each other by 8 mm plywood. inwardly-facing plywood surfaces periodically  repainted  provided by  to  All  were painted flat white, and were  maintain  optical  twin 40 watt fluorescent  consistency.  Lighting  light fixtures running the  length of the array, 45 cm above the water surface.  was full  The entire array  was enclosed in opaque black plastic sheeting such that it was isolated from outside visual disturbances and light sources.  Each aquarium was  similarly separated from the other aquaria in the array and from extraneous  disturbances  by  additional sheeting.  Each 70-L aquarium (50 x 34 x 40 cm) was fitted with a false bottom,  through which a mud slurry  (as  previously  decribed) was  visible.  Given that small amounts of sediment settled out of suspension at high turbidity  levels  (particularly  1400 mg^L ), -1  the  potentially  confounding  e f f e c t s of altered background contrast (Godin and Gregory, in prep.) were avoided.  For substrate, I provided a 5 - 7 mm layer of clear 2 mm  diameter glass beads.  This allowed the Tubifex to burrow  (in  appropriate experiments) and also permitted the constant background slurry  in the false bottom to remain visible.  A 2.5 cm clear syphon  hose was clamped in place at one end of each aquarium.  Each syphon hose  was primed prior to each experimental run before f r y were t r a n s f e r r e d to the aquaria, and could be activated from the front of the array. aquarium would take approximately positioned an airstone in the sediment suspension.  An  3 minutes to drain in this manner.  middle of  each aquarium to maintain the  I  21 Figure  3.1.  Aquarium a r r a y used f o r determinations of foraging A. Schematic representation. B. Photograph.  rate.  22 Experimental  Protocol  Ten fish were placed in each aquarium. of  I added a measured amount  sediment to each of six aquaria to create turbidity levels of 25 -  800 mg-L  in a geometric series (25 x 2 ; where n = 0 - 5).  -1  n  No  sediment was added to the seventh aquarium; which functioned as the control.  I randomized the order of the treatments and the control  within the experimental array  prior  to each experimental run.  were allowed to acclimate to the experimental conditions f o r - 1.5 hrs. before prey were added to the aquaria.  Chinook a period 1  Measured amounts of  prey were added to each aquarium in order of its position within the array.  Only one prey  type was used during an individual run.  Chinook  were allowed to feed f o r an uninterrupted period specific to the prey animal  being For  acclimate  tested.  experiments using Tubifex prey, I allowed the test fish to in 4-L  meshed plastic  holding chambers, within each aquarium.  I added prey to the main body of the aquarium ten minutes before beginning the  trial.  In preliminary  trials, Tubifex were observed  to  commence burrowing into the bead substrate within one minute of introduction  to  aquaria.  A f t e r the appropriate experimental time period had elapsed f o r an individual aquarium, its to drain f o r 3 minutes.  syphon was activated  and the tank  was  permitted  Fish were then netted and t r a n s f e r r e d to a 500  ml container  with a lethal concentration of  anaesthetic.  Fry  methanesulfonate (MS222)  remained in this container f o r  a period of  approximately 10 minutes before I t r a n s f e r r e d them to a sample jar with 5/. formalin.  For  Artemia prey, I began netting immediately a f t e r  one minute experimental feeding period had elapsed. electroshocker  to  facilitate retrieval of  the  I used an aquarium  fish in this case.  The  latter  technique caused the cessation of all feeding, but was not so severe as to cause regurgitation in the chinook.  These techniques were used  23 either on each tank in turn (Artemia trials) or were staggered such that several  tanks  completion  could be operated simultaneously, at  (Drosophila  and  Tubifex  various  stages  of  trials).  Stomach contents were dissected and enumerated f o r Drosophila and Artemia trials.  Contents containing Tubifex were blotted dry  and  weighed to the nearest mg. Turbidity levels were checked by taking water samples while the tanks were being drained. 400  DRT  The water samples were analyzed with a Fisher  Turbidimeter, measuring nephelometric turbidity  units  (NTUs).  Light levels were measured with a Li-Cor 185-A light meter with a quantum sensor. (s850  Lux; i.e.  Illumination  the  light  at  the  intensity  water of  surface  a dull day).  was  s16.5 pE'rrr^-s  Light  levels  -1  were  measured at the tank bottom and are reported along with NTUs in Figure 3.2.  Chapter 3.4 SPATIAL DISTRIBUTION  Experimental  AND  PREDATOR MODELS  Apparatus  All experiments in Chapter 5 were performed using a 1000 L (180 cm x 100 cm x 55 cm) arena, one wall of which was fitted with a 180 cm x 55 cm)  clear  plexiglass observation window (Fig. 3.3).  The tank  was  fitted  with a 2 5 ° slope running the width of the tank from the tank bottom to the water surface.  Therefore, water depth ranged from 0 to 40 cm. A  mixture of gravel covered with a layer of Fraser Estuary mud was used as benthic substrate.  A screen of 5 mm green plastic mesh was positioned  40 cm from the observation window, to restrict the lateral movement of fish in the water column. of 6 regions.  The observation window was marked in a grid  I established these numbered regions in a manner  24 Figure  3.2.  The relationship of turbidity concentration (mg*L~ ) used in foraging rate experiments with measures of light transmission. A. Nephelometric Turbidity Units (NTUs). B. Light energy (pE'm~ s~ ; measured at the tank bottom [37.5 cm depth]; 1 pE'm" *s~ , » 51.2 Lux). 1  2,  1  2  0  0.5  1  1.5  1  2  2.5  Log(Turbidity[mg/L])  3  B loo(LIGHT) = 1.045 - 0.0108 • (TURB) r=> 0.999 (N=5) 2  j  0  50  100  Turbidity (mg/L)  |  u  150  200  25 Figure  3.3.  Arena used during experiments on spatial distribution and predation risk manipulation. A. Schematic representation (lines labeled B - B' and F - F' indicate the track of the bird and fish predator models, respectively; see text, Ch. 5.2 f o r details). B. Photograph.  26 facilitating (e.g. by was  the  subsequent analyses  proximity to  the  surrounded by  the area in front  variously  grouped census data  surface, bottom, etc.).  black  of  of  plastic  The entire  curtain, restricting disturbances. of ambient light through the  observation window and to enclose the observer. in the  inner  curtain  covered when not in immediate use. double fixtured fluorescent  2,  1  The  depending on turbidity  observation  window.  facilitated  Preliminary  Lighting was provided from above by  and  the  visibility  trials  the range of turbidities tested.  in turbid conditions due  to  length of  depth  the  apparatus,  their  of  (Fig. 3.4). fish through  with inanimate  there was no appreciable change in visibility over  These were  Light levels ranged from near 0 to 10.00  turbidity  restricted  Variously positioned 3  observation.  lights running the  60 cm above the water surface. pE*m~ s~  In  the observation window, an additional curtain was  erected to both eliminate the entry x 10 cm slits  apparatus  the  objects  as a function of  indicated depth  Although fish counts were lower  visibility  to  the  observer, I  suspected no differential bias in these data with respect to region of the  arena.  Pre-Experimental  Conditioning  Fish were fed twice each day at 1000 and 2000 hours throughout the entire  course of  experiments.  Drosophila, Artemia, and Tubifex were  again used as prey and were supplied "ad libitum".  The latter two prey  types were introduced to the arena in each of the three depth regions of the arena via glass tubes near the middle or bottom of the water column, respectively.  I added planktonic and benthic prey  to each region in  proportion to the relative volume or area of that region of the tank. Surface prey were added to the surface in a similar manner. the  conditioning phase, I exposed fish to  all subsequently  As part of used  27 Figure 3.4.  The e f f e c t of depth and turbidity concentration (mg-L ) on light level (pETn" *s ), within the experimental arena (Fig. 3.3). -1  2  5  _1  10  15  Depth (cm)  20  25  30  28 treatment  turbidity  levels  two days of clear water. period was identical to Daily, prior to the  for  at  least  one day, following an initial  In all respects, treatment  that  during observation  of the fish in this  days.  lights coming on in the apparatus at 0800 h,  the water supply to the arena was turned o f f and I added the required amount of suspended sediment slurry to establish the appropriate turbidity  level.  The  presence  of  three  airstones  provided circulation  within the tank and maintained the suspension of added sediment.  Water  flow to the arena was restored following the last observation period. Water samples and temperature readings were taken a f t e r each observation period; I added more sediment slurry  Chapter  3.5  Statistics  this time if required.  STATISTICS  generally  as ANOVA, G-test, 1984).  at  consisted of  well described procedures such  linear regression, and various summary statistics  I used the procedures of  Analysis involving foraging rates  SYSTAT  4.0 (Wilkinson  were generally  (Zar  1988) throughout.  restricted  to  the  use  of means of each treatment within a trial, rather than data from individual fish. values  In all cases, I dropped the  from fish in each treatment  the mean.  of  highest and lowest  any given trial before  data  calculating  I have documented any changes to the above procedures in the  appropriate  Methods section.  29 CHAPTER 4  VISUAL ABILITY AND FORAGING BEHAVIOUR  Chapter 4.1  REACTION DISTANCE - VISUAL ABILITY  INTRODUCTION Visual ability Tamura Hester al.  has been  1957; Hairston et  variously  measured in fish (acuity -  al. 1982; Li et al. 1985; contrast  1968; behavioural measures - Vinyard and O'Brien 1976; Confer et  1978).  In most  instances,  this  ability  as the distance at which an animal reacts the is  resolution -  is manifested to objects  in its environment;  term receiving common usage is reaction distance. affected  by several  factors  and Blades  1975; Vinyard  Reaction  including light intensity  O'Brien 1976; Confer et al. 1978), prey  behaviourally distance  (Vinyard and  size (Ware 1971 and 1973; Confer  and O'Brien 1976; Hairston et al. 1982), fish  size (Hairston et al. 1982; Breck  and Gitter  1983; Wanzenbock and  Schiemer 1989), prey movement (Ware 1971 and 1973; Crowl 1989), prey and background colour or contrast (Ware 1971 and 1973; Godin and Gregory in prep.),  and turbidity  deleteriously list.  affects  (for  review: Bruton  Work  factor  in this  in visual range gained by fish of larger  may be negated in turbid water. on reaction  Turbidity  the visual perception of every  Even any advantage  turbidity  1985).  size  In this study, I address the e f f e c t of  distance.  on bluegill sunfish (Lepomis macrochirus - Vinyard and  O'Brien 1976) and lake  trout  (Salvelinus namaycush - Confer et al.  1978) has demonstrated that reaction distance of foraging fish f o r planktonic  prey  is reduced  by turbidity.  Investigations  have shown similar reductions f o r largemouth bass salmoides)  foraging  benthically.  by Crowl (1989)  (Micropterus  30 Chinook salmon may occupy turbid estuaries portion of  their  Simenstad et ability  of  early  life (Levy et  al. 1982).  However,  al. 1979; Levy  no quantitative  Oncorhynchus spp. in turbid water  investigated  the  reaction  distance of  for  a significant  and Northcote 1982;  work  on the  visual  has been published.  juvenile  I  chinook salmon to  planktonic prey in concentrations of suspended sediment ranging from 0 to 400 mg-L . -1  other  Pacific  These levels are common in the Fraser River estuary and coast  rivers.  METHODS  Experimental  Apparatus  The experimental apparatus (Fig. 4.1) consisted of a 200x30x25 cm plexiglass tank.  Test fish were further confined to the centermost 10  cm by two plexiglass partitions running the length of  the aquarium and  to the centermost 160 cm of the long axis by gravel partitions at either end.  Water depth was maintained at 5 cm.  The apparatus was placed o f f  the floor with a mirror positioned at a 45° angle underneath to facilitate  observations from a remote location.  to record observations. reflective  acetate  A videocamera was used  The plexiglass bottom was covered in a  film, which allowed light to  not upward, and effectively  pass freely  acted as "one-way" glass.  were not disturbed by movement below the tank. pE'm~ s~ 2,  1  downward  Therefore, f r y  Illumination of 16.2  at the water surface was provided by doubled-fixtured 40-watt  flourescent  lighting running the  full length of  the  aquarium.  An  airstone was positioned at each end of the tank, outside the view of test  but  subject.  The entire  the  apparatus was enclosed in black opaque plastic  sheeting to limit outside disturbances.  Water was changed once each  31  Figure 4.1.  Schematic representation o f the experimental apparatus used f o r the determination o f reaction distances.  water/turbldlty  32 day,  after  observations.  Conditioning  and Observational  Protocol  A single juvenile chinook was placed in the apparatus and over a period of items.  approximately two weeks, conditioned to strike at single prey  Prey  (live, 7-8 mm, male Artemia) were introduced at a constant  release point 40 cm from the gravel partition at one end of the tank by means of a 4.0 mm diameter glass tube. the subject during this process. glass  tube  containing the  aquarium, where it  prey  in elevated  Subjects to  were required to strike  facilitate  was promptly consumed.  permitted complete verification prey  The observer was not visible to  turbidity  of  its  release  into  This technique  a successful "strike"  conditions (to  the  the  ultimately  and location of  400 mg-L"" , « 275 NTUs). 1  Subsequent analysis of reaction distance required only measurement from the assessed reaction point to the fixed prey location. identified  as  a  the  initiation  of  a  distinct,  The former was  rapid, tail  beat  followed  by a constant acceleration toward the prey in the tube, ending with a strike.  The prey  An observation  tube was left  was  introduced a f t e r  in position between observation periods.  considered invalid if:  the test  1. the  tube (with prey)  fish had oriented toward the prey location;  2. the tube was introduced while the subject was within 60 cm of prey  location; 3. prey  had moved within the  1.0+0.5 cm above the  tank  an initial reaction  the  introduced in this  to  manner  with 1 - 4 "blanks".  was  bottom, or; 4. if prey.  tube to the  a position outside  fish "hesitated"  During experimental runs, prey  with true  the after were  introductions being interspersed  These were introductions containing no prey.  strikes were recorded in over 1000 "blank" runs.  No  Chinook responded only  to the presence of Artemia in the prey tube. Predetermined amounts of sediment slurry were added two hours  33 before levels  observations  to provide the  were randomized with respect  being tested on any single day.  turbidity  treatment.  to  day, with only one  trial  Turbidity level  The f i r s t and last test date f o r any  one fish were clear water treatments to determine any changes in fish response during the duration of the experiment.  I observed none.  The three chinook used in this study were 64, 65, and, 70 mm FL and 2.62, 3.63, and 3.82 g, respectively.  Experiments were run  at  ambient temperatures of 13 - 17°C with temperature never varying by more than  1.5°C  for  any  given individual.  RESULTS  A total of 216 separate reaction distance determinations were made under the above procedure at seven turbidity levels from <1.5 to 400 mg-L .  The e f f e c t  juvenile  chinook  -1  of  turbidity on the median reaction distance of  salmon was best  described by the log-linear  relationship: RD = 32.85 - 11.78 x log T, where,  T  = turbidity  (Fig. 4.2).  An r  confidence taken  for  2  -1  and RD = reaction distance (in cm)  of 0.96 among the medians supported a high degree of this relationship (r =0.72, when all data  separately).  distance  (in mg-L )  2  points were  I observed no marked dissimilarities in the  determinations  between  individual  subjects.  reaction  34 Figure 4.2.  40  The e f f e c t of turbidity on the reaction distance of juvenile chinook salmon f o r Artemia prey (regression is from 13 median values from 3 fish).  r  0I 0  1  1  1  1  i  i  i  i  50  100  150  200  250  300  350  400  Turbidity (mg/L)  35 DISCUSSION  The relationship demonstrated by the chinook was similar to previously  described by  Vinyard  and O'Brien  and by Confer et a I. (1978) f o r lake trout. relationship  did not  exhibit the  (1976) f o r  that  bluegill sunfish  However, the observed  characteristic  threshold type  of  response as demonstrated between light level and either foraging rate (Harden  Jones 1956) or  Confer  et  visual  al. 1978).  ability  in  reaction  distance (Vinyard  This suggests that  a  dissimilar  and O'Brien 1976;  turbidity  and light  affect  manner.  The probability of prey detection by fish has been shown to be proportional to the reaction distance (Ware 1973; Confer and Blades 1975; Hairston  et  with turbidity.  It  will  decline  with  al. is  1982). likely  increasing  Reaction that  the  distance  declines  probability  turbidity  of  Chapter 4.2  a deleterious  effect  FORAGING RATES FOR AND  detection  juvenile chinook salmon in  this study were similar to results demonstrated f o r has  prey  level.  The results I have demonstrated f o r Turbidity  log-linearly  on visual  other species.  ability.  SURFACE, PLANKTONIC,  BENTHIC PREY  INTRODUCTION  Turbidity O'Brien  acts  1976; Confer  to et  reduce  the  visual ability  al. 1978; Chapter  4.1).  rate should decline with increasing turbidity. (1981),  Johnston  Northcote  (1985),  and  Wildish  (1982),  and Breitburg  Sigler  (1988)  of  fish (Vinyard  Consequently, foraging  The work et  and  of  al. (1984),  supports this  Gardner Berg  conclusion.  and These  36 investigations demonstrated strong negative foraging rate  in numerous fish species.  experimental  studies, a large  body of  also exists purporting the negative foraging  fish  species  Noggle 1978; Hart  (e.g.  Ellis  1986; Eccles  effects  of  In addition to evidence  effects  of  1936; Buck  1986; McLeay  turbidity on these  from field  investigations  turbid water on visually  1956; Alabaster 1972; et  al. 1987; Simenstad  1990). However, several studies support a more benign view of turbid conditions.  Boehlert  wisdom, reporting increased their 1000 mg-L ) in the of  that  Pacific  foraging rates  over  -1  and Morgan (1985) depart  clear  herring  Numerous  estuarine  larvae  in moderately  species actively  field investigations  also  established  (Clupea harengus experiments.  (1987b) demonstrated that prefer  pallasi)  turbid conditions (500 -  water controls in laboratory  laboratory, Cyrus and Blaber  several  from the  turbid over  suggest that  clear  foraging ability  Also  juveniles water. may not  be severely impeded by turbidity or may be o f f s e t by advantages concommitent with turbid habitats  (Blaber and Blaber  1980; Levy  and  Northcote 1982; Stone and Daborn 1987; Cyrus and Blaber 1987a). Chinook salmon can be best described as generalist foragers (Keast 1979) possessing relatively  unspecialized feeding morphologies and  search habits (Scott and Crossman 1973).  This species has been observed  to feed on a variety of prey types from assorted microhabitats (Dunford 1975; Levy  et  al. 1979; Healey  pers. obs.).  The e f f e c t  microhabitats  may be dissimilar.  The majority  of  bass (Micropterus (1976) of  al. 1982; Gregory  on foraging behaviour in these  Such studies have not been conducted.  prey.  Crowl's  (1989) investigation of  largemouth  salmoides) reaction distance to crayfish and Moore and  study  flesus) represent predictions  turbidity  et  experimental manipulations regarding turbid waters have  examined planktonic Moore's  of  1982, Simenstad  of  prey  selectivity  important exceptions.  potential  by  flounder (Platichthys  Ware (1973) also made some  consequences of  turbidity  on epibenthic feeding  37 rates.  These have gone largely In the present  foraging rate microhabitats. investigated  by  In the  study, I examine the e f f e c t  juvenile  Surface, for  untested.  chinooK  salmon in three  planktonic,  and benthic  Drosophila, Artemia,  performance  of  various  and  of turbidity on generalized foraging is  Tubifex prey,  respectively.  manipulations described in this and  other subchapters, I have used chinook salmon ranging in mean size from 47 to 69 mm FL. difficulties, it ontogeny  Although the size disparity did create  also presented  an opportunity  on foraging behaviour  some anaytical  to examine the e f f e c t s  in turbid conditions.  of  Therefore, in this  subchapter I present exploratory analyses of the ontogenetic changes in foraging  behaviour.  METHODS  The E f f e c t  of Turbidity on Foraging Rate  Using the methods described in Chapter 3, I conducted experiments determining the foraging rate of juvenile chinook salmon f o r above mentioned prey types. years, 1987 and 1988. trials  at  all  the  three  These experiments were conducted over two  For each prey type, I performed five and three  turbidity  levels  in each  of  these  years,  respectively.  Chinook mean size by trial ranged from 59.1 to 69.6 mm FL in 1987 and 52.5 to  58.3 mm FL  within +3 mm FL f o r  in 1988.  Individual  sizes within each trial  any given trial mean.  ranged  38  The E f f e c t s of Ontogeny on Foraging Rate in Turbid Conditions To analyze the ontogenic aspects of chinook behaviour in foraging trials,  the  data  examined, f o r in question was  from all foraging rate  each of the prey fit  the  types.  "methods"  a "control" run of  f o r the analyses described here. across  the  individual studies  used in this  subchapter  experiment), I deemed it  slope of of  and benthic  (Ch. 3.3)  made  respectively.  the relationship between  the trials, f o r  ascending limb of used  prey,  the  logarithm of  this possible.  I first  -1  -1  for  surface,  determined  treatments  the each  (i.e. the  the described relationships - see Results).  (turbidity  + 1) in calculations  disproportionately weighting the determination of the 0 and 100 mg-L  it  suitable  turbidity and foraging rate, f o r  the four 0 to 100 mg-L many of  (i.e.  The continuity of the methodology used  The above criteria were met by 14, 15, and 13 trials planktonic,  collectively  Provided the experimental trial  criteria  the particular  experiments were  turbidity treatment  levels.  to  avoid  slope by the data from I then performed a  least  squares analysis on the resulting slopes, and the mean size (mm  FL).  I conducted this analysis separately  for  each prey  type.  RESULTS  Surface  Foraging  For significantly 4.1A).  chinook  affected  Highest  treatments (in  juvenile  foraging on Drosophila prey,  foraging rate  foraging r a t e s  (50 - 200 mg*L~ ).  10 minutes)  1  in 1987 and  were  turbidity  (ANOVA df=6,42j p=0.029 - Table attained  in intermediate  turbidity  These rates were 10.7 and 7.7 p r e y f i s h " 1988, respectively  I  (Fig.  4.3).  Chinook  39 Table  A.  4.1.  Analysis of variance of the e f f e c t of turbidity and year of experiment on the foraging rate of juvenile chinook salmon to A. Surface prey (Drosophila), B. Planktonic prey (Artemia), and C. Benthic prey (Tubifex).  Surface Prey  Source of Var i at i on  Sums of Squares  F  DF  Turb i d i ty Year Turbidity x Year  252.6 101.4 86.7  6 1 6  Error  607.4  42  2.911 6.984 0.999  P  X K  NS  K , » » , * * * - p<0.05, 0. 01, 0.001, respectively; NS - p>0.10. B.  Planktonic Prey  Source of Variation  Sums of Squares  DF  Turb i d i ty Year Turbidity x Year  932.9 15.8 42.2  6 1 6  Error  155.9  42  F 41.888 4.269 1.896  P Kfttt  NS  « , * * , * * « - p<0.05, 0.01, 0.001, respect ively; NS - p>0.10. C.  Benthic Prey  Source of Variation  Sums of Squares  F  DF  Turb i d i ty Year T u r b i d i t y x Year  2590.2 1461.0 1100.8  5 1 5  Error  1203.9  36  a  15.490 43.687 6.583  P **» KMX KKK  x,xx,xxx - p<0.05, 0.01, 0.001, respectively; NS - p>0.10. analyses performed without the 25 mg'L" treatment, which was not performed in 1987.  a  1  40 Figure 4.3.  The e f f e c t s of turbidity on mean foraging rate of juvenile chinook salmon feeding on surface prey and the percentage of salmon foraging in 70-L aquaria (Drosophila consumed in 10 minutes; vertical bars indicate standard e r r o r of the mean f o r each trial; N = 8 fish f o r each treatment level f o r each trial). A. 1987 - 5 trials. B. 1988 - 3 trials.  41 exhibited depressed foraging rates significantly  so  in 1987 (t-test,  In 1988, chinook foraging rates  at O and 800 mg-L p=0.016 and  turbidities. Individual  Also,  the  variability  peak  was  was  statistically  with those  different  significant  high; some fish consumed 40 prey  while many others had empty guts.  of  feeding  individual  (Fig.  trials  4.3),  in the  in 1988.  or more,  The e f f e c t s of turbidity level on  foraging rate were similarly described by the proportion of actively  levels,  respectively).  consistent  were observed at  not  treatment  p=0.004,  exhibited trends  in 1987, although peak foraging rates  -1  in both years. Appendices  I have  (Figs.  reported  A,1 and  fish the  details  A.2).  The observed relationship represented a marked departure from the foraging rate expected on the basis of the reaction distance of chinook  in  turbid  Planktonic  conditions  (Ch.  4.1, Fig.  juvenile  4.2).  Foraging  Among chinook foraging on planktonic Artemia prey, highest foraging  rates  treatment  (11.0 - 15.0 preyfish" -min ) 1  low  1  -1  significant (Table treatments. significantly  4.1B).  The e f f e c t  These rates  of turbidity was  approached zero in the 800 rng'L"  1  Foraging rates were not proportional to the percentage of  actively  foraging (Fig. 4.4). different  foraging rates turbidity  were observed at  levels (0 - 100 mg-L" ); reduced rates were demonstrated at  high treatments (400 - 800 mg-L ).  fish  -1  levels  (Table  The 1987 and 1988 trials  4.1B).  In both years,  the  were not  800 mg-L  -1  were significantly lower than those of the 0 - 200 mg-L (Tukey  tests,  p<0.001).  -1  Foraging on planktonic Artemia  prey by chinook juveniles was more consistent than that demonstrated f o r surface  foraging, with generally  in both years  lower  variance  among and within means  (Appendix - Figs. A.6 and A.7 f o r  details).  The "high to low" foraging rate pattern exhibited by these  fish  42 Figure 4.4.  The e f f e c t s of turbidity on mean foraging rate of juvenile chinook salmon feeding on planktonic prey and the percentage of salmon foraging in 70-L aquaria (Artemia consumed in 1 minute; vertical bars indicate standard e r r o r of the mean f o r each run; N = 8 fish f o r each treatment level f o r each trial). A. 1987 - 5 trials. B. 1988 - 3 trials.  c  1 I" 12 co  .c c cS <D  2  0  100  Eg " 0) cb CLLL  «  Turbidity (mg/L)  400  800  400  800  B  200  Turbidity (mg/L)  43 was similar to the fish  (Ch. 4.1, Fig. 4.2).  end of  The asymptotic  aspects  of  the  these  low  turbidity  the relationship could possibly be due to handling time  restrictions not  expectations based on the visual ability of  within  the  have limited the  Benthic  1.0 minute experimental period.  foraging rate  at  turbidity  levels  Search  time may  below 200 mg-L . -1  Foraging  Benthic foraging rates on Tubifex followed the same generalized pattern demonstrated by surface foraging chinook. significant 4.1C).  effect  on foraging rates  Highest foraging rates  Turbidity had a  (ANOVA; df=5,36; p<0.001 - Table  were demonstrated in the  intermediate  turbidities (25 - 200 mg-L ); reduced foraging rates were observed at -1  the  lowest  general  and highest  similarity  treatment  in the  form of  levels the  (Fig. 4.5).  Although I found a  exhibited relationships  between  1987 and 1988, the magnitude of the foraging rate peak was much greater in 1987.  Peak mean foraging rates in the larger 1987 fish were >30 mg  preyfish  - 1  generally  (in  <10 mg.  significant chinook  minutes). For  differences  between  treatments. smaller  5.0  Corresponding rates in 1988 were  1987 trials, multiple comparisons (Tukey  intermediate  test,  p<0.01) in benthic  revealed  foraging rate  turbidities (50 - 100 mg-L" ) 1  and all other  No similar differences could be demonstrated f o r  1988 fish, although the  of  the  same general trend was exhibited.  Foraging rates were loosely mirrored by the proportion of fish actively foraging  at  each  treatment  level (Fig. 4.5).  Within and between  trial  variance was less than that exhibited f o r surface foraging, but was generally  large  As f o r  (see  Appendices  - Fig. A.11-12 f o r  detailed  accounts).  surface foraging, the foraging relationship I observed f o r  benthic prey again represented a marked departure from the foraging rate predicted from the  reaction  distance  of  juvenile  chinook in turbid  44 Figure 4.5.  The e f f e c t s of turbidity on mean foraging rate of juvenile chinook salmon feeding on benthic prey and the percentage of salmon foraging in 70-L aquaria (mg Tubifex consumed in 5 minutes; vertical bars indicate standard e r r o r of the mean f o r each run; N = 8 fish f o r each treatment level f o r each trial). A. 1987 - 5 trials. B. 1988 - 3 trials.  45 conditions  (Ch.  4.1,  Fig.  4.2).  The E f f e c t  of Ontogeny and Turbidity on Foraging Behaviour  For chinook foraging on benthic and surface prey, the e f f e c t of turbid  water  on foraging rate  changed with ontogeny (p<0.01, Fig. 4.6).  Although foraging rate f o r benthic and surface prey increased generally with fish size, this increase intermediate decrease. in the  turbidity  was  less in clear  conditions.  In many instances, I observed a  At smaller fish sizes, turbidity  foraging rate,  whereas  water than in  larger  seems to e f f e c t  a reduction  fish exhibit an increase in  foraging rate from low to intermediate suspended sediment levels (slOO mg-L" ). 1  The chinook I used in the 1987 experimental trials were approximately 15 - 25/. larger I have described in the  (length) than their  1988 counterparts.  preceeding sections, several  differences  As  existed  between trials of these two groups of fish, during benthic and surface foraging experiments.  Compared with the e f f e c t s of fish size  demonstrated in this subchapter, more pronounced departures from the described foraging rate several  other  - turbidity  experiments  (e.g.  relationship were observed in  Fig. 4.8 and 4.10).  Similar ontogenetic e f f e c t s were not demonstrated by chinook foraging  on planktonic prey  (Fig. 4.6B).  However,  changes in feeding  behaviour on Artemia prey may have been masked by handling time e f f e c t s .  46 Figure 4.6.  E f f e c t of size of juvenile chinook salmon on the slope of the ascending limb (0 - 100 mg-L ) of the relationship between foraging rate and turbidity (each point represents a unique run). A. Surface prey - Drosophila. B. Planktonic prey - Artemia. C. Benthic prey - Tubifex (data point identified by the arrow accounted f o r Al'/. of the variance and was omitted from regression analysis). -1  47 DISCUSSION  Effect  of Turbidity on Foraging Rate The  visual  and O'Brien form of ability,  ability  of  1976, Confer  fish  et  declines  in turbid conditions  al. 1978; Crowl 1989; Ch. 4.1).  The  general  this evidence has been consistent between these studies; visual measured  as  increasing turbidity.  reaction  distance,  Many studies have  declines  review: Bruton 1985).  demonstrate Johnston  significant  with  that  on foraging rate in fish  However, many of these same studies did not  effects  at  low levels  and Wildish 1982; Breitburg  1988).  Morgan 1985) describes an increase herring  log-linearly  also demonstrated  suspended sediment has a deleterious e f f e c t (for  (Vinyard  (Heimstra  One study  et  al. 1969;  (Boehlert and  in planktonic foraging by  in turbid conditions, while another  (Moore  larval  and Moore 1976)  reports a shift in the foraging pattern or prey preference in turbid conditions.  An investigation by Godin and Gregory  turbidity-induced increases seemingly ability  in background contrast,  well established evidence  into  question.  The  action  (in prep.), on even brings  the  of  negative  effects  on visual  of  turbidity  on foraging behaviour  has not been demonstrably consistent. My investigations have provided evidence that supports the more established  view of  foraging  rate  However,  at  view.  negative  ultimately  intermediate  Planktonic  impacts of  declined at  turbidity  high levels  levels, my results  foraging by  juvenile  on foraging behaviour; (« >200 mg-L ). -1  support a more flexible  chinook salmon on Artemia prey  the present study follows the well documented pattern. foraging rates elevated  I observed high  at low turbidity conditions and much reduced rates  levels.  distinct, such as  The decline in foraging rate may have been more that  demonstrated by Gardner  in  (1981) f o r  bluegill  at  48 sunfish,  except  that  handling time  expressed foraging rate  in clearer  concerning visual  in turbid  ability  constraints water.  likely  limited  Established  conditions does  the  theory  not  explain the  foraging rates I demonstrated f o r surface and benthic foraging in chinook.  I propose a revision in our  foraging  behaviour  Boehlert elevated  by  these  thinking about turbid water  visual animals.  and Morgan (1985) observed peak foraging rates in  turbidity  conditions f o r  herring  larvae.  Their  tentative  explanation was an enhancement of visual contrast through a more constant  illuminated background, effectively  prey of the larvae. and its e f f e c t possible.  silhouetting  the  rotifer  Work on contrast perception in fish (Hester 1968)  on foraging behaviour (Ware 1973) suggests this may be  My own work (Godin and Gregory in prep.) has also suggested  such a possibility  may  exist  for  juvenile  chinook.  In the  latter  study,  chinook were observed to respond f a s t e r to prey (Artemia) that were more highly contrasted against turbid backgrounds, even with the demonstrated reduction  in reaction  distance  (Ch. 4.1).  My explanation f o r  this  involves detection of prey during the encounter phase of foraging (as defined by Holling 1966).  Prey may be recognized as such, earlier  approach in turbid than clear water. recognition  In this way, a fish may reduce  time in a diminished reactive  suggests this is at  least  on  field.  its  Although my own work  possible, I do not believe  it  provides an  adequate resolution to the dilemma presented here. Contrast enhancement conceivably would enable planktonic prey be more quickly recognized as such. benthic or surface prey. if  turbidity  acted  to  However, the same cannot be said of  Benthic prey could only be better  modify the  to  substrate  characteristics.  contrasted Turbid  environments tend toward a uniform grey-brown background, but this is unlikely  to  appreciably  change in varying  turbidity  phases in a given  system.  Also, in my experiments I have controlled f o r  Ch.  eliminating it  3.3),  as  an explanation.  Surface  this e f f e c t  prey  cannot  (see  assume  49 higher contrast in turbid water. Another  The sky provides the  explanation is required f o r  these  contrast.  results.  Given the variable form of the e f f e c t  of turbidity on foraging  rate and the magnitude of the changes, 1 suggest that a behaviour which is  flexible  with r e s p e c t  to  turbidity  levels  is  responsible.  In  clear  water, when foraging on benthic or surface prey, chinook salmon may choose to forage at a reduced rate, sacrificing the obvious energetic reward f o r some other gain. A moving, foraging animal is more likely to be detected by a predator  than a stationary, vigilant one.  increasingly review:  viewed  as  inherently  Lima and Dill 1990).  more visible to suggest forage  that  In clear  salmon are  accordingly. Higher rates  turbidity  conditions.  subsequent  dangerous f o r  a potential predator  juvenile  The act of foraging has been  water,  many animals  (for  a foraging fish will be  than when in turbid water.  sensitive  to this perceived risk  I and  may be realized at less "risk-prone"  I investigate  these  ideas more thoroughly in  chapters.  Effects of Ontogeny The analyses I have conducted to examine ontogenetic changes in foraging behaviour must be viewed as exploratory.  The results were not  expected when I began my research and their nature was only revealed after  the majority of my work had been completed.  required to fully of  the  describe this phenomenon.  ontogenetic e f f e c t s  is required to  Further study will be  However, facilitate  an understanding the  interpretation  of results of several experiments that may appear inconsistent with the findings I have described in this subchapter.  The results  of  these  experiments may well be consistent, given the size of chinook used during  the  particular  investigation.  50 For chinook foraging on benthic and surface prey, the e f f e c t of turbid water on foraging rate changed with ontogeny.  However, similar  ontogenetic e f f e c t s were not demonstrated by juveniles foraging on planktonic  prey.  Ontogenetic changes in foraging behaviour have received much recent In  attention  these  (for  review  investigations  it  of  basic ideas: Werner  is hypothesized that  and Gilliam 1984).  these  changes  involve  "decisions" based on the costs and benefits of various foraging behaviours.  One of the operating principles to emerge from this work  has been the "minimize u/g" (mortality and Gilliam 1984])  or  [Gilliam  and F r a s e r  should  choose  "minimize u/f" 1987])  a habitat,  rule.  rate: growth rate ratio [Werner (mortality  Under  these  microhabitat,  rate:  feeding rate  ratio  rules, a foraging animal  time, or  environmental condition  in which to forage which minimizes one or both of these ratios, when given a choice (assuming one exists).  As a fish grows, its risk  some function of  its  size (usually  to  predators  will change as  risk  will  decrease).  Therefore, the above ratios will also change as a function  of size. I believe  that  the  ontogenetic  changes in chinook foraging  behaviour in turbid water were consistent with the above hypotheses. The predation risk may be reduced with both size (Werner and Gilliam 1984; Miller  et  al. 1988) and availability  1982; Magnhagen 1988). 1985; Ch. 5).  of  cover  (Savino  and  Stein  Turbidity may act as a form of cover (Bruton  Therefore, as  turbidity  increases, the  relative  cover  to  young fish may be interpreted as increasing, and perceived predation risk  decreasing (see  relatively  low  constraints  Ch. 6 f o r  in clear  are  not  water  full explanation).  Foraging rates  but high in turbid water (if  limiting - again see  Ch. 6 f o r  details).  the As  may be visual its  size increases, the advantages of turbid water to the forager should be reduced.  The reduction in predation risk commensurate with increased  forager size may negate the advantages of cover o f f e r e d by the turbid  51 conditions.  This would seem to suggest that at  should forage  at  higher rates in clear  The "minimize p/g (or and larger  fish  p/f)"  larger  sizes, fish  compared with turbid conditions.  rule would then be satisfied by both smaller  sizes.  The "minimize p/g (or p/f)"  rule seems to be contradicted by the  results 1 have demonstrated.  In clear  should have been expected at  smaller, more vulnerable sizes of chinook.  I observed the reverse. juveniles  water, lower foraging rates  Larger, presumably less vulnerable, chinook  demonstrated relatively  higher rates in intermediate  low feeding rates  at  low turbidity  suspended sediment concentrations.  and  This  result seems to suggest that larger juveniles are more susceptible to predation is  in clear  inconsistent  water  than are  smaller  with existing theory.  conspecifics.  However,  This conclusion  it may be possible that  larger fish are more "sensitive" to their present risk to predators than are  smaller Fish  individuals.  are  more vulnerable  to predation early  in their  life.  Further, the probability of successful capture by a predator of any given et  size  declines rapidly  al. 1988).  Although the  over act  a small range of  of  forager  size (Miller  foraging puts a fish at  risk, quick  growth may be the most effective way of reducing this risk (Werner and Gilliam  1984; Miller  et  al.  1988).  once having attained a larger  It  follows  first  may  seem  In Figure 4.7A),  visual  an  individual  size but still under some risk  predation, may be less likely to subject result, a fish may adjust  that  itself  fish,  to  to that risk.  As a  its foraging behaviour in a manner which at  countei—intuitive. 4.7, I conceptualize  ability  and  gut  capacity  this  problem.  (closed  At  arrows)  small sizes (Fig. constrain  foraging rate while the fish's perceived risk to predators e f f e c t s a reduction in the maximum foraging rate (open arrows).  The relative  magnitude of  are "matched",  the visual constraints and perceived risk  canceling each other, except  at  high turbidity.  At  larger  fish sizes  52 Figure 4.7.  Hypothetical e f f e c t s on foraging rate of variables differentially a f f e c t e d by turbidity and ontogeny. Matched e f f e c t s (smaller fish). 6. O f f s e t e f f e c t s fish), (see text f o r interpretation).  Turbidity  A. (larger  53 (Fig. a  4.7B), visual  higher  point).  limit  because  However  also increases an increase  ability at  continues of  to  constrain  foraging  gut  capacities  (higher  sizes, the  forager's  "sensitivity"  larger  larger  but is " o f f s e t "  in foraging rate  rate,  higher relative to  at  satiation  from the physical constraints, at  but  lower  to  risk  affecting  turbidity  conditions. This section contains to be tested.  a great  deal of  speculation, which remains  I explore other ideas on the perceived risk of predation  in subsequent  chapters.  Chapter 4.3  THE E F F E C T OF TURBIDITY AND  LIGHT ON  FORAGING BEHAVIOUR  INTRODUCTION Many discuss  studies  the  examining foraging in turbid waters  predominant  role  of  light  (Swenson and Matson 1976; Gardner  attenuation  1981; Sigler  et  in turbid conditions al. 1984; Crowl 1989).  Although increasing turbidity has a pronounced e f f e c t of  light  any  (Duntley  direct  inevitably  on the  attenuation  1943 and 1963; Munz 1958; DiToro 1978; Lythgoe 1980),  comparison of  turbidity  with light level can be misleading.  Various fish species have been demonstrated to display thresholds in light  sensitivity  1976; Blaxter  to  feeding success (Vinyard  1966 and 1968; Brett  McFarland 1986). be  with regard  and O'Brien  and Groot 1963; Confer et al. 1978;  Quite predictably, these thresholds have been shown to  species, habitat,  and  size  specific  even  within  taxonomically  related  groups (Henderson and Northcote 1985; Confer et al. 1978; Munz 1958). However, it is not certain whether attributed  to  light  level  alone.  feeding rates in turbid waters can be If  light  level  is  not  responsible  for  54 the that not  foraging relationships turbidity readily  modifies the  explained by  described in Chapter  4.3, it  visual environment  chinook f r y  the  existing  of  would be implied in ways  literature.  I conducted this study to compare the e f f e c t s of light and turbidity  on foraging rates  I wished  to  could be  explained by the  determine  if  for the  surface, planktonic, and benthic  prey.  relationships exhibited in Chapter 4.2,  light levels  commensurate with turbidity  treatment.  METHODS The described  relationship by  the  between  light level and turbidity  following equation:  log(Light)  = 1.01  -  where light was measured in pETrr s~ 2,  nephelometric  could be  turbidity  units  0.0129  1  (Turbidity),  and turbidity  (NTUs)(see  also  was in  Ch. 3.3).  Light  f o r 0 - 200 mg*L" turbidity were measured directly, those f o r 1  remaining two levels were estimated from the regression.  levels the  Reduction in  the light levels required during the course of this experiment was e f f e c t e d using single sheets of onion skin paper layered on a plexiglass shelf  under  the  flourescent  lights to  conditions as measured in turbid water.  simulate the  light  level  The number of sheets of onion  skin was estimated from the following regression:  No.  sheets  This technique was level  of  each of  the  = 9.95  -  11.71 log(Light).  successful in that the corresponding light  turbidity  treatment  conditions could be closely  55 approximated with f r o m 1 25  -  100 s h e e t s o f  800 mg-L ,  respectively.  Three types  of  -1  one  as  respect  to  treatment  trials  turbidity  trial.  those  consisted of  described were  the  control  of (0  the mg-L  replicates  (100  three  light  "treatment"  trials,  control  trials  were  identical in  every  previously  the  following  mg-L  - 1  experimental array  plastic c u r t a i n  experimental  array  turbidity;  surrounding  (Ch.  3).  Light  treatments the  composite  manipulations: one light),  - 1  - 2  The opaque  of  that  The  1.20  pE'm  three  light),  1  - 2 ,  s~  overall  and  three [9  sheets]).  was " l i g h t - p r o o f e d "  with t h e  each aquarium and t h e  entire  shining between  trials  turbidity  light  1  and  The  instead o f  protocol.  1.15 p E * m - s "  (0  entire  except  light r e d u c t i o n s  11.5 p E - r r r ^ s  replicates  - 1  controls,  standard  turbidity;  mg-L  (Ch. 3 and Ch. 4.2).  combination  turbidity;  - 1  the  described of  were  with  similar t o  above  for  Two s t a n d a r d f o r a g i n g r a t e t r i a l s  along The  manipulations  consisted  light  "controls";  "composite"  representing  t r i a l were c o n d u c t e d during this experiment,  each o f the t h r e e p r e y t y p e s . conducted  onion skin p a p e r ,  aquaria was  black  further  r e d u c e d by using black t a p e on t h e plywood e d g e s between t h e aquaria. Following than  from  this  procedure,  the  sensitivity  The  juvenile  47.9 t o  limit  chinook  51.7 mm FL  light of  levels the  in " d a r k "  light  meter  conditions (0.01  salmon used in this  study  (±2.5mm s d , within  trials).  were  less  pE-m~ .s ). 2  ranged  -1  in mean size  R E S U L T S  Surface  Foraging  I observed turbidity  a significant  "control"  trials  when  difference compared  in t h e to  the  trend light  exhibited  by  "treatment"  the trials  56 for  chinook  Foraging  foraging on Drosophila prey  rates  in control  with increasing  turbidity  demonstrated by Foraging The  rates  composite  between  trials  exhibited a decline in foraging rate  (Fig. 4.8A).  The same result  chinook foraging rate were similar across  trial  (Fig.  4.8B)  was  not  in corresponding light  all treatments  indicated  the turbid and light treatments  Planktonic  (ANOVA df=1,18; p=0.011).  levels.  within each trial.  no significant  difference  at the levels examined.  Foraging  In general, the foraging rates on Artemia prey exhibited by chinook in both the turbid controls and the light treatments close  agreement  (Fig. 4.9A).  different in an ANOVA.  The curves  were not  were in  significantly  The composite trial also demonstrated close  agreement between the feeding rates in turbid conditions and those of similarly  reduced  between  the  levels  turbid and light  P=0.014), but between  light  not  large.  (Fig.  treatments  Similarly,  corresponding levels  4.9B).  However, was  difference  significant (ANOVA df=1,4;  a difference  in the  the  was  also  observed  control and treatment  trials  (Fig.  4.9A).  Benthic  Foraging  In intermediate 0.077  treatment  p E - m ^ ; Fig.  rates f o r  - 2  - 1  Tubifex prey  4.10A),  conditions (50 - 200 mg'L ; 3.22 -1  juvenile  chinook  in light treatments  exhibited  lower  foraging  than in turbid controls.  These differences were obscured by large variance and were not significantly  different.  demonstrated  a large  However,  the  and significant  results  from the  composite  trial  (ANOVA df=1,4; p=0.001) difference  57 Figure  4.8.  The e f f e c t on juvenile chinook salmon of turbidity and light level on foraging rate f o r surface prey (Drosophila). A. Mean foraging r a t e (preyfish~ lO min ; vertical bars indicate standard e r r o r ; N= 3 and 2 runs of light and turbidity treatments, respectively; solid line - light trials, dashed line - turbidity trials). B. Composite trial with three replicate treatments each of 100 m g ' L turbidity (1.15 pE'trr^s" ) and "reduced" light (1.20 pE'trT^'s"" ) and one control treatment (<1 mg-L , 11.5 pE*m~2's" ; * on horizontal axes of A indicates treatments compared in B). 1,  -1  1  1  -1  1  Ql  -1  I II I Control  I I I Light  I—,t.,.i Turbid  Treatment  58 Figure 4.9.  The e f f e c t  on juvenile  chinook salmon of  turbidity  and  light level on foraging rate f o r planktonic prey (Artemia). A. Mean foraging r a t e (preyfish" -1.0 min" ; solid line light trials, dashed line - turbidity trials). B. Composite trial, (see caption Fig. 4.8 f o r details) 1  1  59 Figure  4.10. The e f f e c t on juvenile chinook salmon of turbidity and light level on foraging rate f o r benthic prey (Tubifex). A. Mean foraging r a t e (preyfish~ 5.0 min ; solid line light trials, dashed line - turbidity trials). B. Composite trial, (see caption Fig. 4.8 f o r details) 1,  -1  Log(microEinsteins/m /s) 2  26  60  100 •  200  Turbidity (mg/L)  B 26  £ E to  2 0  16  I | DC 10  JL Control  Light  Treatment  Turbid  400  800  -  60 between the turbid and light treatments.  The foraging rates in the  turbid treatment  of the composite trial were approximately 6 - 7  higher than the  light treatments.  to  the  The levels of  the latter  times  were similar  control. I have reported the details of each trial in the Appendices  (Fig.  A.3, 8, and 13, f o r  Drosophila, Artemia, and Tubifex,  respectively).  DISCUSSION  Support f o r the hypothesis - the e f f e c t of turbidity on foraging rate The  is similar to results  of  that this  of  corresponding light intensity  experiment  indicate  able to explain the foraging rates did not  predict  surface  that  - was  weak.  light alone, while possibly  of chinook salmon on Artemia prey,  and benthic foraging rates.  Duntley  (1943)  argued that the dominant feature of turbid water optics is the interference image.  of  the  light signal and subsequent distortion of  In high light conditions, a prey  close range if  the  might not be seen  water is even slightly turbid.  light itself  is a secondary feature  suspended  particles.  Indeed,  object  several  any  visual at  The attenuation  of  of absorption and scattering by  investigations  have  demonstrated that  foraging  rates (Harden Jones 1956; Brett and Groot 1963) and reaction distances (Vinyard  and O'Brien  1976; Confer  levels, above which they sharply. both  lake  Confer et  al. 1978) exhibit threshold light  maximal and below which they  al. (1978) demonstrated that  and brook  respectively),  are  et  trout  reaction distances of  (Salvelinus namaycush and S.  and pumpkinseed sunfish (Lepomis  levels, reaction  distance  to  prey  of  fontinalis,  gibbosus) exhibited  thresholds of 50 - 100 lux and 20 - 50 lux, respectively. light  decline  Above these  a given size was maximized.  61 Vinyard and O'Brien (1976) demonstrated a strong relationship reaction  distance  reaction  distance above  similar to  that  and light  level, but also reported  little  10.8 lux in pumpkinseed sunfish.  reported by Confer et  al. (1978).  between  change in  This value  In their  study  was  of  sockeye salmon f r y , Brett and Groot (1963) observed substantial reductions this  in foraging rate  level  feeding  rates  only  at  light levels  were relatively  below 0.1 Lux.  Above  constant.  Species in closely related taxonomic groups often possess dissimilar et  sensitivity  al. 1978).  At  thresholds (Henderson  the  lower  turbidity  levels  and Northcote tested  in my experiments,  light levels were higher than the thresholds reported f o r salmonids (Brett  and Groot  1963; Confer  et  1985; Confer  al. 1978).  various  Reductions in  chinook foraging rates  should not have been expected at these light  levels  mg-L ).  (i.e.  0  -  100  -1  Foraging rates in the two types of treatments should have been similar  if  "light  turbid water. by chinook.  effects"  were predominant over  "particle  effects"  in  This seems to have been the case f o r planktonic foraging However, this hypothesis is not supported by the benthic  and surface foraging rate results.  Given that the turbid  treatments  demonstrated higher feeding rates than the light treatment runs at intermediate suggested. that  light  turbidity/light These results  level  levels,  do not statistically  alone is responsible f o r  chinook salmon in turbid water. hypothesis either. inconsistent.  a more dynamic process is the  foraging rates  hypothesis exhibited by  However, they o f f e r no support f o r the  On balance, results  Definitive  reject  statements  suggest rejection, but were  cannot  be  justified.  62 CHAPTER 5  MICROHABITAT SHIFTS AND  Chapter 5.1  RESPONSES TO PREDATORS  SPATIAL DISTRIBUTION  INTRODUCTION Often,  relatively  small d i f f e r e n c e s  in the  within habitats can have a pronounced e f f e c t or potential risk  to predators.  For  distribution of  on foraging opportunities  a fish foraging in turbid  these e f f e c t s may be further accentuated.  animals  waters,  In laboratory experiments,  Swenson and Matson (1976) provided evidence of vertical movements of larval  lake  herring  (Coregonus  artedii)  in turbid water.  In the  field,  Swenson (1978) and Bruton (1979) demonstrated changes in the spatial distribution of  smelt (Osmerus  mossambicus), respectively, Bruton food  mordax) and tilapia  in response  (1979 and 1985) concluded that concentrations, but  observed  that  were actively  to  of  elevated  turbidity  modifying their  tilapia moved into food-rich (and turbid)  turbidity  levels.  tilapia were not simply tracking  response to a relaxation of predation risk. effect  (Oreochromis  behaviour.  He  shallows in  Due to the pronounced  on vision (Ch. 4.1), encounter  rates by  foragers  with both predators and prey are likely to be affected by turbidity, even  at  relatively  low  High densities waters of  of  levels. juvenile  turbid estuaries  salmonids are  (Simenstad  et  water estuaries  found in shallow  al. 1982; Murphy et  Northcote and Larkin 1989; Gregory pers. obs.). be the case in clear  often  However, this may also  (Healey 1982; Simenstad et al.  1982) or in clear water tributaries of turbid systems (Gregory obs.).  Therefore,  spatial  distribution  the in  role  of  salmonids  al. 1989;  turbidity remains  in determining fine unclear.  pers. scale  63 Changes  in  salmomd  spatial distributions  ambient conditions have been well documented. observed  mainly  in connection  s o c k e y e salmon f r y in s t r e a m s (O. impact  of  the  vertical  k i s u t c h and 0_. t s h a w y t s c h a on  spatial  downstream displacement o f gairdneri  -  Northcote  1985).  suspended  sediment  or  these  fish.  habitats of microhabitat  associated  These  changes  and N o r t h c o t e  -  distribution  migration  Taylor  been  behaviour  of  Sigler  et  juvenile  investigations  primarily  normally  chinook  of  in spatial distribution, Their work with  the  dealt  and  pulses  of  in n a t u r a l  for  subtle  that  demonstrated  that  bottom  elevated  during  on  (O.  with  studies r e p o r t except  the  salmon  1978; B e r g  encountered  the  Although  has been c o n d u c t e d  a). 1984; Noggle  Also, none o f  closely  1989).  coho salmon and rainbow t r o u t  levels not  (1985).  more  altered  T h e s e changes have  been ignored in the l i t e r a t u r e , work  mykiss=Salmo  to  (Oncorhynchus n e r k a - Levy 1987) o r microhabitat use  turbidity  has largely  with  in r e s p o n s e  of  juvenile  Berg  coho  turbidity  pulses. The changes  present in  controlled  spatial  qualitative  d e s c r i b e s an experiment  distribution  laboratory  a d d r e s s whether  ME  subchapter  in  conditions.  elevated The  experiment  was  levels  under  designed  to  any such changes o c c u r , and if s o , t o a s s e s s t h e  effects  exhibited.  T H O D S  The  chinook  fry  used in this experiment  and 4.64 t 0.36 g in size when i n t r o d u c e d fish  turbidity  investigating  were  related  used.  The  techniques  Fish were date, these  experimental  have  exposed  treatments  been to  into t h e  78.0 t 1.6 mm (FLtSD) arena.  a r e n a , conditioning  previously  only  were  described  one turbidity  Twenty-five  protocol,  in C h a p t e r  treatment  3.4.  level on a given  (0, 25, 5 0 , 100, and 2 0 0 mg*L~ ) being 1  and  randomized  64 with respect to date.  Each treatment was performed on two dates.  additional date of 0 mg-L  One  treatment was performed at both the  -1  beginning and end of the observational phase, f o r a total of twelve experimental days. hours,  Observations were made daily from 0900 to 2100  inclusive,  at  two  hour  intervals.  Observations were made by simple census.  The number of fish  present in each region of the grid (Fig. 3.3) was counted. the  census  was  randomized within  regions being counted.  individual observation  I made three  time, 5 minutes apart,  times, with all  counts within each  these were pooled f o r  analysis.  The order of observation  In instances of  doubt, fish could be assigned to a region by position of the eye.  Data  analysis was conducted by G-test of contingency tables.  RESULTS In  clear  water  controls, the  distribution of  fish  was  significantly affected by the time at which the observations were taken (G-test, p=0.024, df=6). the  Analysis of  significance could be attributed  immediately before  and a f t e r  residuals revealed to the  feeding.  that  much of  observation time periods  Consequently, observations  0900, 1100, 1900, and 2100 hours were dropped from further  at  analysis.  The middle three observation periods (1300-1700 hours) were not significantly  different  (G-test,  p=0.117, df=2).  analyses were conducted using these observations. heterogeneity of  among trials  the turbidity  time  levels.  therefore  justified.  My primary significant  hypothesis  Pooling of  - turbidity  - could not be rejected. effect  of  turbidity  subsequent  G-tests  for  no significant differences  treatment  period was  chinook f r y  revealed  All  for  each  observations by run and  affects  spatial distribution of  Analysis by G-test revealed a  on distribution of  test  fish in the  65 experimental above  hypothesis,  describe  the  differences of  arena  test  results  were  of  turbidity  suggested  respect that  both  to  fish  of  water  fish at g r e a t e r different  expected  only  one  different  dimensions.  In  clear  with t h e  with  surface),  treatments. clear)  the  were  hypothesis  bottom  either (Table  not  These their  water,  significantly  than 20 cm in d e p t h than e x p e c t e d f r o m  by  that  However, t h e number was not  chance (Fig. 5.1). treatment in c l e a r  in c l e a r  which was not  Differences  fully  distributions  5.2.).  (100 m g - L )  between  the  significant  or  not  water.  water  readily  the was  -1  of  significantly  Further,  T h e s e r e s u l t s also s u g g e s t e d t h e e x i s t e n c e o f association  more  l a t e r a l and v e r t i c a l level (Table  the  Significant  simultaneously changing  turbidity  from  to  distributions.  in this s t r a t u m (38.5/).  that  from  significantly  the  turbidity  were  these  on  than 20 cm d e p t h in t u r b i d w a t e r  from  distribution  level  for  more f i s h (55.3X) were at g r e a t e r t h e volume o f  In addition t o  several a posteriori t e s t s  demonstrated  with  in  5.1, p<0.001, df=20).  I conducted  effect  fish  distribution  (Table  (or  a negative  apparent  turbid were  a positive association  among t h e  treatments consistent  turbidity  (i.e. o t h e r with  than  this  5.3).  DISCUSSION  Changes  in v e r t i c a l  demonstrated before.  distribution  relative  to  Swenson (1978) believed t h a t  c o n c e n t r a t e d above a turbidity  turbidity  have  been  zooplankton  wedge, causing smelt t o move into  the  shallow s u r f a c e w a t e r s t o f e e d on t h e z o o p l a n k t o n , accounting f o r observed  changes  in  smelt  distribution.  For  tilapia,  observed  movements were believed t o have been in r e s p o n s e t o b o t h higher availability (Bruton  and a r e l a x a t i o n  1979).  The  present  of  predation  experiment  pressure  provided  from  results  fish  the  inshore food eagles  consistent  with  66 Table 5.1.  Region  The e f f e c t of turbidity concentration on the spatial distribution (as a percentage) of juvenile chinook salmon by region, within an experimental arena (observations pooled by observation period; Region is indicated on the inset schematic of Fig. 3.3; Chi-square is from G-test). Percent of  Turbidity (mg/L" ) 1  Number  Arena Volume  0  100  200  1  26.41  11.20  42.17  28.38  33.98  31.91  2  26.41  35.82  19.57  26. 13  26.21  21.28  3  12. 12  8.44  10.00  4.95  8.74  6.38  4  12. 12  19.50  14.78  10.36  21.36  12.77  5  12. 12  16.04  4.78  16.22  7.77  10.64  6  10.82  8.99  8.70  13.96  1.94  17.02  723  230  222  103  47  N  EE:  X* = 168.60 Schematic  of  1325 p<0.001;  Figure  3.3  25  df=20. indicating  regions.  50  67 Table 5.2A.  The e f f e c t of turbidity on the lateral distribution of juvenile chinook salmon by pooled region (observations pooled by observation period and expressed as percentages; see Table 5.1 f o r Region; Chi-square is from G-test).  Region Number  Percent of Arena Volume  0  1&2  52.81  47.03  61.74  54.50  60.19  53. 19  3,445  36.37  43.98  29.57  31.53  37.86  29.79  6  10.82  8.99  8.70  13.96  1.94  17.02  N  EE= 1325  723  230  222  103  47  X* =39.54 ; Table 5.2B.  Number  3  p<0.001;  Turbidity (mg-L" ) 25 50 100 1  200  df=8.  The e f f e c t of turbidity on the vertical distribution of juvenile chinook salmon by pooled region (observations pooled by observation period and expressed as percentages; see Table 5.1 f o r Region; Chi-square is from G-test). Percent of Arena Volume  Turbidity (mg-L" ) 25 50 100  200  1  0  1&3  5O.0  26.2  60.3  47.7  47.3  52.9  244  50.0  73.8  39.7  52.3  52.7  47.1  542  199  155  93  34  N  EE=1023  regions 5 * 6 omitted from analysis X* =86.35; p<0.001; df=4. a  68 Figure  5.1.  The e f f e c t of turbidity on the proportion of juvenile chinook salmon in the lower 20 cm of a 40 cm deep experimental arena (vertical bars are 95ZCL [after Bailey 1980]; horizontal line represents the proportion expected by chance).  0  50  100  Turbidity (mg/L)  150  200  Table 5.3A.  The e f f e c t of turbidity on percentage of juvenile chinook salmon associated with the bottom (observations pooled by observation period; see Table 5.1 f o r Region; Chi-square is from G-test).  Region  Percent of  Number  Arena Volume  Turbidity (mg-L" ) 1  0  25  50  100  200  U3  38.53  19.64  52.17  33.33  42.72  38.30  3,4,546  61.47  80.36  47.83  66.67  57.28  61.70  723  230  222  103  N  EE=1325  X*=99.14; p<0.001; df=4. X? =16.87; Table 5.3B.  p=0.001; df=3 - f o r  Percent of  Number  Arena Volume  244 N  alone.  Turbidity (mg-L" ) 1  0  25  50  100  200  61.47* ,  44.67  65.65  63.51  52.43  65.96  38.53  55.33  34.35  36.49  47.57  34.04  723  230  222  103  EE=1325  X* =48.43; p<0.001; df=4. X? =5.66;  treatments  The e f f e c t of turbidity on percentage of juvenile chinook salmon associated with the surface (observations pooled by observation period; see Table 5.1 f o r Region; Chisquare is from G-test).  Region  1,3,546  turbid  47  p=0.129 NS;  df=3 - f o r  turbid treatments  alone.  47  70 the observations made in these studies. The results that  turbidity  salmon. water  detailed in this experiment supported the hypothesis  affects  the  spatial  distribution of  juvenile chinook  Fish were found higher in the water column and in shallower at  elevated  turbidity  levels.  The vertical  and horizontal scales  of this experiment were restricted in comparison to those that would be encountered in the broad.  field; however,  the  implications of  First, given the significant movement of f r y  portions of  the  (assuming availability  of  turbid conditions).  Similar  are  to the upper  water columnin turbid conditions, encounter  surface prey may increase relative  rates  with  to planktonic and benthic prey  the prey has not also been affected by the chinook movements may also have  during my foraging rate  experiments (e.g. Chapter  conditions, feeding rates  on surface  prey  to those of planktonic and benthic prey. surface  these results  4.2).  occurred  In turbid  should have increased  relative  I observed this increase  for  foraging on Drosophila. Second, although chinook moved up in the  water column in turbid water, this movement suggested a threshold type of response.  Beyond 25 mg-L"" , the number of test fish in the deeper 1  regions did not decrease as a function of be expected if  the turbidity level as would  the fish were tracking light levels.  However, scale may  have been a factor.  And third, this experiment demonstrated that  turbidity  chinook  this  may  cause  change was not  to  sufficient  alter to  their  spatial distribution, but  explain the  encountered in the previous chapter  (Ch. 4.2).  feeding relationships For  example, the  foraging rates on benthic prey also rose in turbid water. change  in spatial  distribution may  partly  explain increases  rate on surface prey, but it does little to clarify of  turbidity on the foraging rate of  The observed in foraging  the observed  effect  chinook on benthic Tubifex.  These results did not suggest that juvenile chinook were maintaining visual contact  with the  bottom by moving closer to it  demonstrated by juvenile  coho (Berg and Northcote 1985).  Instead,  as fish  71 became dispersed throughout the arena in turbid waters as compared to the clear water controls.  The results were consistent with the  hypothesis that turbidity may act as a form of cover against predation (Bruton 1979 and 1985; Gradall and Swenson 1982) although, the hypothesis  is not directly  Chapter 5.2  supported.  RESPONSES TO MODEL PREDATORS  INTRODUCTION  A beneficial their  effect  reduced susceptibility  times  (for  Guthrie  reviews:  1986).  Miller  However,  of  turbidity  for  foraging  fish,  specifically  to predators, has been postulated many 1976; Simenstad  et  al. 1982; Bruton 1985;  hard evidence has been lacking.  The suggestion  that turbidity acts as a form of cover seems to have been more a reasonable assumption than a supported principle. several (1979)  notable  demonstrated that  he found that lakes.  observations  Blaber  more juvenile and Blaber estuarine  fish of  consistent  tilapia grew  with this hypothesis.  better  in turbid water  (1980) and Cyrus and Blaber  fish in moderately  turbid portions of  (1987b) demonstrated experimentally actively  seek  out  moderate  that  trout  (Salvelinus fontinalis)  became more active  shallows;  many  Cyrus  juvenile  levels.  Gradall  atromaculatus) and  relied less on overhead cover  in turbid conditions.  water  (1987a) observed  estuaries.  turbidity  and Swenson (1982) found that creek chub (Semotilus brook  Bruton  this species avoided similar areas in clear  and Blaber  fishes  There have been  White (1936) observed  and that  foraging rates by piscivorous birds were reduced a f t e r rains had caused a rise  in the  turbidity  of  salmon streams.  Ginetz and Larkin (1976)  correlated turbidity with decreased predation pressure during downstream  72 migrations the  of  juvenile salmonids.  "turbidity  as  cover"  The e f f e c t s  Anecdotal and correlative  support  hypothesis has been considerable.  of manipulations of predation pressure and turbidity  on forager behaviour have not been described in the literature. exists  for  a myriad of  investigations  making processes of  foragers  concerning predator  (reviews: Werner  1983 and  1987; Milinski 1986; Lima  especially  rich  concerning fish.  and  this  mediated decision-  and Gilliam 1984; Dill  Dill 1990).  Much of  There  This  literature  work investigates  is  the  response of foragers to combinations of predation risk, food reward, and accessability of  of  cover. None of  predation simultaneously  with the  predation risk or its own food. conflict. well as  It  acts  to  those  of  its  these  restrict  investigators forager's  manipulated the  ability  to  detect  risk  either  A turbid medium imposes such a the  visual ability  of  the  forager,  principal avian and aquatic predators.  as  Whether it  is primarily the forager or the predator which benefits from these visual constraints has been the subject of debate. "...[turbidity stalking  their  acknowledge  may] provide cover  prey."  Statements such as:  from predators and f o r  predators  (Bruton 1985).  this problem.  I believe he has summarized the problem well.  I , conducted the experiments described in this subchapter, to qualitatively predation cover.  describe the  risk  under  response of  juvenile chinook salmon to  combinations of  turbidity  level and additional  Model bird and fish predators were used throughout.  The  response of the chinook was assessed by using a relative index - change in spatial distribution - to  describe the  risk  aggregations of 22 test fish in the laboratory.  perception state of The magnitude and  duration of a risk-induced response were determined in separate experiments.  loose  73 METHODS Two predator models were used in these experiments: a fish and a bird piscivore.  My use of  to be representative did not  intend  to  these models in this experiment was intended  of the two general classes of salmon piscivores.  conduct  a detailed investigation  differences of their e f f e c t s .  of  the  I  intrinsic  The fish model was that of a spiny  dogfish (Sgualus sp.), 32 cm in length and made of rubber.  The bird  predator was a stuffed museum specimen of an immature glaucous-winged gull (Larus glaucescens), 62 cm in length.  Both of  these  known predators of juvenile salmon (Mace 1983; Hargreaves  species were 1990 and pers.  comm.). Model predators were positioned in the water column and above the experimental  arena.  a speed of for  the  Models were pulled with clear  approximately  monofilament  1 m-s * along fixed guide wires (F-F' -  fish and bird models, respectively  - Figure  3.3).  line and  at B-B',  The guide  wire f o r the bird model traversed  diagonally above the tank at a height  of 40 cm above the water surface.  The fish model was drawn from near  the middle of the water column in the deepest portion of the arena to the surface  at the shallow end.  in a "ready"  When not in use, models were positioned  position behind a curtain outside the view of  the  test  fish.  The Magnitude of the Twenty-two replicates.  Effect  juvenile chinook were used in each of two sequential  These fish were 83.412.7 mm (mean+sd FL)  before, and 87.5+2.9 mm and 83.6+5.1 mm after, replicates,  respectively.  Each  replicate  and 78.8+3.3 mm  in each of  consisted of  the  twelve  days preceeded by 7 days of preconditioning (see Ch. 3).  treatment  The experiment  74 was  structured  turbidity  level  in a crossed, (present  [25  three-factor mg*L  _1  design, with manipulations of:  only] or  absent),  additional cover  (present  or absent), and predator exposure (bird model, fish model, or  absent).  Each of  the twelve experimental days consisted of a unique  combination of treatment ordered  factors.  within each replicate.  positioning plastic  These combinations were randomly  Additional cover  drinking straws vertically,  was provided by  from above the  to within 2 cm of the bottom, uniformly throughout the arena. were intended to represent stems of vegetation.  surface These  A density of 10C-m"  2  was used and seemed reasonable from past work (Savino and Stein 1982). A trial consisted of exposing the chinook to one or neither of models and observing the exposure was facilitated "ready"  position into the  subsequent spatial distribution.  by pulling the view of  the  test  fish to a "holding" position  The model was returned to its  position following observations.  treatment  Model  appropriate model from its  at the opposite end of the guide wire. "ready"  the  In "no model" trials, a sham  was provided by performing identical operations as f o r "model"  trials, except that the model was not pulled into the view of the fish. Observations were conducted a standard 15 seconds a f t e r exposure. Three of the above trials were made on each experimental day at 1300, 1500, and 1700 hours.  Observations were made by visual census.  Regions 1 and 2 were censused separately were counted as a unit.  while Regions 3, 4, 5, and 6  This method allowed the completion of all  observations within 20 seconds.  These observations provided an  "instantaneous"  spatial  assessment  disturbance by a predator.  of  distribution immediately  following  75 The Duration of the E f f e c t - Recovery from Predator Disturbance I measured the duration of by  the  predator, by  videotape  previously outlined interactions days  analysis.  were also from this replicate. I videotaped the  Additional trials  of  elicited  the  were conducted over a period of  following the completion of  procedure,  the post-disturbance behaviour  four  the second replicate; the fish used Using the  previously  spatial distribution of  described the  fish in the  arena f o r 5 minutes prior to and f o r 10 minutes following exposure to the predator models.  The number of fish in or entering each of the  arena's regions was counted throughout sequential increments of 30 seconds each. The four Day -  experimental days  were set  with the following conditions:  1 - additional cover, clear; Day 2 - additional cover,  no additional cover,  turbid; Day 3  turbid; and Day 4 - no additional cover,  clear.  The four treatment runs consisted of two runs each with the bird and fish model trials conducted at two hour intervals on each of the four experimental days, beginning at 1200 hours and ending at 1800 hours. Data were analyzed by chi-square.  The mean frequency of  observations in each region of the arena during the pre-disturbance period was used as an expected value f o r The X  8  calculating a X* statistic.  was then subsequently determined f o r each 30-second time interval  in both the pre- and post-disturbance periods.  The 95X confidence limit  was used to approximate the time taken f o r test fish to return to a predisturbance this of fell  spatial  time as three  distribution within the  recovery  consecutive  below  the  time.  I arbitrarily  time intervals  critical  value of  arena. selected  I have r e f e r r e d the  first  occurrence  in the post-disturbance period which  the  statistic  (X*(cc=.05;df=4)  =  9.488)  as evidence that the fish had recovered from the e f f e c t s of the disturbance. recovery  I took the time elapsed before this occurrence as the  time.  to  In instances where the above criterion could not be  76 satisfied time  within  as  10.0  represent However,  the  duration  minutes.  a  As  complete  as  a  treatments,  was  the  I have  absence  relative  it  of  index  used  of on  experiment, it,  the  stress which  I  recorded  recovery  in c h i n o o k  to  compare  time  the  recovery  may  not  induced by turbidity  the  and  models.  cover  effective.  RESULTS  The  Magnitude o f  Exposure startle  type  rapidly  moved  presented  the  to  of  Effect  either  of  response.  to  the  here  the All  deepest  represented  predator  or  many  region the  of  of  time  models the  the  elicited  test  arena.  period  fish The  within  a  general  immediately  and  observations  15 s e c o n d s  of  this  response. In region  "no  of  predator"  the  presence  or  arena  (Fig.  significant.  These  subchapter  of  water  5.2).  it  was  controlled, and  I  presence effects  of  the  in  was  higher  cover  1),  was  supported  this  those  of  fish  in c l e a r  (Fig.  #2  effect  was  fish viewed  the  reduced  models e f f e c t e d  Region  chinook  one o f  were  Replicate  predator  The  have  120/ m o r e  proportion  additional  results  fish  for  #2)  the  in  the  water,  5.2).  In  reported  both  only  difference in  deepest in  the  one  not the  previous  5.1).  to  proportion  of  5.2B,  (Ch.  Exposure  than  (Region  absence  comparison  (Fig.  controls,  over more  model.  As  this  result  were  the  present  a further  "no  predator"  pronounced  the  effect  for  of  water  in  turbid  water  (Fig  5.2).  the  bird  Between  used.  Results  in  the in  clear  model  size  (Region # 2 )  m o d e l s t h a n when n o m o d e l was  in  controls  stimulus  conservatively. in d e e p  increase  was about  in  not 30/  the  These the  presence  77 Figure  5.2.  The immediate spatial response of juvenile chinook salmon to exposure to predator models in clear and turbid (25 mg*L~ ) conditions; proportion of fish in the deepest region (# 2) of an experimental arena in, A. The absence and B. The presence of additional cover in two replicates (open and shaded bars represent clear and turbid, respectively; vertical bars represent standard e r r o r ; horizontal line represents the proportion of fish expected by chance). 1  A Replicate 1  Replicate 2  1 i  1 I  =  II Bird  11  11 Fish  None  Bird  Fish  None  Model Type  B Replicate 1 1001  Replicate 2 i  Bird  Fish  None  Bird  Model Type  Fish  None  78 and absence  of  additional cover  5.2 and Table 5.4A). predator  were not  significantly  different  (Fig.  The main e f f e c t s of turbidity and presence of a  model were both significant (ANOVA p<0.001; Table 5.4A).  The  interaction between the e f f e c t s of turbidity and the presence or absence of  the  models, was  also  significant  (p<0.001).  The above results were essentially reciprocal to those observed at the surface (Region #1 - Fig. 5.3). predators  and turbidity  was  The presence of either of the two  significant  (ANOVA, p<0.001; Table 5.4B).  Lower percentages of chinook were observed in surface waters in the presence of either of the models. in the case of the bird. in representative  During some trials, none were present  Fish did not occupy the surface water region  proportion in clear  the predator treatment.  water treatments, regardless of  The presence of turbidity e f f e c t e d an increase  in the relative frequency  of  chinook occupying the surface region.  Analysis of variance (Table 5.4B) demonstrated that the differences were significant,  although the  model e f f e c t s  was  not  interaction  between  turbidity  and predator  significant.  The Duration of the E f f e c t Many of the results f o r the duration of the post-disturbance effect  were similar to the above observations.  predators the  arena.  caused a significant In all cases  5.4 and 5.5), lengthy distribution were of  the  change in the  involving the  departures (10 minutes  distribution of  chinook in  bird model in clear  water  from the pre-disturbance  spatial  observed, often  videotaping  Exposure to model  continuing until a f t e r  post-disturbance).  Similar  the  (Fig.  cessation  departures  were observed f o r the fish model (Fig. 5.6 and 5.7), but they were neither  as  strongly  expressed nor  as long-lasting.  In one case  (Fig.  5.7B), the post-disturbance was not different from the pre-disturbance  79 Table  A.  5.4.  Analysis of variance of the e f f e c t s of turbidity, cover, and exposure to predator models on proportions of juvenile chinook salmon located in A. Deeper water (Region #2); and B. Shallower water (Region #1) of an experimental arena (proportional data was arcsine transformed).  Deeper Water (Region #2)  Source of Var i at i on  Sums of Squares  Turbidity(T) Cover(C) Predator(P) T x C T x P C x P T x C x P  1.689 0.015 1.073 0.025 0.460 0.001 0.012  Error  1.468  K,KK,KKX  B.  - p<0.05, 0.01, 0.001,  DF 1 1 2 1 2 2 2  F 69.011 0.614 21.931 1.012 9.391 0.029 0.006  P KKK  NS  KKK  NS  X*K  NS NS  60 respectively; NS - p>0.10.  Sha11ower Water (Region #1)  Source of Var i at i on  Sums of Squares  Turbidity(T) Cover(C) Predator(P) T x C T x P C x P T x C x P  0.342 0.010 0.278 0.000 0.015 0.004 0.004  Error  0.789  K,KK,KKK  - p<0.05, 0.01,  0.001,  DF 1 1 2 1 2 2 2  F 26.020 0.749 10.558 1.010 0.561 0.145 0. 158  60 respectively;  NS - p>0.10.  P KKK  NS  KKK  NS NS NS NS  80 Figure  5.3.  The immediate spatial response of juvenile chinook salmon to exposure to predator models in clear and turbid (25 mg-L ) conditions; proportion of fish near the surface in deep water (Region # 1) of an experimental arena in, A. The absence and B. The presence of additional cover in two replicates (see caption on Fig 5.2 f o r details). -1  Replicate 1  Replicate 2  80  C  o &  £  60  C 40 OJ  o  OJ Q.  Bird  Fish  None  Bird  Fish  None  Model Type  B c  g  Replicate 2  Replicate 1  100 80  c  S  4 0  20  Bird  Fish  None  Bird  Model Type  Fish  None  81 Figure  5.4.  Changes in microhabitat distribution in juvenile chinook salmon, before and a f t e r exposure to a model bird predator, in clear (A. and B.) and turbid (C. and D.) water with additional cover. (The significance of the change in spatial distribution, based on the pre-exposure spatial distribution, was assessed by the Pearson Chi-square statistic; the arrow and vertical line delineate the time of the exposure; to the left of this line is the p r e exposure time, to the right is post-exposure; the horizontal line r e p r e s e n t s the critical X* o.o5 value of 9.488). a=  Time (min)  82 Figure  5.5.  Changes in microhabitat distribution in juvenile chinook salmon, before and a f t e r exposure to a model bird predator, in clear (A. and B.) and turbid (C. and D.) water without additional cover (see caption of Fig. 5.4. f o r details).  Time (min)  83 Figure  5.6.  Changes in microhabitat distribution in juvenile chinook salmon, before and a f t e r exposure to a model fish predator, in clear (A. and B.) and turbid (C. and D.) water with additional cover (see caption of Fig. 5^4. f o r details).  Time (min)  84 Figure  5.7.  Changes in microhabitat distribution in juvenile chinook salmon, before and a f t e r exposure to a model fish predator, in clear (A. and B.) and turbid (C. and D.) water without additional cover Tsee caption of Fig. 5.4. f o r details).  Time (min)  85 spatial  distribution.  Turbidity e f f e c t e d a reduction in both the magnitude and the duration of 5.5D). of  the post-disturbance response in all cases but one (Fig.  I attribute  this  exception  to  random noise, but  subtle lags in post-disturbance e f f e c t s  the possibility  cannot be discounted.  In  only three of the eight turbid treatments, were the post-disturbance periods  statistically  different  from the  pre-disturbance  spatial  distribution. The presence of additional cover appeared to have an unexpected effect  on the  post-disturbance spatial distribution f o r  Whereas juvenile minutes  chinook exhibited recovery  in clear  exceeded the  water  without  duration of  the  cover  times of  (Fig. 5.5),  the  bird model.  approximately  three  times with cover  experiment (Fig. 5.4). This disparity  was  not observed f o r the fish model. Recovery in turbid  time in clear water was approximately 8 times slower than  water  Analysis of  (Fig. 5.8),  when averaged  across  all  treatments.  variance (Table 5.5) demonstrated the main e f f e c t s  of  turbidity and predator accounted f o r 67.3X of the variance in these data,  while cover  was  not  significant.  DISCUSSION Other  than broad generalizations, no significance can be  attributed to the differences in the responses of the test fish toward the two predator  models.  responses by the test water.  Exposure to both models elicited similar  fish; a distinct, rapid movement into deeper  For the gull model, this movement would appear to be an  appropriate  evasive manoeuvre.  However,  this response seems counter-intuitive. expose juvenile  for  the model fish piscivore,  A movement to the bottom would  chinook to predation by  sculpins (Leptocottus  armatus),  86 Figure 5.8.  The e f f e c t of turbidity and additional cover on the recovery time of juvenile chinook salmon a f t e r exposure to model predators (open - clear, shaded - turbid; each bar represents the mean of two measures).  1.2  c E E  1.0  E  0.8  >» 0.6  I O  0.4  O O  )  CC  0.0  0.2  Bird/Cover  Bird/NoCover  Fish/Cover  Fish/NoCover  87 Table  5.5.  Analysis of variance of the e f f e c t s of turbidity, cover, and predator type on recovery time from exposure to model predators (times were log-transformed).  Source of Var i at i on  Sums of Squares  DF  Turbidity(T) Cover(C) Predator(P)  0.763 0.009 0.593  1 1 1  Error  0.649  12  3  14.108 0.166 10.965  » , » * , * » » - p<0.05, 0.01, 0.001, respectively; NS - p>0.10. error term includes the interaction term.  3  ** NS «  88 well known f o r  their  predatory  behaviour  on juvenile salmonids  (Oncorhynchus keta - Mace 1983; Jones 1986). offers  The physiology of  one potential insight into this problem.  fish  Startle responses, such  as those exhibited by the chinook in this experiment have been attributed  to the action of  giant Mauthner cells (Eaton and Bombardieri  1978) in reponse to exposure to large moving objects. described elicit  as  general, any  a response.  object  This type  of  within a certain visually  occurs in many species (Guthrie 1986).  The response is  size range, will  mediated startle  The type of  response  behaviour exhibited  by the chinook here may represent some reflex response, adaptive f o r most  predator  situations,  including most fish piscivores; albeit  not  for  sculpins. The response exhibited by the fish in relation to cover is more curious.  In the presence of an avian predator, a quicker recovery  time  in the absence of cover may be the appropriate response.  "Cover" in  this case, may represent a trap, impeding the safe retreat  of the  forager.  Given the risk  the fish may perceive in this event, a quicker  recovery time during the cover treatments perhaps should not be the expected result.  Also, avoidance responses and the use of cover f o r  chinook may be predator specific.  For the fish model, no differences  were observed in chinook behaviour with respect to cover.  Such e f f e c t s  were expected, given past  It  work  (Savino and Stein 1982).  is possible  that the stem densities I used in the cover treatments were inappropriate to investigate what has recently threshold response (Gotceitas Turbidity  disrupts  the  been revealed to be a  and Colgan 1989). inherent  visual  abilities  of  fish.  The  results I observed may have resulted from the inability of the chinook to detect the case.  the presence of The results  a particular model.  suggest that juvenile chinook modify their  spatial distribution in a manner turbidity  level  (i.e.  the  I maintain this was not  sensitive  to  ANOVA interaction  the risk term  was  and to  the  significant).  89 Still,  I cannot  completely  discount  the  possibility that  resulted from a simple failure to sense the threat. of  the  response  The manifestation  risk cannot easily be separated from the visual recognition of  stimuli  in  this  risk  experiment.  A forager may be at less risk of detection by a visual predator in turbid water, but once detected may be at higher risk to capture. Conversely, the forager may be at less risk in the above circumstances because its escape responses may be more effective.  "Cover" may be only  a body length away f o r a foraging chinook f r y in many turbid systems. Also,  turbidity  a larger Li et  probably  fish predator  al.. 1985).  eliminates  any  advantage  in visual acuity  that  may possess (Tamura 1957; Hairston et al. 1982;  Which of  these  scenarios is the most likely depends  largely on whether or not the predator sees the forager first. In the presence of avian predators, the value of turbidity as a potential form of cover is easily appreciated, humans see water from a similar  visual  perspective.  Turbidity  piscivores in most cases (for  obscures  the  vision of  bird  an exception: Haney and Stone 1988).  White (1936) observed reduced success in two piscivorous birds, a kingfisher  and  conditions.  a merganser, hunting juvenile  Bruton  (1979)  reported  that  salmonids in turbid  tilapia  (Oreochromis  mossambicus) found in the food-rich shallows of a turbid lake grew to be six  times  larger  suggested eagles  than  differential  was  individuals  in a  similar but clear  predation pressure  by  visually  lake.  He  hunting fish  responsible.  The results of the present study suggest that juvenile chinook salmon respond to the presence of a predator threat in both turbid and clear water.  Chinook both responded less intensely and f o r  durations of  time in the  turbid conditions.  shorter  I suggest that fish sensed  the presence of the predator model rather than simply failed to detect it.  Test fish exhibited responses to the presence of models in both  clear and turbid water that significantly departed from non-predator  90 situations.  These results  were consistent  hypothesis (Bruton 1979 and 1985; Blaber Swenson  1982; Simenstad et  al. 1982).  with the  and Blaber  "turbidity  as  cover"  1980; Gradall and  91 CHAPTER 6  A CONCEPTUAL HODEL OF FORAGING BEHAVIOUR UNDER VISUAL CONSTRAINT  Chapter  6.1  INTRODUCTION  The results demonstrated in Chapters 4 and 5 suggest that a tradeoff  may exist between  and risk  of  declines  predation in turbid waters.  log-linearly  predation  the conflicting demands of  risk  with increasing  also  decline  with  Reaction  turbidity.  increasing  foraging ability  distance (Ch. 4.1)  Some  turbidity  types  of  (Ch.  5.2),  although the exact nature of the relationship cannot be determined from my data.  The relationships exhibited by the foraging rates of  chinook salmon f o r turbid  surface, planktonic, and benthic prey  conditions (Ch. 4.2)  will demonstrate decisions  to  both  under various  also suggest such a behavioural tradeoff.  theoretically  sensitive  juvenile I  that an animal may make foraging visual restrictions  and perceived  predation  risk. Throughout the present and preceding chapters, I have r e f e r r e d to the  potential risk  reflects  of  predation as  perceived risk.  This terminology  a more accurate perspective than the conventional view in that  - foraging behaviour perception of  is often  affected  by  the  individual  forager's  risk, not by any measure of absolute risk.  studies (e.g. Werner Hall 1984; Johannes et  et  al. 1983; Gilliam and Fraser al. 1989), the risk  of  In population  1987; Werner  and  predation has often been  measured as the probability of  an animal being killed by a predator.  Recent  1986 and 1988; Mittelbach and Chesson  pond studies (Mittelbach  1987) have demonstrated changes in the foraging behaviour and habitat utilization of  fishes in the  presence  of  potential predators, but in the  absence of predator-derived mortality over extended periods. predation is not necessary to e f f e c t  Actual  changes in foraging behaviour.  The  92 perception of risk may be a more important determinant of foraging behaviour than the more classic view of predation risk.  The term  perceived risk has recently begun to receive more use in the behaviour literature  (Lima  Perceived context  of  and risk  this  Dill  1990).  must be viewed as especially  thesis.  First,  were used during any of  no actual predators  turbidity  are  a function of  exhibited in these  the  juvenile chinook  Second, the observed  on foraging rate of  planktonic, and benthic prey decreasing as  of  within  the investigations documented herein, although  model predators were used in Chapter 5.2. relationships of  important  latter  attributed  turbidity.  chinook f o r  surface,  to perception of  And third, the  risk  differences  relationships by planktonic foraging when  compared with surface and benthic foraging, may be explained in terms of perceived  risk.  perceived  risk  This chapter  will describe  and visual ability  the  manner in which  may be behaviourally  "traded  off"  in  turbid waters to produce the relationships documented in Chapter 4.2.  Chapter 6.2 THE E F F E C T OF VISUAL ABILITY ON FORAGING RATE Visual ability  has  been  variously  defined in the  literature.  The  acuity of the eye is the minimum angle subtended by an object on the retina  which a subject  al. 1985).  is capable of  The contrast  in illumination between  discriminating (Tamura  and background that  distinguish (Hester 1968).  Whereas both of  important  the  the latter (Duntley  et  threshold is defined as the minimum difference  a target  components of  1957; Li  visual ability  an individual can  these features of  fishes  of vision are  in clear  assumes a more prominent role as turbidity levels  1943 and 1963; DiToro 1978).  Because  of  waters, increase  increasing veiling  brightness in the foreground, suspended particles in turbid water act obscure objects  that  would be visible in clear  water  at  equivalent  to  light  93 conditions. visual  The net  ability  of  result  fish  of  in  these properties is a reduction in the  turbid  conditions.  In Chapter 4.1, I demonstrated the e f f e c t s visual  ability  prey.  Turbidity e f f e c t s  foraging  (reaction  fish  for  distance)  of  juvenile  of turbidity on the  chinook  salmon to Artemia  a reduction in the reaction distance of  their  prey.  Reaction  distance  declines log-linearly  with increasing suspended sediment concentration (Vinyard  and O'Brien  1976; Confer  The  effect  of  et  al. 1981; Crowl  turbidity  on reaction  1989; Ch. 4.1, Fig. 4.2).  general  distance (Fig. 6.1) can therefore  be  summarized by: RD a  f(TURB),  where, RD = reaction distance, and TURB = turbidity. encounter function  will also of  the  The probability of  decline with turbidity, because encounter  reaction  rate  is a  distance:  P(prey encounter) a RD, and also,  P(prey encounter)  a  Conclusions concerning the e f f e c t rate have been varied.  1 - f(TURB). of reaction distance on foraging  The generally held view has been that foraging  rate will increase as some function of the volume or area of search, depending on the type of forager and prey. theoretical  construction  of  his  "disc"  effective  In the basic  equation, Holling  (1959)  indicated the rate of successful search is highly dependant upon the distance at which a foraging animal responds to the presence of its prey (i.e.  the  reaction  including any  distance).  recognition or  Other  important  components of  decision time required prior  may also be incorporated into this rate.  to  search, an  attack  In general, foraging rate is  94 Figure  6.1.  The  effect  of  turbidity  on visual ability  Turbidity  (VA).  9 5  likely to increase as some function of the reaction distance (Ware 1 9 7 1 and  1 9 7 3 )  (Fig.  however, this relationship may be asymptotic in  6 . 2 A ) ;  many instances where the Holling "disc" equation is applicable (Fig. 6 . 2 B ) or is not truncated to the ascending limb of the latter relationship (e.g. at reduced reaction distances).  The upper limit  would be defined by the density of prey and the handling time.  Success  rate could be expressed as a probability rather than an absolute value in predictions derived by the "disc" equation or simpler linear or loglinear relationships.  The relationship of probability of feeding  (F ) VA  with reaction distance can be approximated from the following wellestablished principles: P(Fy^) a P(prey encounter), and  P(prey encounter) a RD,  therefore,  P  or alternately,  (  F  V A )  P ( F V A )  A  A  R  1  D  >  "  F  (  T  U  R  B  ) «  where, P(F ) is the probability of feeding, given visual ability ( V A ) . VA  This relationship is simplistic.  However, in this form the burden of  assumptions concerning exact rates and various prey densities are effectively removed.  Chapter 6 . 3  THE E F F E C T OF PERCEIVED RISK OF PREDATION ON FORAGING  RATE  The results of Chapter 5 . 2 and Larkin  1975;  and several authors (White 1 9 3 6 ;  Gradall and Swenson  1982;  Simenstad  et  al.  1982;  Ginetz  96 Figure  6.2.  The e f f e c t of visual ability on: A. Probability of foraging, P(Fy ), and B. Foraging r a t e using Holling's (1959) "disc" equation solved f o r search rate (y. is foraging rate; x is prey density; b is the handling time; T is the time available f o r foraging; a is the search rate). A  Search Rate (a)  97 Gregory pers. obs.) suggest that turbidity e f f e c t s risK  or  the perceived risk  (PR)  P(predator  of  predation in juvenile  encounter)  and,  PR cc P(predator  therefore,  PR  a  a reduction in the  a  chinook salmon:  1 - f(TURB),  encounter),  1 - f(TURB).  All of these observations have been anecdotal or were implied as reasonable conclusions, except  those of  the present  Even my experimental manipulations assume that as  a function  of  turbidity  discussed in the Synopsis of  (Fig. 6.3).  study (Ch. 5.2).  perceived risk  declined  This assumption will be  further  this chapter and will be tested in Chapter  7. The e f f e c t of predation risk on foraging rate has been much studied in the  last  decade, both directly  and indirectly.  There  been many reviews on this topic (e.g. Dill 1983 and 1987; Werner Gilliam  1984; Milinski  1986; Lima  and  Dill 1990).  A  synopsis  have and  of  this  work can be summarized by the simple statement: in the presence of increased predation risk, the foraging rate of nature  of  the  decline however,  is not  entirely  an animal declines. clear.  The  Sih (1986)  observed that movement of one species of mosquito larvae (Culex pipiens) decreases with increasing number of predators (Notonecta undulata) in a log-linear aegypti)  fashion, while that  decreased linearly.  foraging rates investigations  of  the cost of  guppies  reticulata)  (Aedes  these results and  were not investigated.  and Dill 1989; Nonacs  approximations of (Poecilia  mosquito species  The connection between  by mosquito larvae (Abrahams  another  Two  innovative  and Dill 1990) provide  avoiding predation in energetic terms in and  ants  (Lasius  pallitarsis),  Turbidity  99 respectively. tested.  Unfortunately,  Therefore, the functional nature of  deduced from these "minimize p/f" useful  As decline.  studies.  (deaths per  in this  predation  risk  increases,  The nature  log-linear  (Fig.  P(F ) PR  where,  the  foraging rate empirically available most  likely  These  the  It  a  of  functional prey  of  in turn  is proportional to  Chapter  6.4  relationship f o r effect  of  where  the  attempted to be  of  risk.  assumption cannot be  a theoretical  "best  or  sigmoid relationship  reversed  theoretical  that  perceived  similar conclusion regarding  present  the  guess", given  sensitive  predators  probability  of  to  the  (Fig. 6.4B).  successful  proportional to the perceived risk, which  the  visual ability  of  the  predator.  TRADEOFF  The relationships described in the outcomes  foraging will  chinook respond in a manner  is inversely  THE  the  represents  response  capture  of  foraging given the  for  relationships simply state  intuitive  prove  1 - f(PR),  An asymptotic  juvenile  probability  the probability of  and visual ability, the  information. if  (1987) introduced a  6.4A):  logic presented  supported.  will result  were  of- this decline is assumed here  P(Fpp) is the probability Unlike  levels  model which may ultimately  the  Or perhaps more correctly, or  risk  the relationship cannot be  Gilliam and Fraser  unit energy)  two  regard.  foraging will decline. linear  in both studies only  of  well-established  two preceding sections provide working  principles.  which I have provided detailed evidence  turbidity apparent  level on the simplicity  reaction  ends.  distance.  Visual ability  The only  is that  However,  for this  and perceived  the is  risk  100  Figure 6.4.  The e f f e c t of perceived risk of predation on A. Probability of foraging P(FpR), and B. Foraging rate using Holling's (1959) "disc" equation, solved f o r hypothetical e f f e c t s of perceived risk on search rate.  Perceived Risk  101 both directly a f f e c t foraging rate, the former as a sensory constraint and the latter as a behaviour-modifying variable. conflict.  Their e f f e c t s  At low turbidity levels, visual ability is high;  correspondingly high foraging rates should be expected in the absence of a conflicting variable.  However, perceived risk is also potentially  high at low turbidities; therefore foraging rates should be reduced. The reverse of both of these will be manifested at high turbidity levels.  The result of this tradeoff (Fig. 6.5) will be high foraging  rates at conditions intermediate between two turbidity extremes. Clearly, at high turbidity levels (1800 mg-L  -1  - Chapter 4.2) the  visual ability may be reduced to an extent were perceived risk is no longer relevant.  A behavioural decision by an animal which perceives  the risk of foraging to be too high may manifest itself either as the reduction or cessation of foraging activity.  The act of foraging itself  can be an inherently dangerous activity f o r salmonids (Donnelly and Dill 1984; Dill 1987).  Low foraging rates may be observed in visually  superior conditions if these conditions also promote higher perceptions of risk.  In such a situation, an animal may forage more actively in  visually inferior conditions. The predictions of the model depicted in Figure 6.5 were generated by incorporating the previously described assumptions into a multiplicative probability model.  It predicts foraging rate (FR) as a  relative probability, given the probabilities of foraging with the current visual ability and perception of risk: FR a P(F )-P(F ). VA  PR  This model clearly represents a simplification of a complicated behavioural process.  However, in the form I have presented here,  hypotheses concerning the implications of changing perceived risk in turbid and other visually restricted media may be constructed and  102  Figure 6.5.  A conceptual model of the e f f e c t of a behavioural t r a d e o f f between visual ability and perceived risk on relative foraging rate in turbid waters.  FR  a P(F  V A  )-  P(Fp ) n  103 experiments designed to test them. in the  Two of these hypotheses are outlined  subsequent section.  Chapter 6.5  PREDICTIONS OF  The E f f e c t s  OF  FORAGING  THE  MODEL  AND  RE-INTERPRETATION  RATES  of Prey Quality and Microhabitat  The foraging rates of juvenile chinook salmon demonstrated in Chapter 4.2 were consistent with the predictions of the above outlined tradeoff  model.  In predicting the  relationship between  turbidity  and  the foraging rate of salmon f o r benthic and surface prey, the model forces us to make an assumption concerning perceived risk. risk  must be relatively  clear  high while foraging on these  water) relative to planktonic prey.  planktonic  prey  accepted, that behaviour  visual ability  while perceived  operates risk  The model makes either foraging  behaviour  perceived risk  as  a constraint  functionally  acts  as  prey-  foraging  less  rates  on foraging a flexible  risk  versus  benthic  at  to  these  the  predicted  results  of  low turbidity  Chapter  foraging).  while foraging on planktonic The model predicts  levels  prey than f o r either benthic or surface prey (Fig. 6.6). examination of  low  or microhabitat-specific predictions  prey relative to either of the other two prey types. higher  is relatively  confusing results may be explained.  (e.g.. planktonic  Juvenile chinook may perceive relatively  least in  If the assumptions of the model are  parameter, then these apparently about  (at  Observed foraging rates on  may be realized only if  when foraging in clear water.  prey  Perceived  4.2 indicates  for  planktonic  A re-  a strong similarity  relationships.  Juvenile chinook salmon are  opportunistic foragers  (Dunford 1975;  104 Figure  6.6.  Predicted relative perceived risk.  foraging rates  Turbidity  at  two levels  of  105 Levy  et  al. 1979; Healey  1982; Simenstad et  obs.).  Individuals  are  variety  of  However,  prey.  al. 1982; Gregory  morphologically equipped to various  forage  locations in the  column may readily  on a wide  water column will be  occupied at different degrees of risk to predators. water  pers.  The surface of the  be visualized as being inherently  when compared to planktonic and benthic microhabitats.  "dangerous"  Occupation of  near- surface waters subjects a foraging fish to both exposure to predatory birds and also to the possibility of attack piscivorous fish. juvenile  at  The occupation of  more risk  behind while foragers represent  to  from below by  near-bottom microhabitat places a  sculpins (ambush predators),  are  actively  feeding.  especially  Planktonic  foraging may  the least inherently "dangerous" portion of the water column.  Alternately, the fish may have responded to a quality in the prey.  have been numerous (for 1984; Milinski  Lima and Dill 1990). the  relationship  prey  difference  Evidence demonstrating the tendency f o r foragers to accept  higher risk to gain greater Gilliam  from  rewards (usually measured as energy intake)  reviews see: Dill 1983 and 1987; Werner and  1986; Sih  1987; Lima  This body of  exhibited by  1988; Werner  literature  juvenile  and  Hall 1988;  would seem to suggest that  chinook foraging on planktonic  (Ch. 4.2) could be explained on the basis of a prey  quality  difference between Artemia and the two other prey species (Drosophila and Tubifex).  Foraging  juvenile  chinook salmon may exhibit higher  foraging rates on Artemia prey because a lower cost:benefit ratio exists f o r this prey as compared with Drosophila or Tubifex prey. hypothesis must also be considered. occupied by the prey may a f f e c t on this prey. to  The location or  An alternate  microhabitat  a forager's perceived risk while feeding  Microhabitat determines of the risk a forager is exposed  while foraging, usually  1988, Magnhagen  in relation  1988, Dill and Fraser  hypotheses (quality  versus microhabitat)  microhabitats in which the different  to  distance  1984).  from cover  These two  (e.g. Lima  conflicting  may be tested by switching the  prey types are  found.  106 Under the prey quality hypothesis, the foraging behaviour of juvenile chinooK salmon will be similar toward prey of equivalent quality irrespective of microhabitat.  In contrast, the microhabitat  hypothesis predicts that equivalent quality prey will elicit behaviour specific to the microhabitat.  The results of an experiment to  discriminate between these two hypotheses is presented in Chapter 7.1.  The E f f e c t of Enhanced Risk A major assumption of the tradeoff model is that foraging animals perceive (i.e. assess) risk, and that this perception of risk declines with reduced visibility.  However, perceived risk may not reflect the  actual risk of mortality.  Enhancing the risk stimulus should not a f f e c t  foraging rate to as great an extent at high as at low turbidity levels. This assumption may be tested by increasing the actual risk stimulus to the forager.  Given this assumption, any non-visual stimulus effecting  changes in foraging behaviour in clear conditions must elicit a change in foraging rate which is mitigated by the presence of turbidity.  This  must occur because perceived risk will decline as the turbidity level increases (Fig. 6.7).  An experiment to test this assumption is  presented in Chapter 7.2, involving an audible fright-stimulus. The predicted results of such an experiment are that foraging rate will be reduced at low turbidities, but progressively less reduced at higher turbidity levels (i.e. the enhanced risk and "control" curves will converge - Fig. 6.7A).  Should the assumption prove false, there  are two possible outcomes, reflecting some fixed cost of risk avoidance - either a constant or a proportional reduction of foraging rate across all turbidity levels (Fig. 6.7B).  Although measuring the energetic cost  of predator avoidance behaviour has been attempted with some degree of success (Godin and Smith 1988; Abrahams and Dill 1989; Nonacs and Dill  107 Figure  6.7.  Hypothetical e f f e c t o f e n h a n c i n g r i s k stimuli o n f o r a g i n g r a t e f o r p l a n k t o n i c p r e y ( s e e C h a p t e r 4.2). A. Assuming d e c r e a s e in p e r c e i v e d r i s k a s a f u n c t i o n o f t u r b i d i t y . B. A s s u m i n g a d e c r e a s e in f i x e d - r i s k a s a f u n c t i o n o f turbidity.  A 'Normal  Risk'  Turbidity  B 'Normal  Risk'  Turbidity  108 1990), t h e s e f i x e d c o s t s were not e s t i m a t e d as a f u n c t i o n o f r i s k .  This  work has y e t t o be p e r f o r m e d but would be invaluable in a s s e s s i n g the c o s t s o f f o r a g i n g in d i f f e r e n t  environments.  The relationship between turbidity and f o r a g i n g r a t e exhibited by chinook f o r planktonic p r e y is ideal f o r t e s t i n g assumptions about perceived risk.  C l e a r p r e d i c t i o n s o f r e l a t i v e f o r a g i n g r a t e between  turbidity levels can be e s t a b l i s h e d (Fig. 6.7).  This may not be the  c a s e f o r s u r f a c e and benthic f o r a g i n g (Fig. 6.8).  The r e l a t i v e r a t e s  exhibited by chinook f o r a g i n g on t h e s e p r e y may be t o o d e p r e s s e d a t t h e turbidity levels where t h e g r e a t e s t e f f e c t s would be e x p e c t e d (i.e. 0 mg-L ). -1  Chapter  6.6  SYNOPSIS  This c h a p t e r between  visual  proposes  ability  behaviour.  Although  by  chinook  juvenile  model  is  where  an  effect  potentially  on  or  risk  specifically  perception created  salmon in turbid useful  independent two  and  a probability model t o d e s c r i b e a  variable  more  (e.g.  variables  which in t u r n have opposing e f f e c t s mating  behaviour).  to  waters,  in making  in predicting explain the  predictions turbidity,  (e.g.  sensory  tradeoff  foraging  foraging  behaviour  model is general. in o t h e r  light)  has  tradeoffs the  opposite  ability, p e r c e i v e d  on some behaviour  This  (e.g.  risk),  foraging,  109 Figure  6.8.  Hypothetical e f f e c t of enhancing risk stimuli on foraging rate f o r surface and benthic prey (see Chapter 4.2). A. Assuming decrease in perceived risk as a function of turbidity. B. Assuming a decrease in fixed-risk as a function of turbidity.  A  B  Turbidity  Turbidity  110 CHAPTER 7  T E S T S OF THE VISUAL ABILITY-PERCEIVED RISK TRADEOFF  Chapter 7.1  THE E F F E C T OF MICROHABITAT  AND PREY  QUALITY  ON FORAGING DECISIONS  INTRODUCTION In Chapter 4, I demonstrated that the relationship between turbidity  and the foraging rate of  planktonic prey was different surface prey. for  from that exhibited f o r benthic and  The foraging rate of chinook was observed to decline at  high turbidities rates  for  all three  planktonic prey  prey  f o r benthic and surface prey. could be  However,  provided by  chinook foraging  high in low turbidity  were often reduced at  -1  disparity  types.  were consistently  conditions (<50 mg-L ), while they this  the juvenile chinook salmon f o r  these  levels  There are two potential explanations f o r  the  explained by, 1. the  tradeoff  quality  of  model (Ch. 6). the  different  Dissimilarities  prey  or, 2.  the  perceived risk associated with the microhabitat where the prey were found.  In this  study, I test  the prey  quality  and the  microhabitat  hypotheses. Prey  quality  has received considerable attention  by  researchers.  Foragers have been shown to move farther from protective cover, endure higher risk of predation, or exert prey  (Dill and F r a s e r  Magnhagen  more energy to obtain higher quality  1984; Milinski 1986; Real and Caraco 1986;  1988; Lima and Dill 1990; Nonacs  and Dill 1990).  Also,  foragers under varying risk demonstrate different prey preferences (Lima 1988). showing  Dill and F r a s e r this  type  of  (1984) behaviour  and Magnhagen (1988) describe in several  salmonid species.  studies  111 The perceived risk of a foraging fish to predators has been demonstrated to change over relatively short distances (Werner et al. 1983), often  with no actual  Chesson 1987).  predatory  act  occurring (Mittelbach and  The perceived risk of salmon foraging on prey either  at  the surface or bottom could be different from that while foraging in a pelagic  microhabitats.  observed  (Werner  Risk  sensitive  feeding mode changes have been  and Gilliam 1984; Milinski 1986).  Juvenile chinook may  feed more readily in the water column than at the surface or bottom because In  of  a lower perception of  this  study,  risk  while foraging planktonically.  I describe an experiment in which I "switched"  planktonic Artemia prey with surface Drosophila prey such that the former  was artificially  reciprocal treatment  made to float  and the  design, the e f f e c t  isolated from that of  prey  location.  to sink.  food quality was  In a effectively  Given, the conceptual tradeoff  model described in Chapter 6, the prey hypotheses  of  latter  quality and microhabitat  make conflicting predictions concerning chinook foraging  rates on these manipulated prey. The  prey  quality  hypothesis  predicts  similar or  identical feeding  responses regardless of the position of the prey in the water column (i.e.  whether it  Drosophila However,  prey the  is a surface should elicit  microhabitat  or  species-specific  hypothesis predicts  regardless of the prey species. Artemia prey Drosophila  a planktonic prey).  Artemia and  foraging responses. similar feeding responses  Chinook foraging rates on floating  should be similar to those exhibited toward "normal"  prey.  Also,  planktonic Drosophila are  expected to elicit a  similar feeding response in foraging chinook as do "normal" Artemia prey.  The prey quality and microhabitat hypotheses make clear and  conflicting  predictions.  112 METHODS  The juvenile chinook used throughout this experiment were 52.7 54.9 mm FL  in mean size.  Within trial individuals ranged +4 mm FL.  The  basic experimental procedure was the same as that described previously (Ch. 3).  I have mentioned only the necessary  changes here.  Both Artemia and Drosophila prey were used in this experiment but were prepared in such a way as to make the former float and the latter sink.  This  was  facilitated  in Artemia  items over a period of several hours. float  for  up to  an hour, before  by  air  drying individual prey  The resulting prey item would  again sinking.  Sinking Drosophila prey  were pretreated by placing an appropriate number of prey in a jar of 10 mg-L agent  -1  Polysorbate-80  overnight.  Polysorbate-80  used commercially as a food additive.  is an emulsifying  In the present  context, it  was used to reduce the surface tension of water, allowing the prey to absorb water  and sink.  In preliminary  trials, no e f f e c t  of  Polysorbate-  treated food (Oregon Moist Pellets) could be demonstrated on either growth  or  feeding preferences  Preliminary  in juvenile chinook.  conditioning of  the  test  fish to  the  experimental prey  was adjusted from that previously described (Ch. 3), reflecting the additional prey during the  categories.  Test  pre-experimental  no live prey  two  fish also continued to be fed Tubifex  conditioning.  Artemia  were  "heat-killed";  were used in this experiment.  The experimental design consisted of 12 trials at each of seven turbidity  levels 0 - 800 mg-L . -1  items were used in each treatment  A total of  of each trial.  the  320 individual prey Two trials each, using  planktonic Artemia and surface Drosophila prey, were conducted as "control"  trials.  Three  trials  each, using "switched"  prey  surface Artemia and planktonic Drosophila) were performed as trials.  Trials on surface prey and planktonic prey were of  minutes duration respectively.  (i.e. "treatment" 10.0 and 1.0  This procedure was appropriate to  the  113 treatment  of these prey categories in other experiments (see Ch. 3).  addition, one further carried  out  at  respectively. of  These  of  additional  analyses  included coefficient of  Artemia and Drosophila was  trials  allowed description of  the  effect  feeding times on the various prey categories.  Statistical  rates  each of  10.0 and 1.0 minutes experimental feeding times,  the different  significance  trial f o r  In  of  in addition to those  variation  dissimilarity  and the  of  described in Chapter 3,  F-statistic  pooled variances  (Zar  individual fish were log-transformed prior  of variances by treatment concerning normality  for  the  1984).  to  the  and trial, in order to satisfy  made by these  two  Foraging  calculation  the assumptions  statistics.  R E S U L T S Chinook salmon foraging at column (Fig.  7.1B)  level, regardless  exhibited of  the  the surface (Fig. 7.1A) or in the water  similar  prey  foraging  species.  rates  at  each  turbidity  In all cases, I observed  foraging rates consistent with those exhibited toward Artemia prey in previous  experiments (Ch. 4.2).  observed in Chapter 4.2 f o r intermediate  turbidities),  Foraging rates  consistent  Drosophila (i.e. highest rates  were not observed here.  with those at  Given the  size range  of chinook used here, this result was not unexpected (see Ch. 4.2 Effects  of Ontogeny).  outlined f o r  each prey  Experimental duration consistent with the methods type  (i.e. 10.0 and 1.0 minutes f o r  planktonic prey, respectively),  continued to  be the  the number of prey consumed in each experiment.  surface and  prime determinant  of  Chinook exposed to  surface prey f o r one minute consumed fewer prey than in either the 10.0minute Similarly,  trial  (as  expected)  fish exposed to  or  in trials  planktonic prey  with planktonic for  prey  (Fig.  10.0 minutes consumed  more prey than either planktonic prey at a lesser amount of time or  7.1).  114 Figure  7.1.  The e f f e c t of turbidity on foraging rate in juvenile chinook salmon (vertical bars represent standard e r r o r of mean o f trial means). A. Surface foraging (prey in 10.0 minutes) f o r Drosophila (thin solid line) and dried Artemia prey (broken line), and f o r Drosophila (prey in 1.0 minutes - thick solid line). B. Planktonic foraging (prey in 1.0 minutes f o r Artemia (thin solid line) and Polysorbate-80 treated Drosophila (broken line), and f o r Artemia (prey in 10.0 minutes - thick solid line).  A Surface Prey 24 r  d)  20  0  25  60  100  200  400  800  400  800  Turbidity (mg/L) B Planktonic Prey 241  0  25  50  100  200  Turbidity (mg/L)  115 surface prey at the same amount of time.  Chinook consumed planktonic  prey at a f a s t e r rate than surface prey, regardless of the prey species. Although the prey respect  to  treatment,  the  various  (Fig  7.1).  prey  consumed was quantitatively the  qualitative  categories  However,  generally  coefficients  of  different with  relationship with turbidity exhibited similar overall variation  within  the  among  form  individual  trial treatments were generally higher f o r surface prey than f o r planktonic  prey  (usually  above  and below 20/, respectively  - Fig. 7.2).  Again, I found this to be true regardless of the prey species (Fig. 7.2A Artemia; Fig. 7.2B  Drosophila).  Between prey  the pooled variances  within each treatment  usually  Chinook  insignificant.  unique to the microhabitat of  species, differences in  were generally  salmon exhibited patterns  small, and of  variance  foraging but not unique to species.  The results presented in this subchapter are based on the means of individual  trials,  Details of Fig.  these  except  when dealing  with  coefficient  of  variation.  trials may be found in the appendices (Fig. A.4 and  A.9).  DISCUSSION The microhabitat hypothesis - microhabitat e f f e c t s  changes in the  foraging rate of juvenile chinook salmon, independent of prey cannot be rejected.  Surface prey were fed upon at lower rates and in a  more variable manner than planktonic prey irrespective being preyed upon. of  These results  the prey quality hypothesis. Perceived  accessibility 1984; Werner Various  of  affects  of the species  were inconsistent with the predictions  Foraging rates were not prey specific.  predation risk prey  species -  due to the foraging rate  location, proximity, or in fish (Dill and  Fraser  and Gilliam 1984; Magnhagen 1988; Mittelbach 1988).  studies  by  Milinski (for  review: Milinski 1986) demonstrate  that  116  Figure 7.2.  The e f f e c t of turbidity and microhabitat on the coefficient of variation {'/.) in foraging rate by juvenile chinook salmon in individual trials (square - s u r f a c e foraging; circle - planktonic foraging; filled symbols represent "usual" position o f prey, open symbols represent manipulated prey; NS, *,*»,*** - variance not significantly d i f f e r e n t [p>0.10], d i f f e r e n t at p<0.05, p<0.01, p<0.001, respectively). A. Artemia. B. Drosophila.  A  Artemia  100  c  -B  80  I  0  o  .1  40  D  surface  D  o  0)  •  8*° *  •g 1  25  B 120  •  •»  1 1  1  50  Turbidity (mg/L)  100  5 planktonic 1  200  Drosophila NS  C  O100  surface  I  •§» 8 0 «*-  o c  ^  «•—  o  60 40  0)  o O  ao  o © 25  o 60  Turbidity (mg/L)  8  O  _  o  100  200  planktonic  117 in clear  water  sticklebacks  (Gasterosteous  aculeatus)  lower  their  feeding rates in the presence of high Daphnia concentrations. attributed  the change in behaviour  to the increased risk  feeding on the denser plankton and the relaxation of to forage effectively present  study  in such a patch.  suggests  this  fine scale microhabitats. were  similar  in this  He  associated with  vigilance required  For generalist foragers, the  principle also applies to  foraging within  The distances between forager and prey  experiment; thus, distance  to  prey  is unlikely  be a large source of variability.  For the purpose of the present  investigation,  of  any  residual  cost  incorporated into the concept of explanation of microhabitat other  the results  occupied by  explanations  prey  quality.  is that behaviour the  seem  handling or  prey.  accessibility  to  was  The most likely  is influenced by  Given the  type  the  reciprocal manipulation,  unlikely.  Avoidance of high-risk areas by foragers has been demonstrated f o r a great  number of  species (for  review: Lima and Dill 1990).  Behaviour  consistent with predator avoidance has also been demonstrated in cases where a predator was not actually detected (Mittelbach and Chesson 1987; Mittelbach  1988).  Foraging animals may be expected to  dangerous areas.  Particular  foragers  escape some classes of predators. their  exposure, in areas  avoid inherently  may have a limited ability  to  Such foragers may avoid, or limit  accessible to that predator class.  For  juvenile chinook salmon, the surface of the water may represent an unsafe microhabitat. piscivorous silhouette  fish their  strike  from below, using the  targets  the water surface fish.  Not only are predatory birds numerous, but many (Munz and McFarland 1977; Guthrie  potentially  The foraging rates,  background illumination to  is a dangerous location f o r  1986).  small foraging  and associated large variances, of  foraging chinook are consistent with the argument that f r y  Thus,  surface  are  sensitive  to these dangers, regardless of whether they are real or perceived. Studies examining the decisions of foragers with respect to  the  118 air-water interface are lacking.  The present study breaks new ground in  this area of fish foraging ecology.  One of the expected results of this  experiment had been a difference in the qualitative nature of  the  relationship between foraging rate and turbidity among the two prey or microhabitats.  I did not  observe  this  result.  Given the  size of  the  chinook used at the time of my experiments, this should not have been surprising (see Ch. 4.2 - E f f e c t s qualitative  similarity  of  of Ontogeny).  planktonic  have been expected at this size.  and surface  The observed foraging rates should  An experiment over a broad range of  chinook sizes may prove useful in elucidating the e f f e c t s of ontogeny on the by  use of Werner  microhabitat  on finer  scales  than those previously  identified  and Gilliam (1984) and others.  Chapter 7.2  THE E F F E C T OF ENHANCED RISK ON FORAGING RATE IN TURBID WATER  INTRODUCTION An established working principle has been that reduce  the predation risk  (White 1936; Bruton Cyrus risk  and Blaber  of  1979; Blaber  1987a).  and Blaber  Foragers,  predation by altering their  expense of  reduced energy  1984; Milinski 1986; Lima studies demonstrate behaviour predation 1988).  to small fish from visually  that  1988; Lima  acts  to  hunting predators  1980; Simenstad et  including fish, respond to foraging behaviour, often at  al. 1982; increased the  (Dill 1983 and 1987; Werner and Gilliam and  Dill 1990).  fish may dramatically  in the presence of events  intake  turbidity  alter  Long-term their  foraging  potential predators, even without  occurring (Mittelbach  field actual  and Chesson 1987; Mittelbach  That foraging fish change their behaviour in a manner that  119 reduces their energy intake suggests a sensitivity  to the perception of  risk.  foraging rate  In the  present  investigation, I measure  the  of  juvenile chinook salmon at two levels of risk to determine the e f f e c t enhancing  the  risk  stimulus  on foraging behaviour  in turbid conditions.  I test the assumption, made in Chapter 6, that turbidity reduces risk  perceived  by  of  the  foraging juvenile chinook.  The prediction I made in Chapter 6 was that increasing a risk stimulus  uniformly  proportionally  benthic  of  visibility  on foraging rate  as  conditions has turbidity  under enhanced, and baseline, risk  with increasing  experiment  a range  less e f f e c t  Foraging rates converge  across  to  test  this  turbidity.  In this  increases.  conditions should  subchapter, I describe an  prediction using surface, planktonic, and  prey.  A risk stimulus was used to enhance the threat to foraging juvenile chinook salmon. investigations  are  Chapter  5.2.  However,  (Vinyard  and O'Brien  The most common risk  visual  (for  review:  since  turbidity  1976; Confer et  Dill  1987), including  acts to  varying  turbidity  visual.  From  conditions.  a number  and auditory  of  Therefore, the potential  stimuli, I chose  of  ability  4.1), this  investigation.  using a fixed level of  those  reduce visual  al. 1978; Chapter  technique could not be used in the present measure perceived risk  stimuli used in fish  I wanted to  threat stimulus under stimulus had to be non-  mechanical, chemical,  electrical,  sound.  Low frequency sound is part of the sensory repertoire of salmon (Hawkins 1986). environment, sound  particularly  in courtship  Hawkins 1986). by  Many potential predators gadoids (e.g.  and intraspecific  on salmonids in the  marine  cod, haddock, pollock),  use  threat  displays (for  review:  The sound signals of potential predators may be detected  salmon, influencing subsequent behaviour.  sound was an ideal stimulus because its e f f e c t  In the  present  experiment,  on fish behaviour would  not be altered by visual considerations, only by the perception of  the  120 magnitude of  the  risk.  METHODS Tubifex, Artemia, and Drosophila were used as prey in separate experiments. design  with two  and the 3).  levels  previously  of  risk  ("control"  were  described 7 levels of  for  run  all prey  turbidity  trials)  (0 -800 mg-L ; Ch. -1  by  risk  each level of  except Drosophila, where there  level, with all  risk.  levels  The separate  and were blocked into control-risk The risk (i.e.  and "enhanced risk"  Three replicates were performed f o r each level of risk and  turbidity at  Each of these experiments consisted of a two-way factorial  low  clicks)  each aquarium (Fig. 7.3). speaker in a watertight activated  risk  turbidity trials  were run sequentially  pairs.  originating from two  sound signal  sound transducers in  Each transducer consisted of a 7.5 cm, 8-ohm whirlpak bag.  arranged in a parallel  from a remote  during all treatments,  Trials  run simultaneously  stimulus was a 10-watt, 30-Hz, square-wave  frequency  aquarium was  of  were two.  The pair of transducers in each electrical  circuit  location during trials.  but were only activated  and were  They remained in place during "enhanced risk"  trials. Preliminary  trials  established  that  sound elicited a response in  the chinook similar to that exhibited in the presence of predator models (Ch. 5.2). " signals  Test fish moved rapidly to the bottom upon exposure to sound originating  within  the  aquarium.  During  preliminary  trials,  test fish responded to the continuous presence of the stimulus f o r approximately 35 seconds and then resumed normal activity.  The stimulus  was presented in six randomly timed 5-second increments over the course of  an experiment.  response.  This effectively  lengthened the duration of  the  121  122 Within the confines of  the aquaria, the sound environment during  enhanced risK treatments was probably complex.  I did not attempt to  describe these sound patterns other than to observe their e f f e c t s on fish  behaviour.  The turbidity  measurable e f f e c t  level was  unlikely to have had a  on the sound stimulus f o r several reasons.  First, the  sound signal was at a longer wavelength than the size of the sediment particles. concrete  Second, the (similar  to  sound absorption coefficients of  sediment in molecular structure)  brick  are  and  low (0.02 -  0.03).  Third, the density of the medium at 800 mg*L~ was only 0.02/.  higher  than  1  clear  water.  All these  negligible changes in sound quality ranges  tested  (Giancoli  considerations indicated that  probably occurred over  the  turbidity  1980).  The mean size of juvenile chinook used in these experiments increased  over  the  testing  period.  and 66.6+4.9 mm FL  (+ s.d.)  for  respectively.  No significant  Fish sizes were 59.5+4.0, 64.4+3.7,  Tubifex, Artemia, and Drosophila trials,  "within  prey  type"  size were found among the risk or turbidity  differences  in fish  treatments.  R E S U L T S  The e f f e c t of the enhanced risk stimulus on the foraging of juvenile  chinook on surface  form of  prey  (Drosophila)  was unclear.  The general  the relationship between foraging rate and turbidity was similar  to that documented in Chapter 4.2. intermediate  turbidity  conditions.  Foraging rates were highest at This result  was  also expected from  the size range of the fish used throughout these experiments (see Ch. 4.2  - Effects  of Ontogeny).  Generally, the foraging rates in the  enhanced risk treatments were lower than the controls at most turbidity levels  and f o r  most  individual trials  convergence of foraging rates  (Fig.  7.4).  The expected  was observed at higher turbidities (100 -  123  Figure 7.4.  The e f f e c t of turbidity and risk on mean foraging rate on surface prey (number of Drosophila in 10.0 minutes) by juvenile chinook salmon (control risk - solid line; enhanced risk - broken line; vertical bars indicate standard e r r o r of mean of trial means).  0  25  50  100  200  Turbidity (mg/L)  400  800  124 200 mg-L ).  However, chinooK foraging rates  -1  expected.  Foraging rates  in controls.  However,  at 0 mg-L  -1  were not as  were higher in the enhanced risk trials  this  observation  was  not inexplicable.  than  The  e f f e c t of enhanced risk on foraging rate may be expected to be dampened where  the  in this  foraging rates  prey  type).  these levels.  were lowest  Inconsistencies  (i.e.  in the  low and high turbidity results  levels  were more likely  Even random variation may appear to a f f e c t  at  inconsistent  results. The foraging rates of salmon on planktonic Artemia supported the perceived risk hypothesis.  Regardless of the risk treatment,  the  general form of the relationship between foraging rate and turbidity was similar  to  my other  Foraging rates  results  for  were highest  this  prey  type  in low turbidity  (Ch. 4.2, 4.3, and 7.1).  treatments  At most turbidity levels, I found the foraging rates  (1200 mg*L~ ). 1  of the enhanced  risk treatments were lower than those of the control treatments (Fig. 7.5).  This  p<0.05).  difference  At  higher  was  significant  turbidity  at  0 mg-L  -1  levels, foraging rates  (one-tailed in the  t-test,  enhanced  risk and control treatments converged. Foraging rates the  perceived risk  of juveniles on benthic Tubifex prey also supported  hypothesis.  The relationship between  foraging rate  and turbidity again was of the form observed in Chapter 4.2. highest  in intermediate  regardless lower  of  the  turbidity  risk  foraging rates  conditions (25  treatment.  in the  At  elevated  - 100 mg-L ), -1  all turbidity  risk  Rates were  levels, I observed  treatments  (Fig. 7.6).  The  largest differences between the elevated risk and control treatments were  observed at  lower  turbidities  (<100 mg-L ). -1  Again, as  expected  from the perceived risk hypothesis, I observed a convergence of the rates  of  these  treatments  The perceived risk  at  higher turbidity  hypothesis (Ch. 6.5)  levels. predicts that  differences  in foraging rate between enhanced risk and control treatments will decline  with increasing  turbidity.  For  chinook  foraging on planktonic  125  Figure 7.5.  The e f f e c t of turbidity and risk on mean foraging rate on planktonic prey (number of Artemia in 1.0 minutes) by juvenile chinook salmon (control risk - solid line; enhanced risk - broken line; vertical bars indicate standard e r r o r of mean of trial means).  126 Figure 7.6.  The e f f e c t of turbidity and risk on mean foraging rate on benthic prey (wet weight of Tubifex in 5.0 minutes) by juvenile chinook salmon (control risk - solid line; enhanced risk - broken line; vertical bars indicate standard e r r o r of mean of trial means).  14 r C  E 12  0  25  50  100  200  Turbidity (mg/L)  400  800  127 (Artemia) prey, a regression of  these  (ANOVA; df=1,13; p=0.023; r =0.34).  The negative  2  this  relationship  enhanced risk zero).  (Fig.  differences  was  slope demonstrated by  7.7B), indicated a convergence  and control treatments  significant between  (i.e. approaching a difference of  Similar results were not demonstrated by chinook foraging on  surface  (Drosophila)  respectively). foraging  or  benthic (Tubifex)  prey  (Fig. 7.7A and 7.7C,  The perceived risk hypothesis was supported by chinook  on planktonic  prey.  Here, I have reported results based on the means of within  the  trials.  appendices  The  (Fig.  details  A.5,  A.10,  of  each  and  individual trial  are  treatments  recorded in the  A.14).  D I S C U S S I O N  Fish generally respond to only low frequency sound (<300 Hz). comparison, mammals and birds exhibit a much broader sensitivity  By  range  (e.g. to 15 kHz in humans; >300 kHz in bats and some marine mammals). However, are  within  quite  their  sensitive  relatively to  restricted  sound (for  detectability  review: Hawkins  salmon (Salmo salar - Hawkins and Johnstone  range,  1986).  fish  Atlantic  1978) are sensitive to sound  pressure in the "near-field" (<30 to 300 Hz frequencies) but not to "far-field" far-field  sound.  The  sensitivity  is  exact not  biological significance of  clear.  I suggest that  near-  detection  versus of  proximal movement may be more important to these fish (and perhaps other salmonids) given their represent  more confined freshwater  a type of sensitivity  useful f o r  habitats.  It  may also  predator detection.  In the  present study, juvenile chinook rapidly moved to the bottom of the tank in response to the activation of  the 30-Hz, sound stimulus.  This  response was reminiscent of the response exhibited by chinook to the presence  of  predator  models (Ch. 5.2).  Although direct  links with  128 Figure  7.7  The e f f e c t of turbidity (logrmg-L" ]) on the difference between control and enhanced risk foraging rates by juvenile chinook salmon (data points indicate [control minus enhanced risk] f o r the means of each pair of trials). A. Surface foraging - Drosophila. B. Planktonic foraging Artemia (regression significant p=0.023). C. Benthic foraging - Tubifex. 1  I  -18  0  0.5  1  I  1.5  Log(Turbidity[mg/Ll)  I  2  I  2.6  129 predator avoidance and sound detection in fish have not been demonstrated to my knowledge, such a response may be adaptive.  Many  potential fish predators, such as gadoids, produce sound detectable salmon (Hawkins 1986).  Avoiding areas  potentially reduce predation risk. future  where such sound originates would  I recommend this as an area  for  research. At  for  to  increasing  planktonic prey  enhanced  risk  turbidity  levels,  foraging  rates  by  juvenile  chinook  became progressively more similar in control and  conditions.  I suggest, from this  evidence, that  foraging  salmon were responding to a reduction in their perception of risk in the more turbid conditions.  This may have resulted in their  feeding at  higher rates on planktonic Artemia prey. E f f e c t s of enhanced risk on surface and benthic foraging by chinook were inconclusive. expected at At  However, reduced foraging rates were  low turbidity, regardless of  low turbidity, the overall e f f e c t  probably masked.  vigilance  that  turbid conditions manifest of  required in clear water. estuarine result  enhancing the risk  (Ch. 6.5).  stimulus was  least consistent with the perceived risk hypothesis.  requirements  turbid conditions.  treatment  Therefore benthic and surface foraging rates exhibited  by chinook were at I suggest  of  the risk  If  habitats),  a relaxation in the  foraging chinook salmon which would normally Chinook may be more motivated to feed in  prey  density is high (as  this combination of  may often be the case in  food supply and motivation may  in higher daily foraging rates and growth rates in turbid  conditions. high prey  Levy and Northcote (1982) demonstrate high growth rates in density, turbid conditions in the  Fraser  Estuary.  Furthermore, my own work in the Fraser River system suggests that prey densities need not be higher under turbid conditions to e f f e c t  an  increase in foraging rate when compared to clear water environments (Gregory turbid  pers. obs.).  estuarine  I have also observed that  conditions feed  throughout the  juvenile  daylight  salmonids in hours.  This is  130 generally not the case in most clear water systems, where feeding behaviour  exhibits marked diurnal patterns  1987; Angradi and Griffith waters may result  1990).  (Adams et  al. 1987; Levy  Reduced perceived risk  in turbid  in higher chinook foraging rates.  Perceived risk has an impact on the foraging behaviour and habitat choices  of  fish  (Mittelbach  and Chesson 1987; Mittelbach 1988).  Furthermore, these changes in foraging behaviour were demonstrated to e f f e c t a reduction in the energy intake and subsequent growth of bluegill sunfish (Lepomis  macrochirus).  From the  results  of  these  and  my own investigations, I suggest foraging behaviour may be affected by perceived This  risk,  not  necessarily  by  suggestion may be particularly  the  probability  relevant  of  in the  predation  cases  ambush predators, which may not be seen prior to a strike.  itself.  involving Perceptions  of risk related to microhabitat may be all that forearm a foraging juvenile  chinook  predators.  salmon against  possible ingestion by  or  benthic  In turbid conditions, these predators may have their  potential attack  range effectively  reduced.  As it may be difficult  avoid capture by these species once an attack avoidance  aerial  of  detection attains high importance.  to  is initiated, the Turbid conditions may  be likely to reduce such detection and subsequently reduce encounters with predators.  Foraging behaviour may be expected to change to reflect  this reduction in perceived risk.  These ideas must be explored further.  131 CHAPTER 8  Chapter  GENERAL DISCUSSION AND CONCLUSIONS  8.1 GENERAL  Vision as  DISCUSSION  a Constraint  The  visual  ability  of  decreases as a function of et  al.  1981; Ch. 4.1).  fish, measured as  reaction  distance,  turbidity (Vinyard and O'Brien 1976; Confer  Visual  ability  likely  manifests  itself  as  a  constraint on foraging rate by directly affecting the rate of prey encounter (Ware 1971 and 1973; Confer and Blades 1975; Luecke and O'Brien 1981).  In this manner, the  negative  impact of  suspended  sediment on fish vision is easy to appreciate and has been abundantly demonstrated  Turbidity  in the  literature.  and the Risk of  The impact of  Predation  turbidity  on the predation risk of  juvenile fish has  not been convincingly demonstrated in past work, although anecdotal and correlative  information exists  Ginetz and Larkin 1975; Bruton  from many field studies (White 1936; 1979 and 1985; Blaber  Simenstad et al. 1982; Cyrus and Blaber investigation  (Gradall  and Swenson  and Blaber 1981;  1987a) and one laboratory  1982).  The studies I have  presented examine the perception of risk in turbid and clear water in controlled laboratory experiments.  The results of Chapters 5 and 7  suggest that  juvenile  environments.  My work supports the conclusions of the above  investigations  and  chinook salmon perceive  speculations.  less risk  in turbid water  132 Tradeoffs  Between Visual Ability  and Perceived  Risk  in Fish Foraging  Behaviour Visual constraints and reduced perception of risk may be behaviourally  "traded off".  of Boehlert  and Morgan (1985) and Neverman and Wurtsbaugh (in prep.),  demonstrate that tradeoffs that larvae  relating  to  visual ability  cases,  which suggest  and some other  perceived  risk  was  the  variable.  I suggest  additional variable.  and Morgan (1985) suggested increased feeding rates by herring (Clupea  due to field  young fish exhibit foraging rates  in all three  Boehlert  The results of my work (Ch 4.2), and that  to  harengus  pallasi)  in turbid conditions might have  increased prey-background contrast prey.  I cannot  entirely  dismiss  within their this  limited  possibility.  been reactive  Juvenile  chinook salmon have demonstrated decreased reactive times to prey silhouetted against  turbid backgrounds (Godin and Gregory  in prep.).  However, Giguere and Northcote (1987) have demonstrated that full guts in otherwise  transparent  predation by fish.  Chaoborus larvae  The cost of  The visual contrast of a full gut would be  Therefore, increased foraging rates the herring larvae  full gut may suggest.  likelihood of  in terms of predation risk in herring would be  reduced in turbid water. subject  the  Larval herring are also transparent.  increased foraging rates reduced.  increase  to the higher risk  in turbid water would not of predation which its  Neverman and Wurtsbaugh (in prep.) observed peak  foraging rates by young-of-the-year sculpins were highest at intermediate levels.  light  I suspect  levels,  while reduced  a similar  tradeoff  at  higher and lower  in these  results  also.  light However,  my own work suggests that light levels are a poor predictor of foraging rate, except on a coarse scale.  Low light levels may reduce the  perceived risk in some species (sockeye  salmon - Clark and Levy 1988;  sculpin - Neverman and Wurtsbaugh in prep.), whereas perform this  function in others  (tilapia  - Bruton  turbidity may  1979; estuarine young-  133 of-the-year juvenile  fish - Blaber  and Blaber  1981, Cyrus and Blaber 1987a;  chinook salmon - Ch. 5 and Ch. 7).  Turbid Water Foraging in Fishes  Turbidity has often been viewed as detrimental to the foraging activities  of  fishes  1981) especially Confer  et  (Ellis  salmonids (Sigler  al. 1978).  1987). occur beyond  (Noggle  However, only  at  1978; Sigler  et  naturally  al. 1984; Servizi of  forms, may actively  and  of  Martens  chronic exposure in fishes  turbidity, orders  (Wallen 1951).  studies (Blaber and Blaber that  High levels  to salmonid feeding rates, growth,  high levels  1979) demonstrate  1985; Gardner  al. 1984; Berg and Northcote 1985;  physiological responses to  experienced  evidence, other Bruton  deleterious  excessively  levels  et  1972; Bruton  This concern has been justified.  suspended sediment are and survival  1936; Alabaster  In the  of  magnitude  face  of  1980; Cyrus and Blaber  fishes, especially  larval and  this 1987a;  juvenile  seek out turbid waters, where they may exhibit  higher survival rates.  Further,  the active preference  of  turbid over  clear conditions has been demonstrated in the laboratory (Cyrus and Blaber  1987b; Gradall and Swenson 1982).  These observations create  an  apparent paradox, which may be resolved by considering that fish may behaviourally all  of  these  trade  their  situations.  I discovered a clear investigations  off  which  this  predation and visual ability in the  above  dichotomy among conclusions reached. concerned  reported positive e f f e c t s . of  of  In an examination of  reported negative e f f e c t s ; work review  risk  topic, the  human-induced turbidity on naturally  (7  field studies, All of  the  studies)  turbid systems (4 studies)  While I have not conducted a comprehensive dicotomy is suggestive.  134 Salmonid  Life  Chinook  Histories salmon exhibit  the  most  interpopulation variablity  in life  history strategy among all anadromous members of the genus Oncorhynchus (Taylor  1990).  described.  Basically,  two  chinook  life  history  strategies  have been  The first, "stream-type", spend one year in or near  natal stream and migrate to sea as 1+ year old smolt. "ocean-type" (normally underyearling f r y  The second,  from fall adult spawners), migrate to sea as  but rear  f o r a variable amount of time in the  The Harrison River stock, from which the fish of is "ocean-type".  the  estuary.  this study originated,  Although the duration of freshwater  existence has been  shown to be influenced by the growth potential in natal streams 1990), it  is not  influences  life  clear history  how  turbidity  estuarine  productivity  strategy.  Seaward migrating juvenile population-specific  or  (Taylor  estuarine  salmon demonstrate species- or  residency  periods.  Although Healey  (1982)  and Simenstad et al. (1982) both categorize chinook salmon as the most estuarine  dependant of  populations  of  this  the Pacific  salmon species, both also described  species which were transient  estuarine  residents.  Estuarine residency in this species has been demonstrated to range from days to weeks, in 1+ year old smolt, and up to months in young-of-theyear  individuals  correlated  (Simenstad  et  al. 1982).  Residency  duration has  been  with salmon size (Healey 1982).  Many river  systems supporting large salmon populations have turbid  mainstem components (Squamish River - Levy 1977; Taku River - Murphy et al. 1989; Fraser  River  Fraser  individual juvenile  Estuary  - Northcote  and Larkin 1989).  In the  turbid  chinook salmon have been resident  for  periods of up to two months (Levy and Northcote 1982) with residency within the estuary of  spanning March to July in any one year  all salmonid species (Levy  Gregory pers. obs.).  et  a). 1979; Levy  for  juveniles  and Northcote 1982;  This residency period also corresponds to that of  135 peak  discharge Prey  juveniles  and highest  availability  may  turbidity influence  within the estuary.  level in the the  Fraser  residency  River.  time of  salmonid  Prey abundance in the Fraser  River system  has been observed to be several orders of magnitude higher in the estuary than at either downstream or upstream locations (Northcote and Larkin 1989). because of  High foraging rates  system that  In the of  However, juvenile  it  has also been observed in the  chinook found in clear  densities (Harrison  to nearby  turbid areas  with lower  prey  same  water habitats  River) exhibit lower  gut  reduced river  with high  fullness when compared  densities (Gregory  pers. obs.).  same study, predation on juvenile salmonids was observed in 10/  older conspecifics in clear water.  turbid water.  No evidence was found of  availability  in this  system.  Prey  explanation f o r  the duration of  Perceived  in Behaviour  Risk  density  than prey  may only provide a  residency of  their  My work  life  light level  estuary.  Studies ecology and  all fish species found in turbid waters at various history.  Turbidity  (Ch. 4.3) implies that  foraging behaviour a coarse  partial  salmonids in the  My results have obvious implications to the study of behaviour of  this in  I suggest the presence of turbidity may have a more  pronounced, and positive, impact on foraging rates  of  system  high food density, mitigating any negative impact of  visual ability. prey  may be maintained in this  scale.  This is unlikely review.  affects  the e f f e c t  may be correlated  has been especially  communities (for  also  of  ambient  turbidity  stages  light conditions.  on chinook  to ambient light conditions only on  to be universally  true.  well documented on coral  Munz and McFarland 1977).  The e f f e c t  of  reef  Even the  light  related movements of other salmonids have been related to risk of predation  (Levy  1987; Clark  and Levy  1988).  Also,  similar  relationships  136 to those I present in Chapter 4.2, have recently been demonstrated f o r juvenile  sculpins over  in prep.). for  a range of  Perceived  the  relatively  risk lower  of  light levels (Neverman  and Wurtsbaugh  predation may be a possible explanation  foraging rate  of  sculpins in higher  light  conditions. Light e f f e c t s  are not confined to the aquatic environment.  The  foraging behaviour of many nocturnal animals may be reduced during periods  of  Artificial  bright  moonlight (for  increases  in light  review: Lima and Dill 1990).  level have also been demonstrated  to  reduce foraging rates by nocturnal animals (Kotler 1984; Brown et al. 1988).  In all of  these  cases, exposure to predators  illuminated conditions has  been suggested to  reduce  in highly foraging  activity.  Terrestrial animals subject to predation may commonly assess their potential risk by some surrogate, such as the distance to cover (Schneider  1984; Elgar  1986).  In some cases, the  cannot be used as a measure of perceived risk.  proximity to  cover  Cover can be a source of  predation risk f o r some animals, such as marmots (Carey  1985) and  African antelope (Underwood 1982), or a source of risk as well as an escape from it in others, such as some finches (Lima et Clearly, research must ultimately of  foragers  easy  attempt  when investigating related  task; often  an  to measure the perceived risk  behaviour.  This will not be an  a given experimental animal may alter  subtle ways when perceiving elevated  al. 1987).  risk.  its behaviour in  These subtleties may elude  investigator. The question of subtle e f f e c t s may be relevant in the case of  ambush predators. juvenile dilemma.  For  many terrestrial  chinook salmon), ambush predators  and aquatic present  an  animals (including interesting  By the very nature of the hunting strategy of these predators,  avoidance of predation by a forager would be best achieved by avoiding the encounter. foraging  Since these predators remain essentially hidden from the  animal until  the  attack  distance  is relatively  short, it  would  137 benefit the forager to measure risk in a manner that did not rely on the sighting of the predator itself. be  its  perception  learned  experience  inherently of  of  higher  Of more importance to the forager may  risk, possibly genetically  of  times, locations, or  risk.  For  juvenile  inherited or  environmental  through  conditions of  chinook salmon, ambush predators  two general categories - avian and aquatic - make such perceptions  vitally  important.  Chapter  8.2  The reaction  CONCLUSIONS  visual  ability  distance,  of  juvenile  declined  chinook salmon, measured  with increasing  found previous investigations  on other  1976;  None of  Confer  own, indicate  et  al. 1978).  a threshold type  of  turbidity,  similar  species (Vinyard these  as to  that  and O'Brien  investigations, including my  decline in reaction  distance  for  turbidity as has been demonstrated with decreasing light (Harden Jones 1956; Vinyard and O'Brien 1976; Confer et  al. 1978).  These results  and  those of my experiments comparing the e f f e c t s of light and turbidity level  on foraging behaviour  viewed simply  by  (Ch. 4.3)  examining its  suggest that  effect  turbidity  and  equivalent  light  be  on ambient light conditions.  However, f o r planktonic prey this may indeed be the case. rates by chinook on surface  cannot Foraging  and benthic prey were dissimilar in turbid  conditions.  Visual ability was a poor predictor of foraging rate on surface and benthic prey  by juvenile  chinook.  While it could be argued that  planktonic foraging rates by chinook may have been loosely predicted by visual prey. predict to  ability,  this  explanation  is  untenable  An hypothesis based solely increased  clear  water  for  on visual e f f e c t s  foraging rates in intermediate conditions.  Visual  surface  ability  alone  and benthic  is unlikely  turbidity cannot  to  as compared fully  explain  138 the  foraging behaviour  of  juvenile chinook.  The positive e f f e c t s  of  turbidity on perceived risk by chinook  were suggested in experiments involving model predators. piscivore  models  elicited  similar  responses  in juvenile  Avian and fish chinook.  In  clear water, salmon moved into deeper waters closer to the bottom following  exposure to  the  models.  In turbid conditions, both  the  magnitude of the response and the recovery time of salmon following exposure were reduced. of  Experiments in Chapter 7, isolating the  effects  the visual component of risk perception, suggest that a reduced  response in turbid waters was not necessarily due to a failure to detect the  presence  perceived  of  risk  a predator. in  juvenile  It  appears  likely  that  turbidity  chinook.  The more established view purporting detrimental e f f e c t s turbidity  on visual foraging (for  review: Bruton  1985) was  I propose a view of behavioural  flexibility.  turbidity  effects  of  on both  visual  of  re-examined  and found to be inadequate. The  mitigates  ability  and  perceived risk must be appreciated to describe foraging behaviour.  My  findings regarding changes in foraging rate with ontogeny add support to a  more  behaviourally  Although  their  flexible response to visual  turbid conditions, juvenile  ability  turbid water conditions.  may be deleteriously  affected  chinook may be more motivated to  because of their reduced perception of risk.  by  feed  Theoretical maximum  feeding rates may not be attained on short time scales (minutes) f o r some prey due to visual constraints. longer  time  scales  (diurnal)  Fish perceiving less risk subsequently  may  However, foraging rates over  be positively  affected  by  turbidity.  may be more willing to feed at high rates, and  exhibit higher growth  rates.  Salmonids in clear  waters  tend to exhibit highest foraging rates at distinct times of  the day  (Adams  Chinook  et  al. 1987; Levy  salmon in turbid estuarine (Gregory  1987; Angradi and Griffith waters forage actively  1990).  throughout the day  pers. obs.) and exhibit elevated growth rates (Levy and  139 Northcote  1982).  I suggest foraging animals may "trade o f f " of  obtaining food and avoiding predators In  negatively  affects  foragers  (Hobson 1986; Lima and Dill 1990).  behaviour  changes  both  cannot  of be  these  cases, the  including  in conditions of  visibility.  to  many  sensory  in varying positive  turbid  abilities of visibility  and negative  viewed simply as detrimental  the conflicting goals  water,  I suggest  effects. to  reduced  predators  conditions  limited visibility  as well as foraging  in a manner  sensitive  Reduced visibility  a visually  foraging animal.  140  REFERENCES  Abrahams.M.V. and L.M.Dill. 1989. 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An experimental test of the e f f e c t s of predation risk on habitat use in fish. Ecology 64: 1540-1548. White,H.C. 1936. The food of kingfishers and mergansers on the Margaree River, Nova Scotia. J . Biol. Bd. Can. 2:299-309. Wilkinson,L. 1988. SYSTAT: Illinois.  the  Woodhead.P.M.J. 1956. The a light gradient. J .  behaviour of minnows (Phoxinus Exp. Biol. 33:257-270.  Zar.J.H. 1984. Biostatistical New Jersey.  system  analysis.  for  statistics.  Prentice-Hall,  Evanston, phoxinus L.)  Englewood  in  Cliffs,  APPENDIX 1. Figure  A1.  Feeding Trials f o r Drosophila, by Experiment  152  E f f e c t of turbidity on the foraging rate (prey in 10.0 minutes) of juvenile chinook salmon f o r Drosophila prey, 1987 (vertical bars - standard e r r o r ; n = 8 fish per mean).  APPENDIX 1. Figure A2.  Feeding Trials f o r Drosophila, by Experiment  153  E f f e c t of turbidity on the foraging rate (prey in 10.0 minutes) of juvenile chinook salmon f o r Drosophila prey, 1988 (vertical bars - standard e r r o r ; n = 8 fish per mean).  200  Turbidity (mg/L)  400  154  APPENDIX 1. Feeding Trials f o r Drosophila, by Experiment Figure A3.  E f f e c t of A. Light and B. Turbidity on the foraging rate (prey in 10.0 minutes) of juvenile chinook salmon f o r Drosophila prey (vertical bars - standard e r r o r ; n = 8 fish per mean).  A  B  0  _i wi  i  1  1-  1  <—  -1.1 ~ - a a Log(microEir»tein8/irr/8)  o.n  o*i  0.08  28  BO  TOO  200  Turbidity (mg/L)  400  800  APPENDIX 1. Figure  A4.  155  Feeding Trials f o r Drosophila, by Experiment  E f f e c t of turbidity on the foraging rate of juvenile chinook salmon f o r A. Surface Drosophila (prey in 10.0 minutes) and B. Planktonic Drosophila (prey in 1.0 minutes) (vertical bars - standard e r r o r ; n = 8 fish per mean).  Turbidity (mg/L)  w  f  64.9*3.2 mm FL  Turbidity (mg/L)  APPENDIX 1. Figure A5.  Feeding Trials f o r Drosophila, by Experiment E f f e c t of turbidity on the foraging rate (prey in 10.0 minutes) of juvenile chinook salmon f o r Drosophila prey A. "Normal" and B. "Enhanced" risk (vertical bars standard e r r o r ; n = 8 fish per mean).  156  in  APPENDIX 2. Figure  A6.  Feeding Trials f o r Artemia, by Experiment  157  E f f e c t of turbidity on the foraging rate (prey in 1.0 minutes) of juvenile chinook salmon f o r Artemia prey, 1987 (vertical bars - standard e r r o r ; n = 8 fish per mean).  67.6*4.3 mm FL  29  SO  100  200  Turbidity (mg/L)  400  800  APPENDIX 2. Figure A7.  Feeding Trials f o r Artemia, by Experiment  158  E f f e c t of turbidity on the foraging rate (prey in 1.0 minutes) of juvenile chinook salmon f o r Artemia prey, 1988 (vertical bars - standard e r r o r ; n = 8 fish per mean).  n  1  '  •  •  •  1  1  63.8*3.1 mm FL  Turbidity (mg/L)  APPENDIX 2. Figure A8.  Feeding Trials f o r Artemia, by Experiment  159  E f f e c t of A. Light and B. Turbidity on the foraging rate (prey in 1.0 minutes) of juvenile chinook salmon f o r Artemia prey (vertical bars - standard e r r o r ; n = 8 fish per mean).  APPENDIX 2. Figure A9.  Feeding Trials f o r Artemia, by Experiment  160  E f f e c t of turbidity on the foraging rate of juvenile chinook salmon f o r A. Surface Artemia (prey in 10.0 minutes) and B. Planktonic Artemia (prey in 1.0 minutes) (vertical bars - standard e r r o r ; n = 8 fish per mean).  APPENDIX 2. Figure A10.  pi  I 0  1 61  Feeding Trials f o r Artemia, by Experiment  E f f e c t of turbidity on the foraging rate (prey in 1.0 minutes) of juvenile chinook salmon f o r Artemia prey in A. "Normal" and B. "Enhanced" risk (vertical bars - standard e r r o r ; n = 8 fish per mean).  I 28  1  BO  I TOO  I 200  Turbidity (mg/L)  I  400  I 800  ol  I 0  I 28  I 60  I 100  I 200  Turbidity (mg/L)  I 400  I 800  APPENDIX 3. Figure All.  162  Feeding Trials f o r Tubifex, by Experiment  E f f e c t of turbidity on the foraging rate (mg prey in 5.0 minutes) of juvenile chinook salmon f o r Tubifex prey, 1987 (vertical bars - standard e r r o r ; n = 8 fish per mean).  0  28  SO  100  200  Turbidity (mg/L) 66.0*3.0 mm FL  Turbidity (mg/L)  800  400  800  APPENDIX 3. Figure A12.  Feeding Trials f o r Tubifex, by Experiment  163  E f f e c t of turbidity on the foraging rate (mg prey in 5.0 minutes) of juvenile chinook salmon f o r Tubifex prey, 1988 (vertical bars - standard e r r o r ; n = 8 fish per mean).  1  1  1  1  64.3*2.4 mm FL  Turbidity (mg/L)  APPENDIX 3. Figure A13.  Feeding Trials f o r Tubifex, by Experiment  164  E f f e c t of A. Light and B. Turbidity on the foraging rate (mg prey in 5.0 minutes) of juvenile chinook salmon f o r Tubifex prey (vertical bars - standard e r r o r ; n = 8 fish per mean).  APPENDIX 3. Figure A14.  Feeding Trials f o r Tubifex, by Experiment  165  E f f e c t of turbidity on the foraging rate (mg prey in 5.0 minutes) of juvenile chinook salmon f o r Tubifex prey in A. "Normal" and B. "Enhanced" risk (vertical bars - standard e r r o r ; n = 8 fish per mean).  APPENDIX 4.  166  Godin.T.I. and R.S.Gregory (in prep.)  Godin.T.I. and R.S.Gregory, (in prep.). Reaction times o f chinook salmon f r y (Oncorhynchus tshawytscha) to prey in turbid water. Abstract Suspended sediment lowers the visibility of scattering increase  light  the  also scatter  signals in the  visibility  of  prey.  prey  foreground.  to foraging fish by  Turbidity can also act  Particulates  in the  water  to  column may  light in a manner which creates uniform background  illumination, increasing prey  contrast.  A multichambered  experimental  arena allowing independent manipulation of background and foreground turbidities (0-400 mg*L ) _1  chinook salmon f r y  was used to determine the reaction times of  (Oncorhynchus tshawytscha)  Artemia prey over a fixed distance. in the experiments.  to variously  contrasted  Six conditioned subjects were used  Reaction times were 20-40/ f a s t e r with darkened  prey as compared with light prey and 25-37/. f a s t e r f o r prey against turbid as compared to non-turbid backgrounds.  With uniform foreground  and background suspended sediment levels, no significant differences in reaction times were found among conditions ranging from clear to moderately  turbid (<100 mg'L ).  turbid waters, reaction  times  -1  the  latter  within  the  Given the  reduced visual range in  observation suggests the possibility of reduced  visual  field.  faster  APPENDIX 4. Figure  A15.  Godin,T.I. and R.S.Gregory (in prep.)  167  E f f e c t of A. Prey colour, B. Background turbidity, and C. Both foreground and background turbidity, on the reaction time of juvenile chinook salmon f o r Artemia prey (means of individual fish medians; vertical bars are standard deviations; data from Godin and Gregory in prep.).  

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