Open Collections

UBC Theses and Dissertations

UBC Theses Logo

UBC Theses and Dissertations

An analysis of prey detection in cutthroat trout (Salmo clarki clarki) and Dolly Varden charr (Salvelinus… Henderson, Michael Andrew 1982

Your browser doesn't seem to have a PDF viewer, please download the PDF to view this item.

Notice for Google Chrome users:
If you are having trouble viewing or searching the PDF with Google Chrome, please download it here instead.

Item Metadata

Download

Media
831-UBC_1982_A1 H47.pdf [ 7.35MB ]
Metadata
JSON: 831-1.0094968.json
JSON-LD: 831-1.0094968-ld.json
RDF/XML (Pretty): 831-1.0094968-rdf.xml
RDF/JSON: 831-1.0094968-rdf.json
Turtle: 831-1.0094968-turtle.txt
N-Triples: 831-1.0094968-rdf-ntriples.txt
Original Record: 831-1.0094968-source.json
Full Text
831-1.0094968-fulltext.txt
Citation
831-1.0094968.ris

Full Text

AN ANALYSIS OF PREY DETECTION IN CUTTHROAT TROUT (SALMO CLARKI CLARKI) AND DOLLY VARDEN CHARR (SALVELINUS MALMA) by MICHAEL ANDREW HENDERSON B.Sc, University of Western Ontario, 1974 M.Sc, University of Manitoba, 1977 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 th i s thesis as conforming to the required standard THE UNIVERSITY OF BRITISH COLUMBIA July 1982 (c) Michael Andrew Henderson, 1982 In presenting t h i s thesis i n p a r t i a l f u l f i l m e n t of the requirements for an advanced degree at the University of B r i t i s h Columbia, I agree that the Library s h a l l make i t f r e e l y available for reference and study. I further agree that permission for extensive copying of t h i s thesis for scholarly purposes may be granted by the head of my department or by his or her representatives. I t i s understood that copying or publication of t h i s thesis for f i n a n c i a l gain s h a l l not be allowed without my written permission. Department of dLoo/e^tj  The University of B r i t i s h Columbia 1956 Main Mall Vancouver, Canada V6T 1Y3 DE-6 (3/81) i i ABSTRACT Laboratory feeding experiments showed that sympatric Dolly Varden charr (Salvelinus malma) were able to locate and consume prey targets at lower irradiance l e v e l s than sympatric cutthroat trout (Salmo c l a r k i c l a r k i ) but their acuity was poorer. Reaction distance (RD) of both species to a r t i f i c i a l and natural prey targets increased as irradiance l e v e l increased from a visual irradiance threshold (VIT), an irradiance l e v e l below which prey targets were not detected v i s u a l l y (3.G x 101 * photons n r 2 s" 1 for charr and 3.0 x 10 1 5 photons n r 2 s" 1 for trout) to a saturation irradiance l e v e l (SIL) which produced the maximum RD (3.0 x 10 1 6 photons n r 2 s" 1 for charr and 6.6 x 10 1 8 photons n r 2 s~ 1 for tro u t ) . The VIT and SIL were independent of prey type and prey c h a r a c t e r i s t i c s in both species. At a l l irradiance levels greater than the VIT of trout, the RD of trout exceeded that of charr for the same prey type. At a given irradiance level the largest RD in both species occurred in the presence of red irradiance followed in decreasing order by green, yellow and blue irradiance. Reaction distance of trout and charr increased with increases in prey size, movement and contrast. The percent increase in RD was greatest in trout. Between the VIT and the SIL the percent increase in RD was greater at higher irradiance levels in both species. At or above the SIL the percent increase in RD was constant. The central portion of retinas of trout and charr from sympatric and a l l o p a t r i c populations were examined by l i g h t microscopy. The two trout populations had a similar density of cone c e l l s and higher than either charr population. Sympatric charr had the lowest cone c e l l density and a l l o p a t r i c charr intermediate density. Rod c e l l density showed the opposite trend, being highest in sympatric charr, lowest in sympatric and a l l o p a t r i c trout and intermediate in a l l o p a t r i c charr. The cone c e l l mosaic, consisting of a regular array of double and single cones, was the same in a l l four populations. Both cone types were smallest in the two trout populations, largest in the sympatric charr population and intermediate in a l l o p a t r i c charr. The degree of r e t i n a l summation was greatest in sympatric charr, least in the trout populations and intermediate in a l l o p a t r i c charr. In summary, h i s t o l o g i c a l studies indicated that sympatric and a l l o p a t r i c trout possessed the highest l e v e l of v i s u a l acuity while sympatric charr were the most sensitive to low irradiance conditions. Foraging velocity of sympatric trout and charr increased as irradiance increased reaching a maximum at the SIL of each species. From foraging v e l o c i t y , RD and information on the d i e l irradiance regime in Loon Lake I estimated the volume of water searched v i s u a l l y for two natural prey types by trout and charr on a mid-summer day. Below the VIT, only charr were able to locate and consume buried prey targets, presumably by employing their chemosensory system. Differences in v i s u a l and non-visual feeding behaviour in sympatric trout and charr and in r e t i n a l structures of sympatric iv and a l l o p a t r i c trout and charr are generally as expected based on f i e l d studies of their v e r t i c a l d i s t r i b u t i o n and feeding habits. V TABLE OF CONTENTS ABSTRACT i i LIST OF TABLES v i i LIST OF FIGURES x LIST OF PLATES x i i i ACKNOWLEDGEMENTS xiv 1.0 Introduction 1 2.0 MATERIALS AND METHODS 9 2.1 Laboratory Studies 9 2.1.1 Visual Feeding Experiments 9 2.1.2 Foraging Velocity 20 2.1.3 Non-Visual Foraging Behaviour 20 2.2 Irradiance Levels in Loon Lake 22 2.3 Eye Histology 22 3.0 Results 24 3.1 General Feeding Behaviour 24 3.2 Effect of Experience on Reaction Distance 25 3.3 Effect of Food Deprivation and Daily Food Ration on Reaction Distance 28 3.4 Effect of Temperature on Reaction Distance 30 3.5 Effect of Fish Size on Reaction Distance 33 3.6 Effect of Infrared Irradiance on Reaction Distance . 33 3.7 Effect of Irradiance Characteristics on Reaction Distance 36 3.7.1 Irradiance Level 36 v i 3.7.2 Irradiance Quality 39 3.8 Effect of Prey Characteristics on Reaction Distance 42 3.8.1 Prey Size 42 3.8.2 Prey Movement 46 3.8.3 Prey Contrast 51 3.9 Reaction Distance to Natural Prey 54 3.10 Retinal Histology 66 3.10.1 Rod and Cone C e l l Density 72 3.10.2 Cone C e l l Size 74 3.10.3 Degree of Summation 77 3.10.4 Cone C e l l Mosaic 79 3.10.5 Feeding Implications 81 3.11 Effect of Irradiance Level on Foraging Velocity ... 84 3.12 Di e l Variation of Irradiance in Loon Lake 88 3.13 A Model of Visual Prey Searching Potential 94 3.14 Non-Visual Foraging Behaviour 98 4.0 Discussion 101 4.1 Sensory Behaviour in Trout and Charr 101 4.1.1 Visual 101 4.1.1.1 Characteristics of the Irradiance 106 4.1.1.2 Characteristics of the Prey 115 4.1.2 Chemical 120 4.2 Retinal Structure in Trout and Charr 124 4.3 General 132 5.0 References 138 LIST OF TABLES Table 1. Effe c t of food deprivation on mean reaction distance (cm ± 95% CL) of cutthroat trout and Dolly Varden charr to 3 mm a r t i f i c i a l prey targets at an irradiance l e v e l of 4.0 x 10 1 9 photons nr 2 s" 1 29 Table 2. Effe c t of dai l y food ration on mean reaction distance (cm ± 95% CL) of cutthroat trout and Dolly Varden charr to 3 mm a r t i f i c i a l prey target at an irradiance l e v e l of 4.0 x 10 1 9 photons n r 2 s" 1 31 Table 3. Ef f e c t of water temperature on mean reaction distance (cm ± 95% CL) of cutthroat trout and Dolly Varden charr to 3 mm a r t i f i c i a l prey targets at an irradiance l e v e l of 4.0 x 10 1 9 photons n r 2 s~ 1 32 Table 4. Effe c t of t o t a l body length on mean reaction distance (cm ± 95% CL) of cutthroat trout and Dolly Varden charr to 3 mm a r t i f i c i a l prey targets at an irradiance l e v e l of 4.0 x 10 1 9 photons n r 2 s" 1 34 Table 5. Effect of the presence (P) or absence (A) of infrared irradiance on mean reaction distance (cm ± 95% CL) of cutthroat trout and Dolly Varden charr to 3 mm a r t i f i c i a l prey targets. In the presence and absence of infrared irradiance the Vita-Light irradiance l e v e l was 4.2 x 10 1 7 and 3.0 x 10 1 5 photons irr 2 s _ 1 for the trout and charr, respectively 35 Table 6. Effe c t of a r t i f i c i a l prey target size on the v i i i maximum reaction distance (cm) of cutthroat trout and Dolly Varden charr 47 Table 7. Maximum reaction distance (cm) of cutthroat trout and Dolly Varden charr to 1.4-1.6 mm Daphnia rosea and Diaptomus kenai 60 Table 8. Linear regression equations for reaction distance (RD; cm) of cutthroat trout and Dolly Varden charr to various sizes (X; mm) of Daphnia rosea and Diaptomus  kenai at an irradiance l e v e l of 4.0 x 10 1 9 photons m~2 s 1 64 Table 9. Effect of movement of natural prey targets on mean reaction distance (cm ± 95% CL) of cutthroat trout and Dolly Varden charr at an irradiance level of 4.0 x 10 1 9 photons n r 2 s" 1. Moving (M) and stationary (S) Daphnia  rosea and Diaptomus kenai were 1.4 - 1.6 mm in length (N ~ = 1 00) 65 Table 10. Effect of contrast of natural prey targets on mean reaction distance (cm ± 95% CL) of cutthroat trout and Dolly Varden charr at an irradiance l e v e l of 4.0 x 10 1 9 photons n r 2 s" 1. High (H) and low (L) contrast Daphnia rosea and Diaptomus kenai were 1.4 - 1.6 mm in length (N = 100) 67 Table 11. A comparison of the density (± 95% CL) of cone and rod c e l l s in the retinas of sympatric and a l l o p a t r i c of cutthroat trout and Dolly Varden charr (N = 100). ... 73 Table 12. A comparison of cross-sectional cone c e l l size (± 95% CL) at the outer segment e l l i p s o i d l e v e l in the ix retinas of sympatric and a l l o p a t r i c populations of cutthroat trout and Dolly Varden charr (N = 100) 78 Table 13. A comparison of the density of nuclei per c e l l type (± 95% CL) and rates of summation (photoreceptor: bipolar: ganglion c e l l s ) in the retinas of sympatric and a l l o p a t r i c populations of cutthroat trout and Dolly Varden charr (N = 100) 80 Table 14. A q u a l i t a t i v e comparison of behavioural and h i s t o l o g i c a l estimates of v i s u a l acuity and visu a l s e n s i t i v i t y under low irradiance conditions in sympatric and a l l o p a t r i c populations of cutthroat trout and Dolly Varden charr 83 Table 15. Number of strikes and number of buried a r t i f i c i a l prey targets captured (± 95% CL) in s t i l l and moving water by Dolly Varden charr at an irradiance l e v e l less than 6.1 x 101 * photons n r 2 s - 1 (N = 100) 99 X LIST OF FIGURES Figure 1. A contour map of Loon Lake showing the irradiance sampling station. Depths in meters 10 Figure 2. Relative photon d i s t r i b u t i o n over the wavelength spectrum of Vita-Light 13 Figure 3. Relative photon d i s t r i b u t i o n over the wavelength spectrum of Vita-Light passed through blue, green, yellow and red f i l t e r s 15 Figure 4. Effect of experience on the reaction distance of five cutthroat trout and five Dolly Varden charr to 3 mm a r t i f i c i a l prey targets at an irradiance l e v e l of 4.0 x 10 1 9 photons n r 2 s" 1. Each datum point represents the mean of 50 observations. V e r t i c a l l i n e s indicate the range 26 Figure 5. Effect of the quantity of irradiance on the mean reaction distance (± 95% CL) of cutthroat trout and Dolly Varden charr to 1, 3 and 5 mm a r t i f i c i a l prey targets. Sample size per datum point equals 100. 37 Figure 6. Effect of irradiance quality on the mean reaction distance (± 95% CL) of cutthroat trout and Dolly Varden charr to 3 mm a r t i f i c i a l prey targets. The irradiance l e v e l was 1.03 x 10 1 9 photons n r 2 s" 1. Sample size per datum point equals 100 40 Figure 7. Effect of the size of a r t i f i c i a l prey targets on the mean reaction distance (± 95% CL) of cutthroat trout x i and Dolly Varden charr. The irradiance l e v e l used for each curve i s spec i f i e d in photons n r 2 s _ 1 . Sample size per datum point equals 100 43 Figure 8. Effect of movement of 3 mm a r t i f i c i a l prey targets on the mean reaction distance (± 95% CL) of cutthroat trout and Dolly Varden charr at d i f f e r e n t lev e l s of irradiance. Sample size per datum point equals 100 48 Figure 9. Effect of inherent contrast of 3 mm a r t i f i c i a l prey targets on the mean reaction distance (± 95% CL) of cutthroat trout and Dolly Varden charr at di f f e r e n t levels of irradiance. Sample size per datum point equals 100 52 Figure 10. Mean reaction distance (± 95% CL) of cutthroat trout and Dolly Varden charr to Daphnia rosea and Diaptomus kenai 1.4 to 1.6 mm in length at di f f e r e n t irradiance l e v e l s . Sample size per datum point equals 100 56 Figure 11. Effect of the size of Daphnia rosea and Diaptomus kenai on the mean reaction distance (± 95% CL) of cutthroat trout and t Dolly Varden charr at an irradiance l e v e l of 4.0 x 10 1 9 photons n r 2 s - 1 . Sample size per datum point equals 100 61 Figure 12. Swimming v e l o c i t y (cm nr 1 ± 95% CL) of cutthroat trout and Dolly Varden charr while foraging on 3 mm a r t i f i c i a l prey targets at d i f f e r e n t irradiance l e v e l s . 85 Figure 13. Depth-time isopleths of irradiance levels x i i (photons n r 2 s~ 1) in Loon Lake on July 8-9 and July 28-29, 1980 89 Figure 14. The relationship between irradiance l e v e l (photons n r 2 s~ 1) in Loon Lake on July 8-9, 1980 and vi s u a l s e n s i t i v i t y of cutthroat trout and Dolly Varden charr. The upper lin e for each species i d e n t i f i e s the depth at which the irradiance l e v e l i s just s u f f i c i e n t to maximize reaction distance. The lower l i n e marks the depth where the irradiance levels match the vis u a l irradiance threshold. See text for d e t a i l s 92 Figure 15. Volume of water searched by cutthroat trout and Dolly Varden charr for Daphnia rosea and Diaptomus kenai during that portion of the 24 h period on July 8-9, 1980 when the irradiance l e v e l was s u f f i c i e n t to maximize reaction distance and foraging v e l o c i t y . See text for d e t a i l s 96 xi i i LIST OF PLATES Plate 1. Transverse section of the retina of cutthroat trout. 1 visu a l c e l l layer (containing e p i t h e l i a l pigment), 2 external l i m i t i n g membraine, 3 external nuclear layer, 4 external plexiform layer, 5 internal nuclear layer, 6 internal plexiform layer, 7 ganglion c e l l layer, 8 nerve f i b r e layer. X 330 68 Plate 2. Transverse section through the visu a l c e l l layer of the retina of cutthroat trout. C cone, R rod. X 500. 70 Plate 3. Tangential section through the visual c e l l layer of the retina of cutthroat trout. S-single cone c e l l , D-double cone c e l l . X 500 75 xiv ACKNOWLEDGEMENTS I express thanks to my supervisor and friend Dr.' T.G. Northcote for his support and encouragement during the course of th i s study. His comments on e a r l i e r drafts of the manuscript are greatly appreciated. I wish also to thank Drs. M.C. Healey, W. E. N e i l l , J.D. McPhail and C.J. Walters who served on my supervisory committee and made many helpful comments. I am espec i a l l y grateful to Dr. M.A. A l i and his associates at the University of Montreal for their guidance and patience in teaching me the science of histology. Thanks are also given to L. Berg and P. Withler for their assistance in the laboratory and f i e l d . A very special thank you goes to my wife, Debbie, who while busy with her own graduate work always found time to keep my s p i r i t s up, and to our daughter Lindsay who -waited for us to f in i sh. F i n a l l y , I wish to thank no one in pa r t i c u l a r but everyone in general at the Institute of Animal Resource Ecology for providing a very stimulating environment in which to work. 1 1 .0 INTRODUCTION The d i v e r s i t y of food organisms consumed by f i s h i s greater than that for any other group of vertebrates (Nikolsky 1963). Generally the dietary habits of f i s h are c l a s s i f i e d in terms of the major prey types they consume (Hyatt 1979). This has resulted in the i d e n t i f i c a t i o n of four broad groups— herbivores, feeding on phytoplankton and other plant material; d e t r i t i v o r e s , feeding on decaying organic material; carnivores, feeding on benthic invertebrates, zooplankton, t e r r e s t r i a l insects and other vertebrates; and omnivores, feeding on both plant and animal material. While grouping f i s h into these food type categories is a way of bring some order to their vast array of foraging behaviours, i t provides l i t t l e insight into the environment-specific adaptations of these animals that determine their patterns of food a c q u i s i t i o n . The f i r s t step in any predatory sequence i s the detection of prey (Holling 1966). To detect a prey the sensory c a p a b i l i t i e s of a predator must be responsive to the stimuli generated by the prey. In high irradiance environments most f i s h appear to rely on their v i s u a l sensory system for locating prey. Studies on d i e l feeding p e r i o d i c i t i e s show that in many species food i s passed into the gut only during the day (Woodhead 1966, Blaxter 1970). Laboratory studies involving the measurement of feeding rates ( A l i 1959) and the reaction distance to prey (Vinyard and O'Brien 1976) under a range of irradiance conditions, as well as the manipulation of models with d i f f e r e n t v i s u a l c h a r a c t e r i s t i c s (Saxena 1966) i l l u s t r a t e the importance 2 of the v i s u a l system for prey detection in f i s h . While the basic plan of the eye in a l l f i s h is the same, there are a number of st r u c t u r a l adaptations which enhance the s e n s i t i v i t y of species l i v i n g in low irradiance environments. These include tubular shaped eyes (Marshall 1979), the presence of a r e t i n a l tapetum ( A l i and A n c t i l 1977), a high degree of r e t i n a l summation (Walls 1942) and a high density of long rod c e l l s (Lockett 1977). By comparing the eye structure of species from d i f f e r e n t photic environments i t appears that during the course of evolution there has been an interplay of competing selective pressures, resulting in a compromise between various alternative advantages. In the case of f i s h l i v i n g in low irradiance environments, changes in r e t i n a l structure which increase s e n s i t i v i t y also result in lower acuity. Many f i s h l i v e in rocky crevices, on muddy bottoms, in s i l t y r i v e r s and estuaries or in very deep water. In such low irradiance environments other sensory modalities have become important for prey location, most notably the chemical senses. The most extreme example is found in the numerous species of cave f i s h in which the eye has almost disappeared and which rely on chemical cues for locating prey (Walls 1942). Lagodon  rhomboides (Carr et a l . 1976) and Ictalurus spp. (Atema 1971) can orientate precisely to food items by following chemical s t i m u l i . Exploratory behaviour in sharks (Tester 1963), salmon (McBride et a l . 1962) and cod (Brawn 1969) increases in the presence of the appropriate vertebrate or invertebrate extracts. In a few species of f i s h e l e c t r i c a l and mechanical stimuli 3 are also used for locating prey. Scyliorhinus sp. and Raja  clavata can locate their prey, Pleuronectes platessa, solely on the basis of e l e c t r i c a l stimuli generated by the prey (Kalmijn 1971). Other types of f i s h , p a r t i c u l a r l y sharks, can detect prey using sound stimuli (Nelson and Gruber 1963, Banner 1972). Considerable comparative information exists on the form and function of sensory systems in f i s h with major differences in their phylogenetic background and s p a t i a l d i s t r i b u t i o n . Yet, l i t t l e i s known about how sensory systems have evolved in closely related or ec o l o g i c a l l y similar species which occur in sympatry. This is a p a r t i c u l a r l y important consideration in studies on resource partioning between animals. These studies are based on Gause's p r i n c i p l e that two species cannot co-exist i n d e f i n i t e l y on the same l i m i t i n g resource (Harden 1960). While numerous studies have revealed ecological and behavioural differences between seemingly similar sympatric species (e.g. Hartley 1953, Betts 1955, MacArthur 1958, Glova 1978), no attempt has been made to look for differences in the sensory capacities of these same animals. Throughout northern temperate regions there are numerous examples of salmonid species l i v i n g in sympatry and showing spa t i a l and dietary segregation (Newman 1956, Kalleberg 1958, Hartman 1965, Everhart and Waters 1965, Nilsson 1967, Hume 1978). Cutthroat trout ( Salmo c l a r k i c l a r k i ; hereafter referred to as trout) and Dolly Varden charr ( Salvelinus malma; hereafter referred to as charr) commonly occur together in coastal B r i t i s h Columbia lakes (Andrusak and Northcote 1970). 4 When sympatric these f i s h are s p a t i a l l y segregated during the spring and summer. The trout are found in the surface waters and feed primarily on zooplankton and surface, insects. The charr are found in deeper waters and feed on benthic organisms and to a lesser extent zooplankton. Zooplankton i s the only prey resource common in the diet of both f i s h although i t forms a larger portion of the diet of trout (48 to 78%) than of charr (13 to 54%; Armitage 1973). In a l l o p a t r i c situations both f i s h occupy the entire water column and feed on a wide range of benthic, planktonic and surface organisms (Andrusak and Northcote 1971). In a series of laboratory experiments examining the feeding behaviour of sympatric trout and charr, Schutz and Northcote (1972) found that trout captured a greater number of surface prey per unit searching time than did charr. When presented with exposed benthic prey, the rate of prey capture was greater in the charr. Unlike charr, trout were unable to locate buried benthic prey. Although both species showed a decrease in rate of prey capture with decreasing irradiance l e v e l s , the effect was much more pronounced in trout. Differences in the sp a t i a l d i s t r i b u t i o n and feeding behaviour of sympatric trout and charr are c l e a r l y demonstrated. While these differences may reduce dir e c t competition for food resources, l i t t l e i s known about the processes involved in prey detection, p a r t i c u l a r l y how the sensory systems of these two species have evolved to allow them to forage in their respective environments. Without this type of information, i t is d i f f i c u l t to understand and predict the nature of food acquisition in 5 cohabiting species. The objective of this study i s to determine whether there are any differences in the visu a l and chemoreceptive a b i l i t i e s of sympatric trout and charr that are related to observed differences in their s p a t i a l d i s t r i b u t i o n and d i e t . The hypotheses to be tested are as follows: (i) At high irradiance le v e l s , the distance at which prey targets can f i r s t be detected v i s u a l l y i s greater in sympatric trout than in sympatric charr. ( i i ) The minimum irradiance level required for visu a l prey detection is lower in sympatric charr than in sympatric trout. ( i i i ) Changes in the quality of irradiance have the same effect on the distance at which prey targets are f i r s t detected v i s u a l l y in sympatric trout and charr. (iv) At high irradiance l e v e l s , an increase in the size, movement or contrast of prey targets results in a greater increase in the distance at which these targets are f i r s t detected v i s u a l l y in sympatric trout than in sympatric charr. If tests of hypotheses one through three reveal any differences 6 in the v i s u a l a b i l i t i e s of sympatric trout and charr, the retina of these two species w i l l be examined to test the hypothesis: (v) There are differences in r e t i n a l structure of sympatric trout and charr that can explain differences in their v i s u a l reaction to prey targets and that are related to differences in their s p a t i a l d i s t r i b u t i o n . As well, the retinas of a l l o p a t r i c trout and charr w i l l be examined to test the hypothesis: (vi) There are differences in r e t i n a l structure between sympatric and a l l o p a t r i c trout and sympatric and a l l o p a t r i c charr that that are related to observed differences in their s p a t i a l d i s t r i b u t i o n . If differences exist in the v i s u a l a b i l i t i e s of trout and charr, the next step w i l l be to determine the potential volume of water searched per day by each species for d i f f e r e n t prey types. The hypothesis to be tested i s : ( v i i ) There i s no difference in the volume of water searched v i s u a l l y per day by sympatric trout and charr for prey. 7 A test of t h i s hypothesis w i l l require information obtained from the tests of hypotheses one through three, as well as information on the d i e l irradiance levels in Loon Lake and the v i s u a l foraging v e l o c i t y of trout and charr. The hypotheses to be tested are as follows: ( v i i i ) There i s no difference in the number of hours per day that sympatric trout and charr can forage v i s u a l l y . (ix) There is no difference in the visual foraging v e l o c i t y of sympatric trout and charr. The potential importance of the chemoreceptive system for prey detection in sympatric trout and charr w i l l be evaluated by testing the hypothesis: (x) Sympatric trout and charr do not use their chemoreceptive system for locating prey targets. If hypothesis ix is rejected, the following hypothesis w i l l be tested: (xi) The use of the chemoreceptive system for locating prey targets in sympatric trout and charr i s not 8 controlled by the ambient irradiance l e v e l . Tests of the above hypotheses w i l l be used to evaluate the effectiveness of the v i s u a l and chemoreceptive systems of sympatric trout and charr for locating prey in re l a t i o n to the environment in which these f i s h l i v e . 9 2.0 MATERIALS AND METHODS Trout and charr used in behavioural experiments were obtained from Loon Lake, located in the U. B. C. Research Forest, B r i t i s h Columbia (Fig. 1). Most f i s h were caught with trap nets in the early spring. Occasionally additional animals were coll e c t e d with g i l l nets in the summer and f a l l . After being transported to the University of B r i t i s h Columbia the animals were held outside in 1300 L fibreglass tanks. Water temperature varied between 7.6 and 12.1° C over the year. 2.J_ Laboratory Studies 2_.J_.J_ Visual Feeding Experiments Experiments in which f i s h used their visual system to locate prey targets were defined as vis u a l feeding experiments. In these experiments measurements of the reaction distance of the f i s h , the maximum distance between the f i s h and the prey target when the target was f i r s t sighted, were made. A sequence of observable, repeatable behaviours exhibited by the f i s h when a prey target was sighted (see section 3.1) were used to determine the position of the f i s h in these experiments. A l l behavioural observations were made from a Plexiglass tank 300 * 20 * 30 cm. The tank was painted f l a t white except for one s t r i p along the length of one side which was used as a port for observing the f i s h . The unpainted section was covered with a one-way mirror. The radiation source was provided by fluorescent Vita-Light tubes suspended 50 cm above the surface 1. A contour map of Loon Lake showing the irradiance sampling station. Depths in meters. 12 of the water. The tubes were encased in an irradiance-proof box where the amount and quality of irradiance could be regulated with a diaphram and f i l t e r s . Observations at low irradiance levels were made using an infrared irradiance source and viewer. A flow-through system replaced the water in the tank approximately once every 27 minutes. The spectral emission properties of the Vita-Light irradiance source used in thi s study are shown in Fig . 2. Peak emissions occurred at 450 nm, dropping off rapidly as the wavelength decreased and slowly as the wavelength increased from th i s point. The amount of irradiance emitted at 350 and 725 nm re l a t i v e to the amount of irradiance emitted at 450 nm was 25 and 81% respectively. The spectral d i s t r i b u t i o n of the Vita-Light source was similar to that of natural l i g h t on the earth's surface at mid-day (Young 1974). The l i n e voltage of the irradiance source was held constant to ensure the spectral d i s t r i b u t i o n did not change. Spectral transmission c h a r a c t e r i s t i c s of the f i l t e r s used to manipulate irradiance quality are shown in Fig . 3. The wavelength of maximum transmission was 420, 530, 590 and 640 nm in the blue, green, yellow and red f i l t e r s , respectively. Although the t o t a l wavelength range over which transmission occurred was variable among the f i l t e r s , i t was always less than 200 nm. Measurements of irradiance le v e l s were made with a Li-Cor quantum meter (model 185-A) and an attached underwater quantum sensor. Measurements were made 0.2 cm above the water surface. 2. Relative photon d i s t r i b u t i o n over the wavelength spectrum of Vita-Light. RELATIVE PHOTON N U M B E R o o o p o o p o o o 3. Relative photon d i s t r i b u t i o n over the wavelength spectrum of Vita-Light passed through blue, green, yellow and red f i l t e r s . 400 500 600 700 400 500 600 700 WAVELENGTH (nm) 17 The spectral composition of Vita-Light and Vita-Light passed through various coloured f i l t e r s was measured 0.2 cm above the water surface using an International Light spectroradiometer (model 700). Three types of prey, one a r t i f i c a l and two natural, were used in the vis u a l feeding experiments. Cylinders of chicken l i v e r 1 mm in diameter and 1,3 or 5 mm long were used as the a r t i f i c a l prey. Daphnia rosea and Diaptomus kenai , obtained from Loon Lake using a 183 m mesh tow net, were the natural prey. Measurements of Daphnia rosea and Diaptomus kenai were made as in Northcote and Clarotto (1975). The length of Daphnia  rosea was defined as the distance between the anterior end of the head and the base of the spine. For Diaptomus kenai , the metasome and urosome (excluding caudal rami) was measured. A l l prey were introduced to the observation tank at a distance beyond which the f i s h could detect them v i s u a l l y through tubes extending above the tank at one end and 1 cm below the water surface at the other end. The tubes were located at six positions along the length of the tank. The tube used for introduction of prey was randomized between successive t r i a l s . In a l l experiments, except those used to examine the effects of prey motion on reaction distance (see below), the prey targets came to rest on the bottom of the tank. If a f i s h sighted a target before i t came to rest, the reaction distance was not recorded. The position of prey targets and f i s h when they f i r s t detected the targets was determined from a scale located along the back of the tank. 18 The effect of motion of a r t i f i c a l prey targets on the a b i l i t y of trout and charr to detect them was examined by pinning the prey on a small v e r t i c a l l y moving platform. The 70 cm2 clear Plexiglass platform moved at a rate of 5 mm s" 1. Preliminary tests indicated that the f i s h would not respond to the moving platform in the absence of food. Motion in the natural prey, Daphnia rosea and Diaptomus kenai , was stopped by placing the animals in 30° C water for 3 minutes prior to the start of an experiment. The e f f e c t of prey contrast on reaction distance of trout and charr was examined by a l t e r i n g the inherent contrast of prey targets. The inherent contrast of a target (C ) is equal to the difference in the amount of irradiance reflected by the target (L) r e l a t i v e to the background (B)(le Grand 1967). Therefore: Two levels of inherent contrast of a r t i f i c a l prey were used. Low contrast l i v e r targets (C = 0.12) were produced by soaking the l i v e r in water for 24-h. This produced a white coloured target. Unsoaked l i v e r targets, reddish-brown in colour, were used for the high contrast prey (C = 0.75). It was assumed that any differences in the amount or type of chemical stimuli released by fresh and water soaked l i v e r targets had no effect on the reaction distance of trout or charr. The degree of contrast of Daphnia rosea and Diaptomus kenai, although not measured quantitatively, was increased by immersing them b r i e f l y in a 19 saturated solution of Sudan Black B (water insoluable s t a i n ) . Preliminary ' experiments indicated that changing the contrast of a r t i f i c a l and natural prey targets did not affect their p a l a t i b i l i t y to the f i s h . A l l animals used in visual feeding experiments were maintained in the observation tank for a minimum of one week prior to the start of an experiment. During th i s period, they were given d a i l y allotments of fresh l i v e r in excess of the amount they would consume. The quantity and quality of irradiance was set at the same le v e l to be used in the following experiment. In a l l cases, the animals were placed on a 16-h light-8-h dark irradiance regime except during the 24-h period preceding an experiment when irradiance was continuous. During the i n i t i a l transfer of a f i s h from the holding to the observation tank, the water temperature in each was the same. Subsequently, water temperature in the observation tank was changed at a maximum rate of 1° C per day u n t i l the desired experimental temperature was achieved. In a l l visu a l feeding experiments at least five trout and five charr were used. These animals ranged in size from 18.1 to 24.3 cm except in experiments designed to examine the effects of f i s h size on reaction distance. In the l a t t e r set of experiments f i s h size ranged from 10.7 to 23.2 cm. Unless otherwise noted, each datum point represents the mean of 100 repl i c a t e s . The number of replicates per f i s h ranged from 14 to 20. 20 2.J_.2 Foraging Velocity Foraging velocity of trout and charr was measured in the same observation tank used for the vis u a l feeding experiments. At the start of each experiment an a r t i f i c a l prey target was introduced into the tank and th i s was repeated at one minute intervals u n t i l the experiment was terminated. This rate of addition proved s u f f i c i e n t to maintain the searching behaviour of the f i s h . Foraging velocity experiments were conducted under six irradiance levels between 6.1 x 101 * and 4.0 x 10 1 9 photons m~2 s" 1. The distance traversed by each f i s h during a 10-minute period was recorded. Ten f i s h , ranging in size from 18.6 to 20.1 cm, of each species were used at each irradiance l e v e l . The feeding, irradiance and temperature history of f i s h used in foraging v e l o c i t y experiments was i d e n t i c a l to that described e a r l i e r for vis u a l feeding experiments. 2.\_.3 Non-Visual Foraging Behaviour This experiment was designed to determine i f trout or charr could locate a r t i f i c a l prey targets in s t i l l water at sub-visual irradiance l e v e l s . The bottom of the observation tank was marked in a grid of 1 cm squares and then covered to a depth of 2 cm with gravel. Stone sizes of the gravel varied from 0.20 to 0.55 cm. Ten fresh 3 mm l i v e r prey targets were placed underneath the gravel on randomly selected squares while a f i s h was held at one end of the tank by a removable opaque p a r t i t i o n . The start of 21 each experiment was marked by the removal of the p a r t i t i o n . During the next ten minutes the number of prey targets located and consumed by the f i s h was recorded. It was assumed that a target was located when the f i s h began snapping at and moving the gravel immediately above the target. At the end of each experiment the observation tank was drained and the tank and gravel washed to remove any odours associated with the l i v e r . In a second set of experiments the s t i l l water in the observation tank was replaced by turbulent moving water. A l l other conditions were as in the previous experiment. Water motion was created by placing two water pumps at either end of the tank and three at equidistant points along i t s length. The pumps, including intake and outlet, were completely submerged. Each pump moved 7.3 L of water per minute. The pumps were turned on 10 min prior to the start of an experiment which was marked by the removal of the p a r t i t i o n restraining the f i s h and they were l e f t on for the duration of the experiment. The pumps did not create any noise or vibration which could be detected by the observer nor any apparent e f f e c t s on the foraging behaviour of the f i s h . In a t h i r d set of experiments the pumps were removed and the l i v e r targets were placed in sealed transparent glass cy l i n d e r s . Again a l l other conditions were as described in the f i r s t experiment. A l l non-visual foraging experiments were carried out at sub-visual irradiance l e v e l s , using 10 trout and 10 charr. 22 2.2 Irradiance Levels in Loon Lake Die l changes in the irradiance levels in Loon Lake were measured at station 1 (Fig. 1) on July 8-9 and July 28-29, 1981 at 1-h i n t e r v a l s . Irradiance levels were recorded at 1 m interva l s in the upper 40 m of the water column using the Li-Cor quantum meter described e a r l i e r . Percent cloud cover and water surface conditions were recorded at the same time irradiance measurements were made. 2.3 Eye Histology Sympatric trout (19.2 - 20.8 cm) and charr (19.7 - 21.4 cm) used in h i s t o l o g i c a l studies were collected from Loon Lake. A l l o p a t r i c trout (18.0 - 19.6 cm) and charr (18.5 - 20.7 cm) were obtained from Placid and Dickson Lake respectively (Andrusak 1968). Ten animals of each species were collected from each lake and transported a l i v e to the University of B r i t i s h Columbia where they were held at 10° C on a 16-h li g h t 8-h dark irradiance regime for seven days. At the end of one week each animal was beheaded while in a lights-adapted state and the right eye removed. The cornea and lens of each eye was removed and the whole eye cup was fixed in Bouin's for 48-h. The eye cup was then transfered to 70% ethanol and held for further processing. Prior to embedding, a 1 mm section of material lying at the intersection of the dorsal-ventral and temporal-nasal axes of the eye cup was removed and dehydrated. This tissue, containing the retina, was then embedded in Spurr's medium. One-half m 23 transverse and tangential sections were cut on a Reichert OM U3 ultramicrotome. Sections, were stained in methylene blue. Quantitative evaluation of the retina was accomplished with a micrometer f i t t e d to the ocular of a compound microscope. Ten counts of the densities of rod, cone, bipolar and ganglia c e l l s were taken from tangential sections ( A l i and A n c t i l 1976) of each eye. Measurements of the diameter of single cones, and the longest and shortest axes of e l l i p t i c a l l y shaped double cones were made in the region of the e l l i p s o i d outer segments. Ten cones of each type were measured in each retina. Comparison of reaction distance, foraging v e l o c i t y and non-visual foraging behaviour in sympatric trout and charr and r e t i n a l histology in sympatric and a l l o p a t r i c trout and charr were made by analysis of variance. 24 3.0 RESULTS _3.J_ General Feeding Behaviour Trout and charr did not immediately begin feeding when brought into the laboratory. This latent period, although variable among animals, was generally greater for trout than charr. The mean number of days to f i r s t feeding ± 95% confidence l i m i t s of 20 animals of each species was 12 ± 2.1 and 6 ± 1.8 days for trout and charr, respectively. When the animals began to feed i t was obvious they were using their v i s u a l system to locate prey targets. Each attack was preceded by the f i s h orientating to and v i s u a l l y f i x i n g on the prey target. At the same time the forward movement of the animal stopped and the pectoral f i n s flared out. These events, which occurred over approximately 0.5 s, were used to identi f y the position of the f i s h when the target apparently f i r s t became v i s i b l e to i t . The distance between this position and the prey target was used to define reaction distance. Similar behaviours have been associated with the f i r s t sighting of prey targets in Salvelinus namaycush (Kettle and O'Brien 1978, Confer et a l . 1978), Salvelinus f o n t i n a l i s (Confer et a l . 1978), Lepomis  gibbosus (Confer and Blades 1975) and Lepomi s macrochi rus (Werner and Hall 1974, Vinyard and O'Brien 1976) and used to define reaction distance of these species. Following the sighting of an a r t i f i c i a l prey target the f i s h would move rapidly towards i t . On the f i r s t series of approaches the f i s h would not touch or consume the prey. After 25 two •to three days of t h i s type of behaviour the f i s h began to consume the targets but in most cases they were immediately expelled. It was only after prey targets had been present continuously for five to seven days that the f i s h would consume and retain them. Trout and charr moved back and forth along the length of the observation chamber while searching for prey targets resting on the bottom. Occasionally the f i s h , p a r t i c u l a r l y charr, would str i k e at non-prey targets such as small stones and twigs. Often these targets were consumed and rejected several times before the f i s h resumed i t s searching behaviour. While the behaviour of the f i s h at the time of attack indicated targets were being located v i s u a l l y , the consumption and rejection of a single non-prey target several times suggested that other types of sensory stimuli were used in making the decision of whether or not to retain the item. 3.2 Ef fect of Experience on React ion Di stance The reaction distance of trout and charr was recorded for 18 days after they passed through the latent phase and began to consume and retain prey targets. I n i t i a l l y , reaction distance was short in both species but increased to a maximum with increasing previous feeding experience (Fig. 4). Trout attained a maximum reaction distance to prey targets approximately 12 days after the i n i t i a t i o n of feeding. The response of charr was more rapid, reaching their maximum in six days. The range in estimates of reaction distance in both species decreased when 4. Effect of experience on the reaction distance of fi v e cutthroat trout and five Dolly Varden charr to 3 mm a r t i f i c i a l prey targets at an irradiance l e v e l of 4.0 x 10 1 9 photons m~2 s"'. Each datum point represents the mean of 50 observations. V e r t i c a l lines indicate the range. 27 90 80 60 E O 40 LU O IZ < c o O 20 r 0 40 • I i , i I i • • I • • i I i | T i • CUTTHROAT TROUT O < LU cr 30 20 1 0 • I T I T ? ' ' * '* • I I • DOLLY VARDEN CHARR o i o 15 DAYS A F T E R FIRST FEEDINGS 28 they reached their maximum reaction distance. While both trout and charr attained a maximum reaction distance within the 18-day feeding experiment, the absolute values were di f f e r e n t (Fig. 4). The maximum reaction distance for trout feeding on 3 mm prey targets at an irradiance l e v e l of 4.0 x 10 1 9 photons nr 2 s~ 1 was approximately 85 cm. The corresponding value for charr was 35 cm. A l l f i s h used in subsequent experiments had a minimum of 15 days feeding experience. Capture success, a measure of the percent of prey targets captured and consumed on the f i r s t s t r i k e , was monitored in trout and charr during the i n i t i a l 18 days of feeding. There was no s i g n i f i c a n t change (P < .05) in capture success in either species over t h i s period. Capture success was greater in trout than charr averaging 97 and 82% respectively over the duration of the experiment. 3.3 Ef fect of Food Depr ivat ion and Daily Food Rat ion on React ion Di stance The reaction distance of trout and charr to a r t i f i c i a l prey targets was recorded after periods of food deprivation ranging from 0 to 96 h (Table 1). There was no s i g n i f i c a n t difference (P < .05) in reaction distance of either species to 3 mm prey targets at an irradiance l e v e l of 4.0 x 10 1 9 photons n r 2 s" 1 after food was withheld for di f f e r e n t periods of time up to 96 hours. The e f f e c t of the dail y food ration for trout and charr on 29 Table 1. Effect of food deprivation on mean reaction distance (cm ± 95% CL) of cutthroat trout and Dolly Varden charr to 3 mm a r t i f i c i a l prey targets at an i r -radiance l e v e l of 4.0 x 10 1 9 photons n r 2 s" 1. Number of hours of food deprivation Species 0 24 48 72 96 Trout 82.6± 1.6 83.2± 1.2 82.5± 2.4 82.9± 1.8 83.1± 1.7 Charr 34.8± 1.8 33.9± 1.4 33.7± 2.0 34.6± 2.0 34.6± 1.6 30 their reaction distance to a r t i f i c i a l prey targets was examined (Table 2). Ration lev e l s of 1, 3 and 5% of f i s h wet weight were tested. The f i s h were maintained on each ration l e v e l for seven days prior to the start of an experiment. There was no s i g n i f i c a n t difference (P < .05) in the reaction distance of trout or charr at the d i f f e r e n t ration levels tested. While ration l e v e l s and periods of food deprivation had no effect on the reaction distance of trout or charr, reaction distance was greater (P < .05) in trout as described e a r l i e r . 3.4 Ef fect of Temperature on Reaction Di stance Sympatric populations of trout and ^charr are s p a t i a l l y segregated during the summer (Andrusak and Northcote 1971, Hume 1978). During this period the trout are concentrated in the' middle and upper portions of the water column while the benthic orientated charr are found in deeper water. The presence of a thermocline in Loon Lake at approximately 8 m (Northcote and Clarotto 1974) indicates that these species are l i v i n g in environments of dif f e r e n t temperature. Because of the potential importance of temperature dependent v i s u a l a b i l i t i e s in trout and charr, experiments were carri e d out to determine the reaction distance of both species at 5, 10, 15 and 20° C (Table 3), a range in temperatures commonly encountered in Loon Lake. Fish used in this study were acclimated to the experimental water temperature for a period of seven days prior to the start of the experiment. Neither species showed any s i g n i f i c a n t change (P < .05) in reaction distance to 31 Table 2. Effect of d a i l y food ration on mean reaction distance (cm ± 95% CL) of cutthroat trout and Dolly Varden charr to 3 mm a r t i f i c i a l prey target at an irradiance l e v e l of 4.0 x 10 1 9 photons m~2 s" 1. Daily food ration as a percent of f i s h wet weight Species 1 3 5 Trout 84.0 ± 2.2 83.4 ± 2.0 84.1 ± 1.2 Charr 33.7 ± 2.0 34.3 ± 1.9 33.9 ± 1.5 32 Table 3. Effect of water temperature on mean reaction distance (cm ± 95% CL) of cutthroat trout and Dolly Varden charr to 3 mm a r t i f i c i a l prey targets at an i r r a -diance l e v e l of 4.0 x 10 1 9 photons n r 2 s" 1. Spec ies Water temperature (°C) 10 15 20 Trout 84.0 ± 1.1 83.4 ± 1.8 83.9 ± 1.5 83.1 ± 1.7 Charr 34.2 ± 1.8 34.2 ± 1.5 33.6 ± 2.1 34.7 ± 1.4 33 3 mm prey targets at the diff e r e n t water temperatures. 3.5 Ef fect of Fish Size on React ion Distance Trout and charr, ranging in size from 10.7 to 23.2 cm (t o t a l length) were examined to determine i f there were any size dependent changes in visual a b i l i t i e s (Table 4). Over the size-range examined there was no s i g n i f i c a n t change (P < .05) in reaction distance to 3 mm a r t i f i c a l prey targets in either f i s h . The p o s s i b i l i t y exists that the visual system of smaller (younger) animals is less e f f e c t i v e although this was not tested. 3.6 E f f e c t of Infrared Irradiance on React ion Distance Observation of trout and charr at irradiance levels below the s e n s i t i v i t y of the human eye required another method of surveillance. An infrared irradiance source and viewer permitted observation at low irradiance levels but f i r s t i t was necessary to determine i f the f i s h were sensitive to the infrared irradiance. The reaction distance of trout and charr to a r t i f i c a l prey targets was measured at irradiance levels less than those required to produce a maximum reaction distance. Subsequently reaction distance was measured at the same irradiance level but with an infrared irradiance source added (Table 5). Neither species showed any s i g n i f i c a n t change (P > .05) in reaction distance in the presence of infrared i rradiance. 34 Table 4. Effe c t of t o t a l body length on mean reaction distance (cm ± 95% CL) of cutthroat trout and Dolly Varden charr to 3 mm a r t i f i c i a l prey targets at an i r r a -diance level of 4.0 x 10 1 9 photons n r 2 s" 1 . Body length (cm) Species 10.0-14.9 15.0-19.9 20.0-24.5 Trout Charr 83.7 ± 1.0 83.1 ± 1.3 84.4 ± 1.2 34.7 ± 1.2 33.211.9 34.011.7 35 Table 5. Effect of the presence (P) or absence (A) of infrared irradiance on mean reaction distance (cm ± 95% CL) of cutthroat trout and Dolly Varden charr to 3 mm a r t i -f i c i a l prey targets. In the presence and absence of infrared irradiance the Vita-Light irradiance l e v e l was 4.2 x 10 1 7 and 3.0 x 10 1 5 photons nr2 s~ 1 for the trout and charr, respectively. Trout Charr p A ' ~ P A 5 7 . 2 ± 2 . 3 57.4 ± 1.9 17.5 ± 1-7 17.1 ± 1 . 4 36 3 . 2 Effect of Irradiance Characteristics on React ion Di stance The rate at which a predator w i l l encounter prey depends on: 1) the prey density, 2) the r e l a t i v e velocity between the predator and the prey and 3) the distance at which the prey f i r s t becomes v i s i b l e to the predator (Holling 1966). The following experiments were designed to provide information on the effects of two c h a r a c t e r i s t i c s of irradiance, amount and quality, on the reaction distance of trout and charr. The preceding experiments were used to establish a "standard" experimental condition in which the effects of these variables could be assessed. 2 . 2 * 1 Irradiance Level The q u a l i t a t i v e nature of the relationship between reaction distance and irradiance level was similar in trout and charr (Fig. 5). In both species reaction distance increased with increasing irradiance from a v i s u a l irradiance threshold, the irradiance l e v e l below which prey targets were not detected v i s u a l l y , to a saturation irradiance l e v e l which produced the maximum reaction distance. Both the saturation irradiance l e v e l and visual irradiance threshold were species s p e c i f i c and independent of prey size within the precision of t h i s study. The saturation irradiance l e v e l for trout was approximately 6.6 x 10 1 8 photons nr 2 s" 1, more than two orders of magnitude greater than the corresponding value for charr (Fig. 5). Trout had a v i s u a l irradiance threshold of 3.0 x 10 1 5 photons n r 2 s~ 1, 5. Effect of the quantity of irradiance on the mean reaction distance (± 95% CL) of cutthroat trout and Dolly Varden charr to 1, 3 and 5 mm a r t i f i c i a l prey targets. Sample size per datum point equals 100. 39 while the similar value for charr was 3.0 x 101 * photons m~2 s" 1 . 3_.7.2 Irradiance Quality Changes in irradiance quality resulted in s i g n i f i c a n t differences (P < .05) in the reaction distance of trout and charr to 3 mm prey targets (Fig. 6). The largest reaction distance for trout, 58.1 cm, occurred in the presence of red irradiance. This was followed by reaction distances of 49.4, 33.0 ;and 27.1 cm with green, yellow and blue irradiance, respectively. Q u a l i t a t i v e l y , the eff e c t of irradiance quality on reaction distance in charr was the same as in trout with the largest reaction distance occurring in the presence of red irradiance . followed in decreasing order by green, yellow and blue irradiance (Fig. 6). While, the q u a l i t a t i v e response was the same, reaction distance of charr for each q u a l i t y of irradiance tested was approximately 30% of that found in trout. In both species reaction distance to prey targets in the presence of coloured irradiance was s i g n i f i c a n t l y less (P < .05) than reaction distance when the spectral composition of the Vita-Light irradiance source was unaltered (Fig. 5). 6. Effect of irradiance quality on the mean reaction distance (± 95% CL) of cutthroat trout and Dolly Varden charr to 3 mm a r t i f i c i a l prey targets. The irradiance l e v e l was 1.03 x 10 1 9 photons n r 2 s" 1. Sample size per datum point equals 100. f/ WAVELENGTH (nm) 42 3.8 Effect of Prey Characteristics on Reaction Distance 3.8.j_ Prey Size The previous experiments have shown that the quantity and quality of irradiance effects the visual, a b i l i t i e s of trout and charr when measured in terms of their reaction distance to prey targets. For both species, there was an irradiance l e v e l below which the vi s u a l system was not used for prey detection and another above which increases in the irradiance l e v e l resulted in l i t t l e increase in reaction distance. As well, the reaction distance of trout and charr changed under d i f f e r e n t q u a l i t i e s of i rradiance. While the quantity and quality of irradiance present in a visua l predators' environment w i l l a ffect i t s a b i l i t y to detect prey targets, so w i l l c h a r a c t e r i s t i c s of the targets themselves.. A target must subtend some c r i t i c a l angle of the predator's eye before i t w i l l be v i s i b l e (Ware 1971). Consequently, large targets can be seen at greater distances than small targets. The contrast and movement of a target also a f f e c t s the a b i l i t y of a predator to detect i t so that high contrast or moving targets are generally v i s i b l e at greater distances than low contrast or stationary targets (Ware 1971). In the following set of experiments, the effect of prey size, movement and contrast on the reaction distance of trout and charr was examined. Reaction distance increased with prey size in both trout and charr (Fig. 7). At saturation irradiance l e v e l s , 6.6 x 10 1 8 photons m"2 s~ 1 or greater for trout and 3.0 x 10 1 6 photons 7. Effect of the size of a r t i f i c i a l prey targets on the mean reaction distance (± 95% CL) of cutthroat trout and Dolly Varden charr. The irradiance l e v e l used for each curve is specified in photons nr 2 s" 1. Sample size per datum point equals 100. 45 n r 2 s" 1 or greater for charr, reaction distance for any prey size was maximal and did not show a s i g n i f i c a n t increase (P < 0.5) with increasing irradiance l e v e l . Consequently, these data were pooled. The increase in reaction distance with increasing prey size was not linear (Fig. 7). Trout showed a proportionally greater increase in reaction distance between prey 1 and 3 mm in size than they did between prey 3 and 5 mm in s i z e . This trend was reversed in charr, the largest increase in reaction distance occurring between prey 3 and 5 mm in size. The r e l a t i v e increase in the reaction distance of trout and charr to larger prey sizes decreased as the'amount of irradiance decreased below the saturation l e v e l (Fig. 7). At irradiance levels equal to or greater than 6\6 x 10 1 8 photons n r 2 s" 1 trout showed a 54.5% increase in reaction distance as prey size increased from 1 to 5 mm. At an irradiance level of 3.0 x 10 1 6 photons n r 2 s~ 1 the corresponding increase i n reaction distance was 36.3%. Charr showed a 50.2% increase in reaction distance as prey size increased from 1 to 5 mm at irradiance levels equal to or greater than 3.0 x 10 1 6 photons n r 2 s" 1 while at an irradiance l e v e l of 3.0 x 10 1 5 photons n r 2 s" 1 the corresponding increase in reaction distance was 24.9%. Estimates of the maximum reaction distance of trout and charr for each prey size at saturation irradiance levels were obtained using the Michaelis-Menton model: RD = (Rm)(L) (L ) + (L) 46 where RD = the reaction distance of a f i s h to a prey target (cm) Rm = the maximum reaction distance of a f i s h to a prey target (cm) L = the irradiance l e v e l of the experiment minus the irradiance level where the reaction distance equals zero (photons m-2 s- 1 ) L = the half saturation irradiance l e v e l minus the irradiance l e v e l where the reaction distance equals zero (photons n r 2 s~ 1) A non-linear least squares program was used to obtain estimates of the parameters Rm and L . For a l l prey sizes the estimated maximum reaction distance of trout was greater than that of charr by more than a factor of two (Table 6). 3 . 8 . 2 Prey Movement Trout reacted to moving prey targets from a s i g n i f i c a n t l y greater (P < .05) distance than stationary prey targets with the same visu a l properties at irradiance levels greater than 3.0 x 10 1 6 photons n r 2 s~ 1 (Fig. 8). At saturation irradiance l e v e l s , greater than or equal to 6.6 x 10 1 8 photons n r 2 s" 1, the effect of movement of the 3 mm prey targets was additive, increasing reaction distance by approximately 21 cm. This corresponded to an increase in reaction distance of 25.4% above that found for 47 Table 6. Effect of a r t i f i c i a l prey target size on the maximum reaction distance (cm) of cutthroat trout and Dolly Varden charr. Prey size (mm) Species 1 3 5 Trout Charr 57.9 25.5 80.4 33.0 89.9 43. 1 48 Fig. 8. Effect of movement of 3 mm a r t i f i c i a l prey targets on the mean reaction distance (± 95% CL) of cutthroat trout and Dolly Varden charr at d i f f e r e n t levels of irradiance. Sample size per datum point equals 100. 50 stationary prey targets. The increase in reaction distance at subsaturation irradiance levels was less pronounced. When moving prey targets were presented to trout at an irradiance l e v e l of 4.2 x 10 1 7 photons m"2 s~ 1 , reaction distance increased by 5.1 cm or 8.8% greater than that found for stationary targets. Although the mean reaction distance of trout to moving targets at an irradiance l e v e l of 3.0 x 10 1 6 photons m"2 s" 1 was greater than to stationary targets, these data were not s i g n i f i c a n t l y d i f f e r e n t (P > .05). Charr also reacted to moving prey targets at s i g n i f i c a n t l y greater (P < .05) distances than to stationary targets but the increase in reaction distance resulting from prey movement was less than that found in trout (Fig. 8). At saturation irradiance l e v e l s , greater than or equal to 4.2 x 10 1 7 photons n r 2 s" 1, the reaction distance of charr to stationary and moving prey targets was approximately 32 and 37 cm, respectively. This corresponded to a 16.7% increase in reaction distance as the result of prey movement. As found for trout, the effect of prey target movement on the reaction distance of charr decreased as the amount of irradiance decreased below the saturation l e v e l . At 3.0 x 10 1 5 photons n r 2 s" 1 the last irradiance level tested above the v i s u a l irradiance threshold of charr, there was no s i g n i f i c a n t difference (P > .05) in reaction distance to stationary and moving targets. The v i s u a l irradiance threshold of trout and charr was unaffected by movement of the prey targets. 51 3.8.3 Prey Contrast The response of trout and charr to changes in contrast of the prey targets (Fig. 9) was q u a l i t a t i v e l y similar to their response to changes in prey movement (Fig. 8). At irradiance levels greater than or equal to 3.0 x 10 1 6 photons n r 2 s* 1 trout reacted to high contrast (inherent contrast = 0.71) 3 mm prey targets at a s i g n i f i c a n t l y greater distance (P < .05) than they did to low contrast (inherent contrast = 0.20) prey targets. The reaction distance of trout to low contrast prey targets at saturation irradiance l e v e l s , greater than or equal to 6.6 x 10 1 8 photons n r 2 s" 1, was 52.8 cm while high contrast prey targets at the same irradiance l e v e l produced a reaction distance of 80.3 cm. The difference, 27.5 cm, corresponded to a 52.1% increase in reaction distance when high contrast prey targets were used. As the amount of irradiance decreased below the saturation l e v e l , the absolute and r e l a t i v e difference in reaction distance to a high and low contrast prey targets also declined. An irradiance level of 4.2 x 10 1 7 photons n r 2 s~ 1 resulted in a reaction distance of 47.9 and 57.1 cm for low and high contrast target, respectively. This corresponded to a 19.2% increase in reaction distance when high contrast targets were used in place of low contrast targets. There was no s i g n i f i c a n t difference (P > .05) in reaction distance to high and low contrast prey targets at an irradiance l e v e l of 3.0 x 10'6 photons nr 2 s" 1. Charr reacted to high contrast prey targets at a s i g n i f i c a n t l y greater distance (P < .05) than they did to low 9. Effect of inherent contrast of 3 mm a r t i f i c i a l prey targets on the mean reaction distance (± 95% CL) cutthroat trout and Dolly Varden charr at d i f f e r e n t levels of irradiance. Sample size per datum point equals TOO. 54 contrast targets at a l l irradiance levels greater than or equal to 3.0 x 10 1 6 photons n r 2 s" 1 (Fig. 9). While an increase in the contrast of the prey targets resulted in an increase in reaction distance, the absolute and r e l a t i v e change was less than that found in trout. At saturation irradiance l e v e l s , greater than or equal to 4.2 x 10 1 7 photons n r 2 s~ 1, the reaction distance of charr to low contrast prey targets was 26.1 cm. With high contrast prey targets at the same irradiance l e v e l reaction distance was 32.5 cm, a 24.5% increase. The difference in reaction distance to high and low contrast prey targets decreased as the amount of irradiance decreased below the saturation l e v e l . At 3.0 x 10'6 photons n r 2 s" 1 there was no s i g n i f i c a n t difference (P > .05) in reaction distance to high and low contrast prey targets. Differences in prey target contrast had no effect on the vi s u a l irradiance threshold of either species. 3.9 React ion Distance to Natural Prey The preceeding experiments indicated that the reaction distance of trout and charr to a r t i f i c a l prey targets was affected by the quantity and quality of irradiance and prey size, movement and contrast. The objective of the following work was to establish whether reaction distance to natural prey targets was similar to the response to a r t i f i c a l prey. Two zooplankters, the cladoceran Daphnia rosea and the copepod Diaptomus kenai were used. Both were common prey items of Loon Lake trout and charr in the spring and summer (Hume 1978). 55 The v i s u a l irradiance threshold for trout feeding on Daphnia and Diaptomus 1.4-1.6 mm in length was 3.0 x 10 1 5 photons n r 2 s" 1 (Fig. 10), the same le v e l found for trout feeding on 1 to 5 mm a r t i f i c i a l prey targets (Fig. 5). An increase in the irradiance l e v e l to 3.0 x 10 1 6 photons n r 2 s" 1 produced a reaction distance of 4.2 cm for trout feeding on Daphnia. The reaction distance of trout to Diaptomus at th i s irradiance l e v e l was not s i g n i f i c a n t l y d i f f e r e n t (P > 0.5) than that found for Daphnia. At irradiance levels greater than 3.0 x 10 1 6 photons n r 2 s~ 1, there was a s i g n i f i c a n t difference (P < .05) in the reaction distance of trout to the two zooplankters. The average reaction distance of trout to Daphnia at irradiance levels between 4.2 x 10 1 7 and 4.0 x 10 1 9 photons n r 2 s" 1 was 16.2 % greater than the corresponding reaction distance to Diaptomus. At the highest irradiance l e v e l used in this study, 4.0 x 10 1 9 photons n r 2 s" 1, the reaction distance of trout to Daphnia and Diaptomus was 23.8 and 21.3 cm, respect i v e l y . Charr showed an increase in reaction distance to both zooplankters as the irradiance l e v e l increased from 3.0 x 1 0 1 4 photons n r 2 s~ 1 , the vi s u a l irradiance threshold, to 3.0 x 10 1 6 photons n r 2 s _ 1 , the saturation irradiance l e v e l (Fig. 10). The v i s u a l irradiance threshold and saturation irradiance l e v e l for charr feeding on the zooplankters were the same as those established for charr feeding on a r t i f i c i a l prey targets (Fig. 5). While the change in reaction distance of charr to the two zooplankters was q u a l i t a t i v e l y similar to that of trout, 10. Mean reaction distance (± 95% CL) of cutthroat trout and Dolly Varden charr to Daphnia rosea and Diaptomus kenai 1.4 to 1.6 mm in length at d i f f e r e n t irradiance l e v e l s . Sample size per datum point equals 100. / 58 there were important differences in the magnitude of the response. The v i s u a l irradiance threshold of charr was 2.39 x 10 1 5 photons rrr 2 s" 1 lower than the corresponding value for trout. The difference in the saturation irradiance level between the two species was even greater, the saturation irradiance l e v e l for charr being 6.60 x 10 1 8 photons n r 2 s" 1 less than that found in trout. Differences in the reaction distance of trout and charr to the two zooplankters were also evident (Fig. 10). While both species reacted to Daphnia at a s i g n i f i c a n t l y greater distance (P < .05) than they did to Diaptomus at saturation irradiance l e v e l s , the reaction distance of trout to Daphnia was 1.9 times greater than that of charr. The difference in the reaction distance to Diaptomus was somewhat greater, the average reaction distance of trout to Diaptomus at saturation irradiance levels being 2.6 times greater than the corresponding value for charr. There was no s i g n i f i c a n t difference (P > .05) in the reaction distance of charr to the two zooplankters at an irradiance l e v e l of 3.0 x 10 1 5 photons n r 2 s" 1 The r e l a t i v e difference in reaction distance of trout and charr to the two zooplankters was not the same. At saturation irradiance levels the difference in reaction distance of trout to Daphnia and Diaptomus averaged 1.9 cm (Fig. 10). This corresponds to a reaction distance for Daphnia 9.0% greater than found for Diaptomus. At saturation irradiance levels the average difference in the reaction distance of charr to the two zooplankters was 4.1 cm or a reaction distance to Daphnia 47.8% 59 greater than found for Diaptomus. These data suggest that the reaction distance of trout is less sensitive than that of charr to the type of zooplankter encountered, at least when the comparison i s made between the species of cladocerans and copepods used in these experiments. Estimates of the maximum reaction distance of trout and charr to both zooplankters were obtained by f i t t i n g the data in Fig . 10 to the Michaelis-Menton model (Table 7). For both Daphnia and Diaptomus the maximum reaction distance of trout was approximately three times that found for charr. Both trout and charr showed an increase in reaction distance as the size of Daphn ia and Diaptomus increased (Fig. 11). With trout feeding on Daphnia and charr feeding on Daphnia or Diaptomus, the increase was l i n e a r . A s l i g h t departure from l i n e a r i t y occurred when trout were feeding on Diaptomus, reaction distance increasing more rapidly when the size of Diaptomus was increased from 1.25 to 1.75 mm than when i t was increased from 1.75 to 2.25 mm. While the change in reaction distance of trout and charr to a r t i f i c i a l prey targets of d i f f e r e n t sizes was not linear (Fig. 7), these data were not d i r e c t l y comparable to those derived using the natural prey targets due to differences in the range of sizes tested. A r t i f i c i a l prey targets were a l l 1 mm in diameter and 1, 3 or 5 mm long. The length of natural prey targets was r e s t r i c t e d to the i n t e r v a l betwen 0.75 and 2.25 mm. Regressions of reaction distance on prey size showed a s i g n i f i c a n t difference in slope (P < .05) between both species 60 Table 7. Maximum reaction distance (cm) of cutthroat trout and Dolly Varden charr to 1.4-1.6 mm Daphnia rosea and Diaptomus kenai. Species Daphnia rosea Diaptomus kenai Trout Charr 37. 1 12.7 28.6 8.8 11. Effect of the size of Daphnia rosea and Diaptomus  kenai on the mean reaction distance (±95% CL) of cutthroat trout and Dolly Varden charr at an irradiance level of 4.0 x 10 1 9 photons n r 2 s" 1. Sample size per datum point equals 100. 3 0 25 2 0 CUTTHROAT TROUT E o _ 15 UJ o 5 » r -00 r^phnia rosea Diaptomus kenai O _ < LU 18 or 15 DOLLY VARDEN CHARR 10 5 h 0 5 1.0 1.5 2.0 PREY SIZE ( mm ) 63 of f i s h and prey (Table 8). The rate of increase in reaction distance for trout and charr with increasing prey size was greatest where Daphnia were used as prey. For both prey types, the rate of increase in reaction distance was greater in trout than in charr. The reaction distance of trout and charr also was affected by the presence or absence of movement in the two prey species and their l e v e l of contrast with respect to the background. Both trout and charr reacted to moving zooplankters at a s i g n i f i c a n t l y greater distance (P < .05) than they did to stationary individuals although the response was more pronounced in trout (Table 9). The reaction distance of trout to 1.4-1.6 mm Daphnia at saturation irradiance levels increased from 13.7 cm for stationary animals to 23.8 cm for moving animals, a 73.7% increase in reaction distance. The corresponding increase in reaction distance of charr was 45.1%. The increase in reaction distance of trout to moving Diaptomus (Table 9) was greater than the increase found for moving Daphn i a , reaction distance to moving Diaptomus being 171.1% greater than to stationary individuals. The response of charr to moving Diaptomus was similar in magnitude to their response to Daphnia with reaction distance to moving Diaptomus 44.8% greater than was found for the stationary form. Q u a l i t a t i v e l y , the effect of prey movement on the reaction distance of trout and charr was the same for a r t i f i c i a l (Fig. 8) and natural prey types (Table 9) although quantitatively, the increase in reaction distance as the result of prey movement was greater (P < .05) when natural prey targets 64 Table 8 . Linear regression equations for reaction distance (RD; cm) of cutthroat trout and Dolly Varden charr to various sizes (X; mm) of Daphnia rosea and Diaptomus  kenai at an irradiance l e v e l of 4.0 x 10 1 9 photons m"2 s" 1 . Species Prey Equation r 2 Trout Daphnia rosea Diaptomus kenai Charr Daphnia rosea Diaptomus kenai RD = 8 .1 + 1 0 . 4 X 0 . 9 3 RD = 1 2 . 3 + 5 . 7 X 0 . 8 1 RD = 0 . 1 + 7 . 6 X 0 . 9 5 RD = - 0 . 2 + 5 . 0 X 0 . 9 1 65 Table 9. Effect of movement of natural prey targets on mean reaction distance (cm ± 95% CL) of cutthroat trout and Dolly Varden charr at an irradiance l e v e l of 4.0 x 10 1 9 photons nr2 s~ 1. Moving (M) and stationary (S) Daphnia  rosea and Diaptomus kenai were 1.4 - 1.6 mm in length (N = 100). Daphnia rosea Diaptomus kenai Spec ies M S M S Trout 23.8 ± 1.6 13.7 ± 1.8 23.1 ± 1.0 8.5 ± 1.8 Charr 11.9 ± 1.7 8.2 ± 1.0 8.4 ± 1.4 5.8 ± 1.1 66 were used. The response of trout and charr to an increase in the contrast of Daphnia was similar to their response to an increase in movement. Reaction distance of both species to high contrast 1.4-1.6 mm Daphnia was s i g n i f i c a n t l y greater (P < .05) than their reaction distance to low contrast forms at saturation irradiance levels (Table 1.0), reaction distance increasing 22.7 and 24.4% in trout and charr, respectively. While trout also reacted to high contrast Diaptomus at a s i g n i f i c a n t l y greater distance (P < .05) than they did to low contrast animals, there was no s i g n i f i c a n t difference (P > .05) in the reaction distance of charr to the two forms. 3. H) Retinal Histology Gross eye morphology in trout and charr resembles the ty p i c a l teleostean pattern (Walls 1942) and is v i r t u a l l y i d e n t i c a l to that found in Oncorhynchus (Al i 1961). A l l major ocular structures are present in both trout and charr and an examination of these structures at a magnification of 10X reveals l i t t l e difference between the two species. A more detailed comparison of one of these structures, the retina, is given below. The retinas of trout and charr are q u a l i t a t i v e l y similar and consist of several layers (Plate 1). The rods and cones (Plate 2), located in the visu a l c e l l layer, are connected to the second order neurones, the bipolar c e l l s , found in the internal nuclear layer. Ganglion dendrites make synaptic contact Table 10. Effect of contrast of natural prey targets on mean reaction distance (cm ± 95% CL) of cutthroat trout and Dolly Varden charr at an irradiance l e v e l of 4.0 x 10 1 9 photons n r 2 s" 1. High (H) and low (L) contrast Daphnia rosea and Diaptomus kenai were 1.4 - 1.6 mm in length (N = 100). Daphnia rosea Diaptomus kenai Spec ies H L H L Trout 29.2 ± 1.3 23.8 ± 1.6 24.9 ± 1.6 21.3 ± 1.0 Charr 14.8 ± 1.3 11.9 ± 1.5 9.7 ± 1.1 8.4 ± 1.4 68 Plate 1. Transverse section of the retina of cutthroat trout. 1 v i s u a l c e l l layer (containing e p i t h e l i a l pigment), 2 external l i m i t i n g membrane, 3 external nuclear layer, 4 external plexiform layer, 5 internal nuclear layer, 6 internal plexiform layer, 7 ganglion c e l l layer, 8 nerve fibre layer. X 330. 70 Plate 2. Transverse section through the vi s u a l c e l l layer of the retina of cutthroat trout. C cone, R rod. X 500. 72 with bipolar axons in the same layer while axons of the ganglia c e l l s converge to form the optic t r a c t . 3.j_0.j_ Rod and Cone C e l l Density Two types of visual c e l l s , rods and cones, commonly occur in the vertebrate retina (Walls 1942). Under high irradiance conditions, cone c e l l s are used to detect and transmit irradiant energy received by eye to the vi s u a l centers of the brain. Animals l i v i n g in environments with high levels of irradiance generally have a high density of cone c e l l s r e l a t i v e to animals l i v i n g in low irradiance environments (Walls 1942). Increases in cone c e l l density are often associated with increases in visu a l acuity and reductions in s e n s i t i v i t y to irradiance (Walls 1942). Rod c e l l s are responsible for detecting and transmitting irradiant information to the vi s u a l centers of the brain under low irradiance conditions (Walls 1942). High densities of rod c e l l s , common in animals l i v i n g in low irradiance environments (Bowmaker 1976) are associated with poor vis u a l acuity and a high degree of s e n s i t i v i t y to low irradiance conditions (Gruber 1977). The densities of vi s u a l c e l l s in the retinas of trout and charr were high, rods outnumbering cones by more than one order of magnitude (Table 11). Cone density in the retina of sympatric trout was higher (P < .05) than cone density in sympatric charr by a r a t i o of more than 2:1. While cone density in the population of sympatric trout was s l i g h t l y higher than the density found in a l l o p a t r i c trout, the difference was not 73 Table 11. A comparison of the density (± 95% CL) of cone and rod c e l l s in the retinas of sympatric and a l l o p a t r i c of cutthroat trout and Dolly Varden charr (N = 100). Density (.0024 mm"2) Cone Rod 21.2 ± 2.3 9.0 ± 1.8 280.3 ± 6.8 311.2 ± 7.2 20.4 ± 1.9 14.4 ± 1.7 283.3 ± 7.1 302.7 ± 6.4" Spec ies Sympatric (Loon Lake) Trout Charr Allopatr ic Trout (Placid Lake) Charr (Dickson Lake) 74 s t a t i s t i c a l l y s i g n i f i c a n t (P > .05). A comparison of cone density between a l l o p a t r i c and sympatric charr revealed a s i g n i f i c a n t difference (P < .05), the density of cones in the a l l o p a t r i c population being higher than found in the sympatric populat ion. Differences in rod density were evident among only two of the populations examined (Table 11). The density of rods in the retina of sympatric trout was s i g n i f i c a n t l y lower (P < .05) than the density found in sympatric charr, opposite the trend previously noted for cone density in these two populations. There was no s i g n i f i c a n t difference (P > .05) in rod density between populations of sympatric and a l l o p a t r i c trout or sympatric and a l l o p a t r i c charr. 3.JJD.2 Cone C e l l Size Visual acuity depends, in part, on the density of cones in the retina (Tamura & Wisby 1963). In general, animals with very acute vision are characterized by retinas with a high cone density, while animals with poor acuity have a lower cone density (Walls 1942). As the cross-sectional area of the cones w i l l determine the number that can occur in a unit area, cone size can be used as a measure of vis u a l acuity. Two types of cones were i d e n t i f i e d in the retinas of trout and charr. The more abundant double cones, e l l i p t i c a l in cross-section surrounded the c i r c u l a r shaped single cones (Plate 3). Measurements of the diameter of single.cones and length of the long and short axes of double cones were used to 75 Plate 3. Tangential section the retina of cutthroat D-double cone c e l l . X through the vis u a l c e l l layer trout. S-single cone c e l l , 500. i i r * r i *^ • » S 77 describe cone size. Differences in cone size existed among the four populations of f i s h examined. Single cones in sympatric trout were 40.0% smaller (P < .05) than single cones found in the retina of sympatric charr (Table 12). No s i g n i f i c a n t difference (P > .05) existed in the size of single cones in sympatric and a l l o p a t r i c trout. A comparison of the size of single cones between sympatric and a l l o p a t r i c charr showed a s i g n i f i c a n t difference (P < .05), cone size in sympatric charr being 22.2% greater than found in the a l l o p a t r i c population. Similar differences existed in the size of double cones among the four populations. Both axes of the double cones of sympatric trout were s i g n i f i c a n t l y shorter (P < .05) in length than the corresponding axes of the double cones found in sympatric charr (Table 12). As well, the axes of double cones in sympatric charr were s i g n i f i c a n t l y longer (P < .05) than those of a l l o p a t r i c charr. There was no s i g n i f i c a n t difference (P > .05) in the length of either axis between sympatric and a l l o p a t r i c trout populations. 3^ .j_0.3 Degree of Summation The number of v i s u a l c e l l s (rods and cones) that converge on one bipolar c e l l and the number of bipolar c e l l s that converge on one ganglion c e l l i s used to define the degree of summation ( A l i and Wagner 1980). As the degree of summation increases, an animal becomes more sensitive to irradiance but also experiences a decrease in visual acuity ( A l i and Wagner 1980). 78 Table 12. A comparison of cross-sectional cone c e l l size (± 95% CL) at the outer segment e l l i p s o i d l e v e l in the retinas of sympatric and a l l o p a t r i c populations of cutthroat trout and Dolly Varden charr (N = 100). Cone size (um) Single Double cone Species cone L S Sympatric (Loon Lake) Trout 5. 5 + 0. 1 15. 4 + 0. 3 8 .8 + 0. Charr 7. 7 + 0. 1 20. 9 + 0. 2 1 3 .2 + o.: Allopatr ic Trout (Placid Lake) 5. 4 + 0. 2 15. 4 + 0. 3 8 .9 + 0.: Charr (Dickson Lake) 6. 3 + 0. 1 17. 1 + 0. 2 10 .3 + 0. *L - long axis, S - short axis 79 The density of v i s u a l , bipolar and ganglion c e l l s in the retina of sympatric trout was s i g n i f i c a n t l y d i f f e r e n t (P < .05) from that of sympatric charr (Table 13). The resulting degree of summation was lower in sympatric trout which had 39.7 v i s u a l c e l l s for each ganglion c e l l compared to sympatric charr where the corresponding r a t i o was 78.1:1. There was no s i g n i f i c a n t difference (P > .05) in the density of any of the c e l l types in the sympatric and a l l o p a t r i c trout populations and summation rates were si m i l a r . Estimates of the v i s u a l , bipolar and ganglion c e l l densities were s i g n i f i c a n t l y d i f f e r e n t (P < .05) in the sympatric and a l l o p a t r i c charr population as was the degree of summation. The r a t i o of the number of vis u a l c e l l s to each ganglion c e l l in the sympatric charr population was 78.1:1, while a l l o p a t r i c charr had 51.9 v i s u a l c e l l s for each ganglion c e l l . 3.J_0.4 Cone C e l l Mosaic The d i s t r i b u t i o n of cone c e l l s in the retina when viewed through h i s t o l o g i c a l sections taken p a r a l l e l to the r e t i n a l surface are used to describe the cone c e l l mosaic (L y a l l 1957). In some animals the d i s t r i b u t i o n of cone c e l l s appears random, while in other animals these c e l l s are organized into highly d i s t i n c t groupings such as squares or lines (Engstrom 1963). Animals possessing a highly ordered cone c e l l mosaic usually l i v e in environments receiving large amounts of irradiance in contrast to animals l i v i n g in low irradiance environments where 80 Table 13. A comparison of the density of nuclei per c e l l type (± 95% CL) and rates of summation (photoreceptor: bipolar: ganglion c e l l s ) in the retinas of sympatric and a l l o p a t r i c populations of cutthroat trout and Dolly Varden charr (N = 100). Nuclei (.0024 mm'2) Spec ies Photo- Rate receptor Bipolar Ganglion of summation 301.5±5.1 125.9±4.2 320.214.9 91.514.0 Sympatr ic (Loon Lake) Trout Charr A l l o p a t r i c Trout 303.714.6 127.114.7 (Placid Lake) Charr 311.6±3.9 106.8±4.1 (Dickson Lake) 7.6±0.9 4.1±0.8 39.7:16.6:1.0 78.1:22.3:1.0 8.3±1.2 36.6:15.3: 1 .0 6.0±0.7 51.9:17.8:1.0 81 the cone c e l l s often have no i d e n t i f i a b l e pattern (Engstrom 1963). Increases in the degree of organization of the cone c e l l mosaic have been associated with better vis u a l acuity (Engstrom 1963) and movement perception ( L y a l l 1957, A n c t i l 1969, Bathelt 1970). Q u a l i t a t i v e l y , there was no difference in the cone c e l l mosaic among the four populations of f i s h examined. Tangential sections passing through the cone e l l i p s o i d s revealed a pattern of double cones arranged in squares around a central single cone in a l l f i s h examined (Plate 3). Although the mosaic was the same, the area occupied by one unit ( i . e . four double cones surrounding a single cone) was d i f f e r e n t when comparisons were made between some of the populations. One unit of the mosaic from the retina of sympatric trout was smaller in area (P < .05) than one unit in sympatric charr. There was no difference (P > .05) in the area of these units when sympatric and a l l o p a t r i c trout were compared. The unit area in sympatric charr was s i g n i f i c a n t l y greater (P < .05) than the corresponding area in a l l o p a t r i c charr. Differences in the area of one unit of the cone c e l l , mosaic among the four populations was the result of differences in cone c e l l size described above (Table 12). _3._1_0.5 Feeding Implications Three c h a r a c t e r i s t i c s of the retina examined in this study, rod and cone density (Table 11), cone size (Table 12) and degree of summation (Table 13) show differences between sympatric trout and charr while a fourth, the cone c e l l mosaic is the same. 8 2 Sympatric trout have a higher cone density, smaller cone size and lower degree of summation than found in sympatric charr. These differences suggest that sympatric trout possess better v i s u a l acuity than sympatric charr and that the v i s u a l system of sympatric charr is operative under lower irradiance conditions than that of sympatric trout. This supports the results obtained from the behavioural experiments described e a r l i e r (Table 14). Reaction distance is a measure of v i s u a l acuity, a longer reaction distance indicating better acuity. At saturation irradiance l e v e l s , sympatric trout reacted to both a r t i f i c i a l (Fig. 5) and natural prey targets (Fig. 10) at a greater distance than sympatric charr. Although reaction distance declined in both species as the amount of irradiance decreased below the saturation irradiance l e v e l , the v i s u a l irradiance threshold of trout was higher than that found for charr (Fig. 5). While no measurements of reaction distance were obtained for the a l l o p a t r i c populations of trout and charr, the close co r r e l a t i o n between r e t i n a l structure and feeding behaviour in the sympatric populations suggested i t was possible to make qu a l i t a t i v e comparisons of acuity and s e n s i t i v i t y to irradiance for the a l l o p a t r i c populations r e l a t i v e to their sympatric counterparts based on h i s t o l o g i c a l evidence alone (Table 14). There was no difference in any of the four r e t i n a l c h a r a c t e r i s t i c s examined between sympatric and a l l o p a t r i c trout. Consequently, the acuity and s e n s i t i v i t y of a l l o p a t r i c trout was assumed to be the same as that found in the sympatric 83 Table 14. A q u a l i t a t i v e comparison of behavioural and histo-l o g i c a l estimates of visu a l acuity and visu a l s e n s i t i v i t y under low irradiance conditions in sympatric and a l l o p a t r i c populations of cutthroat trout and Dolly Varden charr. Spec ies Acuity S e n s i t i v i t y Beha-vioural Histo-l o g i c a l Beha-viour a l Histo-l o g i c a l Sympatr ic (Loon Lake) Trout High High Poor Poor Charr Low Low Good Good A l l o p a t r i c Trout High Poor (Placid Lake) Charr Intermediate Intermediate (Dickson Lake) 84 population. Estimates of cone density (Table 11), cone size (Table 12) and degree of summation (Table 13) in a l l o p a t r i c charr were found to be intermediate between the same estimates obtained for sympatric trout and charr. This suggested that a l l o p a t r i c charr have better v i s u a l acuity and a higher v i s u a l irradiance threshold than sympatric charr but poorer acuity and a lower v i s u a l irradiance threshold than either trout populat ion. 3^. J_J_ Ef f ect of I rradiance Level on Foraging Veloc i t y The rate at which a visual predator w i l l encounter prey depends in part on the r e l a t i v e v e l o c i t y between the two. Although both species of f i s h used in this study as well as their zooplankton prey move, the r e l a t i v e distance covered by a zooplankter per unit time is so small that i t may be ignored. In the following set of experiments the foraging v e l o c i t i e s of trout and charr at diff e r e n t irradiance levels were measured. This information was used to calculate the r e l a t i v e volumes of water searched by trout and charr for diff e r e n t prey types (see section 3.8). Qu a l i t a t i v e l y , the relationship between foraging v e l o c i t y and irradiance l e v e l was similar in trout and charr (Fig. 12). In both species foraging velocity increased to a maximum with increases in the irradiance l e v e l . The amount of irradiance required to produce the maximum foraging velocity was 6.6 x 10 1 8 and 3.0 x 10 1 6 photons irr 2 s" 1 in trout and charr, respectively. These irradiance levels correspond to those producing the 12. Swimming velocity (cm irr 1 ± 95% CL) of cutthroat and Dolly Varden charr while foraging on 3 mm a r t i f i c i a l prey targets at d i f f e r e n t irradiance l e v e l s . V6 IRRADIANCE LEVEL (photons r i v s 1 ) 87 maximum reaction distance in these two species (Fig. 5). The lowest estimate of foraging v e l o c i t y in trout occurred at an irradiance l e v e l of 3.0 x 10 1 5 photons n r 2 s~ 1, while the irradiance l e v e l producing the minimum foraging velocity in charr was lower at 6.1 x 101 * photons m"2 s" 1. The lowest foraging v e l o c i t y in both species occurred at an irradiance l e v e l less than or equal to their visual irradiance threshold (Fig. 5). At irradiance levels greater than 4.2 x 10 1 7 photons m"2 s" 1 the foraging of v e l o c i t y trout was greater (P < .05) than that of charr (Fig. 12). At lower irradiance levels the estimates of foraging v e l o c i t y for charr exceeded (P. < .05) those for trout. Although both f i s h continued to show some movement at irradiance levels below their v i s u a l irradiance threshold, the associated behaviour was very d i f f e r e n t . The trout usually remained in one position, only occassionally showing brief periods of movement. They did not exhibit any foraging behaviour even in the presence of food. The charr, moving continuously, assumed their sub-visual searching behaviour (see section 3.8). 88 3.j_2 D i e l Variation of I r radiance in Loon Lake There were marked d i e l changes in irradiance at di f f e r e n t depths in Loon Lake (Fig. 13). The f i r s t set of d i e l measurements (July 8-9) were made on a cloudless day while the second set (July 28-29) were made in the presence of 100% cloud cover. Despite the differences in cloud cover the isopleths of irradiance over depth were similar on the two days, the only major difference occurring in the upper meter of the water column between 12:00 and 14:00 h, where the irradiance l e v e l on July 8-9 was approximately an order of magnitude greater than on July 28-29. While the amount of irradiance reaching the surface of a lake i s known to decrease with increasing cloud cover (Hutchinson 1957), these differences are small and d i f f i c u l t to detect in sub-surface waters due to the rapid attenuation of irradiance with depth. The precision of irradiance measurements made in Loon Lake were adequate for the purposes of thi s study. Irradiance levels over the upper 40 m of the water column ranged from 10 1" to 10 2 1 photons m"2 s" 1 (Fig. 13). Maximum values at any depth occurred between 13:00 and 15:00 h while the lowest measurements were made between 24:00 and 03:00 h. The maximum rate of change in irradiance occurred at dusk and dawn. No measurements of irradiance were made below 1.0 x 101 * photons nr 2 s" 1 . Die l change in the depth at which the irradiance l e v e l in Loon Lake was equal to the saturation irradiance l e v e l and the vis u a l irradiance threshold for trout and charr on July 8-9 (Fig. 12) are shown in F i g . 14. Estimates of saturation 13. Depth-time isopleths of irradiance l e v e l s (photons n r 2 s~ 1) in Loon Lake on July 8-9 and July 28-29, 1980. <?0 91 irradiance le v e l s and visual irradiance thresholds were obtained from the behavioural feeding experiments (Fig. 5). Irradiance levels required for visual saturation in trout were present in the water column of Loon Lake between 05:30 and 21:00 h (Fig. 13). The maximum depth at which this value occurred was 16.7 m at approximately 14:00 h. Irradiance levels equal to the visu a l irradiance threshold of trout exceeded 40 m between 09:00 and 18:00 h. Surface irradiance levels were below this threshold between 22:30 and 03:30 h. Su f f i c i e n t irradiance was present in at least part of the water column for saturation of the eye of charr between 04:00 and and 22:00 h (Fig. 14). This irradiance l e v e l exceeded 40 m during the 09:00 to 16:00 h period. Irradiance levels were always greater than the visual irradiance threshold of charr in some part of the water column. The minimum depth reached by this irradiance level was approximately 5.0 m between 24:00 and 03:00 h. These data show that there i s a considerable portion of the lower water column in midsummer where the irradiance l e v e l is s u f f i c i e n t to saturate the eye of charr but not trout. The difference between these levels exceeds 20 m between 07:00 and 20:00 h. While irradiance- levels are inadequate 'for the operation of the trout visual system during much of the night they never decline below the vi s u a l irradiance threshold of charr. 14. The relationship between irradiance l e v e l (photons n r 2 s~ 1) in Loon Lake on July 8-9, 1980 and vi s u a l s e n s i t i v i t y of cutthroat trout and Dolly Varden charr. The upper l i n e for each species i d e n t i f i e s the depth at which the irradiance l e v e l i s just s u f f i c i e n t to maximize reaction distance. The lower l i n e marks the depth where the irradiance l e v e l match the visu a l irradiance threshold. See text for d e t a i l s . 09:00 I2:00 I8:00 14:00 06^00 OSCH TIME (h) 94 3.j_3 A Model of Visual Prey Searching Potential The potential array of prey available to a predator i s ultimately limited by i t s prey detection a b i l i t i e s . Other components of the feeding process such as prey handling and learning behaviour of the predator (Beukema 1968) may a l t e r the nature of this array but only within the framework defined by the prey detection a b i l i t i e s of the predator. The number of prey detected by a v i s u a l f i s h predator i s a function of the volume of water searched and the prey density. The volume of water searched i s a product of the reaction distance of the predator and i t s foraging v e l o c i t y . In this section I have estimated the volume of water searched by trout and charr for various sizes of Daphnia rosea and Diaptomus kenai on a t y p i c a l mid-summer day. The model used i s of the form: VS ( x RD2 ) x D x T where VS volume of water searched (m3) RD maxium reaction distance to a prey (m) (see section 3.4) D distace moved by a predator while foraging (m) (see section 3.6) T number of hours per day that the irradiance l e v e l was s u f f i c i e n t to maximize both reaction distance and foraging velocity (h) (see sections 3.6 and 3.7) 95 Two assumptions of t h i s model are: 1) that while foraging the f i s h search out a c y l i n d r i c a l volume the radius of which equals the reaction distance of the f i s h to a given type of prey and 2) that foraging i s continuous but only when the irradiance l e v e l i s s u f f i c i e n t to maximize both reaction distance and foraging v e l o c i t y . For any size of either prey type, the volume of water searched per day by trout was greater than the volume searched by charr (Fig. 15). When averaged over a l l prey sizes and both prey types, trout searched a volume of water 378.7% greater than the corresponding volume searched by charr. Both trout and charr searched a larger volume of water per day for Daphnia than for Diaptomus of a similar s i z e . The volume of water searched by trout for 1.25 mm Daphnia was 195.8 m3, a volume 36.1% greater than was searched for 1.25 mm Diaptomus. For prey 1.75 mm in length, the volume of water searched by trout for Daphnia was 34.7% greater than the volume searched for Diaptomus. The difference in the volume of water searched per day for Daphnia and Diaptomus was greater in charr than trout. Charr searched a volume 137.0% greater for 1.25 mm Daphnia and 171.3% greater for 1.75 mm Daphnia than for Diaptomus of a similar s i z e . Both trout and charr showed an increase in the volume of water searched per day with increasing prey si z e . 15. Volume of water searched by cutthroat trout and Dolly Varden charr for Daphnia rosea and Diaptomus kenai during that portion of the 24 h period on July 8-9, 1980 when the irradiance l e v e l was s u f f i c i e n t to maximize reaction distance and foraging v e l o c i t y . See text for detaiIs. 77 2 8 0 r 0.7 1.0 "~ 1.5 2.0 2.5 P R E Y SIZE (mm) 98 2 * 1 1 Non-Visual Foraging Behaviour Trout and charr did not react v i s u a l l y to prey targets when the irradiance l e v e l was less than or equal to their v i s u a l irradiance threshold (Fig. 5). At these sub-visual irradiance levels trout remained almost stationary in mid-water in contrast to the charr which continued to move through the observation tank, occasionally capturing prey that had settled to the bottom. This indicated that charr were using a non-visual sensory system for locating prey at these low irradiance l e v e l s . The behaviour of charr at sub-visual irradiance levels was d i f f e r e n t than the behaviour shown when prey targets were located v i s u a l l y (section 3.1). The body of the animal was t i l t e d at a 45° angle r e l a t i v e to the bottom of the tank and i t s chin was close to but not touching the bottom. At the same time the head moved continually from side to side. The following set of experiments was designed to determine i f trout or charr could detect prey targets at irradiance levels below their v i s u a l irradiance threshold, presumably by use of chemoreception. During 10-minute feeding sessions charr located and consumed and average of 4.2 of the 10 buried l i v e r prey targets present (Table 15). When a prey target was located the charr stopped and usually moved backwards 2 to 3 cm. This was followed by the animal picking up a mouthful of gravel in the v i c i n i t y of the target. The gravel was immediately expelled from the mouth. If the target was present in t h i s material i t was retained and consumed. If i t was not, the charr would make two to three more strikes in the same location. If the target had s t i l l not been 99 Table 15. Number of strikes and number of buried a r t i f i c i a l prey targets captured (± 95% CL) in s t i l l and moving water by Dolly Varden charr at an irradiance l e v e l less than 6.1 x 101 * photons n r 2 s' 1 (N =100). Time Spent Water Prey Searching Condition Type (min) Strikes Captured S t i l l Liver 10 16.3 ± 5.1 4.2 ± 2.7 S t i l l Glass 10 0 0 Moving Liver 10 3.8 ± 1.4 1.1 ± 0.6 1 00 located the animal would move on, continuing to search in the manner described e a r l i e r . Charr did not make any strikes when the l i v e r targets were enclosed in glass cylinders (Table 15). Trout, in a similar series of experiments, did not respond to either l i v e r or glass prey targets. Success of the charr in capturing the l i v e r prey targets was based on whether the target was consumed following a s t r i k e . Charr averaged 16.3 strikes per 10 minute feeding session (Table 15). An average consumption rate of 4.2 targets over the same time interval resulted in a capture success of 25.8 %. The number of strikes made by charr on buried l i v e r targets in moving water was s i g n i f i c a n t l y d i f f e r e n t (P < .05) from th e i r response to the same targets in s t i l l water (Table 15). The average number of strikes per feeding session declined from 16.3 in s t i l l water to 3.8 in moving water. While the number of prey captured in moving water was s i g n i f i c a n t l y less (P < .05) than in s t i l l water, the capture success rate was si m i l a r . This indicated that moving water reduced the a b i l i t y of charr to locate the l i v e r prey targets, but once located had no effect on their a b i l i t y to capture the targets. 101 4.0 DISCUSSION 4.j_ Sensory Behaviour in Trout and Charr 4. K l Visual Prior to discussion of results from the vis u a l feeding experiments, a comment is required on two important aspects of the experimental design. The f i r s t concerns the use of a reflex response for identifying the location of a f i s h when a prey target is sighted. The second relates to measurements of radiation in quantum units rather than the more conventional photometric units. Many psycophysical methods involving both reflex responses and training have been used to study how animals perceive their surroundings (Northmore and Yager 1975). These methods, which have been used as ways of inducing an animal to report on the nature of i t s environment, are based on input-output relationships. In this study the visual stimulus was the input while the stereotyped response of the f i s h when a prey target was sighted was the output. This response was used to measure the fis h ' s power of visual perception. Reflex methods are very a t t r a c t i v e because the response of the animal does not wane over time. This i s not the case with other psycophysical methods (Blough and Yager 1972). Consequently, reflex responses have been used to study several irradiance dependent behaviours in f i s h . They have been used to test an hypothesis rel a t i n g to the s p a t i a l d i s t r i b u t i o n of 1 02 Stizostedion vitreum vitreum (Scherer 1975), to establish prey preference in Lepomis macrochirus (Vinyard and O'Brien 1976) and spectral s e n s i t i v i t y in Lepomi s qibbosus (Grundfest 1932), Carassius auratus (Cronly-Dillon and Muntz 1965) and Gasterosteus aculeatus (Cronly-Dillon and Sharma 1968). Blaxter (1964) measured the least amount of irradiance required by Clupea harengus for feeding, avoiding a barrier and phototaxis. Despite the apparent s i m p l i c i t y of the reflex method there are a number of considerations which must precede i t s use. F i r s t i t i s necessary that the response being measured be clear and e a s i l y observed. This is important because ultimately the accuracy of the reflex method is limited by the accuracy with which the experimenter can measure the response. The response of trout and charr to v i s u a l stimuli meets these c r i t e r i a . Secondly, i t is important to choose a response that varies in some predictable way with changes in the stimulus. The reaction distance of trout and charr proved to be a useful response for accessing their v i s u a l a b i l i t i e s with respect to the c h a r a c t e r i s t i c s of the irradiance and the prey. Ideally, the results obtained using a reflex response should be used to generate hypotheses which can be tested using di f f e r e n t methods. In this study, hypotheses related to r e t i n a l structure were developed and tested based on results from the behavioural experiments. Throughout this study measurements of irradiance were made in photons m"2 s" 1 between 400 and 700 nm. The choice of quantum units was based on the nature of photobiological processes. In 1 03 i t s interaction with matter radiation behaves as i f i t were a stream of p a r t i c l e s , known as photons. Each photon car r i e s a discrete amount of energy which is proportional to i t s frequency. If a photon comes in contact with an appropriate photosensitive material (e.g. a v i s u a l pigment) i t w i l l transfer i t s energy to one molecule of that material . If enough photons reach an irradiance receptor per unit time the receptor w i l l assume an e l e c t r o n i c a l l y excited state and convert the energy into neural signals. This threshold w i l l be determined by the quantum e f f i c i e n c y of the reaction. In photosynthesis i t has been calculated that for every molecule of oxygen liberated at least four photons are required (Ramsay 1966). In the human eye the minimum number of photons required for peripheral v i s i o n i s on the order of 800 s~ 1 at the cornea, corresponding to about 80 s" 1 absorbed by the rods (P-irenne 1956). These considerations suggest that photobiological processes"are more l i k e l y to be understood i f radiation i s expressed in terms of photon numbers. Unfortunately most measurements of irradiance r e l a t i n g to f i s h behaviour are made in photometric units. Photometric units are r e l a t i v e measures of the quantity of radiation based on the spectral s e n s i t i v i t y of the average human eye (Arnold 1974). The spectral s e n s i t i v i t y of any eye depends on the type of v i s u a l pigments i t contains. In a survey of the v i s u a l pigments of 518 teleost species ( A l i and Wagner 1975a) none had the same pigments as those found in the human eye. Consequently photometric measurements of irradiance measure neither the t o t a l amount of irradiance available nor the amount that can be 104 s e l e c t i v e l y absorbed by d i f f e r e n t organisms. Prior to the start of the main series of v i s u a l feeding experiments, i t was important to identify any c h a r a c t e r i s t i c s inherent in the experimental design, excluding c h a r a c t e r i s t i c s of the irradiance and the prey, which might aff e c t the v i s u a l perception of the f i s h and, consequently, their reaction distance to prey targets. Based on studies from the l i t e r a t u r e , two features, f i s h size and water temperature were of p a r t i c u l a r concern. In general, eye development appears to be incomplete in young f i s h . These f i s h are often characterized by an incomplete optic tectum (Sharma 1975), a lack of rods (Blaxter 1968,- 1969, Blaxter and Staines 1970), no retinomotor response ( A l i 1959, 1963, Blaxter and Jones 1967) and cone mosaics which are d i f f e r e n t from the adult form (Ahlbert 1975). When these differences are compared with vi s u a l behaviour, they correlate with higher irradiance thresholds (Blaxter 1969, 1975), reduced visu a l acuity (Blaxter 1975) and spectral s e n s i t i v i t i e s that are d i f f e r e n t from the adult (Blaxter 1967). The size of trout and charr, ranging from 10.0 to 23.4 cm, had no effect on their reaction distance to a r t i f i c a l prey targets (Table 4). As a result, i t was assumed that their eyes were f u l l y developed by this stage. This is in agreement with most developmental studies where the eye has been shown to reach i t s adult form by the end of the yolk sac or metamorphosis stage ( A l i and Wagner 1975b). While some visual responses in f i s h do change in older animals, for example bottom colour selection in 105 Salmo qairdneri changes at the age of 14 months, they are probably related to a physiological or ecological "urge to respond" rather than any change in vi s u a l perception (Kwain and MacCrimmon 1969). It has been known for some time that temperature can affect the vis u a l a b i l i t i e s of a poikiotherm (Denton and Pirenne 1954). One known temperature related response is the f l i c k e r fusion frequency. When a f l i c k e r i n g l i g h t stimulus i s presented to a f i s h , each flash e l i c i t s one response when measured as an electroretinogram. If the frequency of the flashes i s increased a l e v e l w i l l be reached where individual components of the electroretinogram fuse so that i t is impossible to relate the stimulus to the response. The frequency at which this occurs i s c a l l e d the f l i c k e r fusion frequency . It has been demonstrated that the f l i c k e r fusion frequency increases with increasing temperature in Carassius auratus (Hanyu and A l i 1963), Salmo  salar (Hanyu and A l i 1964), and Lepomis gibbosus ( A l i and Kobyashi 1967). The speed at which the r e t i n a l e p i t h e l i a l pigment and cones attain a light-adapted state is also temperature dependent, occurring faster at higher temperatures ( A l i 1975). Over a range of temperatures from 5 to 20° C the reaction distance of trout and charr to a r t i f i c a l prey targets did not change (Table 3). While these results cannot be used to test hypotheses related to the effects of temperature on the f l i c k e r fusion frequency or the rate at which an eye attains a light-adapted state, they do suggest that vi s u a l perception in 106 trout and charr, at least as i t is measured in this study, i s temperature independent. _4._1_._1_._1_ Characteristics of the I rradiance The v i s u a l system of an animal is only useful when i t receives s u f f i c i e n t information in the form of irradiance from the environment. Results of a laboratory study by Schutz and Northcote (1972) suggest that both trout and charr use their v i s u a l system for locating prey targets. Yet, at least during part of the year, charr inhabit a deep water environment which receives much less irradiance than the environment inhabited by shallow water trout (Andrusak and Northcote, 1971 ). Results from my study are used to test the hypotheses that the quantity of irradiance does not aff e c t the distance at which trout and charr can detect prey targets and that for any quantity of irradiance the distance at which trout and charr can f i r s t detect prey targets i s the same. Qua l i t a t i v e l y , the effect of the amount of irradiance on the reaction distance of trout and charr to a r t i f i c i a l (Fig. 5) and natural prey targets (Fig. 10) i s the same. In both species, reaction distance increases from a visual irradiance threshold below which prey targets are not detected v i s u a l l y to a saturation irradiance l e v e l above which increases in the amount of irradiance have l i t t l e effect on reaction distance. While the form of thi s relationship is the same in the two species, there are major differences in the magnitude and other c h a r a c t e r i s t i c s of the response. ' The visual irradiance threshold and the 107 saturation irradiance level for charr are approximately one and two orders of magnitude lower respectively than the corresponding values for trout. Also, at irradiance levels greater than 3.0 x 10 1 6 photons m~2 s" 1, the reaction distance of trout i s s i g n i f i c a n t l y greater (p<.05) than that of charr. The magnitude of the change in reaction distance under decreasing irradiance levels i l l u s t r a t e s the importance of this relationship when estimating f i s h feeding rates. If a f i s h is a cr u i s i n g predator, then a 50% decrease in reaction distance decreases the volume searched by a factor of four. If the f i s h i s an ambush predator, consequently searching a volume of water approximated by a hemisphere (O'Brien e_t a_l. 1976), the volume searched decreases by a factor of eight. Reductions in reaction distance may have important consequences for capture success. Once a prey moves outside the reactive volume of a predator the prey has in fact escaped and the predator must begin searching again. As a result, the probability of trout or charr capturing a prey they detect v i s u a l l y decreases as irradiance decreases below saturation l e v e l s . Using the same argument, the probability of a prey escaping the reactive volume of a charr at saturation irradiance lev e l s is greater than in trout due to the lower maximum reaction distance in charr. There are two other methods which can be used to determine the influence of irradiance on v i s u a l prey detection. An analysis of stomach contents over a 24-h period is one method although there are numerous d i f f i c u l t i e s in interpreting this 108 type of data (Jenkins and Green 1977). As well these studies usually relate feeding a c t i v i t y to time of day which can only be used as a r e l a t i v e measure of irradiance. The most common pattern found in this type of analysis i s a diurnal feeding rhythm. For example, adult Clupea harenqus (Muzinic 1931), Pleuronectes platessa (Hempel 1956) and Thunnus  alalunqa (Iverson 1962) have the greatest amount of food in their gut at dusk and dawn and the least at night. It is assumed in these studies that the amount of food i s related to feeding a c t i v i t y and dependent on the irradiance l e v e l . More exact information is obtained from laboratory feeding experiments conducted over a range of irradiance l e v e l s . In most examples of this type of work, radiation is measured in photometric units. For purposes of comparison with this study, i t i s assumed that 1 foot-candle is equal to 5.56 x 10 1 7 photons nr 2 s" 1 (Blaxter 1970). The irradiance levels over which feeding a c t i v i t y declines range from 10 1 3 to 10 1 2 photons n r 2 s~ 1 in Trachurus symmetricus (Hunter 1968) to 10 1 6 to 101 * photons n r 2 s" 1 in Lota lota (Girsa 1961). The decline for most vi s u a l feeders occurs between 10 1 6 and 10 1" photons nr 2 s" 1 (Blaxter 1970). The range in irradiance over which feeding a c t i v i t y declines in four species of P a c i f i c salmon, Oncorhynchus  kisutch, 0. nerka, O. keta and 0. gorbuscha i s between 10 1 7 to 10 1 3 photons n r 2 s~ 1 ( A l i 1959, Brett and Groot 1963). The range in irradiance levels over which reaction distance declines in trout (Fig. 5) is higher than the range over which feeding a c t i v i t y declines in the closely related P a c i f i c salmon. The 109 decline in reaction distance of charr occurrs between 10 1 6 and 10 1" photons n r 2 s~ 1, within the range feeding a c t i v i t y declines in P a c i f i c salmon. While reaction distance i s not a measure of feeding a c t i v i t y , usually expressed as number of prey captured per unit time, i t is a correlate of feeding a c t i v i t y . As the reaction distance of a predator decreases, so to w i l l the rate at which i t encounters prey and therefore, the rate at which i t can consume prey. Between irradiances levels of 10 1 8 and 10 1 5 photons n r 2 s" 1 in trout and 10 1 6 and 101 * photons rn"2 s" 1 in charr reaction distance declines (Fig. 5). A l i (1959) reports that the eyes of P a c i f i c salmon s h i f t from a l i g h t to a dark adapted state at irradiance levels between 10 1 7 and 10 1" photons n r 2 s" 1. Salmo  salar show a similar s h i f t at irradiance levels between 101 * and 10 1 3 photons n r 2 s" 1 ( A l i 1961). Over the irradiance range where the eye of P a c i f i c salmon s h i f t s from a state of l i g h t to dark adaptation, their a b i l i t y to capture prey decreases. This suggests that the reduction in reaction distance in trout and charr to prey targets i s the result of the eyes s h i f t i n g from a l i g h t adapted to a dark adapted state. Any discussion of reaction distance only in terms of the quantity of irradiance i s incomplete. The quality or colour is another important c h a r a c t e r i s t i c of irradiance which af f e c t s vi s u a l perception. The findings in this study support the hypothesis that q u a l i t a t i v e l y there i s no difference in the s e n s i t i v i t y of trout and charr to d i f f e r e n t colours of 1 10 irradiance when s e n s i t i v i t y i s measured in terms of reaction distance (Fig. 6). In both species reaction distance i s greatest in the presence of red irradiance followed in decreasing order by green, yellow and blue irradiance. Although q u a l i t a t i v e l y similar, the magnitude of the response in the two species i s d i f f e r e n t . For any colour of irradiance the reaction distance of trout is greater than that of charr. Early investigators thought that peaks in curves describing the relationship between the magnitude of an irradiance dependent response and irradiance colour could be used to predict the wavelength of maximum absorbance (am) of the visu a l pigments in the eye. It now appears this is not true. Blaxter (1964) found that the shape of the curve for Clupea harenqus varies depending on whether the response being measured is related to phototaxis, feeding or perception of a ba r r i e r . Northmore and Muntz (1974) obtained the same type of result when trying to establish the spectral s e n s i t i v i t y curve for Scardinius erythrophthalmus from behavioural data. In this study, the type of curve obtained when the response of the animal was measured to moving bars of l i g h t , stationary bars of lig h t of various widths and to diffuse l i g h t stimuli was d i f f e r e n t . It seems that in f i s h and many other animals (Muntz 1975b), a wide variety of spectral s e n s i t i v i t y curves may be obtained depending on the experimental conditions. Consequently spectral s e n s i t i v i t y curves can only be used to provide a re l a t i v e index of s i m i l a r i t y in the visual pigments of di f f e r e n t animals subjected to the same experimental conditions rather 111 than absolute estimates of am. The photopic spectral s e n s i t i v i t y curves (Fig. 6) indicate that trout and charr have the same cone v i s u a l pigments. Although scoptic (dark-adapted) s e n s i t i v i t y curves were not determined for these two species, the visu a l pigments of the rods have been measured from r e t i n a l extracts (Munz and Beatty 1965) . As in the P a c i f i c salmon (Beatty 1966) two pigments are found in the rods of trout and charr, retinene one and two with am of 503 and 527 nm, respectively. It i s generally accepted that vi s u a l pigments are adapted to the photic environment in which the animal l i v e s (Lythgoe 1966) . Two hypotheses have been put forward to explain how visual pigments are adapted to their environment. The f i r s t , the s e n s i t i v i t y hypothesis, suggests that visual pigments are adapted to the spectral quality of the ambient irradiance in such a way as to catch the greatest number of photons (Clarke 1936). This hypothesis accounts for the am of vi s u a l pigments for many species in a wide variety of groups including teleost fishes (Denton and Warren 1956, 1957, Munz 1957, 1958) cartilagenous fishes (Denton and Shaw 1956), pinnepids (Lythgoe and Dartnall 1971) and whales (McFarland 1971). The variety of species and locations for which the am of the v i s u a l pigments matches the wavelength of maximum transmission of irradiance in the portion of the water column where the animal l i v e s strongly suggests i t is an ec o l o g i c a l l y rather than a phylogenetically based phenomenon. Although the s e n s i t i v i t y hypothesis works well in some 1 12 situations i t does not account for the d i s t r i b u t i o n of a l l known f i s h v i s u a l pigments (Dartnall and Lythgoe 1965, Lythgoe 1972). These discrepencies led Lythgoe (1966) to suggest that considering s e n s i t i v i t y alone i s misleading as the function of the eye is not merely to catch as many photons as possible but to detect objects by their contrast with respect to the background. The contrast hypothesis shows that in some special cases the v i s i b i l i t y of a target can be increased by having vi s u a l pigments whose am is offset from the spectral quality of the ambient l i g h t . Either of these hypotheses would predict that i f trout and charr l i v e in diff e r e n t photic environments, their v i s u a l pigments should be d i f f e r e n t also. The s i m i l a r i t y in scoptic vi s u a l pigments is not d i f f i c u l t to explain. These pigments are used at dusk and dawn (Muntz 1975b). During these periods in Loon Lake both trout and charr occupy the surface waters (Andrusak and Northcote 1971). During the summer in the daytime trout are concentrated near surface waters while charr often occupy greater depths (Andrusak and Northcote 1971). As a result of attenuation the spectral composition and wavelength of maximum transmission of irradiance at the surface i s very d i f f e r e n t from that in deeper water (Duval e_t a_l. 1973), yet the photopic v i s u a l pigments appear to be the same (Fig. 6). The most probable explanation of this discrepancy l i e s in an understanding of the annual d i s t r i b u t i o n of these two species. Although v e r t i c a l l y segregated in the summer, sympatric trout and charr do not show 1 1 3 any difference in d i s t r i b u t i o n at other times of the year (Andrusak and Northcote 1971, T.G. Northcote, unpublished data). Therefore, at times other than summer there should be no difference in the photopic pigments. Some f i s h exhibit seasonal changes in the am of their v i s u a l pigments (Beatty 1966, Schwanzara 1967) while others show no seasonal change (Bridges and Yoshikami 1970). The pigments of Salmo gairdneri can be altered in the laboratory i f the animal is subjected to a new photic environment but this change takes approximately 50 days to occur (Tsin 1978). It appears that the photopic visual pigments in trout and charr are either unalterable or there is not s u f f i c i e n t time when segregated for the change to occur. The implication of this is at least for part of the year, probably in the daytime during the summer, the photopic vis u a l pigments of trout or charr or both are not the optimum ones for the ambient irradiance environment in which they l i v e . This would result in a decrease in visu a l prey detection a b i l i t i e s . While there are s t a t i s t i c a l l y s i g n i f i c a n t differences in the v e r t i c a l d i s t r i b u t i o n of sympatric trout and charr during the summer, segregation is not complete. When fish i n g with v e r t i c a l g i l l n e t s , some charr are caught near the surface and some trout are caught in deeper water (Andrusak and Northcote 1971, Hume 1978). Consequently, the p o s s i b i l i t y exists that there is both a shallow and deep water form of each species. If this is true and i f the method of c o l l e c t i n g the animals samples only the shallow or deep water form of each species, then t h i s provides a t h i r d explanation for the s i m i l a r i t y of photopic 1 1 4 vis u a l pigments in trout and charr. Results from t h i s and other studies make this p o s s i b i l i t y unlikely. Studies on the v e r t i c a l d i s t r i b u t i o n of sympatric trout and charr from Marion Lake (Andrusak and Northcote 1971) and Loon Lake (Hume 1978), the same lake from which animals in this study were collected, provide no information suggesting there i s more than one form of each species. Secondly, other responses measured in this study using the same animals or animals col l e c t e d at the same time suggest the vi s u a l system of charr i s c h a r a c t e r i s t i c of an animal l i v i n g in a low irradiance environment while that of trout is c h a r a c t e r i s t i c of an animal l i v i n g in a high irradiance environment. Thirdly, h i s t o l o g i c a l studies of the retinas of sympatric trout and charr show clear differences in r e t i n a l structure with no overlap between the two species. F i n a l l y , results of stomach analyses on Loon Lake trout and charr strongly suggest that some individuals of both species caught near the surface had recently been feeding at considerable depths while the stomachs of other individuals caught in the deeper waters, contained prey types c h a r a c t e r i s t i c of surface water (T. G. Northcote, unpublished data). An interesting feature of the spectral s e n s i t i v i t y curves i s that their peak occurs in the red irradiance (Fig. 6). Although there are d i f f i c u l i t i e s in ide n t i f y i n g the am of photopic v i s u a l pigments based on behavioural studies as described e a r l i e r , t h i s peak s e n s i t i v i t y in the longer wavelengths has also been found in Perca flavescens (Cameron 1974), Scardinius erythrophthalmus (Northmore and Muntz 1974) 1 15 and Carassius auratus (Yager 1967) using a variety of behavioural techniques. The adaptive significance of far-red s e n s i t i v i t y seems to result from the fact that lakes are usually coloured by substances that s h i f t the spectral d i s t r i b u t i o n of available irradiance to longer wavelengths (Lythgoe 1975, Muntz 1975b). This is the case in Eunice Lake, a lake adjacent to Loon Lake with a similar o r i g i n and geological setting (Efford 1967), where the wavelength of maximum transmission s h i f t s from approximately 470 nm at the surface to 560 nm at 18 m (Duval e_t a l . 1973). _4.J_.J_._2 Characteristics of the Prey Visual predators can d i s t i n g u i s h the size, form, contrast and movement of an object (Horridge 1968, Prazdnikova 1969). The effect of three of these c h a r a c t e r i s t i c s , size, movement and contrast on the reaction distance of trout and charr are examined in this study. Results indicate that trout and charr are sensitive to changes in a l l three c h a r a c t e r i s t i c s and lead to rejection of the hypothesis that differences in the size, movement or contrast of prey targets do not a f f e c t the distance at which they are f i r s t detected by trout and charr. Brawn (1969) was the f i r s t to establish a relationship between reaction distance and target s i z e . In this study adult cod, Gadus morhua , showed an increase in reaction distance to a r t i f i c a l food targets as the size of the targets increased from 1 to 10 mm. More recently the same relationship has been found in Lepomis qibbosus (Confer and Blades 1975), Lepomis 1 16 macrochirus (Vinyard and O'Brien 1976, Werner and Hall 1974) and Salvelinus namaycush (Kettle and O'Brien 1978) when presented with various sizes and species of copepods and cladocerans. Q u a l i t a t i v e l y , the results from my study p a r a l l e l those described above. The reaction distance of both trout and charr increases as the size of a r t i f i c i a l (Fig. 7) and natural prey targets (Fig. 11) increases. While there are no comparative studies on the reaction distance of co-habiting species, the results reported here show clear differences between trout and charr. At irradiance le v e l s greater than 3.0 x 10 1 6 photons n r 2 s" 1, the reaction distance of trout to any prey size and the rate of increase in reaction distance with increasing prey size i s greater than in charr (Fig. 7). At irradiance levels equal to or less than 3.0 x 10 1 6 photons n r 2 s" 1, the reaction distance of charr exceeds that of trout. The reaction distance of trout and charr become nearly independent of prey size at the lowest irradiance levels used in this study (Fig. 7). Vinyard and O'Brien (1976) found the same relationship for Lepomi s macrochi rus feeding on various sizes of Daphnia pulex at low levels of irradiance. They suggested that the decreased effect of prey size on reaction distance at low irradiance levels was the result of the animal switching to another sensory system for prey detection which was independent of the amount of irradiance. More recently, Eggers (1977) has shown that i t is not necessary to invoke another sensory mechanism to explain these r e s u l t s . In an analysis of contrast theory, he showed that vi s u a l reaction distance under low 1 1 7 irradiance conditions was independent of prey size. The e f f e c t of changes in the amount of movement and contrast of prey targets on the reaction distance of trout and charr i s similar to the effect of changes in prey size. The reaction distance of both species to a r t i f i c i a l prey targets increases as the amount of movement (Fig. 8) or contrast (Fig. 9) increases. The response to changes in the amount of movement (Table 9) and contrast (Fig. 10) of zooplankton prey is the same. In both trout and charr the e f f e c t of increases in amount of movement and contrast on reaction distance is greatest at saturation irradiance l e v e l s . At a l l irradiance l e v e l s , greater than the v i s u a l irradiance threshold of trout, increases in the amount of movement or contrast of prey targets produce a proportionally greater increase in the reaction distance of trout than charr. These results p a r a l l e l those of e a r l i e r studies. Ware (1971) found that the reaction distance of rainbow trout, Salmo gairdneri, to moving prey targets was greater than to stationary prey and that over the range of prey sizes tested (3-15 mm) the effect of target motion was additive. Confer and Blades (1975) showed that the reaction distance of Lepomis  gibbosus to Mesocyclops edax was greater than to other copepods of a similar s i z e . M. edax was the most active prey used in this study suggesting that the reaction distance of L. gibbosus to prey targets increases with increases in target movement. Confer and Blades (1975) found that Lepomis gibbosus had a larger reaction distance to the darkly pigmented forms of 1 18 Daphnia magna than to the l i g h t l y pigmented Daphnia pulex of a similar s i z e . Similar findings have been reported by Kettle and O'Brien (1978), who found that the reaction distance of Salvelinus namaycush to zooplankton from a f i s h l e s s lake was greater than to zooplankton from a lake containing f i s h . They attributed the difference to the high concentration of pigment in the zooplankton forms from the f i s h l e s s lake. Reaction distance of Salvelinus namaycush to intermediately pigmented Daphnia pulex f e l l between the reaction distance found with zooplankton from the f i s h and f i s h l e s s lakes (Kettle and O'Brien 1978). Size, movement and contrast of prey targets affected the a b i l i t y of trout and charr to locate them. An increase in any of these prey c h a r a c t e r i s t i c s increased the reaction distance of the f i s h to them and the. reaction distance was always greater in the trout. This indicates that v i s u a l discrimination is more highly developed in trout than in charr. The difference in v i s u a l discrimination has important implications in terms of the rate at which the two species encounter prey. If swimming speed is the same in both species then the volume of water searched becomes proportional to the square of the reaction distance. As the result of better v i s u a l discrimination in trout an increase in the absolute volume of water scanned by trout due to some factor increasing prey v i s i b i l i t y w i l l be greater than the increase shown by charr at irradiance levels greater than 3.0 x 10 1 6 photons m~2 s" 1. It is d i f f i c u l t to determine which of the three prey 119 c h a r a c t e r i s t i c s examined in thi s study has the greatest effect on v i s u a l perception in trout and charr. A comparison of the proportional change in reaction distance resulting from changes in each prey c h a r a c t e r i s t i c does not provide the answer as there is no single scale which can be used to describe change in the three c h a r a c t e r i s t i c s . Probably the least important c h a r a c t e r i s t i c in visu a l detection is prey movement. While an increase in prey movement increases the reaction distance of trout and charr, the f i s h also respond to non-moving prey. Similar results are obtained with Salmo gairdneri (Ware 1971) and Gadus morhua (Brawn 1969). The effects of prey size and contrast cannot be considered separately. The performence of any visu a l system is r e s t r i c t e d by the minimum contrast threshold required for target detection (Hester 1968, Le Grand 1967). This threshold is not constant but decreases as the angle subtened at the eye (a measure of size) by the target increases (Ware 1971). The contrast threshold also decreases with increasing ambient i r r a d i a t i o n . The upper l i m i t of the contrast threshold is set by the minimum angle that can be detected by the r e t i n a l photoreceptors (Hester 1968). The lower l i m i t i s established by the minimum contrast that can be distinguished by the eye. While i t cannot be determined with certainty what causes the poorer acuity in charr, i t probably i s related to either the minimum contrast threshold or the minimum angle subtending the eye they can detect. The lower density of cones (Table 11) and the higher degree of summation in the retina of sympatric charr (Table 13) r e l a t i v e to trout suggests 120 that i t may be related to the l a t t e r . 4.__._2 Chemical Thus far, my discussion has been r e s t r i c t e d to the visu a l aspects of prey detection in trout and charr. At irradiance levels above their v i s u a l irradiance threshold both species appear to rely exclusively on their v i s u a l system for locating prey targets. However, a l l species depend on more than one sensory mode for interpreting the nature of their surroundings and some species show a s h i f t from one mode to another depending on immediate environmental conditions. While most studies of sensory behaviour in f i s h indicate the importance of the visual system for c o l l e c t i n g information from the environment, some show the importance of the chemosensory system p a r t i c u l a r l y for species l i v i n g under low irradiance conditions. Results from this study support the hypothesis that at sub-visual irradiance levels trout do not use their chemosensory system for locating prey targets but reject the same hypothesis for charr. At irradiance l e v e l s below their v i s u a l irradiance threshold charr can successfully locate buried l i v e r prey targets but do not respond to the same targets sealed in glass cylinders (Table 15). Schutz and Northcote (1972) present some laboratory evidence suggesting that foraging charr use their v i s u a l and chemosensory systems under high irradiance conditions, the chemosensory system to detect buried benthic prey. Although no non-visual foraging behaviour was observed in charr used in this study when the irradiance l e v e l exceeded 121 their v i s u a l irradiance threshold, the prey were never hidden from view of the predator. The fact that charr are associated with the sediment during the daytime in the summer and that large numbers of benthic organisms, consisting of both epibenthic and infaunal forms, are found in their guts at this time (Andrusak and Northcote 1971) suggest that their chemosensory system may be used throughout the day. Charr exhibit two types of non-visual searching behaviour. I n i t i a l l y they swim throughout the tank moving their head from side to side along the bottom. When they come close to a prey target they stop and begin snapping at the sediment. The movement of a chemical stimulus in s t i l l water depends e n t i r e l y on d i f f u s i o n . The d i f f u s i o n results in a concentration gradient which is steep close to the prey and decreases with distance away from the source. This suggests that the two non-visual foraging behaviours are related to the concentration of the stimulus, swimming occurring when the stimulus is detected in the environment and snapping when the gradient becomes steep. The success of charr in locating prey in turbulent water is much less than in s t i l l water (Table 15) although there is no change in the searching behaviour. This i s what would be predicted i f i t is assumed that the charr are using their chemosensory system to locate prey. Although the stimulus is s t i l l present in the turbulent water, i t s d i s t r i b u t i o n is very uneven making i t d i f f i c u l t to locate the prey. Consequently, the chemosensory system in charr, which move into the l i t t o r a l zone at night (Andrusak and Northcote 1971), i s probably less 1 22 e f f e c t i v e during periods of heavy wave action. The p o s s i b i l i t y of charr using their chemosensory system for locating zooplankton is remote. Zooplankton are known to release chemical cues to which f i s h can respond (Johannes and Webb 1970). However, unlike most benthic prey which are fixed in space, a zooplankter acts as an irregular moving source and i t s t r a i l i s e a s i l y disturbed by water movements. The only way to locate a source in such a case is to search the water mass containing the stimulus and rely on other, more d i r e c t i o n a l cues (e.g. vision) in finding the exact source location. It i s reasonable to assume that the sensory systems charr use for prey detection, l i k e other aspects of feeding behaviour, are adaptive to the environment in which the animal l i v e s . Yet, i t i s d i f f i c u l t to access the r e l a t i v e importance of the chemosensory and vis u a l systems in terms of the amount of food they make available to the animal. While charr do consume benthic prey (Andrusak and Northcote 1971) they are not necessarily detected by the chemosensory system. Some portion of the benthic community i s at or just above the sediment-water interface (Ware 1971) and may be detected v i s u a l l y (Schutz and Northcote 1972). That charr choose to use their v i s u a l system for locating prey when irradiance levels are high and the prey are exposed is well documented in t h i s study and by the work of Schutz and Northcote (1972). As well, the rate of capture success in charr is much higher for v i s u a l l y detected prey (82.0%) than for prey located with the chemoreceptive system (25.8%). This suggests that use of the visual system is the most 123 e f f e c t i v e means of detecting prey in charr. However, as night approaches the visual system of charr becomes increasingly unreliable as a prey-sensing modality. During t h i s period their v i s u a l system functions only in the upper few meters of the water column (Fig. 13) and the low level of irradiance at t h i s time l i m i t s their reaction distance to potential prey. It seems reasonable that they may rely extensively on chemical cues emitted by potential prey in locating those prey under low irradiance conditions. Trout are known to be capable of detecting chemical stimuli (Jahn 1976) yet they did not use their chemosensory system as a means of locating prey in this study (Table 14). Possibly the higher concentration of planktonic prey in the surface waters of Loon Lake that they inhabit as well as their more acute vis u a l system provides a s u f f i c i e n t food source hence eliminating the need for using other, probably less e f f e c t i v e sensory systems for locating prey. Although not identifying the sensory system used for detecting prey, Andrusak (1968) did find that the mean gut fullness of sympatric trout was consistently 40 - 50% greater than that of sympatric charr during the spring and summer. This observation provides support for the argument that the a v a i l a b i l i t y of food to trout may be greater than that for charr. It does not a s s i s t though in distinguishing between the r e l a t i v e importance of position of the f i s h in the water column while foraging and the type and structure of the sensory system employed for locating prey in determining food a v a i l a b i l i t y . 1 24 4.2 Ret inal Structure in Trout and Charr The behavioural studies with sympatric trout and charr revealed major differences in their response to visual s t i m u l i . In summary, charr reacted to prey targets at lower irradiance levels than trout ( i . e . the v i s u a l system of charr i s more sensitive to irradiance than that of trout) but their acuity was poorer. The h i s t o l o g i c a l studies were used as a means of further testing the behavioural results but at a d i f f e r e n t level of organization. The hypothesis tested was that there are no differences in r e t i n a l structure between sympatric trout and charr which can account for observed differences in their s e n s i t i v i t y to irradiance or acuity. Based on an examination of five c h a r a c t e r i s t i c s of the retina which have been related to either the l e v e l of s e n s i t i v i t y or acuity in other species, rod and cone density, cone types, cone size and the degree of r e t i n a l summation, the hypothesis was rejected. The r e t i n a l structure of a l l o p a t r i c trout (Placid Lake) and charr (Dickson Lake) was also examined. Although visual s e n s i t i v i t y and acuity were not determined for animals from a l l o p a t r i c populations their v e r t i c a l d i s t r i b u t i o n in the water column i s known. Unlike sympatric populations where trout are taken most frequently at the surface and charr in deeper water during the summer, a l l o p a t r i c trout and charr were commonly found throughout most of the water column (Andrusak and Northcote 1971). The difference in v e r t i c a l d i s t r i b u t i o n was most evident between the two forms of charr, with a l l o p a t r i c charr, unlike the sympatric form, undergoing a d i e l v e r t i c a l 125 migration and commonly taken in the upper 5 m during daylight. As a result of differences in their v e r t i c a l d i s t r i b u t i o n the two forms of each species are exposed to d i f f e r e n t irradiance regimes. Consequently, r e t i n a l structure which is related to the amount of irradiance in the environment and i s used in this study as a correlate of vi s u a l s e n s i t i v i t y and acuity, may be d i f f e r e n t between the two forms. This p o s s i b i l i t y was examined by testing the hypothesis that there are no differences in r e t i n a l structure between sympatric and a l l o p a t r i c trout and sympatric and a l l o p a t r i c charr that relate to differences in their v e r t i c a l d i s t r i b u t i o n . The hypothesis was rejected. The density of rods and cones in the retina of trout and charr is similar to that of other teleosts ( A l i and A n c t i l 1976). The greatest cone density is found in the two trout populations and the least in the population of sympatric charr (Table 11). The difference in cone density among the four populations has important implications in terms of vi s u a l acuity. Visual acuity is determined in part by the cone density. The minimum separable angle (a measure of visual acuity) an animal can resolve ( ) i s determined as follows: (1) where F = focal distance of the lens which i s 2.25 126 (Matthiessen's ratio) times the radius of the lens 0.25 = degree of shrinkage during h i s t o l o g i c a l procedures n = number of cones per 0.01 mm2 This model assumes that image li n e s can only be resolved when they f a l l on cones separated by at least one unstimulated cone (Tamura and Wisby 1963). The smallest estimate of minimum separable angle, 1.8 minutes, occurs in the sympatric trout while sympatric charr have the largest estimate at 2.9 minutes. This suggests, as did the behavioural experiments, that acuity is better in sympatric trout than sympatric charr. The minimum separable angle for a l l o p a t r i c trout, 1.9 minutes, i s similar to that for the sympatric form. A l l o p a t r i c charr have a minimum separable angle of 2.3 minutes. This value i s intermediate between that of sympatric trout and charr and corresponds to their more " t r o u t - l i k e " behaviour in terms of v e r t i c a l d i s t r i b u t i o n and feeding mode (Andrusak and Northcote 1971). High densities of rods are associated with nocturnal and crepuscular a c t i v i t y ( A l i e_t a l . 1977). Although the density of rods is s l i g h t l y higher in both a l l o p a t r i c and sympatric charr than either form of trout (Table 11), the difference is not great. Consequently, i t i s unlikely that rod density i s related to differences in irradiance s e n s i t i v i t y in these two species. Cones types ranging from single to quadruple have been i d e n t i f i e d in the teleost retina (An c t i l 1.969). Based on their 1 27 re l a t i v e proportion in shallow and deep-water species they have been attributed d i f f e r e n t degrees of s e n s i t i v i t y to irradiance. The predominant theory has been that s e n s i t i v i t y to low irradiance conditions increases from single to quadruple cones (Willmer . 1953, O'Connell 1963, Engstrom 1963, Ahlbert 1975, A l i et a l . 1977, A l i and A n c t i l 1977). Single and double cones are present in the retina of trout and charr (Plate 3). Although the actual density of each cone type is d i f f e r e n t between sympatric trout and charr and sympatric and a l l o p a t r i c charr, the result of differences in cone size (Table 12), the proportion of each type in a l l four populations is the same. The r a t i o of double to single cones in the retina of trout and charr, 4 : 1, i s the same as that in Salmo salar and Salmo trutta (Ahlbert 1976). The s i m i l a r i t y in the r a t i o of double cones to single cones in the retina of trout and charr suggests that cone type cannot explain the difference in irradiance s e n s i t i v i t y between sympatric trout and charr nor is i t related to differences in the v e r t i c a l d i s t r i b u t i o n between sympatric and a l l o p a t r i c forms of each species. The basic problem in visi o n i s s t a t i s t i c a l in nature. It i s necessary for the eye to gather a s u f f i c i e n t number of photons to make r e l i a b l e predictions about the nature of the image on the retina. As is the case in s t a t i s t i c s , the greater the s i m i l a r i t y between two populations, the larger the sample required to distinguish them. In vi s u a l terms then, a high l e v e l of acuity or fine discrimination of size, movement or contrast can only occur in a high irradiance environment. 1 28 In a low irradiance environment where photons are at a premium, i t i s not possible to resolve fine d e t a i l . In t h i s situation the primary concern must be to enhance s e n s i t i v i t y to irradiance. One way to accomplish this is to increase the e f f e c t i v e capture area of each receptor. One means of increasing the e f f e c t i v e capture area of a photoreceptor is to increase the cross-sectional area of the receptor. This occurs in the family Percidae ( A l i e_t a_l. (1977). The cones of St izostedion vitreum vitreum which makes crepuscular and nocturnal feeding forays (Ryder 1977) are much larger than the cones of Perca flavescens which i s a daytime feeder. The cross-sectional size of both double and single cones i s smallest in the two trout populations and largest in the population of sympatric charr (Table 12). The difference in cone size between sympatric trout and charr suggests that charr are more sensitive to low irradiance conditions and p a r a l l e l s the results of the behavioural experiments. The intermediate cone size of a l l o p a t r i c charr suggests that they are less sensitive to low irradiance conditions than sympatric charr. This i s supported by the observations of Andrusak and Northcote (1971) which show a l l o p a t r i c charr are commonly taken higher in the water column than the sympatric form. The e f f e c t i v e capture area of a photoreceptor can also be enlarged by connecting a number of receptors in the same area of the retina together so they function as a unit. The concept of s p a t i a l integration in the retina i s usually referred to as 129 summation. It is measured in terms of the number of photoreceptor c e l l s (rods and cones) per bipolar c e l l and the number of bipolar c e l l s per ganglion c e l l . S e n s i t i v i t y to irradiance increases with the degree of summation while acuity is reduced. In general the degree of summation i s highest in f i s h l i v i n g in low irradiance or turbid environments. Stizostedion  canadense which l i v e in a much more turbid environment than Stizostedion vitreum vitreum have a higher rate of r e t i n a l summation ( A l i and A n c t i l 1977). In a study of 20 pelagic and demersal f i s h A n c t i l (1969) i d e n t i f i e d an inverse correlation between the brightness of the environment in which the f i s h l i v e s and the extent of summation. Ahlbert (1975) found summation was much higher in Lucioperca lucioperca, which l i v e in low irradiance environments, than in the cl o s e l y related Perca f l u v i a t i l i s or Acerina cernua which are c h a r a c t e r i s t i c of high irradiance environments. Sympatric charr show the highest level of summation in this study with a ratio of one ganglion c e l l to 22.3 bipolar c e l l s to 78.1 v i s u a l c e l l s (Table 13). The lowest l e v e l of summation, approximately 1:16:38, occurs in the two trout populations. This suggests, as do the results of the behavioural experiments, that sympatric charr are more sensitive to low irradiance conditions than sympatric trout but their acuity is poorer. The level of summation and hence s e n s i t i v i t y to low irradiance conditions and acuity in a l l o p a t r i c charr is intermediate between that of trout and sympatric charr. Again, the difference in r e t i n a l structure 130 between a l l o p a t r i c and sympatric charr appears to be related to differences in the v e r t i c a l d i s t r i b u t i o n and feeding habits of the two populations (Andrusak and Northcote 1971). The mosaic-like arrangement of the vi s u a l c e l l s in the retina of some teleosts has been known for more than a century (Ryder 1895). The major elements of visu a l c e l l mosaics are the cones. Rods do not usually show any pattern of regularity except in very young f i s h (Wagner 1974). Various patterns of visu a l c e l l mosaics have been described for many Europeon (Engstrom 1963) and North American teleosts (Anctil 1969). In some instances these patterns have been related to the behaviour and feeding habits of the f i s h (Anctil 1969, Dathe 1969, Bathelt 1970, Wagner 1972, Ahlbert 1975). In the past, orderly cone c e l l mosaics have been associated with good v i s u a l acuity. It now appears th i s i s not true (Campbell 1975) and that orderly mosaics are probably an adaptational advantage for the discrimination of movement (Wagner 1978). The cone mosaic of sympatric trout and charr is the same (Plate 3) except the actual area of one unit (four double c e l l s surrounding one single c e l l ) i s larger in the charr, the result of their larger cone size (Table 12). Consequently i t appears that although sympatric charr are less sensitive to prey movement than sympatric trout (Fig. 8) i t is unrelated to the cone mosaic. It is more l i k e l y that the decreased s e n s i t i v i t y to movement in charr results from their larger cone size and higher rate of summation, which reduces the le v e l of acuity. While nothing i s known about the re l a t i v e s e n s i t i v i t y of sympatric and 131 a l l o p a t r i c trout and sympatric and a l l o p a t r i c charr to prey movement, the s i m i l a r i t y in the cone mosaic between the two forms of each species suggests that any difference in s e n s i t i v i t y to movement is unrelated to the cone mosaic. Differences in r e t i n a l structure between sympatric trout and charr suggest that, on a r e l a t i v e basis, trout are less sensitive to low irradiance conditions than charr but their acuity i s better. These observations p a r a l l e l those of the behavioural experiments and provide an explanation at the c e l l u l a r l e v e l for differences in the v e r t i c a l d i s t r i b u t i o n and feeding mode of the two species when in sympatry. Retinal structure of a l l o p a t r i c charr i s intermediate between that of sympatric trout and charr, at least when measured in terms of cone density, cone size and level of summation. Again, these differences relate to known behavioural differences, a l l o p a t r i c charr having a v e r t i c a l d i s t r i b u t i o n and feeding mode intermediate between that of sympatric trout and charr. There are no differences in r e t i n a l structure between sympatric and a l l o p a t r i c trout. While the v e r t i c a l d i s t r i b u t i o n of these two populations during the summer i s not i d e n t i c a l the difference is small, a l l o p a t r i c trout most common between 4 and 5 m and sympatric trout most common in the upper 3 m of the water column (Andrusak and Northcote 1971). It i s l i k e l y that the difference in irradiance l e v e l experienced by these two populations is i n s u f f i c i e n t to be refl e c t e d in differences in r e t i n a l structure. 132 4.3 General Behavioural and h i s t o l o g i c a l evidence suggests that the vi s u a l system of sympatric charr i s a compromise between the r i v a l demands for s e n s i t i v i t y to low irradiance conditions and acuity. The vis u a l system of trout on the other hand i s less sensitive to irradiance conditions than the charr's but acuity is better. During the summer sympatric trout and charr are segregated, trout found near the surface and charr at greater depths, often as deep as 25 m (Andrusak and Northcote 1970). Over this depth irradiance levels decrease by approximately three orders of magnitude (Fig. 13). Throughout most of the daylight hours, the depth at which the irradiance is just s u f f i c i e n t to maximize reaction distance in trout i s approximately 20 m higher in the water column than the similar depth for charr. There is no advantage for charr in terms of the volume of water searched per unit time in moving above the depth where their reaction distance i s greatest. At the same time trout must remain in the upper waters to maximize their reaction distance. A model was developed to estimate the volume of water searched by trout and charr for various sizes of Daphnia rosea and Diaptomus kenai during one day in the summer (Fig. 15). For both f i s h the volume of water searched increased with prey size. The largest volumes were searched for Daphnia rosea and for both prey species trout searched a greater volume than charr. The estimates of volume of water searched provides only a r e l a t i v e index of the d a i l y searching potential as the reaction 1 33 distance of the f i s h to the prey in the laboratory is unlikely to be the same as in the f i e l d . Differences in water t u r b i d i t y , spectral composition and amount of background irradiance and spectral r e f l e c t i v i t y of prey surfaces between the f i e l d and the laboratory w i l l contribute to these differences. The model makes two assumptions about the feeding behaviour of trout and charr. F i r s t i t is assumed that both f i s h search a c y l i n d r i c a l volume of water while foraging where the radius of the cylinder equals the reaction distance to a given prey type and si z e . While t h i s is the most common assumption made in estimating the volume of water searched (Confer and Blades 1975) i t is unlikely to be true. Confer et. al. (1978) show that the cross-sectional shape through the search path of Salvelinus  namaycush is not a c i r c l e but a polygon and the distance from the eye to the edge of the polygon is d i f f e r e n t in the dorsal, ventral, nasal and temporal d i r e c t i o n s . Although the cross-section of the search path in trout and charr may not be a c i r c l e the only requirement for estimating the r e l a t i v e volume of water searched is that the cross-sectional shape be the same in the two species.The s i m i l a r i t y in the way trout and charr detect and approach prey targets suggests t h i s i s the case. The second assumption of the model is that searching is continuous but only when the irradiance l e v e l is s u f f i c i e n t to maximize both reaction distance and searching v e l o c i t y . This assumption is more d i f f i c u l t to evaluate as l i t t l e i s known about the short term movements of either of these species in the lake. Certainly the swimming speeds measured in this study and 1 34 used in the model are within the range that can be maintained for long periods of time without resulting in muscular fatigue in salmon and charr (Beamish 1980). The f i s h in Loon Lake are stunted, seldom reaching sizes greater than 20 cm (Hume 1978). It i s l i k e l y that food supplies are marginal requiring searching at a l l times when irradiance i s s u f f i c i e n t . Theoretical and experimental studies have shown that two eco l o g i c a l l y similar species l i k e trout and charr cannot co-exist i n d e f i n i t e l y on the same l i m i t i n g resource (Grinnell 1904, Lotka . 1925, Volterra 1926, Gause 1934, Park 1962). To reduce or eliminate competition for food (or any other common resource) sympatric species must p a r t i t i o n their environment in either space or time. Sympatric trout and charr do th i s , at least during the spring and summer by occupying d i f f e r e n t parts of the water column (Andrusak and Northcote 1971). Nilsson (1967) i d e n t i f i e s two types of segregation which occur in salmonid communities. Interactive segregation implies that ecological differences between species (eg. in food or habitat selection) are often magnified through interaction while selective segregation refers to species which have evolved differences s u f f i c i e n t l y great to be eco l o g i c a l l y isolated in the sense of evolu t i o n i s t s . Results from this study suggest that segregation between trout and charr in Loon Lake is se l e c t i v e . Differences in r e t i n a l morphology and consequently vis u a l behaviour are f u l l y expressed in s o l i t a r y animals and probably evolved as s p e c i f i c benefits towards the coexistence of the two species. This conclusion is supported by the results of other 1 35 studies on these two species. In a laboratory study Schutz and Northcote (1972) observed differences in feeding behaviour between s o l i t a r y trout and charr from Loon Lake and these differences were not magnified through interaction. More recently Hume (1978) separated and transferred sympatric trout and charr from Loon Lake to separate f i s h l e s s lakes. After a two-year sampling period there were no marked differences in either the diet or v e r t i c a l d i s t r i b u t i o n between the sympatric and a l l o p a t r i c populations. Again the implication was that segregation was due to genetically based selective forces. Laboratory studies show that trout are very aggressive towards charr. When paired, trout always dominate charr and when feeding, trout usually take a s i g n i f i c a n t l y greater proportion of the available food than charr (Schutz and Northcote 1972; Rosenau 1978). Consequently, i t i s l i k e l y that when trout and charr invade a f i s h l e s s lake, trout, through their aggressive highly competitive behaviour, are able to occupy the "optimal habitat" in terms of their own requirements and r e s t r i c t charr to other portions of the aquatic environment. If this is true then there should be no difference in the v e r t i c a l d i s t r i b u t i o n between a l l o p a t r i c and sympatric trout populations. While Andrusak and Northcote (1971) found that the depth at which the greatest number of trout were taken during the summer was not the same for sympatric and a l l o p a t r i c populations, the difference, less than 2 m, was small. Results from th i s study show no difference in r e t i n a l structure between sympatric and a l l o p a t r i c trout indicating that the vis u a l system of animals 136 from both populations is most e f f e c t i v e in the same portion of the water column. Charr, unlike trout, show major differences in summertime v e r t i c a l d i s t r i b u t i o n , feeding habits and r e t i n a l structure between sympatric and a l l o p a t r i c populations. In terms of these three characters a l l o p a t r i c charr are more " t r o u t - l i k e " than the sympatric form. This supports the trout dominance hypothesis and suggests that i f charr evolve independently of trout then charr can "choose", unrestricted, that portion of the aquatic habitat in which to l i v e . Consequently, i t seems that the dominance of trout over charr has forced charr, when sympatric with trout, to occupy the deeper water. This, in turn, has resulted in the selection for a vi s u a l system in charr which is very sensitive to low irradiance conditions. Implicit in the above is the concept that segregation between sympatric trout and charr need not always be either interactive or s e l e c t i v e . Interactive segregation may indeed occur in the early stage of coexistence with trout dominating charr and out competing with them for the available food. However, results from this study and others (Schutz and Northcote 1972, Hume 1978) c l e a r l y suggest that with time, selective pressures cause genetic changes in various morphological and behavioural characters and result in selective segregation. Although the vis u a l systems of trout and charr seem clos e l y related to their c h a r a c t e r i s t i c summertime s p a t i a l positioning, the obvious question is what about other times of the year when 1 37 segregation breaks down (Andrusak and Northcote 1970)? Although eye pigments may vary seasonally in response to changing environmental conditions (Beatty 1966), eye morphology does not. Consequently eye morphology cannot be optimal at a l l times of the year. Fish must perform many functions and l i k e other animals one of the most important i s the procurement of food. North temperate f i s h put on most of their growth during the spring and summer when the water is warm and food is abundant (Kelso and Ward 1977). Therefore i t appears that the visual systems of trout and charr have evolved in such a way as to maximize their e f f i c i e n c y in the time and environment when food is most abundant and thereby maximize growth, fecundity and sur v i v a l . 138 5.0 REFERENCES Ahlbert, I.-B. 1975. Orginization of the cone c e l l s in the retinae of some teleosts in r e l a t i o n to their feeding habits. Ph.D. Thesis. University of Stockholm. 29 p. Ahlbert, I.-B. 1976. Orginization of the cone c e l l s in the retinae of salmon (Salmo salar) and trout (Salmo trutta) in r e lation to their feeding habits. Acta Zool. 57: 13-35. A l i , M. A. 1959. The ocular structure, retinomotor and photobehavioural responses of juvenile P a c i f i c salmon. Can. J. Zool. 37: 965-996. A l i , M. A. 1961. Histophysiological studies on the juvenile A t l a n t i c salmon (Salmo Salar) retina. I I . Responses to l i g h t intensity, wavelengths, temperature and continuous l i g h t or dark. Can. J. Zool. 39: 511-526. A l i , M. A. 1963. Correlation of some r e t i n a l and morphological measurements from the A t l a n t i c salmon (Salmo s a l a r ) . Growth 27: 57-76. A l i , M. A. 1975. Retinomotor responses, p. 313-355. In M. A. A l i (ed.). Vision in fishes. Plenum Press. New York. A l i , M. A. and H. Kobayashi. 1967. Temperature: influence on the electroretinogram-flicker fusion frequency in the sunfish (Lepomis qibbosus L.). Rev. Can. B i o l . 26: 341-345. A l i , M. A. and H.-J. Wagner 1975a. Visual pigments: phylogeny and ecology, p. 481-516. In M. A. A l i (ed.). Vision in fishes . Plenum Press. New York. A l i , M. A. and H.-J. Wagner. 1975b. Dist r i b u t i o n and development of retinomotor responses, p. 36.9-396. I_n M. A. A l i (ed.). Vision in fishes. Plenum Press. 'New York. 139 A l i , M. A. and M. A n c t i l . 1976. Retinas of fishes: an a t l a s . Springer-Verlag. New York. 284 p. A l i , M. A. and M. A n c t i l . 1977. Retinal structure and function in the walleye (Stizostedion vitreum vitreum) and the sauger (S. canadense) . J F i s h . Res. Board Can. 34: 1467-1474. A l i . M. A., R. A. Ryder and M. A n c t i l . 1977. Photoreceptors and vi s u a l pigments as related to behavioural responses and preferred habitats of perches (Perca spp.) and pikeperches (Stizostedion spp.). J. Fish Res. Board Can. 34: 1475-1480. A l i , M. A. and H.-J. Wagner.1980. Vision in charrs: a review and perspectives, p. 391-422. In E. K. Balon (ed.). Charr: salmonid fishes of the genus Salvelinus. W. Junk Press. The Hague. A n c t i l , M. 1969. Structure de la retine chez quelques teleosteens marins du plateau continental. J. Fish. Res. Board Can. 26: 597-628. Andrusak, H. 1968. Interactive segregation between adult Dolly Varden (Salvelinus malma) and cutthroat trout (Salmo  c l a r k i c l a r k i ) in small coastal B r i t i s h Columbia lakes. M.Sc. Thesis. University of B r i t i s h Columbia. 76 p. Andrusak, H. and T. G. Northcote. 1970. Management implication of s p a t i a l d i s t r i b u t i o n and feeding ecology of cutthroat trout and Dolly Varden in coastal B r i t i s h Columbia lakes. B.C. Fish. Wildl. Br. Fish. Mgmt. Publ. 13. 14 p. Andrusak, H. and T. G. Northcote. 1971, Segregation between adult cutthroat trout (Salmo c l a r k i ) and Dolly Varden charr (Salvelinus malmal in small coastal B r i t i s h Columbia lakes. J. Fish. Res. Board Can. 28: 1259-1268. Armitage, G. N. 1973. Character displacement and v a r i a b i l i t y in lacustrine sympatric and a l l o p a t r i c Dolly Varden (Salvelinus malma) populations. M.Sc. Thesis. University of B r i t i s h Columbia. 119 p. 140 Arnold, G. P. 1974. The measurement of irradiance with pa r t i c u l a r reference to marine biology, p. 1-25. I_n R. Brainbridge, G. C. Evans and 0. Rackham (eds.). Light as an ecological factor. Blackwell S c i e n t i f i c Press. London. Atema, J. 1971. Structures and functions of the sense of taste in c a t f i s h (Ictalurus n a t a l i s ) . Brain Behav. Evol. 4: 273-294. Banner, A. 1972. Use of sound in predation by young lemon sharks, Negaprion b r e v i r o s t r i s . B u l l . Mar. S c i . 22: 251-283. Bathelt, D. 1970. Experimentelle und verliechende morphologische Untersuchungen am v i s u e l l e n System von Teleostiern. Zool. Jahrb. Abt. Anat. Ontog. 87: 402-470. Beamish, F. W. H. 1980. Swimming performance and oxygen consumption of the charrs, p. 739-748. In E. K. Balon (ed.). Charrs: salmonid fishes of the genus Salvelinus. W. Junk Publishers. The Hague. Beatty, D. D. 1966. A study of the succession of v i s u a l pigments in salmon (Oncorhynchus). Can. J. Zool. 44: 429-455. Beatty, D. D. 1975. Rhodopsin-porphyropsin changes in paired-pigment fishes, p. 635-644. I_n M. A. A l i (ed.). Vision in fishes. Plenum Press. New York. Betts, M. M. 1965. The food of titmice in oak woodlands. J. Anim. Ecol. 34: 282-268. Beukema, J.J. 1968. Predation by the three-spined stickleback (Gasterosteus aculeatus L.): the influence of hunger and experience. Behaviour 30:1-126. Blaxter, J. H. S. 1964. Spectral s e n s i t i v i t y of herring, Clupea  harengus L. J. Exp. B i o l . 41:155-162. Blaxter, J. H. S. 1968. Visual thresholds and spectral s e n s i t i v i t y in herring larvae. J. Exp. B i o l . 48: 39-53. 141 Blaxter, J . H. S. 1969. Visual thresholds and spectral s e n s i t i v i t y in f l a t f i s h larvae. J. Exp. B i o l . 51: 221-230. Blaxter, J . H.'S. 1970. Light-animals-fishes, p. 213-320. In 0. Kinne (ed.). Marine Ecology, Vol. 1, Part 1. John Wiley. New York. Blaxter, J . H. S. 1975. The eyes of l a r v a l f i s h , p. 427-443. In M. A. A l i (ed.). Vision in fishes. Plenum Press. New York. Blaxter, J. H. S. and M. P. Jones. 1967. The development of the retina and retinomotor responses in herring. J. Mar. B i o l . Ass. U.K. 47: 677-697. Blaxter, J. H. S. and M. Staines. 1970. Pure-cone retinae and retinomotor responses in l a r v a l teleosts. J. Mar. B i o l . Ass. U.K. 50:449-460. Blough, D. S. and D. Yager. 1972. Visual psychophysics in animals, p. 732-763. I_n D. Jameson and L. Hurvich (eds.). Handbook of sensory physiology, VII. Springer-Verlag. B e r l i n . Bowmaker, J.A. 1976. Vision in pelagic animals, p. 213-240. In R. C. Newell (ed.). Adaptation to the environment: essays on the physiology of marine animals. Butterworth Publ. London. Brawn, V. M. 1969. Feeding behaviour of cod (Gadus morhua)• J. Fish. Res. Board Can. 26: 583-596. Brett, J. R. and C. Grott. 1963. Some aspects of olfactory and visual responses in P a c i f i c salmon. J. Fish. Res. Board Can. 20: 287-303. Bridges, C. D. B. and S. Yoshikami. 1970. The rhodopsin-porphyropsin system in freshwater fishes: e f f e c t s of age and photic environment. Vision Res. 10: 1315-1332. 142 Cameron, N. E. 1974. Chromatic v i s i o n in a teleost f i s h , Perca  f l u v i a t i l i s L. Ph.D. Thesis. University of Sussex. 88 p. Campbell, A. 1975. The area of the stimulus e l i c i t i n g response as a factor in mirror image reversal, p. 749-753. I_n M. A. A l i (ed.). Vision in fishes. Plenum Press. New York. Carr, W. E. S., A. R. Gondeck and R. L. Delanoy.1976. Chemical stimulation of the feeding behaviour in the p i n f i s h , Lagondon rhomboides : a new approach to an old problem. Comp. Biochem. Physiol. A. 54:161-166. Clarke, G. L. 1936. On the depth at which fishes can see. Ecol. 17: 452-456. Confer, J. L. and P. I. Blades. 1975. Omnivorous zooplankton and planktivorous f i s h . Limnol. Oceanogr. 20: 571-579. Confer, J. L., G. L. Howick, M. H. Corzette, S. L. Kramer, S. Fitzgibbon and R. Landesberg. 1978. Visual predation by planktivores. Oikos 31: 27-37. Cronly-Dillon, J. R. and W. R. A. Muntz. 1965. The spectral s e n s i t i v i t y of the goldfish and the clawed tadpole under photic conditions. J. Exp. B i o l . 42: 481-493. Cronly-Dillon, J. R. and S. C. Scharma. 1968. Effect of season and sex on the photic spectral s e n s i t i v i t y of the three-spined stickleback. J. Exp. B i o l . 49: 679-687. Dartnall, H. J. A. and J. N. Lythgoe. 1965. The spectral clustering of v i s u a l pigments. Vision Res. 5: 81-100. Dathe, H. H. 1969. Vergliechende Untersuchungen an der retina mitteleuropaischer Subwasserfische. Z. Mikrosk. Anat. Forsch. 80: 269-319. Denton, E. J. and M. H. Pirenne. 1954. The v i s u a l s e n s i t i v i t y of the toad, Xenopus laevis . J. Physiol. 125: 181-207. 143 Denton, E. J. and T. I. Shaw. 1956. The visual pigments of some deep-sea elasmobranchs. J. Mar. B i o l . Ass. U.K. 43: 65070. Denton, E. J. and F. J. Warren. 1956. Visual pigments in deep-sea f i s h . Nature (Lond). 178: 1059. Denton, E. J. and F. J. Warren. 1957. The photosensitive pigments in the retinae of deep-sea f i s h . J. Mar. B i o l . Ass. U.K. 36: 651-652. Duval, W. S., T. G. Brown and G. H. Geen. 1973. A submersibile spectroradiometer and data aqu i s i t i o n system. J. Fish Res. Board Can. 30: 313-316. Efford, I. E. 1967. Temporal and s p a t i a l differences in phytoplankton productivity in Marion Lake, B r i t i s h Columbia. J. Fish. Res. Board Can. 24: 2283-2307. Eggers, D. M. 1977. The nature of prey selection by planktivorous f i s h . Ecol. 58: 46-59. Engstrom, K. 1963. Cone types and cone arrangements in the teleost retinae. Acta Zool. 44: 179-243. Everhart, W. H. and C. A. Waters. 1965. L i f e history of blueback trout (Arctic charr, Salvelinus alpinus (Linnaeus)) in Maine. Trans. Am. Fish. Soc. 94: 393-397. Gause, G.F. 1934. The Struggle for Existence. Williams and Wilkins Co. Baltimore. 163 p. Girsa, I. I. 1961. A v a i l a b i l i t y of food animals to some fishes at d i f f e r e n t conditions of illumination. (Russ.) Trudy Soveshch. i k h t o l . Kom 13:335-359. (Transla. Mar. Lab. Aberdeen 717). Glova, G. J. 1978. Pattern and mechanism of resourse partioning between stream populations of juvenile coho salmon (Oncorhynchus kisutch) and coastal cutthroat trout (Salmo  c l a r k i c l a r k i ) . Ph.D. Thesis. University of B r i t i s h Columbia. 170 p. 1 44 Gr i n n e l l , J. 1904. The orig i n and d i s t r i b u t i o n of the chestnut-backed chickadee. Auk. 21:364-382. Gruber, S.H. 1977. The visu a l system of sharks: adaptations and c a p a b i l i t y . Amer. Zool. 17:453-469. Grundfest, H. 1932. The s e n s i b i l i t y of the sunfish, Lepomis, to monochromatic radiation of low i n t e n s i t i e s . J. Gen. Physiol. 15: 307-328. Hanyu, I. and M. A. A l i . 1963. F l i c k e r fusion frequency of the electroretinogram in light-adapted goldfish at various temperatures. Science 140: 662-663. Hanyu, I. and M. A. A l i . 1964. Electroretinogram and i t s f l i c k e r fusion frequency at di f f e r e n t temperatures in light-adapted salmon (Salmo s a l a r ) . J. C e l l . Comp. Physiol. 63: 309-322. Harden, G. 1960. The competitive exclusion p r i n c i p l e . Science 131: 1292-1297. Hartley, P. H. T. 1953. An ecological study of the feeding habits on English titmice. J. Anim. Ecol. 22:261-268. Hartman, G. F. 1965. The role of behaviour in the ecology and interaction of underyear1ing coho salmon (Oncorhynchus  kistuch) and steelhead trout (Salmo gairdneri). J. Fish. Res. Board Can. 22: 1035-1081. Hemmings, C. C. 1974. The v i s i b i l i t y of objects underwater, p. 543-545. In R. Brainbridge, G. C. Evans and 0. Rackham (eds.). Light as an ecological factor. Blackwell S c i e n t i f i c Press. London. Hempel, G. 1956. Studien zur Tagesperiodik der Akt der Fische. 2. Die Nahrungsaufnahme der Scholle. Kurze Mitt. Inst. Fisch. B i o l . Univ. Hamberg 6: 22-37. Hester, F. J. 1968. Visual contrast thresholds of the goldfish (Carassius auratus). Vision Res. 8: 1315-1335. 145 Hobson, E. S. 1963. Feeding behaviour in three species of sharks. Pac. S c i . 17: 171-194. Holanov, S. H. and J. C. Tash. 1978. Particulate and f i l t e r feeding in threadfin shad, Dorosoma petenense , at d i f f e r e n t l i g h t i n t e n s i t i e s . J. Fish Res. Board Can. 13: 619-625. Holling, C. S. 1966. The functional response of invertebrate predators to prey density. Mem. Ent. Soc. Can. 48: 1-86. Horridge, G. A. 1968. Interneurons, their orign, action, s p e c i f i c i t y , growth and p l a s t i c i t y . W. H. Freeman and Co. San Francisco. 436 p. Hume, J. M. B. 1978. Planktivorous feeding and habitat u t i l i z a t i o n in sympatric and experimentally segregated populations of coastal cutthroat trout (Salmo c l a r k i  c l a r k i ) and Dolly Varden charr (Salvelinus malma). M.Sc. Thesis. University of B r i t i s h Columbia. 137 p. Hunter, J. R. 1968. E f f e c t s of l i g h t on schooling and feeding of jack mackeral, Trachurus symmetricus. J. Fish. Res Board Can. 25: 393-407. Hutchinson, G.E. 1957. A t r e a t i s e on limnology. I. geography, physics and chemistry. John Wiley and Sons. New York. 1015 P -Hutchinson, G. E. 1967. A t r e a t i s e on limnology. I I . introduction to lake biology and the limnoplankton. John Wiley and Sons. New York. 1115 p. Hyatt, K. D. 1979. Feeding strategy, p. 71-113. I_n W. S. Hoar, D. J. Randall and J. R. Brett (eds.). Fish physiology VIII: bioenergeties and growth. Academic Press. New York. Ishiwata, N. 1968. Ecological studies of the feeding of fishes. I I I . degree of hunger and satiation amount. B u l l . Jap. Soc. S c i . Fish. 34: 604-607. 146 Iverson, R. T. B. 1962. Food of albacore tuna Thunnus germo (Lacepede) in the central and north eastern P a c i f i c . Fishery B u l l . Fish Wildl. Ser. U.S.A. 62:459-481. Jahn, L. A. 1976. Responses to odours by f i n g e r l i n g cutthroat trout from Yellowstone Lake. Prog. Fish-Cult. 38: 207-210. Jenkins, B. W. and J. M. Green. 1977. A c r i t i q u e of f i e l d methodology for determining f i s h feeding p e r i o d i c i t y . Env. B i o l . Fish. 1: 209-214. Johannes, R. E. and K. L. Webb. 1970. Release of dissolved organic compounds by marine and freshwater invertebrates, p. 257-273. I_n D. W. Hood (ed.). Symposium on organic matter in natural waters. University of Alaska. Kalleberg, H. 1958. Observations in a stream tank of t e r r i t o r i a l i t y and competition in juvenile salmon and trout (Salmo salar L. and Salmo trutta L.). Rep.Inst. Freshwater Res. Drottningholm 39: 55-98. Kalmijn, A. J. 1971. The e l e c t r i c sense in sharks and rays. J. Exp. B i o l . 55: 371-383. Kelso, J. R. M. and F. J. Ward. 1977. Unexploited percid populations of West Blue Lake, Manitoba, and their interactions. J. Fish Res Board Can. 34: 1655-1669. Kettle, D. and W. J. O'Brien. 1978. Vu l n e r a b i l i t y of the Arct i c zooplankton species to predation by small lake trout (Salvelinus namaycush). J. Fish . Res. Board Can. 35: 1495-1500. Kwain, W.-H. and H. R. MacCrimmon. 1969. Age and visi o n as factors in bottom colour selection by rainbow trout, Salmo  gairdneri . J. Fish. Res. Board Can. 26: 687-693. Le Grand, Y. 1967. Form and space v i s i o n . Indiana University Press. Bloomington. 367 p. 147 Lockett, N. A. 1977. Adaptations to the deep-sea environment, p. 67-192. I_n F. C r e s c i t e l l i (ed.). Sensory Physiology, VII. Springer-Verlag. B e r l i n . Lotka, A.J. 1925. Elements of Physical Biology. Williams and Wilkins Co. Baltimore. (Reprinted 1956 by Dover Publ. New York as Elements of Mathematical Biology.) L y a l l , A.H. 1957. Cone arrangement in the teleost retinae. Q.J. Microsc. S c i . 98:189-201. Lythgoe, J. N. 1966. Visual pigments and underwater v i s i o n , p. 375-391. In R. Brainbridge, G. C. Evans and 0. Rackham (eds.). Light as an ecological factor. Blackwell S c i e n t i f i c Press. London. Lythgoe, J. N. 1968. Visual pigments and visu a l range underwater. Vision Res. 8: 997-1011. Lythgoe, J. N. 1972. The adaptation of vis u a l pigments to the photoic environment, p. 297-328. I_n H. J. A. Dartnall (ed.). The handbook of sensory physiology, VII. Springer-Verlag. B e r l i n . Lythgoe, J. N. 1975. Problems in seeing colours in water, p. 619-634. I_n M. A. A l i (ed.). Vision in fishes, Plenum Press. New York. Lythgoe, J. N. and H. J. A. Da r t n a l l . 1971. A deep-sea rhodopsin in a mammal. Nature (Lond). 227: 995-956. MacArthur, R. H. 1958. Population ecology of some warblers in northeastern coniferous forests. Ecol. 39: 599-619. Marshall, N. B. 1979. Developments in deep-sea biology. Blanford Press. London. McBride, J. R. and D. R. Ilder, E. E. Jones and M. Tomlinson. 1962. Olfactory perception in juvenile salmon. I. Observations on response of juvenile sockeye to extracts of food. J . Fish. Res. Board Can. 19: 327-334. 1 48 McFarland, W. N. 1971. Cetacean vis u a l pigments. Vision Res. 11: 1065-1076. McFarland, W. N. and D. M. Al l e n . 1977. The effect of e x t r i n s i c factors on the two d i s t i n c t i v e rhodopsin-porphyropsin systems. Can. J. Zool. 55: 1000-1009. Muntz, W. R. A. 1971. Sensory processes and behaviour, p. 31-76 . I__n J. L. McGaugh (ed.). Psychobiology. Academic Press. New York. Muntz, W. R. A. 1975a. Visual pigments and the environment, p. 565-577. I_n M. A. A l i (ed.). Vision in fishes. Plenum Press. New York. Muntz, W. R. A. 1975b. Behavioural studies of vis i o n in a f i s h and possible relationships to the environment, p. 705-717. In M. A. A l i (ed.). Vision in fishes. Plenum Press. New York. Munz, F.'W. 1957. Photosensitive pigments from the retinas of deep-sea fishes. Science 125: 1142-1143. Munz, F. W. 1958. Photosensitive piments from the retinas of certain deep-sea fishes. J. Physiol. (Lond). 140: 220-225. Munz, F. W. and D. D. Beatty. 1965. A c r i t i c a l analysis of the visu a l pigments in trout and salmon. Vision Res. 5: 1-117. Muzinic, S. 1931. Der Rhythmus der Nahrungsaufnahme beim Hering. Ber.dt wiss. Kommn Meeresforsch 6: 62-64. Nelson, D. R. and S. H. Gruber. 1963. Sharks: attraction by low frequency sounds. Science 142: 975-977. Newman, M. A. 1956. Social behaviour and i n t e r s p e c i f i c competition in two trout species. Physiol. Zool. 29: 64-81 . 1 49 Nikolsky, G. V. 1963. The ecology of fishes. Academic Press. New York. Nilsson, N. A. 1967. Interactive segregation between f i s h species, p. 295^313. In S. D. Gerking (ed. ). The b i o l o g i c a l basis of freshwater f i s h production. Blackwell S c i e n t i f i c Publications. Oxford. Northcote, T. G. and R. Clarotto. 1975. Limnetic macrozooplankton and f i s h predation in some coastal B r i t i s h Columbia lakes. Verh. Internat. Verein. Limnol. 19: 1593-1598. Northmore, D. P. M. and W. R. A. Muntz. 1974. Effects of stimulus size on spectral s e n s i t i v i t y in a f i s h (Scardinius erythrophthalmus) measured with a c l a s s i c a l conditioning paradigm. Vision Res. 14: 503-514. Northmore, D. P. M. and D. Yager. 1975. Psycophysical methods for investigation of vision in fishes, p. 689-704. In M. A. A l i (ed.). Vision in fishes. Plenum Press. New York. O'Brien, W. J., N. A. Slade and G. L. Vinyard. 1976. Apparent size as the determinant of prey selection by b l u e g i l l sunfish (Lepomis macrochirus). Ecology 57: 1304-1310. O'Connell, C. P. 1963. The structure of the eye of Sardinops caerulea, Engraulis mordax and four other pelagic marine tele o s t s . J. Morph. 113: 287-330. Park, T. 1962. Beetles, competition and populations. Science 138:1369-1375. Pearson, W. H. and S. E. M i l l e r . 1980. Chemoreception in the food searching and feeding behavior of the red hake, Urophycis chuss (Walbaum). J. Exp. Mar. B i o l . 48: 139-150. Pirenne, M. H. 1956. Physiological mechanisms of vi s i o n and the quantum nature of l i g h t . B i o l . Rev. 31: 194-241. 150 Prazdnikova, N. V. 1969. P e c u l i a r i t i e s of the d i s t i n c t i o n of visua l images by f i s h , from Behaviour and reception in f i s h (1967), trans. R. M. Howland. Bureau of Sports Fisheries and W i l d l i f e . Washington, D.C. Ramsay, J. A. 1966. The experimental basis of modern biology. Cambridge University Press. Cambridge. 339 p. Rosenau, M. L. 1978. Int e r s p e c i f i c aggression in Dolly Varden char (Salvelinus malma) and coastal cutthroat trout (Salmo  c l a r k i clarki ) T~B.Sc. Thesis. University of B r i t i s h Columbia. 45 p. Ryder, J. A. 1885. An arrangement of the r e t i n a l c e l l s in the eyes of fishes p a r t i a l l y simulating compound eyes. Proc. Acad. Natl. S c i . U.S.A. 161-166. Ryder, R. A. 1977. Effects of ambient l i g h t variations on the behaviour of yearling, subadult and adult walleye (Stizostedion vitreum vitreum). J. Fish. Res. Board Can. 34: 1481-1491. Saxena, A. 1966. Lernkapacitat, Gedachtnis und Transpositions-vermogen bei Forellen. Zool. Jahresber., Abt. A l l g . Zool. Physiol. Tierre 69: 63-94. Scharma, S. C. 1975. Development of the optic tectum in brown trout, p. 411-418. I_n M. A. A l i (ed.). Vision in fishes. Plenum Press. New York. Scherer, E. 1975. Over-head l i g h t intensity and v e r t i c a l positioning of walleye, St izostedion vitreum vi treum. J. Fish. Res. Board Can. 33: 289-292. Schutz, D. C. 1969. An experimental study of feeding behaviour and interactions in coastal cutthroat trout (Salmo c l a r k i  c l a r k i ) and Dolly Varden (Salvelinus malma). M.Sc. Thesis. University of B r i t i s h Columbia. 81 p. Schutz, D. C. and T. G. Northcote. 1972. An experimental study of feeding behaviour and interaction in coastal cutthroat trout (Salmo c l a r k i c l a r k i ) and Dolly Varden (Salvelinus malma). J . Fish Res. Board Can. 29: 555-565. 151 Schwanzara, S. A. 1967. The vi s u a l pigments of freshwater fishes. Vision Res. 7: 121-148. Tamura, T. 1957. A study of vi s u a l perception in f i s h , e s pecially on resolving power and accomodation. B u l l . Jap. Soc. S c i . Fish. 22: 536-557. Tamura, T. and W. J. Wisby. 1963. The visual sense of pelagic fishes especially the visu a l axis and accomodation. B u l l , of Mar. S c i . of the Gulf and Caribbean. 13: 433-448. Tester, A. L. 1963. The role of o l f a c t i o n in shark predation. Pac. S c i . 17: 145-170. Tsin, A. T. C. 1979. The vi s u a l pigment composition of rainbow trout. Vinyard, G. L. and W. J. O'Brien. 1975. Dorsal l i g h t response as an index of prey preference in b l u e g i l l (Lepomis macrochirus). J. Fish Res. Board Can. 32: 1860-1863. Vinyard, G. L. and W. J. O'Brien. 1976. Effect of l i g h t and tu r b i d i t y on the reactive distance of b l u e g i l l (Lepomis macrochirus). J. Fish . Res. Board Can. 33: 2845-2849. Volkova, L. A. 1973. The effect of l i g h t intensity on the a v a i l a b i l i t y of food organisms to some fishes in Lake Baikal. J. of Ichthyology 13: 591-602. Volterra, V. 1926. Variations and fluxuations of the number of individuals of animal species l i v i n g together, p. 409-448. In R. N. Chapman (ed.). Animal ecology. McGraw-Hill Co. New York. Wagner, H.-J. 1972. Vergliechende Untersuchungenuber das Muster der Sehzellen und Horizontalen in der Teleostier-Retina (Pisces) . Z. Morphol. Tierre 72: 77-130. Wagner, H.-J. 1974. Die Entwicklung der Netzhaut von Nannacara  anomala (Cichlidae: Teleostei) mit besonderer Berucksichtigung regionaler Differenzierungsunterschiede. Z. Morphol. Tierre 79: 113-131. 152 Wagner, H.-J. 1978. C e l l types and connectivity patterns in mosaic retinas. Adv. Anat. Embr. and C e l l B i o l . 55. Walls, G. L. 1942. The vertebrate eye and i t s adaptive radiation. Cranbrook Institute of Science. Bloomfield H i l l s , Michigan. 948 p. Ware, D. M. 1971. The predatory behaviour of rainbow trout (Salmo gairdneri). Ph.D. Thesis. University of B r i t i s h Columbia. 151 p. Ware, D. M. 1972. Predation by rainbow trout (Salmo gaird n e r i ) : the influence of hunger , prey density and prey s i z e . J. Fish. Res. Board Can. 29: 1193-1201. Werner, E. E. and D. J. H a l l . 1974. Optimal foraging and the size selection of prey by the b l u e g i l l sunfish. Ecol. 55: 1042-1052. Westlake, D. F. 1965. Some problems in the measurement of radiation underwater. Photochem. Photobiol. 4: 849-868. Willmer, E. N. 1953. Determining factors in the evolution of the retina in vertebrates. Symp.Soc. Exp. B i o l . 7: 377-394. Woodhead, P. M. J. 1966. The behaviour of f i s h in r e l a t i o n to l i g h t in the sea. Oceanogr. Mar. B i o l . Ann. Rev. 4: 337-403. Yager, D. 1967. Behavioural measures and theoretical analysis of spectral s e n s i t i v i t y and spectral saturation in the g o l d f i s h . Vision Res. 7: 707-727. Young, J. E. 1974. Spectral composition of l i g h t and growth of higher plants, p. 134-159. In R. Brainbridge, G. L. Evans and 0. Rackham (eds.). Light as an ecological factor. Blackwell S c i e n t i f i c Press. London. Zaret, T. M. and W. C. Kerfoot. 1975. Fish predation on Bosmina  l o n q i r o s t r i s : body size selection versus v i s i b i l i t y s e lection. Ecol. 56: 233-237. 

Cite

Citation Scheme:

        

Citations by CSL (citeproc-js)

Usage Statistics

Share

Embed

Customize your widget with the following options, then copy and paste the code below into the HTML of your page to embed this item in your website.
                        
                            <div id="ubcOpenCollectionsWidgetDisplay">
                            <script id="ubcOpenCollectionsWidget"
                            src="{[{embed.src}]}"
                            data-item="{[{embed.item}]}"
                            data-collection="{[{embed.collection}]}"
                            data-metadata="{[{embed.showMetadata}]}"
                            data-width="{[{embed.width}]}"
                            data-media="{[{embed.selectedMedia}]}"
                            async >
                            </script>
                            </div>
                        
                    
IIIF logo Our image viewer uses the IIIF 2.0 standard. To load this item in other compatible viewers, use this url:
https://iiif.library.ubc.ca/presentation/dsp.831.1-0094968/manifest

Comment

Related Items