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Pattern learning and spatial memory in rufous hummingbirds (Selasphorus rufus) McIntyre, Gordon D. 1995

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PATTERN LEARNING AND SPATIAL MEMORY IN RUFOUS HUMMINGBIRDS (Selasphorus rufus) by Gordon D. M c l n t y r e B . S c , U n i v e r s i t y of B r i t i s h Columbia Vancouver, B.C. 1980 A THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF SCIENCE i n THE FACULTY OF GRADUATE STUDIES (Department o f Zoology) We a c c e p t t h i s t h e s i s as c o n f o r m i n g t o t h e r e q u i r e d s t a n d a r d THE UNIVERSITY OF BRITISH COLUMBIA FEBRUARY 1995 © GORDON D. MCINTYRE, 1995 In presenting this thesis in partial fulfilment of the requirements for an advanced degree at the University of British Columbia, I agree that the Library shall make it freely available for reference and study. I further agree that permission for extensive copying of this thesis for scholarly purposes may be granted by the head of my department or by his or her representatives. It is understood that copying or publication of this thesis for financial gain shall not be allowed without my written permission. Department of 2°<M-OGy-< tg^^/tH? "S7iJ2>'&$ The University of British Columbia Vancouver, Canada Date DE-6 (2/88) Abstract I n t h i s s t u d y I examined s p a t i a l l e a r n i n g and memory i n r u f o u s hummingbirds. I n l a b o r a t o r y e x p e r i m e n t s , hummingbirds r a p i d l y l e a r n e d 2 - d i m e n s i o n a l p a t t e r n s o f r e w ards. They used landmarks t o f i n d reward s i t e s . Once b i r d s were v i s i t i n g most f e e d e r s i n r e w a r d i n g a r e a s and a v o i d i n g most f e e d e r s i n non-rewarding a r e a s , t h e y p e r s i s t e d i n t h e same a r e a s a f t e r t h e i r p r o f i t a b i l i t i e s were r e v e r s e d . T h i s i s s t r o n g e v i d e n c e f o r c o g n i t i v e mapping. P e r s i s t e n c e s u b s i d e d r a p i d l y once the b i r d s ' b e h a v i o u r was no l o n g e r a p p l i c a b l e , f o l l o w e d r a p i d l y by l e a r n i n g t h e a l t e r e d r e w a r d p a t t e r n s . The t y p e s of landmark i n f o r m a t i o n I p r o v i d e d s i g n i f i c a n t l y i n f l u e n c e d b o t h the r a t e and p e r s i s t e n c e o f l e a r n i n g . Hummingbirds l e a r n e d more r a p i d l y u s i n g edge landmarks t h a n c e n t r a l landmarks. They a l s o u sed c o l o u r i n f o r m a t i o n about reward q u a l i t y embedded i n b o t h k i n d s o f m arkers, a l t h o u g h t h i s was not a s t r o n g b e n e f i t t o l e a r n i n g . I n one e xperiment, hummingbirds l e a r n e d b o t h s p a t i a l memory t a s k s and s p a t i a l a s s o c i a t i o n s . They l e a r n e d s p a t i a l a s s o c i a t i o n s more r a p i d l y t h a n s p a t i a l memory t a s k s , a c h i e v i n g a h i g h r a t e o f performance a f t e r a v e r y s h o r t t i m e i n t e r v a l . A l t h o u g h s p a t i a l memory t a s k s r e q u i r e d a s l i g h t l y l o n g e r l e a r n i n g p e r i o d , the b i r d s ' p e r formance was e v e n t u a l l y comparable t o t h a t on s p a t i a l a s s o c i a t i o n t a s k s . The speed of forming s p a t i a l a s s o c i a t i o n s between cue and reward s i t e s depended s t r o n g l y on the d i s t a n c e between them, altho u g h hummingbirds e v e n t u a l l y achieved comparable performance r e g a r d l e s s of s e p a r a t i o n . B i r d s were more r e s i s t a n t to change on s p a t i a l memory tasks than s p a t i a l a s s o c i a t i o n t a s k s . G r e a t e r s e p a r a t i o n s between cue and reward r e s u l t e d i n more r e l i a n c e on s p a t i a l memory and g r e a t e r p e r s i s t e n c e of these memories i n the f a c e of change. Time spent f o r a g i n g on rewarding p a t t e r n s a f f e c t e d the b i r d s ' p e r s i s t e n c e when the p a t t e r n changed. A f t e r l o n g e r experience of s u c c e s s f u l l y u s i n g a p a t t e r n of fe e d e r s , b i r d s p e r s i s t e d longer i n f o r m e r l y rewarding be h a v i o u r s . Time spent u s i n g a p a t t e r n of fee d e r s i n f l u e n c e d s p a t i a l memory tasks much more than s p a t i a l a s s o c i a t i o n ones. Table of Contents A b s t r a c t i i T a b l e o f C o n t e n t s i v L i s t o f T a b l e s v i i L i s t o f F i g u r e s v i i i Acknowledgements x Chapter 1 . G e n e r a l I n t r o d u c t i o n 1 T a c t i c s o f S u r v i v a l 1 L e a r n i n g 1 Components o f L e a r n i n g 2 Memory 4 S p a t i a l Memory 7 R o l e o f L e a r n i n g i n S p a t i a l Memory 9 C o g n i t i v e Maps 11 Cues and Landmarks 13 Cues 15 Landmarks 16 R o l e o f Cues and Landmarks i n L e a r n i n g 17 O u t l i n e o f S t u d i e s 18 Chapter 2 . P a t t e r n L e a r n i n g and P e r s i s t e n c e o f S p a t i a l Memory i n Rufous Hummingbirds 19 S e c t i o n I . I n t r o d u c t i o n 19 L e a r n i n g 19 Advantages o f L e a r n i n g 2 0 D i s a d v a n t a g e s o f L e a r n i n g 21 A l t e r n a t i v e s t o l e a r n i n g 21 Complex environments 22 M a t h e m a t i c a l m o d e l l i n g 23 P e r c e p t i o n o f t h e environment 25 E x p e r i m e n t a l p r o t o c o l s 27 C u r r e n t s t u d y 2 8 S e c t i o n I I . M a t e r i a l s and Methods 3 0 S u b j e c t s 30 E x p e r i m e n t a l Environment 30 T r a i n i n g 32 E x p e r i m e n t a l P r o c e dures 33 S e c t i o n I I I . R e s u l t s 37 I n i t i a l Performance 37 D u r a t i o n of Exposure and P a t t e r n R e v e r s a l s 40 V i s i t a t i o n P a t t e r n s 45 S e c t i o n IV. D i s c u s s i o n 53 Advantages o f L e a r n i n g 53 i v F a c t o r s A f f e c t i n g L e a r n i n g 53 Cues 53 S e a r c h Techniques 54 S t a b i l i t y 56 C o s t s o f L e a r n i n g . . . 57 Samp l i n g 57 Change 58 E x p e c t a t i o n s and P e r s i s t e n c e 59 R e l e a r n i n g A f t e r a Change 62 C o n c l u s i o n s 63 Chapter 3 . Landmark Forms and S p a t i a l Memory i n Rufous Hummingbirds 64 S e c t i o n I . I n t r o d u c t i o n 64 S p a t i a l Memory 64 Cues and Landmarks 64 Cues 65 Landmarks 66 R o l e o f Cues and Landmarks i n L e a r n i n g 66 C u r r e n t Study 67 S e c t i o n I I . M a t e r i a l s and Methods 69 S u b j e c t s . . . 69 E x p e r i m e n t a l Environment 69 E x p e r i m e n t a l D e s i g n 71 T r a i n i n g 7 5 E x p e r i m e n t a l Procedures 7 6 S e c t i o n I I I . R e s u l t s 79 Performance I n d i c a t o r s 7 9 I n i t i a l L e a r n i n g 79 D i f f e r e n c e s Between Treatments 83 S w i t c h E f f e c t 89 V i s i t a t i o n P a t t e r n s 90 S e c t i o n IV. D i s c u s s i o n 93 Use o f A r r a y Markers 93 L i n e s v e r s u s C e n t r e s 93 L i n e s v e r s u s C o l o u r s 95 C o g n i t i v e Maps 96 Chunking 98 E n v i r o n m e n t a l Change, C o m p l e x i t y and t h e S w i t c h E f f e c t . . 99 C o n c l u s i o n s 103 Chapter 4 . S p a t i a l A s s o c i a t i o n and S p a t i a l Memory i n Rufous Hummingbirds 105 S e c t i o n I . I n t r o d u c t i o n 105 S p a t i a l A s s o c i a t i o n L e a r n i n g 105 S p a t i a l Memory 107 L e a r n i n g P r o c e s s e s 107 D i f f e r e n c e s i n L e a r n i n g 109 v Advantages and Di s a d v a n t a g e s 110 U n c e r t a i n t y and P e r c e p t i o n I l l C u r r e n t Study 113 S e c t i o n I I . M a t e r i a l s and Methods 116 S u b j e c t s 116 E x p e r i m e n t a l Environment 117 T r a i n i n g 118 E x p e r i m e n t a l Procedures 119 S e c t i o n I I I . R e s u l t s 121 I n i t i a l L e a r n i n g 121 S w i t c h E f f e c t 123 Time, D i s t a n c e , and t h e I n t e r a c t i o n E f f e c t 123 D i f f e r e n c e s i n P e r s i s t e n c e 125 S e c t i o n IV. D i s c u s s i o n 128 A s s o c i a t i o n , S p a t i a l A s s o c i a t i o n and S p a t i a l Memory.... 129 Cue D i s t a n c e 129 D u r a t i o n o f Exposure 132 Advantages and Disadvantages 132 Memory Load 137 C o n c l u s i o n s 139 Chapter 5. G e n e r a l D i s c u s s i o n 141 What C o n d i t i o n s Produce L e a r n i n g ? 141 How i s L e a r n i n g R e v e a l e d i n Performance? 142 What i s Lea r n e d about t h e i r Environments and How? 143 P a t t e r n L e a r n i n g : 143 Chunking 144 S p a t i a l Memory........ 146 C o g n i t i v e Maps 146 Landmarks and Cues 147 Ex p e c t a n c y and P e r s i s t e n c e 149 F u t u r e S t u d i e s 151 L i t e r a t u r e C i t e d 155 v i L i s t of Tables C h a p t e r 2 T a b l e 1. R e g r e s s i o n a n a l y s i s of c o r r e c t v i s i t s v e r s u s t r i a l number f o r each o f the t r e a t m e n t s 37 T a b l e 2. R e g r e s s i o n a n a l y s i s o f i n i t i a l p e r f o r m a n c e v e r s u s n a t u r a l l o g o f t r i a l 40 T a b l e 3. Comparison of performance b e f o r e and a f t e r t h e s w i t c h 42 T a b l e 4. Comparison o f t o t a l v i s i t s b e f o r e and a f t e r t h e s w i t c h 42 T a b l e 5. Comparison o f t o t a l c o r r e c t v i s i t s b e f o r e and a f t e r t h e s w i t c h 42 T a b l e 6. R e g r e s s i o n a n a l y s i s o f improvement i n p o s t - s w i t c h performance u s i n g b o t h performance i n d i c a t o r s 43 C h a p t e r 3 T a b l e 7. L i n e a r r e g r e s s i o n s of t o t a l c o r r e c t f i r s t v i s i t s on t r i a l number f o r the f i r s t 50 t r i a l s 83 T a b l e 8. L i n e a r r e g r e s s i o n s of p r o p o r t i o n o f c o r r e c t f i r s t v i s i t s on t h e n a t u r a l l o g o f t r i a l number f o r t h e f i r s t 50 t r i a l s 84 T a b l e 9. L i n e a r r e g r e s s i o n s o f t o t a l i n c o r r e c t f i r s t v i s i t s on t h e n a t u r a l l o g of t r i a l number f o r t h e f i r s t 50 t r i a l s 84 T a b l e 10. Ranked means of t r e a t m e n t s from Tukey a n a l y s i s . 8 8 T a b l e 11. L i n e a r r e g r e s s i o n s of t o t a l i n c o r r e c t f i r s t v i s i t s on t h e n a t u r a l l o g o f t r i a l number f o r t h e 10 t r i a l s a f t e r t h e s w i t c h 90 T a b l e 12. L i n e a r r e g r e s s i o n s o f p r o p o r t i o n c o r r e c t on t h e n a t u r a l l o g o f t r i a l number f o r t h e 10 t r i a l s a f t e r t h e s w i t c h 91 C h a p t e r 4 T a b l e 13. D i f f e r e n c e s between average p r o p o r t i o n c o r r e c t and random v i s i t a t i o n f o r a l l t r e a t m e n t s i n t h e f i r s t 10 m i n u tes o f e x p e r i m e n t a l runs 121 T a b l e 14. P o s t - s w i t c h performance o f b i r d s i n t h e d i f f e r e n t t r e a t m e n t s 125 v i i L i s t of Figures C h a p t e r 2 F i g u r e 1. S t y l i z e d r e p r e s e n t a t i o n o f one q u a r t e r s p a t t e r n f o r t h e f e e d e r a r r a y 34 F i g u r e 2. P r o p o r t i o n of f i r s t v i s i t s p e r t r i a l t h a t were c o r r e c t (rewarding) averaged o v e r b l o c k s o f 5 t r i a l s and a l l b i r d s i n each tr e a t m e n t f o r each o f t h e 4 t r e a t m e n t s 38 F i g u r e 3. Number o f c o r r e c t v i s i t s p e r t r i a l ( a v eraged o v e r b l o c k s o f 5 t r i a l s and a l l b i r d s i n each t r e a t m e n t ) f o r each o f t h e 4 t r e a t m e n t s . 3 9 F i g u r e 4. Average number of i n c o r r e c t v i s i t s f o r each o f th e 4 . exposure t r e a t m e n t s 41 F i g u r e 5. Average number o f i n c o r r e c t v i s i t s by b i r d s f o r each o f t h e t r e a t m e n t s i n the 5 t r i a l s i m m e d i a t e l y f o l l o w i n g t h e p a t t e r n r e v e r s a l 44 F i g u r e 6. D i f f e r e n c e s i n number o f i n c o r r e c t v i s i t s ( e r r o r s ) by b i r d s i n each o f t h e t r e a t m e n t s i n t h e p e r i o d f o l l o w i n g t h e p a t t e r n r e v e r s a l 46 F i g u r e 7. T o t a l o f a l l v i s i t s t o each f e e d e r ( a l l b i r d s on a l l t r e a t m e n t s , b e f o r e and a f t e r s w i t c h ) 48 F i g u r e 8.'. T o t a l of a l l v i s i t s t o each f e e d e r i n t h e f i r s t 10 t r i a l s ( a l l b i r d s on a l l t r e a t m e n t s , b e f o r e and a f t e r s w i t c h ) 49 F i g u r e 9. Sample v i s i t t r a j e c t o r i e s o f 6 d i f f e r e n t b i r d s on t h e i r f i r s t 10 v i s i t s of T r i a l 1 51 F i g u r e 10. Sample t r a j e c t o r i e s f o r one b i r d on t h e f i r s t 10 v i s i t s o f T r i a l s 1 - 6 52 C h a p t e r 3 F i g u r e 11. S t y l i z e d r e p r e s e n t a t i o n s o f t h e a r r a y markers used f o r t h e e i g h t t r e a t m e n t s d e s c r i b e d i n t h e t e x t . . 7 2 F i g u r e 12. T o t a l c o r r e c t v i s i t s p e r t r i a l ( averaged a c r o s s a l l b i r d s i n each tr e a t m e n t and a c r o s s b l o c k s o f 10 t r i a l s ) f o r a l l t r e a t m e n t s 80 F i g u r e 13. Number o f i n c o r r e c t f i r s t v i s i t s p e r t r i a l a v e r a g e d f o r a l l b i r d s i n each o f t h e 8 t r e a t m e n t s . . . 81 F i g u r e 14. P r o p o r t i o n o f f i r s t v i s i t s p e r t r i a l t h a t were t o r e w a r d i n g f e e d e r s , averaged f o r a l l b i r d s i n each o f th e 8 t r e a t m e n t s 82 F i g u r e 15. Summary o f Tukey a n a l y s i s o f t o t a l i n c o r r e c t f i r s t v i s i t s p e r t r i a l averaged f o r a l l b i r d s i n each o f t h e 8 t r e a t m e n t s 86 F i g u r e 16. Summary o f Tukey a n a l y s i s o f p r o p o r t i o n o f f i r s t v i s i t s t h a t were c o r r e c t p e r t r i a l , a v e r a g e d f o r a l l b i r d s i n each o f the 8 t r e a t m e n t s 87 v i i i Figure 17. Total v i s i t s by a l l birds to non-rewarding locations i n t r i a l s 46 - 50 of a l l treatments 92 Chapter 4 Figure 18. Percent of v i s i t s that were to the correct feeder for each of the 9 treatments 122 Figure 19. Box plots of number of v i s i t s by birds to the formerly good feeder aft e r the feeder switch 124 Figure 20. Tukey honestly s i g n i f i c a n t difference analysis of differences i n mean post-switch foraging success. 127 ix Acknowledgment 8 I would esp e c i a l l y l i k e to thank my advisor, Lee Gass, for his support and encouragement during my thesis work. My research committee, Don Ludwig, Jamie Smith and Don Wilkie also provided sound advice and a great deal of patience throughout t h i s study. Many people provided technical support and assistance that greatly eased the pains of doing t h i s research. They a l l deserve my thanks. Don Brandys and Tony Lum puzzled with me over numerous e l e c t r i c a l design questions. G r a n v i l l e Williams went beyond the c a l l of duty i n producing cages and other materials for my experiments and maintenance of the b i r d s . Charles Mathieson and A l a s t a i r Blatchford were fountains of computer programming knowledge. Chris Harvey Clark, Arthur Vanderhorst, and Armin Tepper helped us through numerous d i f f i c u l t i e s with animal care. My fellow s t a f f members i n the Science Department of Vancouver Community College always provided encouragement and support. B i l l Milsom allowed us to borrow lab equipment at 1:00 a.m. and probably saved several birds' l i v e s as a r e s u l t . Very special thanks go to my labmates and fellow veterans, Mark Roberts and Gayle (one of these days I ' l l get your .name right) Brown for t h e i r friendship, help and support throughout my work. The rapport between us kept us at least somewhat sane. I reserve my f i n a l thank-yous for my family. My fiancee Lorraine, my mother Brenda, my brother John, and my other family and friends provided the moral support (and occasional needed nagging) that kept me going. This research was p a r t i a l l y funded by an operating grant (NSERC) to Lee Gass. x Chapter 1 . General Introduction Tactics of Survival Animals must carry out a number of tasks i n t h e i r everyday existence i n order to ensure t h e i r s u r v i v a l and reproduction. These include finding food, shelter and mates and avoiding predators. For s o c i a l animals, finding ways to coexist with t h e i r compatriots i s another important task. Foraging has been extensively studied (see review by Schoener, 1987) perhaps because i t i s easy to quantify i n an experimental setting. Learning Learning i s an important aid to s u r v i v a l . It i s a change i n an animal, as a result of experience, that can a l t e r the animal's behaviour i n given circumstances (Hintzman, 1978). Examples of learning range from nudibranchs learning to avoid e l e c t r i c shock to humans learning new languages. Generally, learning can be divided into two broad categories: non-associative and a s s o c i a t i v e . Non-associative learning i s the simple habituation or s e n s i t i z a t i o n to a stimulus, such as i n the nudibranch 1 General Introduction example (Raven and Johnson, 1989). A s s o c i a t i v e l e a r n i n g i s th e development o f an a s s o c i a t i o n between two s t i m u l i o r between a s t i m u l u s and response. Most examples o f complex l e a r n i n g s uch as language a c q u i s i t i o n , s p a t i a l n a v i g a t i o n , f o r a g i n g and o t h e r s a r e a s s o c i a t i v e . There a r e a number o f t h e o r i e s about l e a r n i n g p r o c e s s e s . Two dominant s c h o o l s o f thought a r e b e h a v i o u r i s m and c o g n i t i v i s m . B e h a v i o u r i s t s b e l i e v e t h a t l e a r n i n g s h o u l d be d i s c u s s e d i n terms o f o b s e r v a b l e b e h a v i o u r s (Hintzman, 1978). E s s e n t i a l l y , t hey t r e a t a n i m a l s as b l a c k boxes. The i n t e r n a l p r o c e s s e s i n v o l v e d i n l e a r n i n g a t a s k a r e e i t h e r c o n s i d e r e d u n i m p o r t a n t , because they a r e u n o b s e r v a b l e , by some members o f t h i s group, o r a r e c o n s i d e r e d m e c h a n i s t i c a l l y by o t h e r workers who t a k e a s i m i l a r a p p r o a c h t o t h e b e h a v i o u r i s t s . A second s c h o o l o f thought c o n s i d e r s b e h a v i o u r i n h u m a n i s t i c terms and t r e a t s t h e p r o c e s s e s o f a n i m a l l e a r n i n g as i f they were e q u i v a l e n t t o t h e thought p r o c e s s e s found i n humans. T h i s group i s i n t e r e s t e d i n me n t a l e v e n t s l i k e i d e a s , thoughts and purposes (Hintzman, 1978) . I n my view, n e i t h e r approach o f f e r s t h e s o l e t r u t h about l e a r n i n g and b o t h o f f e r v a l u a b l e i n s i g h t s i n t o t h e p r o c e s s e s i n v o l v e d . Components of Learning Perhaps t h e most b a s i c i d e a i n a s s o c i a t i v e l e a r n i n g i s th e l i n k a g e between s t i m u l u s and re s p o n s e . An a n i m a l r e p e a t e d l y p r e s e n t e d w i t h a s t i m u l u s , each t i m e f o l l o w e d 2 General Introduction c l o s e l y by a reward on completion of a s p e c i f i c response, w i l l l i n k the items together into a stimulus-response association (Damianopoulos, 1989). One requirement for t h i s association to be made i s that the stimulus and r e i n f o r c e r be c l o s e l y linked i n space and time. Either temporal or s p a t i a l separation between the reward and stimulus weaken the a b i l i t y of the animal to associate the items (Gibbon et al., 1988; Pinel et al., 1986). In a few cases, however, i t has been possible to demonstrate learning i n the absence of reinforcement. In some cases the mere contiguity of stimulus and response can create a learned association between the two (Hintzman, 1978). In most cases, though, reinforcement i s an important element of formation of the stimulus-response association. This l i n k i n g of stimulus and response i s affected by the frequency and value of the reinforcement: Low value rewards, infrequent rewards or variable rewards can reduce the speed and degree of learning (Gibbon et al., 1988; Morris and Capaldie, 1979). C o g n i t i v i s t s assume that animals carry out actions that y i e l d rewards or avoid punishment due to internal motivation or the i n t r i n s i c value of the stimulus to the animal (Gleitman, 1974) . Behaviourists attempt to deal only with observable behaviours, either ignoring motivation, or acknowledging i t s existence but treating i t mechanistically. 3 General Introduction Another aspect that involves and af f e c t s motivation i s the expectancy of an event occurring. This concept has been promoted by the cognitive school (Hintzman, 1978). These workers propose that animals develop expectations about rewards and future events based on past experience. None of these behavioural processes can occur, however, without the a b i l i t y to use past experience through memory. Memory "Memory" refers to processes through which experiences and learning are retained over time (Hintzman, 1978; Goelet et al., 1986), and we are just beginning to understand them. At least three d i f f e r e n t types of memory have been suggested, based on d u r a b i l i t y of the memory. The least durable of these i s working memory that i s used during a task. S l i g h t l y more permanent i s short term memory, that l a s t s beyond the task at hand but which i s s t i l l measured i n minutes or hours. F i n a l l y , long term memory can p e r s i s t for days or throughout an animal's l i f e t i m e . Working memory i s used i n the extreme short term. Generally, the difference between working memory and short term memory i s not well understood. Some authors tend to doubt i t s existence as a separate form of memory from short term memory (van L u i j t e l a a r et al., 1989). The two may or may not be d i s t i n c t processes with d i f f e r i n g p h y s i o l o g i c a l bases, but workers agree the purpose of working memory i s to re t a i n only those elements of experience necessary to 4 General Introduction a c c o m p l i s h t h e immediate t a s k a t hand. These memories a r e "throwaways M (Maki, 1987) t h a t a r e a c q u i r e d q u i c k l y , used i m m e d i a t e l y and f o r g o t t e n . S h o r t t e rm memory i n c l u d e s t h o s e i t e m s w h i c h an a n i m a l may need t o r e c a l l beyond t h e immediate t a s k but w h i c h a r e not r e t a i n e d i n d e f i n i t e l y . T h i s form o f memory seems t o i n v o l v e c o v a l e n t m o d i f i c a t i o n s o f e x i s t i n g p r o t e i n s t h a t r e g u l a t e t h e a c t i v i t i e s o f the neurons and t h e i r synapses. (Barnes, 1988; G o e l e t et al., 1986). Long term memory i n c l u d e s e v e r y t h i n g r e t a i n e d i n d e f i n i t e l y . These memories a l s o i n v o l v e p r o t e i n s , but t h r o u g h m o d i f i c a t i o n of t h e e x p r e s s i o n o f s p e c i f i c genes i n neurons ( G o e l e t e t al., 1986; M a t t h i e s , 1989; Thompson, 1986) . I f l o n g term memory r e q u i r e s g e n e r a t i o n o f new p r o t e i n s , l o n g t e rm memories s h o u l d d e v e l o p more s l o w l y t h a n w o r k i n g o r s h o r t term memory. The d i f f e r e n c e between s h o r t and l o n g term memory i s i n some ways analogous t o t h e d i f f e r e n c e between hormone t y p e s . I n t h i s c a s e , s h o r t term memory i s s t o r e d i n a r f a s h i o n s i m i l a r t o p r o t e i n based hormones such as a d r e n a l i n . B o t h p r o v i d e immediate responses t h a t a r e s h o r t l i v e d . Long term memory i s s t o r e d i n a f a s h i o n s i m i l a r t o s t e r o i d hormones l i k e t e s t o s t e r o n e . Here t h e e f f e c t s t a k e l o n g e r t o d e v e l o p but can s u r v i v e i n d e f i n i t e l y . W i c k e l g r e n (197 9) s u g g ested t h a t t h e hi p p o c a m p a l , l i m b i c a r o u s a l system p l a y s a key r o l e i n t r a n s f e r r i n g i t e m s 5 General Introduction from w o r k i n g memory t o l o n g term memory by i s o l a t i n g t h e a l t e r e d neurons from c o n t i n u i n g i n p u t s w h i l e c e l l u l a r s t r u c t u r e s h i f t s d u r i n g c r e a t i o n o f l o n g t erm memories. W h i l e some workers have suggested m u l t i p l e forms o f w o r k i n g memory, i n c l u d i n g a form used s o l e l y f o r remembrance of s p a t i a l r e l a t i o n s h i p s , ( G a l l i s t e l , 1990; I n u i , 1988; R o b e r t s , 1988), o t h e r s suggest t h a t t h e r e i s no e v i d e n c e f o r m u l t i p l e forms o f w o r k i n g memory, and t h a t b o t h s p a t i a l and n o n - s p a t i a l l e a r n i n g o c c u r by s i m i l a r p r o c e s s e s i n t h e v e r y s h o r t t e rm (Ennaceur and M e l i a n i , 1992). I n t h e l o n g term, however, t h e r e do seem t o be d i f f e r e n c e s . F o r example, Nadel and W i l l n e r (1980) s u g g e s t e d t h a t some a s p e c t s of s p a t i a l memory can be used v i a s h o r t term o r w o r k i n g memory but a c o g n i t i v e map o f an a n i m a l ' s s u r r o u n d i n g s i s too l a r g e f o r s h o r t t e r m s t o r a g e and s p a t i a l r e f e r e n c e t o a c o g n i t i v e map i s f u n d a m e n t a l l y d i f f e r e n t from use of cues. I t s h o u l d be remembered, however, t h a t a n i m a l s a t t e n d t o many senses a t once, a l l o f w h i c h i n v o l v e a t l e a s t s l i g h t l y d i f f e r e n t s e n s o r s , pathways, n e u r a l p r o c e s s i n g mechanisms and s t o r a g e s i t e s , so t h a t a t l e a s t s e v e r a l o v e r l a p p i n g b r a i n a r e a s w i l l be i n v o l v e d i n most l e a r n i n g t a s k s and memories a r e u n l i k e l y t o be e n t i r e l y i s o l a t e d from each o t h e r i n s i n g l e l o c a t i o n s i n t h e b r a i n ( S q u i r e , 1986). Many groups o f advanced a n i m a l s , i n c l u d i n g b i r d s and humans, may share many o f t h e same o r s i m i l a r n e u r a l s t r u c t u r e s and f u n c t i o n s (Bingman e t al., 1989; 6 General Introduction G r i f f i n , 1976; MacPhail, 1982; Olton, 1985). Species differences may be important (MacPhail, 1982), such as l a t e r a l i z a t i o n of s p a t i a l memory i n food storing birds (Clayton, 1993; Clayton and Krebs, 1993 and 1994) and possibly humans (de Renzio, 1982), or v a r i a t i o n i n r e l a t i v e hippocampal size coupled with v a r i a t i o n i n re l i a n c e on s p a t i a l memory (Sherry and Vaccarino, 1989; Sherry et a l . , 1989), but there i s general agreement that the basic p r i n c i p l e s are widely applicable. Spatial Memory "Spatial memory" refers to the processes by which animals remember locations i n th e i r environment. Growing numbers of species are known to use s p a t i a l memory i n various ways. Among vertebrates for instance, female bats use s p a t i a l memory to locate t h e i r young i n colonies of several thousand pups (McCracken, 1993), monkeys use i t to locate f r u i t i n a three-dimensional jungle environment (Menzel, 1991), and f i s h locate nests and define t e r r i t o r i e s with the help of s p a t i a l memory (Warburton, 1990) . Among birds, s p a t i a l memory i s used i n both foraging and t e r r i t o r i a l i t y (Balda and Kamil, 1988; Gass and Montgomerie, 1981; Gass and Sutherland, 1985; Shettleworth, 1983), and i s f l e x i b l e enough to cope with rapidly changing conditions (Valone and Girardeau, 1993; Vander Wall, 1991; van L u i j t e l a a r et al., 1989; Wilkie, 1986b; Wilkie et al., 1981; Wunderle and Martinez, 1987; Zentall et al., 1990). 7 General Introduction Invertebrates also use s p a t i a l memory. Ants use a combination of s p a t i a l memory and olfactory cues to return to food sources or nest locations (Collett et al., 1992; Haefner and C r i s t , 1994; Holldobler, 1980). Hoverflies use s p a t i a l memory to return to an unmarked location i n mid-air (Co l l e t t and Land, 1975). Spatial memory i n honeybees i s well documented and studied. For example, they use s p a t i a l memory to return to flower patches (Wellington and Cmiralova, 1979), to f i n d the hive and to navigate within the hive (Dyer, 1991), and i t i s p l a s t i c enough to allow them to reorient to a l t e r a t i o n s of landmarks, such as may occur aft e r swarming to a new nest lo c a t i o n (Dyer, 1993). The use of s p a t i a l memory affords d i s t i n c t energetic and ecological advantages (Valone, 1991) . Modelling studies suggest that using s p a t i a l memory to forage can provide greater than a f i v e - f o l d energy advantage over completely random search and a three to f i v e - f o l d advantage over systematic searching. (Armstrong et al., 1987; Benhamou, 1994). Benhamou's studies also suggest that even animals with more li m i t e d learning a b i l i t i e s such as desert arthropods use s p a t i a l memory to gain these energetic advantages. Similar energetic advantages apply to d i f f e r e n t kinds of organisms performing similar ecological tasks such as t e r r i t o r i a l defense, nest building, and brood protection ( G a l l i s t e l , 1990; Gould and Marler, 1987; Kramer and Weary, 8 General Introduction 1991; Wolf et al., 1972). The p h y s i o l o g i c a l and e c o l o g i c a l d i f f e r e n c e s between s p e c i e s make t h e b r o a d based n a t u r e o f t h e s e advantages remarkable, and have p r o v i d e d one o f t h e c o r n e r s t o n e s o f b e h a v i o u r a l e c o l o g y (Gray, 1987; Schoener, 1987). L e a r n i n g e n a b l e s a n i m a l s t o make more e f f e c t i v e use of env i r o n m e n t s , a l t h o u g h t h e advantages o f s p a t i a l l e a r n i n g d i s a p p e a r i f i r r e g u l a r t e m p o r a l v a r i a b i l i t y i s t o o g r e a t (Bowers and Adams-Manson, 1993; N i s h i m u r a , 1994). A s i d e from t h e e n e r g e t i c and o t h e r p h y s i o l o g i c a l c o s t s o f s t o r i n g memories, i t becomes i n c r e a s i n g l y l i k e l y as t e m p o r a l v a r i a b i l i t y i n c r e a s e s t h a t the c o s t o f f o r a g i n g (or o t h e r ways o f u s i n g memories) w i l l be wasted. Role of Learning in Spatial Memory I f s p a t i a l memory i s p h y s i o l o g i c a l l y e x p e n s i v e , as most wor k e r s assume i t t o be, then s i m p l i f i c a t i o n s o f t h e p r o c e s s o f remembering and u s i n g e x p e r i e n c e s h o u l d be advantageous. E s p e c i a l l y t o t h e e x t e n t t h a t a n i m a l s can g e n e r a l i z e what t h e y l e a r n about t h e i r environments a c r o s s s i t u a t i o n s , t h e y s h o u l d be a b l e t o use t h e i r environments e f f e c t i v e l y w i t h a minimum o f s t o r e d i n f o r m a t i o n . F o r example, l e a r n i n g t h a t a l l r e d t u b u l a r f l o w e r s o f a c e r t a i n shape a r e w o r t h v i s i t i n g s h o u l d not be much more d i f f i c u l t t h a n l e a r n i n g t h a t a p a r t i c u l a r f l o w e r i s r e w a r d i n g , but c l e a r l y i t i s more u s e f u l . 9 General Introduction S e v e r a l s t u d i e s have p r o v i d e d e v i d e n c e t h a t o p e r a n t b e h a v i o u r s e l i c i t e d i n l a b o r a t o r y e n v i ronments t o demon s t r a t e t h e use o f s p a t i a l memory a r e e q u i v a l e n t t o n a t u r a l f o r a g i n g a c t i v i t i e s ( D a l l e r y and Baum, 1991; M e l l g r e n and Elsmore, 1991) . Numerous s t u d i e s have d e m o n s t r a t e d t h a t use o f s p a t i a l memory i n n a t u r e i s a t o o l t h a t i n c r e a s e s f o r a g i n g e f f i c i e n c y , t o l o c a t e dens o r h i v e s o r t o f i n d mates (Bowers and Adams-Manson, 1993; Haccou et al., 1991; Kramer and Weary, 1991; Menzel, 1991; R o b i n s o n and Dyer, 1993). The a b i l i t y t o l e a r n s p a t i a l i n f o r m a t i o n i s not u n i v e r s a l ; t h e r e a r e d i s t i n c t s p e c i e s d i f f e r e n c e s . A n i m a l s as c l o s e l y r e l a t e d as b l u e t i t s and marsh t i t s , f o r example, have g r e a t l y d i f f e r e n t s p a t i a l memory a b i l i t i e s . The marsh t i t , a f o o d s t o r i n g b i r d , has e x c e l l e n t s p a t i a l memory a b i l i t i e s , w h i l e t h e b l u e t i t , w h i c h does not cache foo d , cannot p e r f o r m s i m i l a r l e a r n i n g t a s k s . A s i m i l a r d i s p a r i t y e x i s t s between t h e c l o s e l y r e l a t e d j a y and jackdaw ( C l a y t o n and K r e b s , 1994). S i m i l a r r e s u l t s have been found i n o t h e r c o r v i d and p a r i d b i r d s p e c i e s ( B a l d a and K a m i l , 1989; S h e t t l e w o r t h and Krebs, 1986). Even i n s p a t i a l l y o r i e n t e d s p e c i e s t h e r e i s d e f i n i t e v a r i a t i o n i n t h e a b i l i t y t o use s p a t i a l memory. I n s e c t s s uch as bees, wasps and a n t s seem t o r e l y most h e a v i l y on dead r e c k o n i n g based on remembered landmarks, w i t h a v e r y l i m i t e d a b i l i t y t o g e n e r a l i z e and produce c o g n i t i v e maps o f 10 General Introduction t h e i r surroundings (Collett et al., 1992; C o l l e t t et al., 1993; Dyer, 1991; Dyer, 1993; Greggers and Menzel, 1993). Birds and mammals, on the other hand, often produce complex cognitive maps, as evidenced by t h e i r a b i l i t y to f i n d novel routes, avoid obstacles and vary t h e i r behaviour to respond to novel environmental changes (Bingman et al., 1988; C o l l e t t , 1987; E l l e n et al., 1984; Etienne et al., 1990; Gass and Sutherland, 1985; Menzel, 1973; Vander Wall, 1991) . While i t may be possible for animals to remember dead reckoning paths (a series of movement vectors) between locations, there are ways to simplify s p a t i a l memory tasks by b u i l d i n g up map-like images of the environment. Humans do t h i s regularly (Giraudo and Perauch, 1988), and i t seems l i k e l y , based on a range , of studies, that animals do also (Aadland et al., 1985; Gould, 1985; Maki et al., 1979; Nadel and Willner, 1980; O'Keefe and Conway, 1980; Tolman, 1948). Cognitive Maps A cognitive map i s an internalized representation of an animal's environment including the geometric relationships between locations i n that environment ( G a l l i s t e l , 1989 and 1990; Gould, 1986c). The evidence for the use of cognitive maps i n animals other than humans i s circumstantial, but storing memories of the environment i n such a fashion should be greatly advantageous. While animals with l i m i t e d cognitive a b i l i t i e s such as ants are less behaviourally f l e x i b l e , there i s ample evidence that animals such as 11 General Introduction mammals and birds go beyond i n e r t i a l reckoning and simple repetitions of past a c t i v i t i e s (Tolman, 1948) . The concept of a cognitive map i n any animal i s s t i l l not u n i v e r s a l l y accepted. In a fashion s i m i l a r to the s p l i t between c o g n i t i v i s t s and behaviourists there are two schools of thought on s p a t i a l navigation. One group, championed by authors such as Dyer (1991, 1993), have suggested that animals r e l y on dead reckoning, or movement along a set of remembered vectors, to navigate. Others, such as Gould (1986a and 1986c) , argue that the a b i l i t y to f i n d novel paths and navigate with only a subset of previous cues and landmarks precludes the sole use of s i m p l i s t i c navigational tools as dead reckoning i n many animals. Cognitive maps of the environment provide numerous navigational advantages. Monkeys and chimps minimize the distance t r a v e l l e d to reward sources (MacDonald and Wilkie, 1990; Menzel, 1991; Menzel, 1973), gerbils orient themselves i n novel locations with reference to objects they could only be remembering at the time (Thinus-Blanc and Ingles, 1985), and rats store multiple maps simultaneously, allowing for f l e x i b l e exploitations of th e i r environment (Maki et al., 1979) . We understand poorly at best how animals develop maps of t h e i r environments. I believe that i t i s l i k e l y that the process begins with either random sampling forays or systematic sampling forays and that p r i o r experience l i k e l y 12 General Introduction b i a s e s use o f t h e s e methods. A n i m a l s ' s e a r c h p a t t e r n s a r e t i e d t o t h e i r e c o l o g i c a l needs (Root and K a r e i v a , 1984) and t o a b i l i t i e s g a i n e d t h r o u g h e v o l u t i o n (Gould, 1986c) . From t h e o r i g i n a l t r i a l and e r r o r i n v e s t i g a t i o n o f t h e v a l u e o f d i f f e r e n t p o r t i o n s o f the t e r r a i n , an a n i m a l can b e g i n t o remember s e t s o f r e w a r d i n g and non-rewarding s i t e s . Perhaps some a n i m a l s cannot move beyond t h i s s t a g e . I n t h e case o f b i r d s such as hummingbirds, however, we know t h a t t h e y s y n t h e s i z e t h e s e s e t s o f p l a c e s i n t o s t r u c t u r e s t h a t i n c o r p o r a t e s p a t i a l , g e o m e t r i c r e l a t i o n s h i p s among elements ( S u t h e r l a n d and Gass, i n p r e s s ; S u t h e r l a n d , 1985; Thompson, 1994). These b i r d s , a l o n g w i t h groups such as p r i m a t e s , r o d e n t s and o t h e r s , can a p p a r e n t l y g e n e r a t e complex maps t h a t a l l o w h i g h l y f l e x i b l e movement and e x p l o i t a t i o n o f t h e i r environments (Bowers and Adams-Manson, 1993; E l l e n e t a l . , 1984; S h o l l , 1987). Cues and Landmarks P a r t o f t h e p r o c e s s of d e v e l o p i n g a map o f t h e environment i n v o l v e s l e a r n i n g t he p o s i t i o n s o f r e c o g n i z a b l e landmarks. W i t h o u t cues o r landmarks a n i m a l s a r e presumably l i m i t e d t o dead r e c k o n i n g as a means o f n a v i g a t i o n . Landmarks, by t h i s d e f i n i t i o n , a r e any permanent o r semi-permanent i t e m s t h a t a n i m a l s can sense and use as n a v i g a t i o n a l a i d s . T y p i c a l l y , we t h i n k o f a landmark as a p h y s i c a l i t e m t h a t an a n i m a l can e a s i l y see; however, i t c o u l d be an a r e a o f s p e c i f i c w ind c u r r e n t s o r a s i t e where 13 General Introduction an odour, o r any o f a number o f o t h e r s e n s o r y phenomena, i s maximized. I t must be c o n s i s t e n t enough, however, f o r the a n i m a l t o become c o n d i t i o n e d t o i t s p r e s e n c e and t o l e a r n t o a s s o c i a t e i t w i t h some s p e c i f i c reward o r t a s k i n a p a r t i c u l a r p l a c e o r a r e a . There i s c o n s i d e r a b l e o v e r l a p between t h i s d e f i n i t i o n o f a landmark and t h e d e f i n i t i o n o f a reward cue. I w i l l d e f i n e a reward cue as an i n d i c a t o r o f reward t h a t i s s p e c i f i c a l l y l i n k e d t o t h a t reward i n space and t i m e (and i n a 1:1 r a t i o : one cue, one reward), and a reward landmark as a n a v i g a t i o n a l a i d t h a t i n d i c a t e s an a r e a c o n t a i n i n g one o r more reward s i t e s . The e v i d e n c e h i n t s t h a t an a n i m a l d e a l s w i t h e n v i r o n m e n t a l i n f o r m a t i o n d i f f e r e n t l y , depending on whether t h a t i n f o r m a t i o n i s a cue o r a landmark. I n p r a c t i c e , however, t h a t d i f f e r e n c e i s much more d i f f i c u l t t o d i s c e r n . I t may be u n i m p o r t a n t whether we l a b e l an i t e m as a landmark o r a reward cue a n d . i n many cases t h e r e w i l l be c o n s i d e r a b l e o v e r l a p between them. D i f f e r e n t i a t i n g between them i s d i f f i c u l t s h o r t o f i n v a s i v e s u r g i c a l t e c h n i q u e s , s uch as work by D. S h e r r y ( p e r s . comm., 1992) w h i c h s u g g e s t s t h a t landmarks r e g i s t e r i n areas o f the b r a i n used f o r l o n g - t e r m memory w h i l e cues a r e p r o c e s s e d i n s h o r t term memory. T h i s memory s t o r a g e d i f f e r e n c e makes sense i f landmarks a r e p a r t o f an a n i m a l ' s c o n t i n u i n g map o f t h e w o r l d , w h i l e cues, a l t h o u g h used f o r s i m i l a r purposes and o f t e n permanent 14 General Introduction features of the landscape, are associated with a transient reward event. Cues Previous studies of sp a t i a l memory and learning have d i f f e r e n t i a t e d several types of cue information. Cues may provide d i r e c t i o n a l information, marking the s i t e of a reward. This type of cue i s common i n many studies i n which, for instance, a l i g h t comes on to mark the half of a screen that contains food (Suzuki et al. , 1980). Cues may also provide information about p r o f i t a b i l i t y . This same l i g h t provides the most basic information about reward quality, at the same time marking one side as o f f e r i n g a p o s i t i v e reward and the other as o f f e r i n g no reward. Other experiments have used cues to provide more de t a i l e d information such as the number of food items present at a s i t e (Roberts, 1988), the quality of a nectar source (Bogdany, 1978; C o l l i a s and C o l l i a s , 1968; Dreisig, 1989; Greggers and Menzel, 1993), or the type of food present (Sherry, 1984). The amount and kind of information that could be provided by a cue i s highly f l e x i b l e and depends as much on the experimenter as on the nature of cues themselves; whether the information i s actually conveyed to the animal, of course, depends on the animal. Almost any information which an animal can be trained to detect or d i f f e r e n t i a t e can be provided by a cue. This includes duration of reward 15 General Introduction p e r i o d s , reward v a r i a b i l i t y , event sequences and many o t h e r forms o f i n f o r m a t i o n ( C o l w i l l and R e s c o r l a , 1985; Pepperberg, 1987; R e s c o r l a , 1986; R o b e r t s , 1988; S e l f and G a f f a n , 1983) . Landmarks Landmarks a r e n a v i g a t i o n a l a i d s a n i m a l s use t o n a v i g a t e t h r o u g h t h e i r e nvironments. S t u d i e s o f landmark use sug g e s t t h a t a n i m a l s remember s e v e r a l c h a r a c t e r i s t i c s o f them. They d i s t i n g u i s h landmarks on the b a s i s o f s i z e , f o r example, and p r e f e r t o use l a r g e landmarks f o r n a v i g a t i o n ( B e n n e t t , 1993). Shape, c o l o u r and o t h e r s i m i l a r i n f o r m a t i o n about landmarks i s remembered and used by a n i m a l s i n . l e a r n i n g (Cheng e t al., 1987a; Vander W a l l , 1991). A n i m a l s a l s o remember t h e d i s t a n c e between landmarks and t h e i r accompanying s e t s o f reward s i t e s (Bennett, 1993; Cheng et al., 1987b; C o l l e t et al., 1992), and t h i s i n f o r m a t i o n i s v i t a l t o n a v i g a t i o n . Moving a landmark causes a n i m a l s t o miss t h e reward s i t e by t h e same d i s t a n c e as t h e s h i f t i n landmark l o c a t i o n (Cheng, 1986 and 1988; T i n b e r g e n , 1932; T i n b e r g e n and K r u y t , 1938; Vander W a l l , 1982; Warburton, 1990). A n g u l a r d i r e c t i o n t o l o c a t i o n s i s a l s o remembered and moving t h e landmarks used i n t r i a n g u l a t i o n may have a s i m i l a r e f f e c t on assumed reward l o c a t i o n (Cheng, 1989; Tengo e t al., 1990) . Cheng and o t h e r s have suggested t h a t a n i m a l s use landmarks as n a v i g a t i o n a l a i d s by c a l c u l a t i n g v e c t o r s 16 General Introduction between the landmark and the reward s i t e (Cheng, 1988) . This hypothesis does not account for a l l the ways that animals use landmarks (Spetch et al., 1992), but may s t i l l play a ro l e i n landmark navigation where landmarks and rewards are clos e l y associated and there are few confounding objects. Role of Cues and La^HmaT-Trg in Learning Animals use landmark and cue information to develop cognitive maps of the i r surroundings, as f i r s t suggested by Tolman i n 1948. I n i t i a l sampling forays provide information that the animal learns to associate with the rewards i t obtains during these forays. Early navigation may consist of dead reckoning, but as an animal learns to i d e n t i f y landmarks, more f l e x i b l e and ef f e c t i v e approaches to the reward s i t e s become possible and as i t learns the cues there i t can ignore non-rewarding or less rewarding s i t e s altogether. Eventually, i t may t i e together information about i n d i v i d u a l reward locations into patterns that require less information storage and less time to locate and exploit repeatedly. This process of chunking or generalizing s p a t i a l information about t h e i r environments (cognitive mapping) i s found i n a number of vertebrate species and may be found i n invertebrates as well (McNamara et al., 1989; Olton, 1985; S h i f f r i n et al., 1976). 17 General Introduction Outline of Studies In t h i s thesis I examine several aspects of s p a t i a l memory and i t s role i n foraging using rufous hummingbirds {Selasphorus rufus). These birds have several advantages for learning and behavioural studies. One advantage i s that t h e i r small size and space requirements allow them to be maintained without excessive space requirements. Their second advantage i s that they have an extremely high metabolic rate, and require food often. This ensures that they are highly motivated to learn various foraging tasks. Their high feeding rates, compounded with t h e i r advanced learning a b i l i t i e s , allows the completion of complex learning experiments i n a short period of time and with r e l a t i v e l y short t r a i n i n g requirements. The f i r s t set of experiments examines the r o l e of experience i n s p a t i a l pattern learning, e s p e c i a l l y as a function of environmental i n s t a b i l i t y . In my second set of experiments I study how v i s i b l e cues and landmarks a f f e c t s p a t i a l pattern learning and the r e l a t i v e importance of d i f f e r e n t kinds of v i s u a l c h a r a c t e r i s t i c s to learning. The f i n a l set of experiments examines the contrasting e f f e c t s of s p a t i a l memory and s p a t i a l association memory. 18 Chapter 2 Pattern Learning and Persistence of Spatial Memory in Rufous HnmrnHnqVi-i rriff Section I. Introduction Learning Learning aids e f f e c t i v e use of available resources. Estes (1994) described an individual as a c t i v e l y sampling alternate courses of action, generating expectations and sel e c t i n g those most l i k e l y to succeed. In the laboratory, many learning experiments have dealt with simple environments, i n which rats choose one arm of a maze, or pigeons .learn a pecking protocol i n order to receive a reward (Bolhuis et al., 1987; Bond et al., 1981; C o l w i l l and Dickinson, 1980; Spetch et al., 1992; Wilkie, 1986a). In these experiments i t i s often the case not only that the environment i s si m p l i f i e d but that the learning tasks required of the animal are straightforward. This approach s i m p l i f i e s and controls the variables presented to the study animal i n order to better understand some p a r t i c u l a r aspect of learning. 19 Pattern Learning and Persistence I n n a t u r a l environments, however, l e a r n i n g i s seldom such a c l e a n and s t r a i g h t f o r w a r d a f f a i r . The c h a r a c t e r i s t i c s o f a r e f u g e o r f o r a g i n g environment may change w i t h t h e time o f day, l i g h t i n g c o n d i t i o n s , and weather. Prey c h a r a c t e r i s t i c s such as shape, a c t i v i t y and l o c a t i o n v a r y i n almost a l l cases (Dawkins, 1971a and 1971b; Dukas and E l l n e r , 1993; Dukas and Waser, 1994; Lawrence, 1989). Food s i t e s f o r n e c t a r i v o r e s such as hummingbirds change c o l o u r , s i z e , shape and e n e r g e t i c p r o f i t a b i l i t y on a d a i l y b a s i s (Armstrong et al., 1987; Gass and S u t h e r l a n d , 1985; Wolf and Ha i n s w o r t h , 1991) . Food a v a i l a b l e from p a r t i c u l a r s o u r c e s may be absent, r i c h e r o r p o o r e r on subsequent v i s i t s (Gass et al., 1976; Weis, 1983; Wunderle and M a r t i n e z , 1987) . Not o n l y do t h i n g s change, but t h e y o f t e n change u n p r e d i c t a b l y i n n a t u r a l e n v i r o n m e n t s , and a n i m a l s must t o l e r a t e t h i s i n t h e i r d e c i s i o n - m a k i n g . As a consequence o f t h e s e c o m p l e x i t i e s , r e s e a r c h e r s must be c a r e f u l i n e x t r a p o l a t i n g r e s u l t s o f s i m p l e l a b o r a t o r y s t u d i e s t o t h e b e h a v i o u r o f a n i m a l s i n t h e w i l d (Beecher and St o d d a r d , 1990) . Advantages of Learning I n many s i t u a t i o n s i t b e n e f i t s a n i m a l s t o l e a r n t h e c h a r a c t e r i s t i c s o f t h e i r environments, e s p e c i a l l y t h o s e f a c t o r s t h a t most a f f e c t t h e i r f i t n e s s . These i n c l u d e such o b v i o u s t h i n g s as t h e h a b i t s o f p r e d a t o r s , s i t e s o f r e f u g e , and l o c a t i o n s o f f o o d (Krebs and D a v i e s , 1984) . I n s t a b l e 20 Pattern. Learning and Persistence environments, individuals of a given species who learn are more f i t (Benhamou, 1994; Valone, 1992) . Disadvantages of Learning The disadvantages of learning include the time and energy spent sampling the environment (Forkman, 1991; Valone, 1992) and processing information (Blough and Blough, 1990; M. Brown, 1992; Brown and Cook, 1986) . One study found that foraging with no p r i o r expectation ( i . e . learning) to guide exploration was only 4 per cent e f f e c t i v e (Vander Wall, 1991) so the exploration required for learning i s expensive. Another disadvantage i s the energetic cost of remembering (Bullock, 1993; C a p e l l i et al. , 1986; M i l l e r , 1956). Alternatives to learning Animals presumably use learning due to i t s energetic advantages. Other foraging strategies may be preferred i n resource poor or unstable environments, where t h i s advantage i s less prevalent. Similarly, learning need not be used i f a simpler strategy w i l l produce successful foraging. Such strategies include random foraging, or the use of simple rules of thumb to govern behaviour. Wolf and Hainsworth (1983 and 1991) found no evidence of memory use by hummingbirds foraging i n resource l i m i t e d environments. Under conditions of heavy competition, random behaviour that cannot be predicted by competitors may be advantageous (Bryant and Church, 1974). Bees taking nectar from flowers 21 Pattern Learning and Persistence often s t a r t at the bottom of the plant and give up when they encounter a poor blossom, demonstrating a simple systematic foraging pattern (Dreisig, 1989; Pyke, 1978; Pyke and Cartar, 1992) . Pa r a s i t i c wasp-like insects (Torymus capite) search for a host for a fixed time then give up (Weis, 1983) . Such rules of thumb are the basis of the marginal value theorem, which states that animals should use t h e i r environments i n ways that maximize t h e i r rates of return, including the use of p r i o r knowledge (learning) when i t i s advantageous (Bond, 1980; Charnov, 1976; Krebs and Davies, 1984) . Complex environments Learning i s advantageous for many animals i n many sit u a t i o n s . In p e r f e c t l y stable environments animals need only learn once; however, learning consolidated over a period of time tends to be less f l e x i b l e than newly learned tasks (Gould, 1986c). In extreme cases, long term exposure to a stable environment can lead to ca n a l i z a t i o n or automation of behaviour (Gass, 1985; Tierney, 1986) . Learning can also be a response to rapid l y changing, unpredictable environments (Tierney, 1986). Too much unp r e d i c t a b i l i t y , however, can negate the value of learning by reducing the effectiveness of memories (Bowers and Adams-Manson, 1993; Nishimura, 1994). Thus, the reliance of animals on learning and memory varies with the complexity of the environment (Bond et al., 1981; K i l l e e n and Fetterman, 22 Pattern Learning and Persistence 1988; Warburton, 1990), and there i s experimental evidence that animals prefer complex, changing environments (Denny, 1975). Learning seems to be enhanced i n such complex environments (Gleitman, 1963), esp e c i a l l y i f the surroundings are fa m i l i a r to the animal (Biederman et al., 1973). Despite the importance of understanding the effects of p r e d i c t a b i l i t y on learning, our a b i l i t y to study t h i s important factor has been limited (Eisenberger, 1988; Papaj, 1988), p a r t l y because of the p r a c t i c a l d i f f i c u l t i e s of creating p r e c i s e l y variable environments i n the laboratory. Testing of some of these theories has concentrated on such changes as variations i n reward leve l s or patch q u a l i t y (Caraco, 1982; Dow and Lea, 1987; Kacelnik et a l . . 1987; Regelmann, 1985). Other factors i n u n p r e d i c t a b i l i t y that have been examined i n the laboratory include persistence i n patches (Lima, 1983, 1984), responses to variance i n the l e v e l of reward (Stephens and Paton, 1986) and scheduling of returns to cached food ( G i l l , 1988; Sherry, 1985) . Mathematical modelling Mathematical modelling has been an important t o o l for developing theories about learning i n complex, changing environments (Booth, 1986; Caraco and Lima, 1987; Colwell, 1974; Fagan and Young, 1978; Laming and Scheiwiller, 1985; McNamara, 1982; McNamara and Houston, 1985b, 1987). The use 23 Pattern Learning and Persistence of such models has allowed researchers to examine complex tasks that are d i f f i c u l t to duplicate i n the laboratory (Cahoon, 1984; Cain, 1985; Haefner and C r i s t , 1994). These modelling exercises have provided us with insight into natural learning processes that can be applied i n a r t i f i c i a l i n t e l l i g e n c e systems to test the f e a s i b i l i t y of our learning theories (Devi and Sarma, 1986; Faris and Maijer, 1988; Fuchs and Haken, 1988a and 1988b; Haken, 1988; Hobbs, 1986; Park, 1985; Selfridge and Nesser, 1960) or tested experimentally (Stephens and Paton, 1986). One use of mathematical modelling has been to examine the i n t e r n a l processes of learning and memory. Based on a combination of modelling and experimentation, Kacelnik et al. (1987) suggested that animals store t h e i r memories of the environment by a means that can be modelled as an exponentially weighted moving memory window. Si m i l a r l y , McNamara and Houston (1985b) suggested that a weighted moving memory window i s an accurate model of learning. If memory window models are v a l i d , then memory can be swamped or overcome by large inputs of new and varied experience. This t h e o r e t i c a l expectation was corroborated experimentally by Nishimura (1994). The ideas proposed i n these memory window models suggest that experience of an environment (both time spent i n an environment and number of experiences) contributes to what and how much an animal learns about i t s surroundings. 24 Pattern Learning and Persistence R e t e n t i o n o f a memory, then, s h o u l d depend on b o t h t i m e s i n c e rewards were o b t a i n e d ( r e i n f o r c e m e n t ) and i n t e r v e n i n g o r i n t e r t r i a l e x p e r i e n c e . T h i s e x p e c t a t i o n has been c o n f i r m e d by s e v e r a l a u t h o r s ( C a p a l d i e and M i l l e r , 1988; C a p a l d i e e t al., 1987a and 1987b; H u l s e , 1978; K a m i l and M a u l d i n , 1975) . I n c r e a s i n g c o m p l e x i t y c o u l d a d v e r s e l y a f f e c t t h e a b i l i t y t o l e a r n and remember (Hochberg and M c A l i s t e r , 1953; L a v e r t y , 1994) s i n c e i t p r o v i d e s more t h i n g s t o remember, swamping a memory window. Perception of the environment The a d a p t i v e s i g n i f i c a n c e of l e a r n i n g has been examined under v a r i o u s but l i m i t e d c o n d i t i o n s (Damianopolous, 1989; Denning, 1989; D r a u l a n s , 1988; Dukas and V i s s c h e r , 1994; Dukas and Waser, 1994; G l e i t m a n , 1963; Johannson et al. , 1980) . When s h o u l d an a n i m a l l e a r n about i t s environment and when s h o u l d i t f o r a g e randomly o r by some s i m p l e r u l e o f thumb? I f t h e environment i s s u f f i c i e n t l y p r e d i c t a b l e , l e a r n i n g t h e l o c a t i o n s o f i n d i v i d u a l f o o d s o u r c e s w i l l save energy and f o r a g i n g time (Bond, 1980; Vander W a l l , 1982). Most f o o d s t o r i n g b i r d s who r e l y on l e a r n i n g and memory t o r e l o c a t e f o o d caches, f o r i n s t a n c e , a r e t e r r i t o r i a l and l i v e i n s e a s o n a l environments ( R o b e r t s , 1979) . These b i r d s e x p e r i e n c e change i n t h e i r environments but many o f t h e changes a r e i r r e l e v a n t t o t h e i r f o r a g i n g and even when r e l e v a n t , a r e o f t e n p r e d i c t a b l e and c o n s i s t e n t . I f c o n s i s t e n t environments f a v o u r l e a r n i n g , t h e q u e s t i o n can be 25 Pattern Learning and Persistence r e f i n e d t o ask how c o n s i s t e n t environments must be f o r l e a r n i n g about them t o be advantageous. D i s c u s s i o n s o f e n e r g e t i c advantages o f t e n l e a d t o c o n s i d e r a t i o n s o f o p t i m a l f o r a g i n g , w h i c h has been a dominant theme i n b e h a v i o u r a l s t u d i e s f o r about 30 y e a r s now (Charnov, 1976; McNamara and Houston, 1985a; R o b e r t s , 1991; Tamm and Gass, 1986). I t i s apparent, however, t h a t a n i m a l s do t h i n g s t h a t a r e not e a s i l y e x p l a i n e d by o p t i m a l i t y c o n c e p t s such as energy m a x i m i z a t i o n (Forkman, 1991; Gass, 1985; M a i e r et al., 1988; R o b e r t s , 1991). They do not always o p t i m i z e t h e i r e f f o r t s but i n s t e a d adopt l e s s e f f i c i e n t approaches w h i c h s t i l l meet t h e i r needs (Stephens, 1981) . I t i s i m p o r t a n t t o p l a c e b e h a v i o u r s i n t o t h e l a r g e r c o n t e x t o f t h e a n i m a l s ' v a r i o u s a c t i v i t i e s when e x a m i n i n g a n i m a l b e h a v i o u r s i n c e a n i m a l s must t r a d e o f f b e n e f i t s from one a c t i v i t y w i t h i t s a s s o c i a t e d c o s t s and i t s e f f e c t s on o t h e r a c t i v i t i e s ( G e t t y and P u l l i a m , 1993; Lima, 1984; Smith, 1974) . O p t i m a l i t y cannot e x p l a i n b e h a v i o u r u n l e s s i t i s c o u p l e d w i t h i n f o r m a t i o n - p r o c e s s i n g h y p o t h e s e s (Bond, 1980; Todd and K a c e l n i k , 1993) . A n i m a l s w i t h knowledge o f t h e i r environments a r e not l i m i t e d t o s i m p l e r u l e s o f thumb such as l e a v i n g a p a t c h when f o o d i n t a k e r a t e s b e g i n t o drop. L e a r n i n g i n t h e s e s i t u a t i o n s a l l o w s f o r more s o p h i s t i c a t e d d e c i s i o n making. 26 Pattern Learning and Persistence What i s optimal to do at any moment can depend on what an animal has done to learn about i t s environment, which often displays recognizable s p a t i a l structure. In turn, learning can be modified by perceptions of consistency. I intend to explore the role of p r e d i c t a b i l i t y i n s p a t i a l pattern learning, since the a b i l i t y to return to food sources i s a fundamental requirement for many animals' s u r v i v a l . The need to forage successfully, coupled with the advantages of learning, suggests that there i s strong s e l e c t i o n for the a b i l i t y to learn patterns of food s i t e s and s p a t i a l maps of the environment. Spatial memory has been studied i n many animals and conditions, ranging from g o l d f i s h to honeybees to humans (Aadland et al., 1985; Garber, 1988a and 1988b; Gould, 1987; Jue et al., 1989; Shettleworth et al., 1990; Spetch and Edwards, 1986; Woodard and Bitterman, 1973). Rufous hummingbirds, the species used i n my study, can learn s p a t i a l patterns, as demonstrated by Sutherland and Gass (in press). Experimental protocols Sutherland (1985) studied the a b i l i t y of hummingbirds to learn patterns of rewarding feeders d i s t r i b u t e d i n a two dimensional array. He allowed birds to learn a pattern of feeders over a series of 3 0 t r i a l s and then suddenly reversed the pattern, so that a l l rewarding feeders became non-rewarding and vice versa. Complete and sudden reversal of a learned pattern produced a s i g n i f i c a n t drop i n 27 Pattern Learning and Persistence performance (successful feeder v i s i t a t i o n s dropped below chance). He repeated this procedure with four d i f f e r e n t patterns of feeders on the array, each providing a 50 per cent chance of reward with random feeder v i s i t a t i o n . The patterns included "halves" where the rewarding feeders were a l l on either the l e f t or right hand side of the array, "quarters" where the top l e f t quarter and bottom right quarter of the array were rewarding (or vice versa), "checkerboard" where the array consisted of eight groups of four rewarding feeders arranged i n squares alternated with eight groups of four unrewarding feeders arranged i n squares, and "random" where rewarding feeders were located randomly on the array (although the random pattern presented at the sta r t of the experimental run remained the same for a l l runs) . From this study he concluded that the hummingbirds had learned the pattern of rewarding feeders and expected the pattern to p e r s i s t . Current study In order to examine the effect of experience on the persistence of behaviours that r e l y on s p a t i a l memory I performed s i m i l a r experiments using the "quarters" pattern, but varying the number of t r i a l s birds were exposed to the pattern of feeders before a sudden and complete reversal of the pattern. If the strength of s p a t i a l memory or the strength of reliance on i t develops with experience, i n the sense that i t per s i s t s longer i n the face of no 28 Pattern Learning and Persistence reinforcement, then as the pre-switch exposure increases the drop i n performance afte r the switch should increase i n magnitude or duration. 29 Pattern Learning and Persistence Section II. Materials and Methods Subjects I n t h i s experiment I used 12 n a i v e , a d u l t r u f o u s hummingbirds, (Selasphorus rufus): 4 males and 8 f e m a l e s . The b i r d s were c a p t u r e d i n the f i e l d (10 n e a r R o s e w a l l Creek, Vancouver I s l a n d , B.C., and 2 i n t h e U.B.C. r e s e a r c h f o r e s t n o r t h o f Maple Ridge, B.C.) and m a i n t a i n e d i n i n d i v i d u a l 0.6 x 0.6 x 1.0 m f i b r e g l a s s mesh cages f o r one t o two months p r i o r t o t e s t i n g . Throughout th e p e r i o d o f c a p t i v i t y t h e p h o t o p e r i o d was m a i n t a i n e d a t 14L:10D. E x c l u d i n g t e s t p e r i o d s , t h e b i r d s were s u p p l i e d w i t h e i t h e r Roudybush hummingbird d i e t o r N e k t a r P l u s hummingbird d i e t ad libitum on weekdays. On weekends, b i r d s were p r o v i d e d w i t h 25% s u c r o s e s o l u t i o n w i t h added v i t a m i n s ( A v i t r o n a v i a n v i t a m i n supplement) and m i n e r a l s ( A v i m i n a v i a n m i n e r a l supplement). At a l l t i m e s o u t s i d e o f t e s t p e r i o d s , a d u l t Drosophila were a v a i l a b l e . Experimental Environment I c o n d u c t e d a l l t r a i n i n g and e x p e r i m e n t s i n a room 1.1 x 2.6 x 2.6m h i g h w i t h overhead f u l l - s p e c t r u m f l u o r e s c e n t l i g h t s . W a l l s and c e i l i n g , except t h e f e e d e r a r r a y , were a u n i f o r m l i g h t green c o l o u r and t h e f l o o r was a u n i f o r m sand c o l o u r . A s i n g l e , stand-mounted, 1.7 m h i g h p e r c h was. a t 30 Pattern Learning and Persistence the centre of the room, f i t t e d with a photocell to signal a r r i v a l s and departures to a computer monitoring the room. On one end wall of the room a 1.0 x 1.0 m dark green metal panel extended from just below the c e i l i n g . Inset into t h i s panel were 64 feeders i n a square 8 x 8 array-spaced at 10.5 cm v e r t i c a l l y and horiz o n t a l l y . Each feeder consisted of a 2.0 cm length of 1.67 mm I.D. Intramedic polyethylene tubing which had been flame heated and bent to form a terminal reservoir at one end. The r e s u l t i n g feeder tube resembled a small smoker's pipe, whose bowl was an open nectar reservoir and whose stem served as a f l o r a l c o r o l l a . The stem of the feeder extended through a photodarlington photodetector and a 4 mm hole d r i l l e d i n the metal array panel and was flush with the front of the panel. Each hole was surrounded by an orange 19 mm Avery la b e l punched with a 6 mm centre hole. A computer recorded a r r i v a l s , departures, and v i s i t durations for the perch and each individual feeder, using signals from the photocells. Recording was accurate to about 10 ms. Before each t r i a l I supplied rewarding feeders with 2 ]il of 22% sucrose solution (weight/weight) from a repeating dispenser (Hamilton PB-600-1). This volume i s within the normal range of nectar volumes found i n f l o r a l species used by rufous hummingbirds (Armstrong, 1986; Carpenter et al., 1983; Gass and Roberts, 1992). Between t r i a l s the array was covered by a beige r o l l e r b l i n d 31 Pattern Learning and Persistence o p e r a t e d from o u t s i d e t h e e x p e r i m e n t a l chamber by a p u l l c o r d . Training Each b i r d was t r a i n e d f o r t h r e e days i m m e d i a t e l y p r i o r t o t e s t i n g . F o r the f i r s t two days b i r d s l i v e d i n t h e i r cages but were f e d maintenance foo d ad libitum from a f e e d e r marked i d e n t i c a l l y t o thos e i n t h e e x p e r i m e n t a l chamber. On t h e morning o f the t h i r d day o f t r a i n i n g , b i r d s and th e t r a i n i n g f e e d e r s from t h e i r home cages were moved t o t h e e x p e r i m e n t a l chamber (the f e e d e r a r r a y was c o v e r e d by t h e b l i n d ) . The s o l e p e r c h i n the room was r a i s e d t o a h e i g h t o f 2.4 m and t h e f e e d e r was p l a c e d d i r e c t l y i n f r o n t o f t h i s p e r c h . As t h e b i r d became accustomed t o u s i n g t h i s p e r c h i t s h e i g h t was g r a d u a l l y d e c r e a s e d t o 1.7 m, t h e h e i g h t of th e c e n t r e o f t h e f e e d e r a r r a y . A f t e r t h e b i r d was accustomed t o t h e f e e d e r and p e r c h i n t h i s arrangement, t h e f e e d e r was moved from i t s p o s i t i o n near t h e c e i l i n g t o d i r e c t l y i n f r o n t o f t h e co v e r e d a r r a y u n t i l t h e b i r d a g a i n f e d r e g u l a r l y . Next, a l l 64 a r r a y l o c a t i o n s were p r o v i d e d w i t h 2 u l o f 22% s u c r o s e s o l u t i o n , t h e home cage f e e d e r was removed, and t h e a r r a y was uncovered u n t i l t h e b i r d f e d from s e v e r a l f e e d e r s . The a r r a y was then c o v e r e d , t h e f e e d e r s r e f i l l e d , and a new t r a i n i n g t r i a l was begun. Once t h e b i r d was c o n s i s t e n t l y v i s i t i n g t he p a n e l , and showed no o r m i n i m a l l e v e l s o f p o s i t i o n a l b i a s (based on i n f o r m a l e s t i m a t i o n o f any u n t r a i n e d p r e f e r e n c e f o r s p e c i f i c p o r t i o n s 32 Pattern Learning and Persistence o f t h e f e e d e r a r r a y and i f n e c e s s a r y e n f o r c e d by t e m p o r a r i l y c o v e r i n g a r e a s o f t h e a r r a y t h a t t h e b i r d had not been f o r a g i n g o u t s i d e o f u n t i l t he b l o c k i n g o f p r e f e r r e d f e e d e r s caused f o r a g i n g t o become more widespread) i t was put t h r o u g h a s e r i e s o f 10-20 sham t r i a l s w i t h a l l f e e d e r l o c a t i o n s r e w a r d i n g t o accustom i t t o t h e 1 minute t r i a l and 5 minute i n t e r t r i a l p e r i o d s t o be used d u r i n g t e s t i n g t h e f o l l o w i n g day. Experimental Procedures On t h e day o f t e s t i n g each b i r d was p r e s e n t e d w i t h one of two m i r r o r image q u a r t e r s p a t t e r n s o f r e w a r d i n g and non-r e w a r d i n g f e e d e r s , s e l e c t e d randomly ( F i g . 1) . I n b o t h c a s e s , r e w a r d i n g f e e d e r s c o n t a i n e d 2 ]il o f 22% s u c r o s e s o l u t i o n (weight/weight) a t t h e b e g i n n i n g o f each t r i a l , making 64 u l o f n e c t a r a v a i l a b l e each t r i a l : a p p r o x i m a t e l y t w i c e t h e p r e f e r r e d meal s i z e o f r u f o u s hummingbirds under normal c o n d i t i o n s (Diamond et a l . , 1986). The t r e a t m e n t and b i r d used on any day was dete r m i n e d by a s c h e d u l e t h a t exposed each b i r d t o one o f the p r e - s w i t c h exposure t r e a t m e n t s . The o r d e r o f the t r e a t m e n t s was randomised, as was p a t t e r n o r i e n t a t i o n . I n each t r e a t m e n t a b i r d was p r e s e n t e d w i t h i t s o r i g i n a l p a t t e r n f o r a f i x e d number o f t r i a l s . Then t h e p a t t e r n was suddenly s w i t c h e d (changed t o i t s m i r r o r image) between two t r i a l s , so t h a t a l l p r e v i o u s l y r e w a r d i n g a r r a y l o c a t i o n s were now non - r e w a r d i n g and vice 33 O O O O t t f t O O O O i t i i o o o o t t t i o o o o i t t i • • • t o o o o ••••oooo ••••oooo ••••oooo Figure 1. S t y l i z e d representation of one quarters pattern for the feeder array (not to scale). Each c i r c l e represents one feeder. S o l i d black c i r c l e s represent rewarding feeders, and open c i r c l e s are empty feeder locations. 34 Pattern Learning and Persistence versa. The four treatments consisted of pre-switch exposures of 10, 20, 30 and 40 t r i a l s . The subject b i r d was fasted for 15-2 0 minutes immediately preceding the test period. Although t r i a l s lasted one minute, birds could stop feeding and return to the perch at any time. I ignored any t r i a l i n which the subject did not v i s i t the feeder panel. Previous studies (Sutherland, 1985) as well as p i l o t studies by myself have shown that hummingbirds remove a l l nectar from the feeders when a volume of 2ul i s used. For t h i s reason, I treated a l l second and subsequent v i s i t s to any feeder during a t r i a l as non-rewarding. For analysis of r e s u l t s I treated only the f i r s t v i s i t s to rewarding feeders i n each t r i a l as correct v i s i t s . I treated f i r s t v i s i t s to non-rewarding feeders as incorrect v i s i t s and ignored r e v i s i t s to feeders during any given t r i a l for determining performance and foraging success. At the end of each t r i a l I covered the feeder array and r e f i l l e d rewarding feeders which the b i r d had emptied during the t r i a l . After an i n t e r t r i a l period of 5 minutes I uncovered the array and began the next t r i a l . At the end of the i n i t i a l exposure period, I covered the feeder array and emptied and flushed a l l feeders. I then f i l l e d the 32 newly rewarding feeders and carried out 40 more t r i a l s with t h i s reversed feeder pattern. At the end of the experimental 35 Pattern Learning and Persistence r u n , t h e b i r d was r e t u r n e d t o i t s home cage and a l l f e e d e r s were emptied and f l u s h e d . 36 Pattern Learning and Persistence Section I I I . Results I n i t i a l Performance B i r d s i n a l l f o u r t r e a t m e n t s improved a t s i m i l a r r a t e s ( F i g . 2 ) . I n i t i a l l y , t h e i r performance was near chance, t h e n improved r a p i d l y t o 80% t o 90% c o r r e c t v i s i t a t i o n s by about 20 t r i a l s . These a r e d e c e l e r a t i n g monotonic c u r v e s . I examined f o o d consumption t o t e s t t h e a p p l i c a b i l i t y of two performance i n d i c a t o r s and found t h a t . b i r d s f e d from t h e f e e d e r a r r a y a t a r e l a t i v e l y c o n s t a n t r a t e d u r i n g t h e day ( F i g . 3 ) . There i s c o n s i d e r a b l e v a r i a b i l i t y i n t h e s e c u r v e s ; however, b i r d s d i d not s i g n i f i c a n t l y change t h e i r f e e d i n g r a t e (amount o f s u c r o s e consumed e v e r y t r i a l ) i n a p p r o x i m a t e l y h a l f o f the t r e a t m e n t s (Table 1 ) . Changes i n f e e d i n g r a t e s throughout t h e co u r s e o f t h e ex p e r i m e n t s were p o o r l y e x p l a i n e d by t h e number o f t r i a l s spent w i t h a c o n s i s t e n t p a t t e r n o f r e w a r d i n g f e e d e r s , as shown by t h e low r ^ v a l u e s ; t h i s was t r u e f o r a l l t r e a t m e n t s . Pre-switch Trials Post-switch Trials A l l Trials F P r2 F P r2 F P r2 Switch 10 4.317 0.071 0.350 3 .287 0.078 0.079 8.450 0.006 0.150 Switch 20 3 .585 0.075 0.166 5.101 0.03 0 0.118 9 .244 0.004 0.138 Switch 3 0 9.688 0.004 0.257 9 .832 0.003 0.205 2.253 0.138 0.036 Switch 40 7.969 0.008 0.173 0.014 0.907 0.000 8.920 0.004 0.102 T a b l e 1. R e g r e s s i o n a n a l y s i s of c o r r e c t v i s i t s v e r s u s t r i a l number ( s i n c e t he assumption i s t h a t t h e r e l a t i o n s h i p w i l l be l i n e a r and f l a t ) f o r each o f t h e t r e a t m e n t s . Treatment names r e f e r t o t h e number o f t r i a l s b e f o r e r e v e r s a l o f the p a t t e r n o f r e w a r d i n g f e e d e r s . 37 Figure 2. Proportion of f i r s t v i s i t s per t r i a l that were correct (rewarding) averaged over blocks of 5 t r i a l s and a l l birds i n each treatment for each of the 4 treatments. Curves i n the l e f t panel are performance before the pattern reversal and curves i n the right panel are performance a f t e r the r eversal. Blocks of 5 t r i a l s a f t e r the pattern reversal are numbered from 1 to standardize alignment of curves from each treatment. The s o l i d l i g h t l i n e i s the performance of birds when the pattern was switched a f t e r 10 t r i a l s , the s o l i d bold l i n e represents birds switched a f t e r 20 t r i a l s , the dotted l i n e i s a f t e r 30 t r i a l s and the dashed l i n e i s a f t e r 40 t r i a l s . 38 Figure 3. Number of correct v i s i t s per t r i a l (averaged over blocks of 5 t r i a l s and a l l birds i n each treatment) for each of the 4 treatments. Curves i n the l e f t panel are performance before the pattern reversal and curves i n the right panel are performance aft e r the reversal. Blocks of 5 t r i a l s a f t e r the pattern reversal are numbered from 1 to standardize alignment of curves from each treatment. The s o l i d l i g h t l i n e i s the performance of birds when the pattern was switched a f t e r 10 t r i a l s , the s o l i d bold l i n e represents birds switched a f t e r 20 t r i a l s , the dotted l i n e i s a f t e r 30 t r i a l s and the dashed l i n e i s af t e r 40 t r i a l s . 39 Pattern Learning and Persistence P r o p o r t i o n c o r r e c t i s the most w i d e l y used i n d i c a t o r o f performance ( F i g . 2 ) . S i n c e the number o f c o r r e c t v i s i t s s t a y e d r e l a t i v e l y c o n s t a n t throughout t h e e x p e r i m e n t a l r u n s , I was con c e r n e d t h a t p r o p o r t i o n c o r r e c t may be a weaker t e s t of p erformance than t o t a l i n c o r r e c t ( f i r s t ) v i s i t s p e r t r i a l . As a consequence, I have p r e s e n t e d b o t h v a l u e s when t h e r e i s a d i f f e r e n c e . The averages of the i n c o r r e c t v i s i t s t o t h e a r r a y by b i r d s i n each t r e a t m e n t a r e p r e s e n t e d i n F i g u r e 4. B i r d s improved s i g n i f i c a n t l y i n performance d u r i n g t h e i n i t i a l l e a r n i n g p e r i o d i n a l l t r e a t m e n t s (Table 2 ) . Treatment P r o p o r t i o n C o r r e c t I n c o r r e c t V i s i t s F v a l u e p r o b a b i l i t y F v a l u e p r o b a b i l i t y S w i t c h 10 27 .799 0.001 8.358 0.020 S w i t c h 2 0 8.356 0.010 2 .108 0 .164 S w i t c h 3 0 92.064 0.000 54.303 0 .000 S w i t c h 40 8.393 0.006 37 .589 0.000 T a b l e 2. R e g r e s s i o n a n a l y s i s of i n i t i a l p e rformance v e r s u s n a t u r a l l o g o f t r i a l ( t o improve l i n e a r i t y o f r e g r e s s i o n s ) . V a l u e s f o r b o t h performance i n d i c a t o r s a r e g i v e n . Treatment names r e f e r t o t h e number o f t r i a l s b e f o r e t h e r e v e r s a l of t h e p a t t e r n o f r e w a r d i n g f e e d e r s . P r o b a b i l i t i e s a r e t h e chance o f no d i f f e r e n c e . Duration of Exposure and Pattern Reversals • Performance f o r a l l 4 t r e a t m e n t s dropped s h a r p l y i m m e d i a t e l y a f t e r t he q u a r t e r s p a t t e r n o f f e e d e r s was r e v e r s e d . Performance was s t r o n g l y s i g n i f i c a n t l y b e t t e r i n th e 5 t r i a l s i m m e d i a t e l y b e f o r e t h e s w i t c h t h a n i n t h e 5 t r i a l s i m m e d i a t e l y a f t e r (Table 3 ) . As w e l l , b i r d s i n 40 Figure 4. Average number of incorrect v i s i t s for each of the 4 exposure treatments. Curves i n the l e f t panel are performance before the pattern reversal and curves i n the right panel are performance aft e r the reversal. Blocks of 5 t r i a l s a f t e r the pattern reversal are numbered from 1 to standardize alignment of curves from each treatment. The s o l i d l i g h t l i n e i s the performance of birds when the pattern was switched aft e r 10 t r i a l s , the s o l i d bold l i n e represents birds switched aft e r 20 t r i a l s , the dotted l i n e i s a f t e r 30 t r i a l s and the dashed l i n e i s a f t e r 40 t r i a l s . 41 Pattern Learning and Persistence treatments with greater numbers of t r i a l s before the switch (30 and 40 t r i a l treatments) required more v i s i t s per t r i a l to obtain the amount of nectar they required (Table 4) , which remained r e l a t i v e l y constant (Table 5). Treatment t value p r o b a b i l i t y Switch 10 5.022 0 .000 Switch 20 4.102 0.001 . Switch 30 7 .160 0 .000 Switch 40 6.208 0.000 Table 3. Comparison of performance before and a f t e r the switch. Figures are based on the average proportion correct for a l l birds i n each treatment for the 5 t r i a l s immediately before and the 5 t r i a l s immediately a f t e r the reversal. Treatment names refer to the number of t r i a l s before the reversal of the pattern of rewarding feeders. P r o b a b i l i t i e s are the chance of no difference. Treatment t value p r o b a b i l i t y Switch 10 -1.522 0.203 Switch 2 0 1.989 0 .118 Switch 3 0 3 .595 0.023 Switch 40 3.066 0.037 Table 4. Comparison of t o t a l v i s i t s before and a f t e r the switch. Figures are based on the average number of v i s i t s per t r i a l for a l l birds i n each treatment for the 5 t r i a l s before and the 5 t r i a l s a f t e r the re v e r s a l . Treatment names refer to the number of t r i a l s before the reversal of the pattern of rewarding feeders. P r o b a b i l i t i e s are the chance of no difference. Treatment t value p r o b a b i l i t y Switch 10 -5.573 0 .005 Switch 20 -2.173 0.099 Switch 30 -2.166 0.096 Switch 40 0.000 1.000 Table 5. Comparison of t o t a l correct v i s i t s before and af t e r the switch. Figures are based on the average number of correct v i s i t s per t r i a l for a l l birds i n each treatment for the 5 t r i a l s immediately preceding the pattern reversal and the 5 t r i a l s immediately following the reversal. Treatment names refer to the number of t r i a l s before the reversal of the pattern of rewarding feeders. P r o b a b i l i t i e s are the chance of no difference. 42 Pattern Learning and Persistence Performance improved a g a i n o v e r the nex t f i v e t o t e n t r i a l s u n t i l i t was a t o r near t h e l e v e l j u s t b e f o r e t h e p a t t e r n s w i t c h . Improvement f o l l o w i n g t h e s w i t c h was s t r o n g l y s i g n i f i c a n t i n a l l cases u s i n g e i t h e r p e r f o r m a n c e measure, showing t h a t b i r d s i n a l l t r e a t m e n t s l e a r n e d t h e new p a t t e r n s o f r e w a r d i n g f e e d e r s d u r i n g t h e 40 p o s t - s w i t c h t r i a l s ( T a b le 6 ) . Treatment I n c o r r e c t V i s i t s P r o p o r t i o n C o r r e c t F v a l u e p r o b a b i l i t y F v a l u e p r o b a b i l i t y S w i t c h 10 56.698 0.000 • 55.550 0 .000 S w i t c h 2 0 13.530 0.001 30.744 0.000 S w i t c h 3 0 38.850 0.000 53.234 0.000 S w i t c h 40 57.516 0.000 66.127 0 .000 T a b l e 6. R e g r e s s i o n a n a l y s i s of improvement i n p o s t - s w i t c h p erformance u s i n g b o t h performance i n d i c a t o r s (measured a g a i n s t t h e n a t u r a l l o g o f t r i a l t o improve l i n e a r i t y ) . C a l c u l a t i o n s a r e based on averages o f t h e pe r f o r m a n c e o f a l l b i r d s i n a t r e a t m e n t . Treatment names r e f e r t o t h e number o f t r i a l s b e f o r e the r e v e r s a l o f t h e p a t t e r n o f r e w a r d i n g f e e d e r s . As p r e d i c t e d , t h e i n t e n s i t y and d u r a t i o n o f t h e performance drop was r e l a t e d t o t h e d u r a t i o n o f exposure t o th e p a t t e r n b e f o r e t h e s w i t c h ( F i g . 5 ) . Drop i n performance a f t e r t h e s w i t c h i n c r e a s e d i n magnitude as d u r a t i o n o f exposure i n c r e a s e d ( p o s i t i v e l y s l o p e d l i n e a r r e g r e s s i o n f i t t e d t o t h e 5 t r i a l averages o f t o t a l i n c o r r e c t v i s i t s : F = 42.280, r = 0.811, r e s i d u a l df = 22, p = 0.000). Even e x c l u d i n g t h e z e r o p o i n t , the r e l a t i o n s h i p between b i r d p e rformance and exposure i s s t r o n g l y s i g n i f i c a n t ( p o s i t i v e l y s l o p e d r e g r e s s i o n a n a l y s i s e x c l u d i n g t h e z e r o p o i n t : 43 Figure 5. Average number of incorrect v i s i t s per t r i a l by-birds for each of the treatments i n the 5 t r i a l s immediately following the pattern reversal (the maximum incorrect v i s i t s possible i s 32) . The X axis shows the number of t r i a l s birds experienced before the switch. The l i n e passes through the average performance for each treatment. Individual points show the results for each b i r d (3 per treatment, and 12 for the zero point) . The beginning of each experimental run exposes birds to a novel pattern with no previous exposure to a similar pattern, so i t i s equivalent to a switch a f t e r a zero t r i a l exposure to the pattern, providing the f i f t h point. Insets show sample performances for birds i n individual treatments (shaded c i r c l e s surround these values). 44 Pattern Learning and Persistence F =23.914, r = 0.840, residual df = 10, p = 0.001). While the r e l a t i o n s h i p does not appear lin e a r , a non-linear f i t to t h i s l i n e w i l l be even stronger, since a straight l i n e underestimates the strength of t h i s r e l a t i o n s h i p . This p o s i t i v e relationship between persistence of formerly rewarding behaviour and previous rewarding experience was not l i n e a r , but sigmoid; persistence increased l i t t l e i f any below 20 t r i a l s of i n i t i a l experience and l i t t l e beyond 30 t r i a l s , but increased markedly between 20 and 3 0 t r i a l s . The greater drop i n performance by birds with longer exposures to the pattern produced a range of errors between treatments that was i n i t i a l l y large and was t y p i c a l l y greatest between the 10 t r i a l and 40 t r i a l pre-switch treatments i n the period immediately following the switch (Fig. 6). This difference i n response by the birds . to the pattern reversal (measured by incorrect v i s i t s ) gradually decreases during the 40 post-switch t r i a l s u n t i l differences due to any remaining treatment effect are masked by random v a r i a t i o n i n performance among t r i a l s i n each treatment. V i s i t a t i o n Patterns Several potential sources of error could produce re s u l t s s i m i l a r to those I found. F i r s t , I needed to rule out the p o s s i b i l i t y of unplanned cues to rewarding feeders. There could conceivably be v i s u a l traces of nectar, marks on the array or any of a number of other p o s s i b i l i t i e s . If such cues were available and birds knew how to use them, 45 2 0 D i f 0 1 1 1 1 1 0 10 20 30 40 Trials after switch Figure 6. Differences i n number of incorrect v i s i t s (errors) by birds i n each of the treatments i n the period following the pattern reversal. The l i n e represents the maximum range of differences i n the number.of errors between the 4 treatments. This range i s greatest immediately following the switch, and decreases throughout the course of the remaining t r i a l s . 46 Pattern Learning and Persistence they should v i s i t more rewarding feeders than chance (50% correct) on the f i r s t t r i a l , but the birds did not d i f f e r s t a t i s t i c a l l y from random v i s i t a t i o n (t = 1.494, df = 11, mean difference = 0.066, p <= 0.163), providing no evidence for i n i t i a l use of external cues. Posit i o n a l biases (which i n some protocols could a l t e r v i s i t a t i o n patterns enough to affect performance measures) were not a major concern due to the diagonally symmetric nature of the quarters pattern and the randomised presentation of the two versions of the pattern i n my protocol. These two factors (randomisation and a symmetric pattern), ensured that birds with horizontal or v e r t i c a l biases would s t i l l encounter equal numbers of rewarding and non-rewarding feeders. Birds did show some po s i t i o n a l bias (Fig. 7) . They s i g n i f i c a n t l y preferred feeders higher . i n the room (Kolmogorov-Smirnov test of observed v i s i t s versus a uniform d i s t r i b u t i o n : Maximum difference = 0.391, p = 0.000). There were both v e r t i c a l and horizontal biases i n v i s i t patterns as well (K-S test of v i s i t s versus v e r t i c a l uniformity: Maximum difference =0.59, p = 0.004, K-S test of v i s i t s versus horizontal uniformity: Maximum difference = 0.63, p = 0.001). Birds were most heavily biased towards higher feeders during the f i r s t 10 t r i a l s (Fig. 8), although this bias did decrease over time as seen i n Figure 7. 47 Figure 7. Total of a l l v i s i t s to each feeder ( a l l birds on a l l treatments, before and a f t e r switch). If no p o s i t i o n a l bias occurred the height of the g r i d at each feeder l o c a t i o n would be the same, producing a f l a t surface. This figure was produced using a step-smoothing algorithm. As a r e s u l t , each feeder location i s represented by 16 g r i d u n i t s . 48 Figure 8. Total of a l l v i s i t s to each feeder i n the f i r s t 10 t r i a l s ( a l l birds on a l l treatments) . If no p o s i t i o n a l bias occurred the height of the g r i d at each feeder l o c a t i o n would be the same, producing a f l a t surface. This figure was produced using a step-smoothing algorithm. As a r e s u l t , each feeder location i s represented by 16 g r i d u n i t s . 49 Pattern Learning and Persistence While birds exhibited p o s i t i o n a l bias, t h e i r i n i t i a l explorations of the array (on the f i r s t t r i a l ) were not predictable (Fig. 9), and did not appear to be systematic or ordered. Birds began to explore a l l areas of the array a f t e r t h e i r i n i t i a l v i s i t s , but they showed no obvious systematic and consistent v i s i t a t i o n patterns over time (Fig. 10) . 50 o o o o o o o o $ o o o o (fcooo ® o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o ^ a o o o o o o<$d® o o o o 0(S^f-4oOOO o o e o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o <$>o® o o o o o o o o o o o o o 0-e-fe.O\O e^)o o o o o tef o o o o o o o o o o o o o o o o o o o o o o o o o o o 0,0 00 0 0 0 0 o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o Figure 9. Sample v i s i t t r a j e c t o r i e s of 6 d i f f e r e n t birds on t h e i r f i r s t 10 v i s i t s of T r i a l 1. Each box represents the feeder array and i l l u s t r a t e s a di f f e r e n t b i r d . In a l l cases shown, the top right and bottom l e f t quarters of the array were rewarding. The s o l i d l i n e marking each array shows the v i s i t a t i o n sequence during the t r i a l . The arrow head represents the d i r e c t i o n of travel and black dots represent feeders v i s i t e d during the t r i a l . 3 5 0(p(^® o o o o 0 Jb olht) o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o 2 o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o i ® o o o o o o o * OOOOOOOf) 0 0 ( ^ ) 0 0 0 0 o o o V e o o o o o o o o o o o o o o o <s> o o o o o o o o 0 0 0 0 0 ( ^ 0 o o o o o o o o o o o o o o o o 4 O ^ t ^ O O O O ^ f f O O O O 0 0 ^ 0 0 0 0 o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o oooooooo oooooooo OOOOOOM o o o o ®-® ^ 6 oooooooo oooooooo oooooooo 6 Of^OOOOO MOOOOOO 0-4)0000 00 GOOOOOOO ^ o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o Figure 10. Sample t r a j e c t o r i e s for one b i r d on the f i r s t 10 v i s i t s of T r i a l s 1 - 6. Each box represents the feeder array and i l l u s t r a t e s a diff e r e n t t r i a l . The top l e f t and bottom right quarters of the array were rewarding.' T r i a l numbers are to the l e f t of each box. The s o l i d l i n e marking each array shows the v i s i t a t i o n sequence during the t r i a l . The arrow head represents the di r e c t i o n of tr a v e l and black dots represent feeders v i s i t e d during the t r i a l . 52 Pattern Learning and Persistence Section IV. Discussion The b i r d s i n t h i s experiment l e a r n e d a s i m p l e p a t t e r n i n a v e r y s h o r t t i m e , c o n s i s t e n t l y a c h i e v i n g o v e r 80% s u c c e s s a f t e r about t e n t r i a l s . T h e i r r a p i d l y i m p r o v i n g p e r f ormance s u g g e s t s t h a t i n a n o v e l environment t h e y b e g i n l e a r n i n g reward p a t t e r n s r i g h t away, c o r r o b o r a t i n g t h e r e s u l t s o f S u t h e r l a n d (1985). Advantages of Learning M o d e l l i n g s t u d i e s i n d i c a t e l e a r n i n g can reduce s e a r c h t i m e s f o r h i d d e n o b j e c t s t o a t l e a s t one t h i r d o f n a i v e p e r f o r m a n c e (Benhamou, 1994). S i n c e t h e r e w a r d i n g f e e d e r s were uncued, l e a r n i n g t h e p a t t e r n p r o v i d e d a means t o reduce energy spent on f o r a g i n g . I n a p r e d i c t a b l e e n v i r o n m e n t , l e a r n i n g i s an e f f i c i e n t approach t o f o r a g i n g . L e a r n i n g t h r o u g h i n c r e a s e d e x p e r i e n c e i n a s t a b l e environment p r o v i d e s more e f f i c i e n t f o r a g i n g because s e a r c h t i m e i s red u c e d and f o o d i s l o c a t e d more r a p i d l y ( G i l l i n g h a m and B u n n e l l , 1989) . Factors Affecting Learning Cues P a s t s t u d i e s have shown t h a t g l o b a l and d i s t a l cues beyond t h o s e p r e s e n t e d i n t e n t i o n a l l y can be an i m p o r t a n t s o u r c e o f i n f o r m a t i o n f o r f o r a g i n g a n i m a l s ( O l t o n , 1990; 53 Pattern Learning and Persistence Spetch and Edwards, 1988; Suzuki et al. , 1980; van L u i j t e l a a r et al., 1989). There was no evidence here that birds used such things as odours or small v i s i b l e traces of nectar to i n i t i a l l y locate rewarding feeders, but t h e i r bias towards high feeders indicates that cues outside of the array (such as the arrangement of c e i l i n g and walls, echoes, or even gravity) play some role i n t h e i r s p a t i a l explorations. Since p r o f i t a b i l i t y was uncued, the arrangement of feeders on the array, combined with d i s t a l cues such as p o s i t i o n i n the room, should have played a primary r o l e i n learning. Using d i s t a l cues to locate rewards without s p e c i f i c l o c a l cues i s harder than using l o c a l cues (Spetch and Edwards, 1988). In my experiment, feeder p o s i t i o n was cued (by a surrounding orange ring) but not feeder q u a l i t y . Search Techniques In learning feeder quality, the birds used t r i a l and error exploration during i n i t i a l t r i a l s . Early feeding f l i g h t t r a j e c t o r i e s (Figs. 8 and 10) suggest that i n i t i a l exploration was not random, but I could f i n d no evidence for systematic search (stereotyped series of v i s i t s with predictable rules about direction, number of v i s i t s or other c h a r a c t e r i s t i c s of the v i s i t ) to t h e i r explorations. In a study on hummingbird foraging i n the wild (Wolf and Hainsworth, 1991), hummingbirds used random but area r e s t r i c t e d search; that i s , they showed no predictable 54 Pattern Learning and Persistence sequence of movements yet s t i l l remained within a r e s t r i c t e d area of a patch on a given bout rather than moving f r e e l y throughout the entire patch. In my experiments, once birds located rewarding feeders they tended to return to those locations within and between bouts and sample areas around those s i t e s . When these searches were not rewarding, birds might search nearby areas to see i f more distant places might be better. T r i a l and error combined with area r e s t r i c t e d search has also been seen i n species such as badgers (Mellgren and Roper, 1986) and Japanese monkeys (Menzel, 1991) and i n models simulating e f f i c i e n t foraging t a c t i c s (Ollason, 1983). Systematic search patterns have also been seen, especially i n insects such as bumblebees and honeybees (Dreisig, 1989; Menzel, 1985). It appears that search techniques are t i e d to the unique needs of each species and to the situ a t i o n (Root and Kareiva, 1984) . Some times my birds quickly found one rewarding quarter of the array but were extremely slow to locate the other one. I selected i n t e r t r i a l periods and reward amounts so birds could e a s i l y maintain t h e i r weight throughout the day, that may have reduced t h e i r motivation to feed. Using longer i n t e r t r i a l periods (e.g. Sutherland, 1985) or decreasing the amount or quality of rewards could have forced greater exploration of the array, but I chose to minimize r i s k to the animals, since I was already concerned about t h e i r o v e r a l l health. 55 Pattern Learning and Persistence S t a b i l i t y Learning i s most e f f e c t i v e i n stable environments (Nishimura, 1994). Caching birds such as Clark's Nutcrackers have surroundings that r e t a i n s i m i l a r c h a r a c t e r i s t i c s for long periods of time. These birds can learn and remember food caches for at least 6 months (Balda, 1980; Balda and Kamil, 1992). Chickadees, who also cache food, can r e t a i n cache memory for at least 4 weeks (Hitchcock and Sherry, 1990). Spatial learning a b i l i t i e s are a consequence of the normal d i s t r i b u t i o n of resources for species (Bond et al., 1981) . Animals discount the value of unpredictable resources (Bowers and Adams-Manson, 1993). As a broad generalization, animals i n stable environments appear to have better a b i l i t i e s to learn and remember tasks dealing with stable items than animals who must deal with continual and unpredictable change i n similar items. Thus, while caching species remember stored food locations for long periods, the continual depletion and renewal of hummingbird nectar sources over days to months i n the same l o c a t i o n biases them not to remember individual flower q u a l i t i e s during feeding bouts. When they do show evidence of foraging memory within bouts i n a patch they usually exhibit win-shift behaviour, avoiding. previously successful locations (Cole et al., 1982). Similar r e s u l t s have been seen i n other nectariv'orous species such as bananaquits 56 Pattern Learning and Persistence (Wunderle and Martinez, 1987) . This does not mean that nectar feeding animals have i n f e r i o r s p a t i a l memory or learning a b i l i t i e s but that they learn and remember items that are l i a b l e to remain stable such as c h a r a c t e r i s t i c s of rewarding flower types. Their s p a t i a l memories are also evident at coarser s p a t i a l scales, as they c l e a r l y remember the q u a l i t y of patches of flowers (Armstrong et al., 1987; Cole et al., 1982; Gass and Sutherland, 1985; M i t c h e l l , 1989; Valone, 1992), and whole foraging habitats (Armstrong, 19?.; Gass, 1978b; Sutherland et a l . , 1992; Tamm, 1987). Costs of Learning Sampling Once the birds learned the general pattern of rewarding feeders, the number of incorrect v i s i t s dropped to a small but continuing amount. While most of these incorrect choices were probably errors, some were probably ongoing sampling of the environment by the b i r d i n an attempt to detect changes i n reward location, as seen i n other animals (Draulans, 1988; Gass, 1985; Kramer and Weary, 1991; Tamm, 1987; Wilkie et al., 1981). Sampling and mistakes cannot be distinguished i n most protocols, including mine. Sampling i s a way for an animal to continue exploring i t s environment and test for change, as ' i n exploration of novel items by rats to improve t h e i r knowledge of t h e i r surroundings (Pinel et al. , 1986); however, i f uncertainty increases greatly> animals explore less and spend more time 57 Pattern Learning and Persistence e x p l o i t i n g known r e s o u r c e s i n s t e a d of s e a r c h i n g f o r a d d i t i o n a l ones (Forkman, 1991). Change L e a r n i n g can be a d i s a d v a n t a g e i n t h e f a c e o f major changes i n an a n i m a l ' s s u r r o u n d i n g s , such as t h e sudden and complete r e v e r s a l o f the p a t t e r n i n t h i s e x p e r i m e n t . Performance dropped s t r o n g l y and s i g n i f i c a n t l y a f t e r t h e r e v e r s a l o f t h e f e e d e r p a t t e r n ; i t dropped below chance f o r th e f i r s t few t r i a l s a f t e r the s w i t c h ( t y p i c a l l y 3 - 5 t r i a l s ) . D u r i n g t h i s s h o r t p e r i o d o f poor p e r f o r m a n c e a f t e r t h e s w i t c h , b i r d s i n c u r r e d a c o s t t h a t d i r e c t l y r e f l e c t e d t h e i r p e r s i s t e n c e w i t h what they had l e a r n e d b e f o r e t h e s w i t c h i n s t e a d o f i m m e d i a t e l y changing t h e i r b e h a v i o u r t o e x p l o r e t h e new p a t t e r n . W h i l e the number o f c o r r e c t v i s i t s r emained r e l a t i v e l y c o n s t a n t , r e f l e c t i n g hummingbirds' t e n d e n c i e s t o f o r a g e i n ways t h a t p r o v i d e c o n s t a n t energy i n t a k e s (Tooze and Gass, 1984), b i r d s who e x p e r i e n c e d more t r i a l s b e f o r e t h e s w i t c h r e q u i r e d more v i s i t s p e r t r i a l t o o b t a i n t h e same amount o f n e c t a r a f t e r t h e s w i t c h . B e f o r e t h e s w i t c h , l e a r n i n g was advantageous because i t r e d u c e d f o r a g i n g e f f o r t d u r i n g t h e p e r i o d o f p a t t e r n s t a b i l i t y . I n an e x t r e m e l y v a r i a b l e environment i n w h i c h t h e p a t t e r n o f p r o f i t a b i l i t y changed o f t e n and u n p r e d i c t a b l y , r e l i a n c e on s p a t i a l l e a r n i n g would c o n t i n u e t o i n c u r c o s t s w i t h each change. B o t h r e s o u r c e p o o r environments and h i g h l y v a r i a b l e environments can overcome 58 Pattern Learning and Persistence t h e v a l u e o f l e a r n i n g ( N i s h i m u r a , 1994) . S i m i l a r p e r s i s t e n c e i n t h e f a c e o f change w i t h s i m i l a r a s s o c i a t e d c o s t s was seen i n r u f o u s hummingbirds by S u t h e r l a n d (1985) and i n Anna's hummingbirds by C o l l i a s and C o l l i a s (1968). A drop i n performance and i n c r e a s e i n e x p l o r a t i o n was a l s o seen i n g o l d f i s h (Warburton, 1990) and chipmunks (Kramer and Weary, 1991) . Expectations and Persistence As e x p e r i e n c e w i t h t h e s t a b l e p a t t e r n i n c r e a s e d , p e r formance f o l l o w i n g t he p a t t e r n r e v e r s a l dropped more. A n i m a l s use p a s t e x p e r i e n c e t o gauge f u t u r e r e t u r n s (Bowers and Adams-Manson, 1983). U n t i l t h e p a t t e r n was r e v e r s e d t h e r e was no r e a s o n f o r t h e b i r d s t o d i s c o u n t t h e v a l u e o f u s i n g t h e i r s p a t i a l memory o f the p a t t e r n t o g u i d e f o r a g i n g b o u t s . G i v e n my e x p e r i m e n t a l d e s i g n , t h e b i r d s had no way t o e x p e c t t h e unexpected and reduce t h e i r p e r s i s t e n c e w i t h l e a r n e d b e h a v i o u r s ; however, my r e s u l t s t r o n g l y s u g g e s t s t h a t hummingbirds weight t h e i r p a s t e x p e r i e n c e i n c r e a s i n g l y h e a v i l y as t h e i r e x p e r i e n c e i n s t a b l e e n v i r o n m e n t s i n c r e a s e s . A n i m a l s a c t as i f t h e i r most r e c e n t e x p e r i e n c e i s t h e most i m p o r t a n t f o r t h e purposes o f g u i d i n g f u t u r e c h o i c e s (Haccou e t al., 1991; Haefner and C r i s t , 1994; Todd and K a c e l n i k , 1993), and d i s c o u n t l e s s r e c e n t e v e n t s as a f u n c t i o n o f t h e ti m e s i n c e t h e y were l e a r n e d and t h e number of i n t e r v e n i n g e x p e r i e n c e s (McHose and P e t e r s , 1975; 59 Pattern Learning and Persistence McNamara et al., 1989). These c o n c e p t s were i n c o r p o r a t e d i n t o t h e memory window models suggested by s e v e r a l s e t s o f a u t h o r s ( K a c e l n i k et al., 1987; McNamara and Houston, 1985b), but a r e d i s t i n c t from t h e p r i m a c y e f f e c t , a p r e f e r e n c e f o r i n f o r m a t i o n a c q u i r e d e a r l y i n t r a i n i n g ( M a c P h a i l , 1982), and the re c e n c y e f f e c t , a p r e f e r e n c e f o r i n f o r m a t i o n a c q u i r e d most r e c e n t l y ( C r y s t a l and S h e t t l e w o r t h , 1994; G a f f a n , 1992; G a f f a n , 1994; Kesner e t a l . , 1994; O l t o n , 1985; Reed, 1994; W r i g h t , 1994). O t h e r models o f s p a t i a l memory a l s o i n c o r p o r a t e t h e i d e a t h a t t i m e s i n c e l e a r n i n g a f f e c t s memory g u i d e d b e h a v i o u r s ( S p e t c h , 1990; W i l k i e and Kennedy, 1987; W i l k i e et al., 1990). The s i g m o i d shape o f t h e c u r v e seen i n t h i s e x p e r i m e n t ( F i g . 5) i m p l i e s t h a t by t e n t r i a l s , b i r d s had a l r e a d y begun t o e x h i b i t p e r s i s t e n c e i n t h e f a c e o f changes i n t h e p r o f i t a b i l i t y o f r e w a r d i n g f e e d e r s . Over t h e n e x t t h i r t y t r i a l s t h e i r p e r s i s t e n c e i n c r e a s e d t o a maximum. The maximum change i n b i r d performance a f t e r t h e s w i t c h may c o r r e s p o n d t o a d u r a t i o n o f exposure a t w h i c h t h e b i r d s t r e a t e d t h e l e a r n e d p a t t e r n s as i f th e y had always e x i s t e d . T h i s p o i n t may c o r r e s p o n d r o u g h l y t o t h e s i z e o f t h e memory window f o r t h i s k i n d of l e a r n i n g t a s k f o r t h e s e b i r d s . I n t h i s i n t e r p r e t a t i o n , l o n g e r d u r a t i o n s o f exposure t o c o n s i s t e n t p a t t e r n s c o u l d not produce a l a r g e r s u r p r i s e e f f e c t because t h e y had exceeded t h e s i z e o f t h e w o r k i n g memory windows o f t h e a n i m a l s . F u r t h e r , t h e i n i t i a l l e v e l 60 Pattern Learning and Persistence portion of the curve would correspond to a period when, for the animals, the patterns of rewarding feeders were s t i l l new and had not been f u l l y learned. The r a p i d l y increasing persistence near the i n f l e c t i o n point of the curve may represent a period of rapidly increasing expectations about s t a b i l i t y of the pattern. This general strategy of rapidly learning to r e l y on past experience, strong but ephemeral resistance to change, and more rapid abandonment of newly learned responses makes sense for animals i n a natural environment. An animal i n a novel s i t u a t i o n , i f i t r e a l i z e s that i t s s i t u a t i o n i s new, w i l l be u n l i k e l y to r i s k wasting energy by stereotyping i t s foraging before i t i s certain of the location, abundance, and p r e d i c t a b i l i t y of food sources. A l t e r n a t i v e l y , i t i s u n l i k e l y to abandon i t s perception of i t s environment i n a f a m i l i a r s i t u a t i o n when i t experiences minor v a r i a t i o n s i n i t s foraging success; that i s , the persistence of learned behaviours, or behavioural i n e r t i a , makes ec o l o g i c a l sense. Generally, behaviours based on short term experiences tend to be more f l e x i b l e , while consolidated memories and experiences are less f l e x i b l e (Gould, 1986c). Hull (1943) applied a s i m i l a r p r i n c i p l e when he described habit strength (the strength of an association between stimulus and response) which he believed increased with increasing reinforcement. 61 Pattern Learning and Persistence These same p r i n c i p l e s s h o u l d a p p l y t o t h e memory window h y p o t h e s i s . I n a v a r i a b l e h a b i t a t , o l d e r i n f o r m a t i o n i s l e s s l i k e l y t o remain v a l i d due t o ongoing e n v i r o n m e n t a l change, and we know t h a t r e l i a n c e on s p a t i a l memory v a r i e s w i t h t h e t e m p o r a l and s p a t i a l c o m p l e x i t y o f t h e environment (Warburton, 1990) . I n a complex environment, t o o much i n f o r m a t i o n can o v e r l o a d memory c a p a c i t y ( N i s h i m u r a , 1994) . I n t h e case o f a hummingbird f o r a g i n g , t h i s c o m p l e x i t y c o u l d be g e n e r a t e d by t e r r i t o r i a l r a i d s by i n t r u d e r b i r d s (Ewald and B r a n s f i e l d , 1987; Ewald and C a r p e n t e r , 1978; Ewald and O r i a n s , 1983; G i l l and Wolf, 1979), new n e c t a r p r o d u c t i o n (George, 1980), m a t u r a t i o n o f new f l o w e r s and d e t e r i o r a t i o n o f o l d blooms (Gass et a l . , 1976), changes i n t h e q u a l i t y o f whole p a t c h e s o f f l o w e r s (Gass and S u t h e r l a n d , 1985), o r a m y r i a d o f o t h e r i t e m s . G i v e n a l i m i t e d a b i l i t y t o remember p a s t e v e n t s , more r e c e n t items s h o u l d a l s o be g i v e n h i g h e r w e i g h t i n g t o reduce the impact o f memory f a d i n g o v e r t i m e , w h i c h i s a common problem (Aronsohn e t al., 1978) t h a t can l e a d t o i n c r e a s i n g e r r o r s i n s p a t i a l t a s k s ( B o l h u i s et al., 1987; Sp e t c h , 1990; S t r i j k s t r a and B o l h u i s , 1987). Relearning After a Change The r e d u c t i o n i n f o r a g i n g s u c c e s s i n d u c e d by t h e p a t t e r n r e v e r s a l e v e n t u a l l y l e d t o t h e b i r d s c h a n g i n g t h e i r f o r a g i n g b e h a v i o u r , v i s i t i n g p r e v i o u s l y u n r e w a r d i n g f e e d e r s w h i c h t h e y had been a v o i d i n g . T h i s change too k a s h o r t t i m e , o c c u r r i n g o v e r f i v e t o t e n t r i a l s (or 30 t o 60 m i n u t e s 62 Pattern Learning and Persistence of actual time) . During t h i s period, some birds d i d not v i s i t the feeder array, v i s i t e d one or two formerly good feeders and then gave up, or fed repeatedly at non-rewarding feeders, but none of them immediately began intensive exploration of the array for changes i n p r o f i t a b i l i t y of formerly non-rewarding feeders. Over the course of f i v e to ten t r i a l s a f t e r the switch, the birds learned the new feeder pattern, eventually returning to performance l e v e l s above 80% correct. Conclusions These experiments have corroborated e a r l i e r findings that hummingbirds learn 2-dimensional patterns quickly (Sutherland, 1985). More importantly, they demonstrate persistence of learned patterns i n the face of sudden change as a function of experience of s t a b i l i t y before the change. This persistence dissipates rapidly, however (in t h i s case under the pressure of severely reduced foraging p r o f i t a b i l i t y ) , and the birds soon learn the a l t e r e d reward pattern. Hummingbirds seem disposed to a strategy of rapid learning i n spite of or perhaps because of the problems imposed by u n p r e d i c t a b i l i t y . 6 3 Chapter 3 Landmark Forms and Spatial Memory in Rufous Hummingbirds. Section I. Introduction Spatial Memory Spatial memory i s the process by which animals remember locations i n t h e i r environment. Among b i r d species, s p a t i a l memory i s used for tasks such as navigating, foraging and defending t e r r i t o r i e s (Balda and Kamil, 1988; Gass and Montgomerie, 1981; Shettleworth, 1983). Spa t i a l memory affords d i s t i n c t energetic and ecolog i c a l advantages (Valone, 1991). Modelling studies suggest that using s p a t i a l memory to forage can provide greater than a f i v e - f o l d energy advantage over completely random search and a three to f i v e - f o l d advantage over systematic searching (Armstrong et a l . , 1987; Benhamou, 1994) . Cues and Landmarks One component of developing a map of the environment i s to learn the positions of recognizable landmarks and cues to 64 Landmark Forms a s s o c i a t e i t e m s i n t h e environment w i t h e x p e c t e d r e s u l t s . I w i l l d e f i n e a reward cue ( h e r e i n a f t e r termed "cue") as an i n d i c a t o r o f reward t h a t i s a s s o c i a t e d w i t h t h a t r e w a r d i n space and ti m e (and i n a 1:1 r a t i o ) , and a reward landmark ( h e r e i n a f t e r termed "landmark") as a n a v i g a t i o n a l a i d t h a t i n d i c a t e s an a r e a c o n t a i n i n g reward s i t e s . I n many f o r a g i n g cases t h e r e w i l l be c o n s i d e r a b l e o v e r l a p between t h e s e two a i d s t o l o c a t i n g f o o d , because t h e d i f f e r e n c e between a r e a s and s p e c i f i c l o c a t i o n s may be u n c l e a r ; f o r example an a r e a may c o n t a i n o n l y one p o t e n t i a l s i t e . D i f f e r e n t i a t i n g between t h e s e ways o f r e l a t i n g t o t h e environment i s d i f f i c u l t not o n l y i n p r a c t i c e , b u t i n p r i n c i p l e . I t may be unimportant whether t o l a b e l a g i v e n o b j e c t as a landmark o r a cue. For my p u r p o s e s , I w i l l g e n e r a l l y use t h e term landmark t o d e s c r i b e t h e f e a t u r e s I used i n my e x p e r i m e n t a l a r r a y s , because I i n t e n d e d them t o d e l i m i t groups o f f e e d e r s , not i n d i v i d u a l f e e d e r s . These f e a t u r e s do, however, c o n t a i n i n f o r m a t i o n t h a t c o u l d be c o n s i d e r e d t o be cue i n f o r m a t i o n . Cues There a r e s e v e r a l c a t e g o r i e s o f cues. D i s t a l cues a r e s e p a r a t e d by some v a r i a b l e d i s t a n c e from t h e reward s i t e (Brown, 1994; Brown and Gass, 1993; Schenk, 1987; S u t h e r l a n d e t al., 1987). L o c a l cues a r e near t h e reward s i t e ( S p e t c h and Edwards, 1988), c o n t i g u o u s cues a d j o i n t h e reward s i t e (Brown and Gass, 1993; P i n e l et al., 1986), and g l o b a l cues 65 Landmark Forms have a more tenuous r e l a t i o n s h i p w i t h a s p e c i f i c r e w a r d s i t e ( S p e t c h and Edwards, 1988). G l o b a l cues (and i n some ca s e s d i s t a l cues) i n c l u d e many items t h a t o t h e r a u t h o r s would c a l l landmarks. Examples of g l o b a l cues i n a l a b o r a t o r y s e t t i n g i n c l u d e p o s i t i o n s o f the w a l l s , overhead l i g h t s and d o o r s . Landmarks I have d e f i n e d landmarks as n a v i g a t i o n a l a i d s a n i m a l s use t o l o c a t e reward s i t e s ( f o o d i s o n l y one k i n d o f r e w a r d ) . T h i s d e f i n i t i o n s u g g ests a t l e a s t two ways t o use t h e s e a i d s . I d e f i n e d landmarks i n t h e m i d d l e o f f o r a g i n g p a t c h e s as c e n t r e landmarks. I n n a t u r e , t h i s c o u l d be a t r e e s u r r o u n d e d by n e c t a r - p r o d u c i n g b e r r y bushes, t h e c e n t r a l s t a l k o f a f l o w e r i n g p l a n t , o r a r o c k i n t h e m i d d l e o f a t e r r i t o r y . A second type of landmark d e f i n e s t h e edge o f an i t e m . A s t r e a m a t the edge of a t e r r i t o r y o r a f e n c e s u r r o u n d i n g a v e g e t a b l e garden c o u l d b o t h s e r v e as edge landmarks. Role of Cues and Landmarks in Learning A n i m a l s use landmark and cue i n f o r m a t i o n t o d e v e l o p c o g n i t i v e maps of t h e i r s u r r o u n d i n g s (Tolman, 1948), and t h i s r e q u i r e s t h e use o f s p a t i a l memory. The a b i l i t y t o use s p a t i a l l e a r n i n g i s not u n i v e r s a l ; t h e r e a r e d i s t i n c t s p e c i e s d i f f e r e n c e s i n s k i l l l e v e l s . V a r i o u s s t u d i e s have s u g g e s t e d t h a t a n i m a l s , i n c l u d i n g p r i m a t e s , have d i f f i c u l t y l e a r n i n g t a s k s i n w h i c h t h e r e i s a s p a t i a l s e p a r a t i o n 66 Landmark Forms between reward s i t e s and reward cues (Pinel et a i . , 1986); hummingbirds, however, regularly use landmarks and cues to navigate towards reward s i t e s that are separated from reward cues, and t h i s behaviour can be duplicated i n a laboratory environment (Brown and Gass, 1993). Current Study The a b i l i t y of hummingbirds to use s p a t i a l information has been demonstrated i n laboratory and f i e l d experiments (G. Brown, 1992; Cole et al. , 1982; C o l l i a s and C o l l i a s , 1968; Gass, 1978a and 1978b; Gass and Sutherland, 1985; Gass et al., 1976; M i l l e r and Gass, 1985; M i l l e r et a l . , 1984; Thompson, 1994) . One recent study f a i l e d to f i n d evidence of s p a t i a l memory use by foraging hummingbirds, but the authors suggested possible methodological reasons for the f a i l u r e (Wolf and Hainsworth, 1991). In t h i s experiment I examine how rufous hummingbirds use edge and centre landmarks i n a s p a t i a l memory task. I expect birds to learn faster with edge landmarks than centre landmarks. Both types of landmark provide navigational information to f i n d p r o f i t a b l e feeders, but edge landmarks also delimit groups of rewarding feeders and can be used for tri a n g u l a t i o n due to the shape of the l i n e s I use for edge landmarks. Of special interest i s the information provided by these landmarks that helps animals to locate p o t e n t i a l food sources and assess t h e i r quality. In some treatments I 67 Landmark Forms p r o v i d e cues t o p r o f i t a b i l i t y i n t h e landmarks and e x p e c t t h e s e cues t o f u r t h e r speed l e a r n i n g . C h a p t e r 2 demonstrated t h a t hummingbird l e a r n i n g and use o f s p a t i a l memory a r e s e n s i t i v e t o e n v i r o n m e n t a l changes. By cha n g i n g the environment, we can e s t i m a t e t h e degree o f r e l i a n c e on memory. Here I a g a i n s u d d e n l y change t h e p r o f i t a b i l i t y o f d i s t r i b u t i o n s o f f e e d e r s t o probe l e a r n i n g and memory. I n one tre a t m e n t I move cues t o f e e d e r p r o f i t a b i l i t y s i m u l t a n e o u s l y w i t h t h e change i n p r o f i t a b i l i t y t o a s s e s s t h e use o f t h e s e cues by t h e b i r d s . I e x p e c t b i r d s t o be l e s s s u r p r i s e d by t h i s t r e a t m e n t and r e c o v e r more r a p i d l y from t h i s r e v e r s a l t h a n from uncued r e v e r s a l s . 68 Landmark Forms Section II. Materials and Methods Subjects I n t h i s experiment I used 6 a d u l t , female r u f o u s hummingbirds, (Selasphorus rufus) c a p t u r e d i n t h e f i e l d n e a r t h e R o s e w a l l Creek salmon h a t c h e r y , Vancouver I s l a n d , B.C. i n May 1991 and m a i n t a i n e d i n i n d i v i d u a l 0.6 x 0.6 x 0.6 m w i r e mesh cages f o r s e v e r a l months p r i o r t o t e s t i n g , d u r i n g w h i c h t i m e t h e y were used i n o t h e r l e a r n i n g e x p e r i m e n t s . Due t o poor h e a l t h , one b i r d was r e p l a c e d d u r i n g t h e c o u r s e o f t h e t r e a t m e n t sequence, b r i n g i n g t h e t o t a l number o f b i r d s t o seven ( a l l f e m a l e ) . Throughout t h e p e r i o d o f c a p t i v i t y t h e p h o t o p e r i o d was m a i n t a i n e d on a s c h e d u l e t h a t mimicked s e a s o n a l v a r i a t i o n under c o n d i t i o n s i n the w i l d . E x c l u d i n g t e s t p e r i o d s , t h e b i r d s were s u p p l i e d w i t h e i t h e r Roudybush hummingbird d i e t o r N e k t a r P l u s hummingbird d i e t ad libitum on weekdays. On weekends, t h e y had 25% s u c r o s e s o l u t i o n w i t h added v i t a m i n s ( A v i t r o n a v i a n v i t a m i n supplement) and m i n e r a l s ( A v i m i n a v i a n m i n e r a l supplement). Experimental Environment I c onducted a l l t r a i n i n g and ex p e r i m e n t s i n two rooms, each o f w h i c h was 1.1 x 2.6 x 2.6 m h i g h w i t h o v e r h e a d f u l l -s p e c t r u m f l u o r e s c e n t l i g h t s . W a l l s and c e i l i n g , e x c e p t t h e 69 Landmark Forms f e e d e r a r r a y , were a uniform l i g h t green c o l o u r and the f l o o r was a uniform sand c o l o u r . A s i n g l e , stand-mounted, 1.7 m h i g h perch was l o c a t e d at the c e n t r e of each room. Each p e r c h was f i t t e d w i t h a p h o t o c e l l to s i g n a l a r r i v a l s and d e p a r t u r e s . On one end w a l l of each room a 1.0 x 1.0 m dark green, metal p a n e l extended from j u s t below the c e i l i n g . Inset i n t o t h i s panel were 64 feeders i n a square 8 x 8 a r r a y spaced at 10.5 cm v e r t i c a l l y and h o r i z o n t a l l y . Each feeder c o n s i s t e d of a 2.0 cm l e n g t h of 1.67 mm I.D. Intramedic p o l y e t h y l e n e t u b i n g which had been flame heated and bent to form a t e r m i n a l r e s e r v o i r at one end. The r e s u l t i n g f e e d e r tube resembled a small smoker's pipe, whose bowl was an open n e c t a r r e s e r v o i r and whose stem served as a f l o r a l c o r o l l a . The stem of the feeder extended through a p h o t o d a r l i n g t o n p h o t o d e t e c t o r which b r i d g e d a 4mm h o l e d r i l l e d i n the metal a r r a y p a n e l . The t i p of the feeder was f l u s h w i t h the f r o n t of the p a n e l . Each hole was surrounded by an orange 19 mm Avery l a b e l punched wi t h a 6 mm c e n t r e h o l e . Perch and feeder a r r a y p h o t o c e l l s l e d to a computer which rec o r d e d a r r i v a l s , departures, and v i s i t d u r a t i o n s , a c c u r a t e to about 10 ms. Before each t r i a l I s u p p l i e d each rewarding feeder w i t h 2 u l of 22% sucrose (weight/weight) from a Hamilton PB-600-1 r e p e a t i n g d i s p e n s e r . T h i s volume i s w i t h i n the normal range of n e c t a r volumes found i n f l o r a l s p e c i e s used by rufous hummingbirds (Armstrong 1986; 70 Landmark Forms C a r p e n t e r e t al., 1983; Gass and R o b e r t s , 1992). Non-r e w a r d i n g f e e d e r s were l e f t empty, as a p r e v i o u s s t u d y showed t h a t b i r d s behaved t h e same i f f e e d e r s were empty o r f i l l e d w i t h w a t e r ( S u t h e r l a n d and Gass, i n p r e s s ) . Between t r i a l s t h e a r r a y was c o v e r e d by a b e i g e r o l l e r b l i n d o p e r a t e d from o u t s i d e the e x p e r i m e n t a l chamber by a p u l l c o r d . I n s e v e r a l c a s e s , an 8 mm videocamera, i t s t r i p o d and c o n t r o l c a b l e s were a l s o p r e s e n t i n t h e chamber t o a l l o w me t o v i d e o t a p e t h e s e s s i o n and o b t a i n a n e c d o t a l i n f o r m a t i o n about p e r f o r m a n c e . Experimental Design Treatments were d e s i g n e d t o compare t h e u t i l i t y o f edge and c e n t r e landmarks i n s p a t i a l p a t t e r n l e a r n i n g and t o e v a l u a t e t h e a d d i t i o n a l u t i l i t y o f p r o v i d i n g i n f o r m a t i o n i n t h e s e landmarks about the e n e r g e t i c q u a l i t y o f groups o f f e e d e r s . Landmarks were p a t t e r n s o f l i n e s (edge landmarks) o r c o l o u r e d d i s k s ( c e n t r e s ) , and t h e y were e i t h e r c o l o u r e d d i f f e r e n t l y i n r e w a r d i n g and non-rewarding s e c t o r s o f t h e a r r a y o r were a u n i f o r m c o l o u r throughout t h e a r r a y . Two t r e a t m e n t s combined edge and c e n t r e landmarks but p r o v i d e d q u a l i t y i n f o r m a t i o n o n l y i n one o f t h e two. F i n a l l y , i n one t r e a t m e n t t h a t p r o v i d e d i n f o r m a t i o n about q u a l i t y , I examined t h e e f f e c t s o f moving landmarks a l o n g w i t h p r o f i t a b l e f e e d e r s . 71 0 o o o o o 0 0 0 o 0 o 0 0 o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o 0 0 o o o o o o o o o o o o o o o 0 o o o o o o o o 0 o#o o o o#o 0 o o o o o o o o o o o o o o o o o o o o o o o o o 0 o o o o#o o o o#o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o# o o o o o o o o o o O O O 0 o o#o 0 O O O 0 o o o o o o o o o o# o o o o o o o o o o o o o o o o o o o o o o Figure 11. S t y l i z e d representations of the array markers used for the eight treatments described i n the text (not to s c a l e ) . In each diagram the u n f i l l e d c i r c l e s represent feeder locations marked by orange labels. Top l e f t : P l a i n array. Top r i g h t : Centre landmarks. Bottom l e f t : Edge landmarks. Bottom r i g h t : Both edge and centre landmarks. 72 Landmark Forms The b a s i c forms f o r t h e s e t r e a t m e n t s a r e shown i n s t y l i z e d r e p r e s e n t a t i o n s i n F i g u r e 1 1 . I use t h e acronyms l i s t e d below t o r e p r e s e n t t h e t r e a t m e n t s i n t h e graphs and t a b l e s o f t h e r e s u l t s s e c t i o n . The e i g h t t r e a t m e n t s f o r t h i s e x p e r i m e n t were ( i n e x p e c t e d o r d e r o f i n c r e a s i n g p e r f o r m a n c e o v e r s i x t y t r i a l s ) : 1 . P l a i n . A p l a i n a r r a y i n whi c h a l l f e e d e r s were marked o n l y w i t h t h e orange f e e d e r s t i c k e r s t h a t were p r e s e n t i n a l l t r e a t m e n t s (top l e f t diagram i n F i g . 1 1 ) . 2 . P l a i n C e n t r e s ( P l c t r ) . A 1 i n c h c i r c u l a r A v e r y l a b e l i n th e c e n t r e o f each o f the f o u r q u a d r a n t s o f t h e a r r a y . A l l f o u r l a b e l s were the same c o l o u r ( F i g . 1 1 , t o p r i g h t ) . 3 . C o l o u r e d C e n t r e s ( C l c t r ) . Same as P l c t r , b ut t h e l a b e l s i n r e w a r d i n g s e c t o r s were a d i f f e r e n t c o l o u r t h a n t h o s e i n n o n - r e w a r d i n g s e c t o r s ( F i g . 1 1 , top r i g h t ) . 4 . P l a i n L i n e s ( P l i n e ) . L i n e s of 6 mm d r a f t i n g t a p e s u r r o u n d i n g t h e f o u r s e c t o r s o f t h e a r r a y . A l l f o u r s q uares were of one c o l o u r ( F i g . 1 1 , bottom l e f t ) . 5 . C o l o u r e d L i n e s ( C l i n e ) . Same as P l i n e but r e w a r d i n g s e c t o r s were marked w i t h a d i f f e r e n t c o l o u r t h a n non-r e w a r d i n g s e c t o r s ( F i g . 1 1 , bottom l e f t ) . 73 Landmark Forms 6. P l a i n L i n e s w i t h C o l o u r e d C e n t r e s ( P l c c t ) . Squares of one c o l o u r s u r r o u n d i n g the f o u r s e c t o r s , w i t h l a b e l s o f two c o l o u r s marking r e w a r d i n g and n o n - r e w a r d i n g q u a r t e r s ( F i g . 1 1 , bottom r i g h t ) . 7 . C o l o u r e d L i n e s w i t h P l a i n C e n t r e s ( C l p c t ) . L a b e l s o f one c o l o u r i n each q u a r t e r w i t h squares o f d i f f e r e n t c o l o u r s d i f f e r e n t i a t i n g r e w a r d i n g and n o n - r e w a r d i n g q u a r t e r s ( F i g . 1 1 , bottom r i g h t ) . 8. C o l o u r e d L i n e S w i t c h (Clnsw). D i f f e r e n t l y c o l o u r e d s q u a r e s m a r k i n g the r e w a r d i n g and n o n - r e w a r d i n g q u a r t e r s ( F i g . 1 1 , bottom l e f t ) . When I r e v e r s e d t h e p r o f i t a b i l i t y of f e e d e r s , I a l s o r e v e r s e d t h e landmark p a t t e r n so t h a t t h e c o l o u r e d squares t h a t had p r e v i o u s l y been a s s o c i a t e d w i t h r e w a r d i n g f e e d e r s m a i n t a i n e d t h i s a s s o c i a t i o n . G l o b a l landmarks such as w a l l s , f l o o r and o t h e r room p a r a p h e r n a l i a cannot be e l i m i n a t e d from t h e e x p e r i m e n t , even i n a c o n t r o l s i t u a t i o n , and t o the e x t e n t t h a t b i r d s a t t e n d t o them, t h e y w i l l always add some u n d e r l y i n g n o i s e t o measures o f performance. S i n c e t h e s e f e a t u r e s remained c o n s t a n t a c r o s s a l l e x p e r i m e n t a l t r e a t m e n t s ( d i f f e r e n c e s between e x p e r i m e n t a l rooms s h o u l d have been c a n c e l l e d out by r a n d o m i s a t i o n o f room use a c r o s s t r e a t m e n t s ) , I i g n o r e d them i n my a n a l y s i s , assuming t h a t any s y s t e m a t i c e f f e c t s w ould c a n c e l o u t . 74 Landmark Forms I n each t r e a t m e n t t h e o r i g i n a l reward and landmark p a t t e r n c o n t i n u e d f o r 50 t r i a l s , t h e n t h e reward p a t t e r n was s w i t c h e d t o i t s m i r r o r image f o r 10 more t r i a l s so t h a t a l l p r e v i o u s l y r e w a r d i n g a r r a y l o c a t i o n s were now n o n - r e w a r d i n g and v i c e versa. The t e n t r i a l p e r i o d a f t e r t h e r e v e r s a l o f th e p a t t e r n o f r e w a r d i n g f e e d e r s i n d i c a t e s d i f f e r e n c e s i n th e p e r s i s t e n c e w i t h w h i c h b i r d s used p r e v i o u s l y l e a r n e d knowledge and t h e i r r e s i s t a n c e t o new l e a r n i n g . Each b i r d i n t h e experiment was exposed t o each o f t h e e i g h t t r e a t m e n t s . The o r d e r of t h e s e t r e a t m e n t s was randomized f o r each b i r d as was t h e arrangement o f p r e - and p o s t - s w i t c h p a t t e r n s , the e x p e r i m e n t a l room used, and t h e landmark c o l o u r s seen. Training Each b i r d was t r a i n e d f o r t h r e e days i m m e d i a t e l y p r i o r t o t e s t i n g . F o r t h e f i r s t two days a b i r d l i v e d i n i t s cage but was f e d ad libitum from a s t a n d a r d commercial u n l i m i t e d volume f e e d e r marked i d e n t i c a l l y t o t h o s e i n t h e e x p e r i m e n t a l chambers. On t h e morning o f t h e t h i r d day o f t r a i n i n g , t h e b i r d was moved t o an e x p e r i m e n t a l chamber w i t h t h e t r a i n i n g f e e d e r from i t s home cage (the e x p e r i m e n t a l f e e d e r a r r a y was c o v e r e d by t h e b l i n d ) . The s o l e p e r c h i n t h e room was r a i s e d t o a h e i g h t o f 2.4 m and t h e f e e d e r was p l a c e d d i r e c t l y i n f r o n t o f t h i s p e r c h . When t h e b i r d was u s i n g t h i s p e r c h n o r m a l l y , i t was g r a d u a l l y l o w e r e d t o 1.7 m, 75 Landmark Forms l e v e l with the centre of the covered feeding array. When the b i r d was using both feeder and perch, the feeder was moved d i r e c t l y i n front of the centre of the covered array. Once the b i r d was again feeding regularly, a l l 64 array locations were provided with 2 u l of 22% sucrose solution, the home cage feeder was removed, and the array was uncovered u n t i l the b i r d had fed from several feeders. The array was then covered, the feeders r e f i l l e d , and a new tr a i n i n g t r i a l was begun. Once the b i r d was consistently v i s i t i n g the panel, and showed minimal or no p o s i t i o n a l bias (based on informal estimation of any untrained preference for s p e c i f i c portions of the feeder array and i f necessary-enforced by temporarily covering areas of the array that the b i r d had not been foraging outside of u n t i l the blocking of preferred feeders caused foraging to become more widespread) i t was put through a series of 10-20 sham t r i a l s with a l l feeder locations p r o f i t a b l e i n order to accustom i t to the 1 minute t r i a l and 5 minute i n t e r t r i a l periods to be used during t e s t i n g the following day. Experimental Procedures On the day of testing each b i r d was presented with one of two randomly selected mirror image patterns of rewarding and non-rewarding feeders (Figure 1 i n Chapter 1) with one of the sets of markings described i n Experimental Design (Figure 11) . In each case, feeders i n the rewarding portions of the array were f i l l e d with 2 p i of 22% 76 Landmark Forms ( w e i g h t / w e i g h t ) s u c r o s e s o l u t i o n a t t h e b e g i n n i n g o f each t r i a l . T h i s p r o v i d e d a p o t e n t i a l f o r 64 \il o f n e c t a r t o be t a k e n i n each t r i a l and exceeded th e p r e f e r r e d meal s i z e o f r u f o u s hummingbirds under normal c o n d i t i o n s (Diamond et al., 1986) t o m i n i m i z e s t r e s s t o the b i r d s . Lime g r e e n and l i g h t b l u e landmarks were used f o r a l l t r e a t m e n t s ; b o t h c o n t r a s t e d w e l l w i t h t h e d a r k g r e e n p a n e l . I n t r e a t m e n t s u s i n g o n l y one c o l o u r , g r e e n o r b l u e was randomly a s s i g n e d . When b o t h c o l o u r s were p r e s e n t , t h e one a s s o c i a t e d w i t h r e w a r d i n g s e c t o r s f o r t h e f i r s t 50 t r i a l s was a s s i g n e d randomly. Each e x p e r i m e n t a l r u n c o n s i s t e d o f s i x t y one m i n u t e t r i a l s w i t h f i v e minute i n t e r t r i a l p e r i o d s . T h i s was i n t e n d e d t o a l l o w t h e b i r d s t o m a i n t a i n t h e i r w e i g h t t h r o u g h o u t t h e e x p e r i m e n t a l r u n . A l t h o u g h t r i a l s were one m i n u t e i n l e n g t h , b i r d s c o u l d s t o p f e e d i n g and r e t u r n t o t h e p e r c h a t any t i m e . D u r i n g t h e i n t e r t r i a l p e r i o d , t h e f e e d e r a r r a y was c o v e r e d by a b l i n d so t h a t t r i a l s o f f e r e d t h e o n l y o p p o r t u n i t y t o see t h e a r r a y and any a r r a y m a r k i n g s as w e l l as t h e o n l y o p p o r t u n i t y t o f e e d . Emptied r e w a r d i n g f e e d e r s were r e f i l l e d d u r i n g t h e i n t e r t r i a l p e r i o d . I m m e d i a t e l y p r e c e d i n g t h e f i r s t t r i a l , t h e s u b j e c t was f a s t e d f o r 15-20 m i n u t e s , o r 2 t o 3 normal meals. I i g n o r e d any t r i a l i n w h i c h t h e s u b j e c t d i d not v i s i t t h e f e e d e r p a n e l , imposed the normal i n t e r t r i a l i n t e r v a l and c o n t i n u e d as b e f o r e . P r e v i o u s s t u d i e s by S u t h e r l a n d (1985) 77 Landmark Forms and myself have shown that hummingbirds remove a l l nectar from the feeders when a volume of 2ul i s used. For t h i s reason, I treated a l l second and subsequent v i s i t s to feeders during t r i a l s as non-rewarding. At the end of f i f t y t r i a l s , I temporarily halted the experiment, emptied, flushed and dried a l l rewarding feeders and f i l l e d a l l previously non-rewarding feeders. In a l l but one treatment I l e f t array markings unchanged. In Treatment 8 (the coloured l i n e switch treatment), I changed the landmark l i n e s so that the colour formerly associated with rewarding feeders was s t i l l associated with rewarding feeders but i n the opposite quarters of the array to the period of the previous 50 t r i a l s . Once I had completed the appropriate changes I restarted the experiment; t h i s usually took 5 to 10 minutes. After these changes, I continued for an a d d i t i o n a l ten t r i a l s using the same procedures as i n the f i r s t f i f t y t r i a l s . After the l a s t t r i a l , I returned the b i r d to i t s home cage, flushed a l l feeders, and removed the array markings. 78 Landmark Forms Section III. Results Performance Indicators I measured learning by the proportion of correct f i r s t v i s i t s i n each t r i a l out of the t o t a l v i s i t s to f i l l e d feeders and by the t o t a l incorrect f i r s t v i s i t s to feeders. In Chapter 2 I emphasized that t o t a l incorrect v i s i t s was a stronger indicator than proportion correct when birds can s a t i a t e themselves during t r i a l s . In t h i s experiment, however, birds could not always obtain s u f f i c i e n t food to maintain t h e i r weight throughout s i x t y t r i a l s . Birds increased t h e i r feeding (total correct f i r s t v i s i t s ) over the course of the experimental runs i n s i x out of eight treatments (Fig. 12); this was s i g n i f i c a n t for four of the eight treatments (see Table 7 for summary s t a t i s t i c s ) . I n i t i a l Learning As i n Chapter 2, learning proceeded for a l l treatments as decelerating monotonic curves (Figs. 13 and 14). The differences between treatments l i e i n the rate of learning ( i n i t i a l slope) and i n peak performance. Since the learning rates were not constant, I tested the s i g n i f i c a n c e of the learning by l i n e a r regression of the appropriate performance indi c a t o r on the natural log of the t r i a l number. 79 24 18 CO "CO > •4—• o © i _ o O 12 0 - P L I N E ••• P L C T R • P L C C T — P L A I N - C L P C T — C L N S W — C U N E • - C L C T R J 3 4 Blocks of 10 Trials 6 Figure 12. Total correct v i s i t s per t r i a l (averaged across all birds i n each treatment and across blocks of 10 t r i a l s ) for a l l treatments. The X axis i s divided into blocks of 10 t r i a l s . The pattern was reversed af t e r block 5 ( t r i a l 50). Acronyms i n the legend correspond to the descriptions of treatments i n Methods. Pline = p l a i n l i n e s . P l c t r = p l a i n centres. Plcct = p l a i n lines and coloured centres. P l a i n = p l a i n array. Clpct = coloured l i n e s and p l a i n centres. Clnsw = coloured l i n e markers switched a f t e r the pattern reversal. Cline = coloured l i n e s . C l c t r = coloured centres. 80 Trial Trial Figure 13. Number of incorrect f i r s t v i s i t s per t r i a l averaged for a l l birds i n each of the 8 treatments. Two treatments are shown i n each panel. Acronyms for treatments are f u l l y described i n the methods section. Clnsw = coloured l i n e markers switched aft e r the pattern r e v e r s a l . Clpct = coloured l i n e s and p l a i n centres. Cline = coloured l i n e s . Plcct = p l a i n lines and coloured centres. Pline = p l a i n l i n e s . C l c t r = coloured centres. P l c t r = p l a i n centres. Plain = p l a i n array. 81 0 0 1 1 1 L - — 1 1 1 o.o 0 10 20 30 40 50 60 0 - 1 0 20 30 40 50 60 Trial Trial CLNSW CLPCT 10 20 30 40 50 60 0 Trial 10 20 30 40 50 60 Trial Figure 14. Proportion of f i r s t v i s i t s per t r i a l that were to rewarding feeders, averaged for a l l birds i n each of the 8 treatments. Two treatments are shown i n each panel. Acronyms for treatments are f u l l y described i n the methods section. Clnsw = coloured l i n e markers switched a f t e r the pattern reversal. Clpct = coloured l i n e s and p l a i n centres. Cline = coloured l i n e s . Plcct = p l a i n l i n e s and coloured centres. Pline = p l a i n l i n e s . C l c t r = coloured centres. P l c t r = p l a i n centres. Plain = p l a i n array. 82 Landmark Forms Treatment F value Probability Y intercept Slope 1. Pla i n 17 .899 0.000 12.142 0.072 2. P l c t r 35.107 0.000 11.387 0.076 3. C l c t r 4.302 0.043 15.699 0.044 4. Pline 102.399 0.000 6.52 0 .174 5. Plcct 0.206 0.652 18.422 0.000 6. Cline 0 .190 0.664 18.452 0.01 7. Clpct 0.096 0 .758 20.853 -0.007 8. Clnsw 0.476 0.493 18.612 0.014 Table 7. Linear regressions (since the r e l a t i o n s h i p i s assumed to be l i n e a r and f l a t ) of t o t a l correct f i r s t v i s i t s on t r i a l number for the f i r s t 50 t r i a l s . Acronyms for treatments are f u l l y described i n the methods section. Clnsw = coloured l i n e markers switched a f t e r the-pattern reversal. Clpct = coloured l i n e s and p l a i n centres. Cline = coloured l i n e s . Plcct = p l a i n l i n e s and coloured centres. Pline = p l a i n l i n e s . C l c t r = coloured centres. P l c t r = p l a i n centres. P l a i n = p l a i n array. Improvement i n performance was strongly s i g n i f i c a n t for a l l 8 treatments using proportion correct for the f i r s t 50 t r i a l s . Measuring performance by t o t a l incorrect indicated s i g n i f i c a n t improvement for birds i n 7 out of 8 treatments, with birds i n the p l a i n l i n e treatment showing the lone i n s i g n i f i c a n t improvement (Tables 8 and 9). Differences Between Treatments Birds learned the patterns d i f f e r e n t l y i n the 8 treatments (Fig. 13 and 14) ; repeated measures ANOVA of proportion correct using 5 t r i a l blocks as the repeated measures was strongly s i g n i f i c a n t : F(7,40 df) = 13.875, p = 0.000. Differences i n t o t a l incorrect f i r s t v i s i t s were s i m i l a r l y highly s i g n i f i c a n t (repeated measures ANOVA of the f i r s t 50 t r i a l s for 5 t r i a l blocks: F (7,40 df) = 5.289, p « 0.000) . 83 Landmark Forms Treatment F value Probability Y intercept Slope 1. Pla i n 68.599 0.000 0 .628 0.058 2. P l c t r 13 .215 0.001 0.738 0.028 3. C l c t r 134.565 0.000 0 .573 0.078 4. Pline 42.581 0.000 0.676 0.064 5. Plcct 463.101 0 .000 0 .596 0 .101 6. Cline 279.550 0.000 0.644 0.094 7. Clpct 170.072 0.000 0.642 0.096 8. Clnsw 199.572 0.000 0.618 0 .102 Table 8. Linear regressions of proportion of correct f i r s t v i s i t s on natural log of t r i a l number for the f i r s t 50 t r i a l s . Acronyms for treatments are f u l l y described i n the methods section. Clnsw = coloured l i n e markers switched a f t e r the pattern reversal. Clpct = coloured l i n e s and p l a i n centres. Cline = coloured l i n e s . Plcct = p l a i n l i n e s and coloured centres. Pline = p l a i n l i n e s . C l c t r = coloured centres. P l c t r = p l a i n centres. Plain = p l a i n array. Treatment F value Probability Y intercept Slope 1. Pla i n 21.736 0.000 6.453 -0.835 2. P l c t r 6.894 0.012 4.468 -0.387 3. C l c t r 32 .463 0 .000 8.030 -1.229 4. Pline 0.749 0.391 1.961 -0.120 5. Plcct 245.653 0 .000 9 .502 -2 .358 6. Cline 198.277 0 .000 7 .428 -1.926 7. Clpct 143.252 A AAA V • \J \J V 8.487 -2 .256 8. Clnsw 182 .978 0.000 8.733 -2 .326 Table 9. Linear regressions of t o t a l incorrect f i r s t v i s i t s on natural log of t r i a l number for the f i r s t 50 t r i a l s . Acronyms for treatments are f u l l y described i n the methods section. Clnsw = coloured l i n e markers switched a f t e r the pattern reversal. Clpct = coloured l i n e s and p l a i n centres. Cline = coloured l i n e s . Plcct = p l a i n l i n e s and coloured centres. Pline = p l a i n l i n e s . C l c t r = coloured centres. P l c t r = p l a i n centres. P l a i n = p l a i n array. Since the ANOVAs showed s i g n i f i c a n t differences i n performance between treatments I conducted Tukey honestly s i g n i f i c a n t difference analyses to contrast p a i r s of in d i v i d u a l differences i n both measures (Figs. 15 and 16). 84 Landmark Forms In general, there were few s i g n i f i c a n t differences i n performance (based on treatment means) i n early t r i a l s , but increasing differences throughout the period leading up to the pattern switch af t e r t r i a l 50. Differences between treatments reached a maximum in t r i a l s 30 - 40. From t r i a l 40 - 50, the Tukey tests show that performance was s i g n i f i c a n t l y better on arrays marked with l i n e s than on p l a i n arrays or those marked only with centres. Immediately a f t e r the switch there were again few s i g n i f i c a n t differences i n performance, but the differences reappeared more rapidl y during t h i s period of relearning than they appeared i n the i n i t i a l learning phase. Performance from t r i a l 56 to t r i a l 60 reveals a number of s i g n i f i c a n t l y d i f f e r e n t responses to the pattern switch. Tukey analyses show 2-tailed differences only. I compared sets of these pairwise differences to indicate the order of d i f f i c u l t y of the treatments (Table 10) . In most cases the r e s u l t i n g ranks correspond c l o s e l y with my predictions. For the f i r s t 50 t r i a l s , I expected that performance would increase i n the order: p l a i n , p l a i n centres, coloured centres, p l a i n l i n e s , p l a i n l i n e s with coloured centres, coloured lines and coloured l i n e switch (tied), with the best performance from birds v i s i t i n g an array marked with coloured lines and p l a i n centres. The observed rankings d i f f e r only i n the poor performance of the birds on the coloured centres pattern. 85 14 12 H 3 6 io H 3i 1 2 H 5 2 8 4 5" 6. !6" 1 . 2 " 4 . 5 -?: 8 " 3. 2a 1-4-5" 1, 3 2. 5. 4' 67 36 3' 2B| 44-i 2 i 3-1 7' 5' T 41 7 6 5 "I 8 ~ ~ 1 56 11 16 21 26 31 46 51 Trial Number Figure 15. Summary of Tukey analysis of t o t a l incorrect f i r s t v i s i t s per t r i a l averaged for a l l birds i n each of the 8 treatments. Results along the x axis are grouped into blocks of 5 t r i a l s , with axis numbers i n d i c a t i n g which t r i a l begins the 5 t r i a l block. The switch occurred immediately before t r i a l 51. Lines connecting treatments indicate that there was not a s i g n i f i c a n t difference i n performance for the birds i n these treatments during the indicated block. Numbers ref e r to the di f f e r e n t treatments: 1 = p l a i n array, 2 = p l a i n centres, 3 = coloured centres, 4 = p l a i n l i n e s , 5 = p l a i n l i n e s and coloured centres, 6 = coloured l i n e s , 7 = coloured l i n e s and p l a i n centres, 8 = coloured l i n e markers switched a f t e r the pattern reversal. 86 p r o P 0 r t 1 o n C o r r e c t 0.6 0.55 H 0.5 0.45 0.95 - 7 • 6 . 0.9 - 8 " 5 . 87" 2 • 0.85 - 6- 4 • 25-0.8 -4 - 3 • 0.75 -2' 4 " 1-1-0.7 -16 • 7 B 3 " Am 58" 0.85 -4 6 . 5" J : 6B. 87 8 B 57-6 • 5 • 1 3 7 6 1 8' 5' 3 . 1' 2' 67» 3 " 2" 1-f i l 4-3 . 1" 7 . 5 • 2 I 7 6 1 75 " 1 3 2 "1 I I 1 1 1 -r-11 16 21 28 31 36 41 Trial Number 46 51 56 Figure 16. Summary of Tukey analysis of proportion of f i r s t v i s i t s per t r i a l that were correct, averaged for a l l birds i n each of the 8 treatments. Results along the x axis are grouped into blocks of 5 t r i a l s , with axis numbers in d i c a t i n g which t r i a l begins the 5 t r i a l block. The switch occurred immediately before t r i a l 51. Lines connecting treatments indicate that there was not a s i g n i f i c a n t difference i n performance for the birds i n these treatments during the indicated group of t r i a l s . Numbers r e f e r to the d i f f e r e n t treatments: 1 = p l a i n array, 2 = p l a i n centres, 3 = coloured centres, 4 = p l a i n l i n e s , 5 = p l a i n l i n e s and coloured centres, 6 = coloured l i n e s , 7 = coloured l i n e s and p l a i n centres, 8 = coloured l i n e markers switched a f t e r the pattern reversal. 87 Landmark Forms Treatment Pre- Switch Only Post--Switch Only Complete Run Prop Tot Comb Prop Tot Comb Prop Tot Comb Corr Inc Rank Corr Inc Rank Corr Inc Rank 1. Plain 2 1 1.5 2.5 2 2 2 2 2 2. Plctr 3 3 3 2.5 3 3 3 3 3 3. Clctr 1 2 1.5 1 1 1 1 1 1 4. Pline 5 4 4 5 4 4 5 4 4.5 5. Plcct 4 5 5 7.5 5.5 6.5 4 5 4.5 6. Cline 7.5 7 6.5 4 5.5 5 6.5 6 6 7. Clpct 6 8 8 6 7 6.5 6.5 8 7 8. Clnsw 7.5 6 6.5 7.5 8 8 8 7 8 T a b l e 10. Ranked means of t r e a t m e n t s from Tukey a n a l y s i s . I n t h i s t a b l e a rank of 8 i n d i c a t e s t h a t b i r d s i n t h i s t r e a t m e n t p e r formed b e t t e r than b i r d s i n any o t h e r t r e a t m e n t , w h i l e a rank o f 1 i n d i c a t e s t h e w o r s t p erformance o f any group o f b i r d s . Prop. C o r r . r a n k i n g s based on p r o p o r t i o n c o r r e c t . T o t . I n c . = r a n k i n g s based on t o t a l i n c o r r e c t f i r s t v i s i t s . Comb. Rank = Average o f the two r a n k s . Numbers i n t h e p r e -s w i t c h o n l y column a r e averages o f t h e ra n k s f o r t h e f i r s t 50 t r i a l s . The p o s t - s w i t c h o n l y column shows averag e s from t r i a l s 51 - 60. Complete r u n d a t a a r e averages a c r o s s a l l 60 t r i a l s . Acronyms f o r t r e a t m e n t s a r e f u l l y d e s c r i b e d i n the methods s e c t i o n . Clnsw = c o l o u r e d l i n e markers s w i t c h e d a f t e r t h e p a t t e r n r e v e r s a l . C l p c t = c o l o u r e d l i n e s and p l a i n c e n t r e s . C l i n e = c o l o u r e d l i n e s . P l c c t = p l a i n l i n e s and c o l o u r e d c e n t r e s . P l i n e = p l a i n l i n e s . C l c t r = c o l o u r e d c e n t r e s . P l c t r = p l a i n c e n t r e s . P l a i n = p l a i n a r r a y . A f t e r t h e p a t t e r n r e v e r s a l I e x p e c t e d a s i m i l a r o r d e r o f performance as i n the f i r s t 50 t r i a l s , but w i t h b i r d s i n the c o l o u r e d l i n e s w i t c h p a t t e r n o u t p e r f o r m i n g t h o s e i n any o t h e r t r e a t m e n t . A g a i n , the observ e d r a n k i n g s c o r r e s p o n d e d w e l l w i t h t h e s e e x p e c t a t i o n s . B i r d s i n t h e c o l o u r e d c e n t r e s t r e a t m e n t p e r f o r m e d s u r p r i s i n g l y p o o r l y a g a i n , w h i l e t h o s e w i t h p l a i n l i n e s and c o l o u r e d c e n t r e s showed s u r p r i s i n g l y good r e c o v e r y from t h e p a t t e r n r e v e r s a l . 88 Landmark Forms O v e r a l l , I e x p e c t e d t h e o r d e r o f performance t o be p l a i n , p l a i n c e n t r e s , c o l o u r e d c e n t r e s , p l a i n l i n e s , p l a i n l i n e s w i t h c o l o u r e d c e n t r e s , c o l o u r e d l i n e s , c o l o u r e d l i n e s w i t h p l a i n c e n t r e s and c o l o u r e d l i n e s w i t c h . The o b s e r v e d r a n k i n g s f o l l o w e d t h e s e p r e d i c t i o n s w i t h t h e e x c e p t i o n o f b i r d s u s i n g t h e a r r a y marked w i t h c o l o u r e d c e n t r e s , on w h i c h performance was p o o r e s t . Switch E f f e c t B i r d s i n t h e 8 t r e a t m e n t s responded d i f f e r e n t l y t o a p a t t e r n r e v e r s a l as shown g r a p h i c a l l y ( F i g s . 13 and 14) and by Tukey a n a l y s i s (Table 10; F i g s . 15 and 1 6 ) . R a n k i n g s o f b i r d p erformance a f t e r the p a t t e r n r e v e r s a l were d i f f e r e n t t h a n b e f o r e t h e r e v e r s a l . B i r d s u s i n g a r r a y s w i t h b o t h l i n e s and c e n t r e s performed r e l a t i v e l y more p o o r l y a f t e r t h e s w i t c h (compared t o o t h e r t r e a t m e n t s ) t h a n b e f o r e . The most o b v i o u s d i f f e r e n c e i n r e s p o n s e s t o p a t t e r n r e v e r s a l s was between c o l o u r e d l i n e and t h e c o l o u r e d l i n e s w i t c h t r e a t m e n t s , w h i c h I used s p e c i f i c a l l y t o t e s t t h e e f f e c t o f p a t t e r n r e v e r s a l s on l e a r n i n g . I moved t h e r e w a r d i n g c o l o u r s w i t h t h e r e w a r d i n g f e e d e r s i n t h e c o l o u r e d l i n e s w i t c h t r e a t m e n t but not i n t h e c o l o u r e d l i n e t r e a t m e n t . When t h e c o l o u r e d i n d i c a t o r o f p r o f i t a b i l i t y f o l l o w e d t h e movement o f p r o f i t a b l e f e e d e r s , b i r d s made ma r k e d l y fewer e r r o r s a f t e r t h e s w i t c h (compared t o t h e same p a t t e r n when f e e d e r s were s w i t c h e d but landmark p a t t e r n s s t a y e d t h e same). 89 Landmark Forms B i r d s i n a l l t r e a t m e n t s l e a r n e d t h e new p a t t e r n o f r e w a r d i n g f e e d e r s as shown by t h e s i g n i f i c a n t l i n e a r r e g r e s s i o n s o f performance on t h e n a t u r a l l o g o f t r i a l number ( T a b l e s 11 and 12). Treatment F v a l u e P r o b a b i l i t y Y i n t e r c e p t S l o p e 1. P l a i n 89.780 0.002 240.096 -57 .790 2. P l c t r 20.590 0.002 210.157 -50.358 3. C l c t r 24.413 0.001 292 .914 -70.625 4. P l i n e 36.071 0.000 274.380 -66.603 5. P l c c t 14.579 0.005 240.830 -58.853 6. C l i n e 34.356 0.000 406.061 -99.362 7. C l p c t 14.569 0.005 285.390 -69 .648 8. Clnsw 44.806 0.000 286.374 -70 .246 T a b l e 11. L i n e a r r e g r e s s i o n s o f t o t a l i n c o r r e c t f i r s t v i s i t s on n a t u r a l l o g o f t r i a l number f o r t h e 10 t r i a l s a f t e r t h e s w i t c h . Acronyms f o r t r e a t m e n t s a r e f u l l y d e s c r i b e d i n t h e methods s e c t i o n . Clnsw = c o l o u r e d l i n e m arkers s w i t c h e d a f t e r t h e p a t t e r n r e v e r s a l . C l p c t = c o l o u r e d l i n e s and p l a i n c e n t r e s . C l i n e = c o l o u r e d l i n e s . P l c c t = p l a i n l i n e s and c o l o u r e d c e n t r e s . P l i n e = p l a i n l i n e s . C l c t r = c o l o u r e d c e n t r e s . P l c t r = p l a i n c e n t r e s . P l a i n = p l a i n a r r a y . V i s i t a t i o n Patterns When b i r d s had g a i n e d c o n s i d e r a b l e e x p e r i e n c e w i t h t h e p a t t e r n o f r e w a r d i n g f e e d e r s ( t r i a l s 46 - 50) , t h e y made most e r r o r s t o non-rewarding f e e d e r s b o r d e r i n g t h e groups o f r e w a r d i n g f e e d e r s ( F i g . 17) . B i r d s v i s i t e d n o n - r e w a r d i n g f e e d e r s b e s i d e r e w a r d i n g f e e d e r s f o u r t i m e s more o f t e n , on average, t h a n t h e y v i s i t e d o t h e r n o n - r e w a r d i n g l o c a t i o n s (0.096 v e r s u s 0.025 ti m e s p e r t r i a l , r e s p e c t i v e l y ) . 90 Landmark Forms Treatment F value Probability Y intercept Slope 1. Pla i n 33.616 0.000 -9.740 2 .588 2. P l c t r 17.391 0.003 -7 .129 1.940 3. C l c t r 24.826 0.001 -12.989 3 .388 4. Pline 41.334 0.000 -11.212 2 .962 5. Plcct 13.752 0.006 -9 .722 2 .616 6. Cline 24.297 0.001 -13 .897 3.643 7 . Clpct 11.946 0.009 -9.046 2 .448 8. Clnsw 81.525 0 .000 -8.513 2 .327 Table 12. Linear regressions of proportion correct on natural log of t r i a l number for the 10 t r i a l s a f t e r the switch. Acronyms for treatments are f u l l y described i n the methods section. Clnsw = coloured l i n e markers switched a f t e r the pattern reversal. Clpct = coloured l i n e s and p l a i n centres. Cline = coloured l i n e s . Plcct = p l a i n l i n e s and coloured centres. Pline = p l a i n l i n e s . C l c t r = coloured centres. P l c t r = p l a i n centres. Plain = p l a i n array. Birds can remember rewarding locations, as demonstrated by t h e i r high performance on f i r s t v i s i t s , but they continued to r e v i s i t unrewarding feeders during a t r i a l . Even i n the f i n a l 5 t r i a l s before the switch, birds r e v i s i t e d feeders regularly, averaging 4.84 r e v i s i t s per rewarding location per t r i a l . Thus, only about 20% of "correct" v i s i t s were rewarding. 91 Figure 17. Total v i s i t s by a l l birds to non-rewarding locations i n t r i a l s 46 - 50 of a l l treatments. V i s i t s to rewarding locations are not shown. This figure was produced using a step smoothing algorithm. As a re s u l t , each feeder lo c a t i o n i s represented by 16 g r i d units. 92 Landmark Forms Section IV. Discussion Use of Array Markers The hummingbirds learned the d i s t r i b u t i o n of rewarding feeders under a l l sets of experimental conditions. The si m i l a r shapes of the i n i t i a l performance curves for a l l 8 treatments suggests that the birds used s i m i l a r processes to learn a l l of the treatments. Given t h i s , the s i g n i f i c a n t differences between the curves represent the r e l a t i v e usefulness of v i s u a l aids i n locating rewarding feeders. Adding markers to the p l a i n array sped up learning the array; birds more rapidly approached asymptotic performance with markers, and achieved a higher asymptote. The rankings of the d i f f e r e n t treatments indicate that edge markers are more useful locators of patches than centre marks and that providing a colour indicator to p r o f i t a b i l i t y i n the landmarks provides some learning benefits to the b i r d s . Lines versus Centres The strongest and most obvious difference between these treatments i s that lines were much more e f f e c t i v e aids to learning than central marks, which were l i t t l e better than a p l a i n array. Among several possible reasons for the sup e r i o r i t y of l i n e s , the most feasible i s that for hummingbirds, perhaps because of how they move during foraging, information delimiting the edges of patches i s 9 3 Landmark Forms more useful than information indicating t h e i r centres. Geometry i s an important aspect of landmark use (Cheng, 1986; Cheng and G a l l i s t e l , 1984; G a l l i s t e l , 1989 and 1990) . My edge landmarks were arranged into 4 squares surrounding feeders that were a l l either rewarding or non-rewarding. Birds could have used these edge landmarks to develop s p a t i a l rules of thumb about p r o f i t a b i l i t y based on e i t h e r l e f t - r i g h t and up-down movement i n r e l a t i o n to a set of l i n e s , or in-out orientations i n r e l a t i o n to the squares. Birds using arrays marked only with centre landmarks could form rules about near and far feeders i n r e l a t i o n to the landmarks. Alternatively, they could use vector o r i e n t a t i o n from eit h e r type of landmark to f i n d p r o f i t a b l e feeders, i n a fashion s i m i l a r to that suggested by Cheng (1989 and 1990). This vector sum model of orientation has some flaws though, e s p e c i a l l y i n r e l a t i o n to diagonal vectors, which animals seem to have more d i f f i c u l t y using. Another possible explanation for the difference between edge and centre landmarks i s that the differences i n the t o t a l amount of colour added to the array (centres = 20.3 cm^, lines = 566.4 cm^) was s u f f i c i e n t to make the l i n e s more useful. There may be some truth to t h i s second p o s s i b i l i t y . In general, animals prefer to use large landmarks near t h e i r rewards over others (Bennett, 1993; Cheng, 1989) . The l i n e form of array mark may provide a 94 Landmark Forms l a r g e landmark t h a t i s more u s e f u l t o a f o r a g i n g hummingbird t h a n t h e s m a l l e r c e n t r a l p l a c e mark. Lines versus Colours There was a s t r o n g d i f f e r e n c e between t h e u s e f u l n e s s o f b o t h k i n d s o f landmarks, per se, and landmarks w i t h r e w a r d i n f o r m a t i o n . There was a much s t r o n g e r d i f f e r e n c e between forms ( l i n e s v e r s u s c e n t r e s ) t h a n t h e r e was between p r e s e n c e o r absence o f reward i n f o r m a t i o n ( c o n t r a s t i n g o r same c o l o u r e d m a r k e r s ) . Adding c o l o u r as an i n d i c a t o r o f p r o f i t a b i l i t y d i d not s i g n i f i c a n t l y i n c r e a s e p e r f o r m a n c e but th e i n t e r a c t i o n o f c o l o u r and form d i d p r o v i d e a b e n e f i t t o l e a r n i n g . The s i g n i f i c a n t i n t e r a c t i o n e f f e c t c o u l d have s e v e r a l p o s s i b l e meanings. V a r i o u s a u t h o r s have d e m o n s t r a t e d t h a t a n i m a l s can a t t e n d t o s e v e r a l t y p e s o f s t i m u l i a t once ( C l a y t o n and Krebs, 1994; Gass and Montgomerie, 1981; G i r a u d o and Perauch, 1988; G l e i t m a n , 1963; G o u l d and M a r l e r , 1987; O l t o n , 1990; R e s c o r l a , 1986; R o b e r t s e t a l . , 1988; S a t t a t h and T v e r s k y , 1987; S h e r r y , 1984; S p e t c h and Edwards, 1988; V a l l o r t i g a r a and Z a n f o r l i n , 1989) . The b i r d s i n t h i s experiment a l s o a t t e n d e d t o two t y p e s o f i n f o r m a t i o n a t once; t h e y p e r f o r m e d b e t t e r when p r o v i d e d w i t h t h e c o m b i n a t i o n o f landmarks and i n f o r m a t i o n about p r o f i t a b i l i t y t han w i t h u n i f o r m a r r a y m a r k e r s . What do t h e s e d i f f e r e n c e s i n u s e f u l n e s s mean e c o l o g i c a l l y ? V a r i o u s a u t h o r s have d e m o n s t r a t e d t h e i m p o r t a n c e o f c o l o u r i n hummingbird f o r a g i n g . C o l l i a s and 95 Landmark Forms C o l l i a s (1968) used simple preference tests i n outdoor feeders to show that Anna's hummingbirds use colour cues i n choosing feeders of di f f e r e n t quality. M i l l e r et al. (1984) and Wheeler (1980) also demonstrated that colour i s an important v i s u a l cue for hummingbirds. A l l of these studies, however, demonstrated that colour i s less important than p o s i t i o n a l cues. The effect of colour was also overshadowed i n my study, i n th i s case by the type of marker. Cognitive Maps I believe that birds w i l l use these d i f f e r i n g landmark forms as an int e g r a l part of a cognitive map of t h e i r environments. Edge landmarks may help birds delimit patch boundaries, es p e c i a l l y during a period of area r e s t r i c t e d search a f t e r a reward s i t e has been located and exploited by techniques such as random search. The larger o v e r a l l area of the edge landmarks may also have f a c i l i t a t e d learning. Information about the quality of food locations i s presumably another component necessary for a successful cognitive map. The cognitive map concept has been challenged repeatedly i n the l i t e r a t u r e (M. Brown, 1992; C o l l e t t et al., 1986; C o l l e t t et a l . , 1993; Dyer, 1991 and 1993; Restle, 1957) but has gained wide acceptance by many authors (de Renzio, 1982; Ellen, 1980; G a l l i s t e l , 1989; Giraudo and Perauch, 1988; Gould and Marler, 1987; Nadel and Willner, 96 Landmark Forms 1980; Okaichi, 1987; O'Keefe and Conway, 1980; Olton, 1990; Sholl, 1987; Spetch and Honig, 1988; Srinivasan et al., 1989; Sutherland and Dyck, 1984; Thinus-Blanc and Ingle, 1985) . Skeptics suggest that at least some groups of animals, e s p e c i a l l y invertebrates, r e l y on dead reckoning to navigate rather than a remembered representation of the environment and argue that the evidence for cognitive mapping i s weak (Collett et a l . , 1993; Dyer, 1991). Another a l t e r n a t i v e to cognitive mapping i s the maintenance of a l i s t of s p e c i f i c locations with no reference to the geometric organization of these locations with respect to each other (M. Brown, 1992). Map-using animals should be capable of more adaptable movement patterns than those using dead reckoning or those checking l i s t s , including finding a goal s i t e from a novel environmental po s i t i o n (Ellen et a l . , 1984; G a l l i s t e l , 1989; Gould and Marler, 1987; Menzel, 1991; Nadel and Willner, 1980; Schenk, 1987; Sutherland and Dyck, 1984; Thinus-Blanc and Ingle, 1985) or navigating without using l o c a l landmarks i n a stereotyped fashion (Gould, 1986c; Kramer and Weary, 1991; Morris, 1981; Olton, 1990). The birds i n my experiment were not constrained to approach the feeder array from a novel position, (navigation through a known landscape from a novel position i s a common test for mapping) , but there was no evidence for repeated, stereotyped or 97 Landmark Forms s y s t e m a t i c movements w i t h i n t h e a r r a y (an i n d i c a t i o n o f t h e use o f dead r e c k o n i n g ) . Chunking L e a r n i n g a p a t t e r n o f f e e d e r s i s an i m p o r t a n t s t e p i n t h e development o f an o v e r a l l c o g n i t i v e map. I f b i r d s l e a r n a s p a t i a l p a t t e r n o f r e w a r d i n g f e e d e r s r a t h e r t h a n l e a r n i n g a s e t o f i n d i v i d u a l r e w a r d i n g l o c a t i o n s , t h e y c o u l d g a i n t h e advantage o f reduced i n f o r m a t i o n s t o r e d i n memory. T h i s p r o c e s s i n v o l v e s g r o u p i n g items such as e n v i r o n m e n t a l c h a r a c t e r i s t i c s i n t o u n i t s i n memory; t h i s i s known as c h u n k i n g . Humans do t h i s ( F i s k and L l o y d , 1988; Hemenway and Palmer, 1978; S h i f f r i n et al. , 1976), and i t has a l s o been d e s c r i b e d i n s e v e r a l a n i m a l s p e c i e s ( O l t o n , 1985; S u z u k i e t a l . , 1980; V a l l o r t i g a r a and Z a n f o r l i n , 1987 and 1989). The p r o c e s s o f l e a r n i n g a group o f s p a t i a l l y d i s t r i b u t e d components as an o v e r a l l p a t t e r n was de m o n s t r a t e d i n hummingbirds by S u t h e r l a n d and Gass ( i n p r e s s ) . Tolman, who suggested t h e concept o f c o g n i t i v e maps i n 1948, b e l i e v e d t h a t b r o a d l y a p p l i c a b l e and i n c l u s i v e maps were t h e norm, and t h a t n a r r o w l y d e f i n e d maps o r s e t s o f i n s t r u c t i o n s were t h e r e s u l t o f in a d e q u a t e cues, r e s t r i c t e d t r a i n i n g , o r s t r o n g m o t i v a t i o n s . I f t h i s i s t r u e , a map i n t h i s experiment might i n c l u d e not o n l y t h e p a t t e r n o f f e e d e r s , but a l s o t h e l o c a t i o n and d i s t a n c e from t h e p e r c h t o t h e a r r a y , and t h e l o c a t i o n of w a l l s , l i g h t s and doors i n 98 Landmark Forms the experimental chamber. Several studies have suggested the importance of such global cues i n s p a t i a l learning (Bennett, 1993; Spetch and Edwards, 1988; Spetch and Honig, 1988; Suzuki et a l . , 1980). Environmental Change, Complexity and the Switch E f f e c t Information about temporal changes i n reward s i t e s i s an important aspect of cognitive mapping and e f f e c t i v e foraging i n general (Biebach et a l . , 1989; G a l l i s t e l , 1989); however, the scale of temporal change i s important i n examining i t s effects (Gass, 1985; Gass and Montgomerie, 1981; Gass and Roberts, 1992). Hummingbirds i n my experiments did not learn to avoid depleted feeders during the course of a t r i a l , but learned to avoid empty feeders across a series of t r i a l s . The tendency to explore or sample the surrounding environment i s strongly affected both by the actual q u a l i t y of the environment and the animal's memories and perceptions of i t . For instance, animals change t h e i r foraging strategies more rapidly i n response to temporal v a r i a t i o n s i n reward when they possess information about several or many foraging s i t e s than i f they know only one food source (Mitchell, 1989). Animals with such r e s t r i c t e d information rapid l y change t h e i r behaviour only i f there i s an environmental change and they possess s u f f i c i e n t information about the environment. 99 Landmark Forms The switch i n this experiment demonstrated that hummingbird s p a t i a l memory i s resistant to sudden change. As Chapter 2 demonstrated, th i s resistance i s r e l a t e d to the number of t r i a l s i n which a b i r d has experienced s t a b i l i t y i n i t s environment. The results from th i s experiment into array markings also suggest (although not strongly) that when birds learn more about t h e i r environment and have more v i s u a l cues providing unchanging information, they are less l i k e l y to change t h e i r behaviour i n the face of sudden and unpredictable change, as shown by the comparatively poorer performance of birds i n treatments with both edge and centre landmarks. If the cues i n t h e i r environment change, however (as demonstrated i n the movement of coloured l i n e s a f t e r the switch i n one treatment), they are less r e s i s t a n t to change (Roberts et al., 1988). Performance by birds i n the treatment where array markers (coloured lines) moved with the rewarding feeders showed that the birds are able to track changes i n the array markers. The performance of birds on t h i s pattern af t e r the switch was better than any other. This result indicates that the birds learned to associate the colour of array markers with feeder q u a l i t y and followed the colour cues instead of r e l y i n g on s p a t i a l memory of feeder locations. The association between colour and reward, which was "portable", was balanced against the s p a t i a l memory of past reward locations. The birds i n t h i s 100 Landmark Forms treatment showed a small drop i n performance a f t e r the switch but recovered more rapidly than birds i n any other treatment. Their use of s p a t i a l memory was f l e x i b l e enough to rapi d l y adapt to rearrangement of groups of feeders. Responses to the switch reveal no simple patterns that apply to a l l treatments. The type of array markings had l i t t l e e f f e c t on the l e v e l to which performance dropped a f t e r the switch. Immediately a f t e r the switch, birds i n a l l treatments (excepting the treatment where p r o f i t a b i l i t y indicators followed the switch i n feeder p r o f i t a b i l i t y ) performed s i m i l a r l y , dropping to levels of foraging success which were s t a t i s t i c a l l y indistinguishable from each other. By the second block of 5 t r i a l s a f t e r the switch, however, birds returned to the pre-switch order of performance, with birds using arrays with edge landmarks performing better than those with p l a i n arrays or centre landmarks only. In a review of the timing of behaviour, K i l l e e n and Fetterman (1988) suggested that the richness or complexity of the environment affects animals' foraging. Studies with various animals have shown a si m i l a r l i n k between environmental richness and foraging. Chipmunks vary t h e i r exploratory behaviour based on the p r e d i c t a b i l i t y and richness of the environment (Kramer and Weary; 1991) . Rats use systematic l i n e a r foraging when food i s e a s i l y v i s i b l e , but become se l e c t i v e i n t h e i r search when the food i s hidden ( I l e r s i c h et a l . , 1988). Gerbils reduce exploration and 101 Landmark Forms become s h o r t term energy m a x i m i z e r s when u n p r e d i c t a b i l i t y i n c r e a s e s (Forkman, 1991). Bee f o r a g i n g i s a d a p t e d t o t h e t e m p o r a l and s p a t i a l p a t t e r n s o f t h e i r n a t u r a l f o o d s o u r c e s ( L a v e r t y and P l o w r i g h t , 1988; Menzel, 1985). Nor i s t h i s v a r i a b i l i t y i n ' s e a r c h l i m i t e d t o f o r a g i n g . B i r d s i n fragmented f o r e s t s appear t o l o c a t e new b r e e d i n g s i t e s by random s e a r c h f o r s u i t a b l e s i t e s ( H a i l a et al., 1993). Chipmunks may a d j u s t t h e i r s e a r c h t e c h n i q u e s t o t e m p o r a l and e n v i r o n m e n t a l c o n d i t i o n s b o t h i n f o r a g i n g and o t h e r t a s k s such as s e a r c h i n g f o r a mate (Kramer and Weary, 1991), as may o t h e r s p e c i e s (Gibb, 1961; G u i l f o r d and Dawkins, 1987; Warren and Warren, 1973). H e l l e r (1980) s u g g e s t s t h a t a n i m a l s b e g i n f o r a g i n g i n a p a t c h by u s i n g l i m i t e d c r i t e r i a f o r f o o d s o u r c e s , t h e n b r o a d e n i n g t h e i r c r i t e r i a as t i m e i n a p a t c h i n c r e a s e s . V a r i o u s forms of s e a r c h a r e l i k e l y an i n i t i a l s t e p i n a n a i v e e x p l o r a t i o n o f an a n i m a l ' s environment. Once a r e w a r d i n g s i t e has been found and e x p l o i t e d (perhaps by random s e a r c h f o r a l i m i t e d s e t of f o r a g i n g c r i t e r i a ) , t h e f o r a g e r may r e s t r i c t i t s e l f t o s e a r c h around t h a t s i t e (Wolf and H a i n s w o r t h , 1991), a l t h o u g h t h i s s t e p i s v a r i a b l e and depends on t h e a n i m a l ' s knowledge of t h e s u r r o u n d i n g environment ( M i t c h e l l , 1989), i t s m o t i v a t i o n (Forkman, 1991), t h e v a r i a b i l i t y o f the environment (Kramer and Weary, 1991) and a number of o t h e r f a c t o r s (Weiss, 1983). I f random s e a r c h h e l p s l o c a t e new f o o d s o u r c e s , a r e a r e s t r i c t e d 102 Landmark Forms search i s an e f f e c t i v e way to define the boundaries of food sources. The birds i n my experiments may be t r e a t i n g one sector of the array i n a similar fashion to a compound inflorescence or a bush or some other form of r e s t r i c t e d patch. Once birds had experienced a number of t r i a l s they made most errors ( f i r s t v i s i t s to non-rewarding feeders) at feeders adjoining the rewarding feeders. This may be due to uncertainty about the edges of the rewarding patch or may be sampling of areas around the rewarding patch to detect changes i n p r o f i t a b i l i t y . Eventually the animal w i l l learn the reward s i t e s and values of the rewards i n i t s environment. The locations and values of the rewards should be a major portion of i t s cognitive map. In order to return to the known reward s i t e s , however, the animal must use information from landmarks and cues to navigate through i t s environment (Cheng, 1986; G a l l i s t e l , 1989 and 1990; Shettleworth and Krebs, 1986). The markers provided on the array presumably provided information to as s i s t i n th i s step i n map formation. Conclusions This experiment demonstrates that hummingbirds use landmarks to locate reward s i t e s . The form of these landmarks i s important, and hummingbirds learn patterns of rewarding feeders more rapidly and better using edge landmarks than with central landmarks. They also use 103 Landmark Forms information about reward quality conveyed by the colour of these markers, although the effect of reward information does not provide a very strong benefit to learning. Once birds have learned t h e i r surroundings, they p e r s i s t i n using t h i s knowledge u n t i l they have s u f f i c i e n t evidence that t h e i r memories are no longer a valuable source of information in. foraging. The strength of t h i s persistence may be related to the success they have achieved i n t h e i r environment before a change. Persistence of use of s p a t i a l memories can be reduced by providing information i n d i c a t i n g that a change has occurred. 104 Chapter 4 S p a t i a l Association and Spatial Memory i n Rufous Hummingbirds Section I. Introduction I n t h i s experiment I examined t h e c o n t r a s t i n g e f f e c t s o f s p a t i a l a s s o c i a t i o n and s p a t i a l memory by v a r y i n g t h e p e r i o d o f exposure t o a p a t t e r n o f r e w a r d i n g f e e d e r s and t h e s p a t i a l s e p a r a t i o n between a cue t o p r o f i t a b i l i t y o f a f e e d e r and t h a t f e e d e r . T h i s s t u d y was a l s o i n t e n d e d t o t i e t o g e t h e r some o f t h e a s p e c t s o f s p a t i a l l e a r n i n g d i s c u s s e d i n C h a p t e r s 2 and 3. S p a t i a l Association Learning S i m p l e a s s o c i a t i v e l e a r n i n g i s t h e p r o c e s s o f a s s o c i a t i n g a c o n t i g u o u s cue and response s i t e . T y p i c a l examples o f s i m p l e a s s o c i a t i v e l e a r n i n g i n c l u d e a r a t p r e s s i n g t h e c o r r e c t b a r i n a group o f b a r s t o o b t a i n a reward o r a s s o c i a t i n g movement t o t h e c o r r e c t arm o f a maze w i t h a f o o d reward (Bond et a l . , 1981; C o l w i l l , 1985; Hoffmann and M a k i , 1986; M a c k i n t o s h , 1983; M a k i , 1979). I n t h e s e s i t u a t i o n s , t h e a n i m a l l e a r n s t o r e s p o n d a t t h e same l o c a t i o n as t h e s t i m u l u s . I n o t h e r s i t u a t i o n s , however, 105 Spatial Association and Spatial Memory there may be a displacement i n space between the stimulus and the response or reward si t e s (Rumbaugh et al., 1989). In such cases, many animals have d i f f i c u l t y learning the task without special t r a i n i n g protocols and lengthy t r a i n i n g periods (Davis, 1974; Pinel et a l . , 1986; Schrier et a l . , 1963; S t o l l n i t z and Schrier, 1962). For the purposes of th i s study I define s p a t i a l association learning as the process of associating a s p a t i a l l y separated cue and reward (Bowe, 1984; Brown and Gass, 1993). Simple as s o c i a t i v e learning, i n which the reward and cue are contiguous, i s a much simpler task for animals to learn i n both natural and laboratory environments and has been heavily documented (for instance Aadland et al., 1985; Balda et al., 1986; Bond et al., 1981; Bruce and Herman, 1987; Clayton and Krebs, 1993 and 1994; Cole et al., 1982; C o l w i l l , 1985; Dallery and Baum, 1991; Dawkins, 1971a and 1971b; G a l l i s t e l , 1989; Gillingham and Bunnell, 1989; Fuchs and Haken, 1988a). In nature, however, there are various examples of animals learning to associate a separated cue and response or reward s i t e . The use of marks on banner petals to assess nectar q u a l i t y of flowers by bees (Gori, 1989), and the use of c i r c l i n g vultures by predators to locate prey (Houston, 1983; Rabenold, 1983 and 1987) are both examples of s p a t i a l association learning. Brown and Gass (1993) demonstrated the a b i l i t y of hummingbirds to carry out s p a t i a l association 106 Spatial Association and Spatial Memory-learning tasks i n a laboratory environment a f t e r a short and simple t r a i n i n g period. S p a t i a l Memory Simi l a r l y , f a c i l i t y with s p a t i a l memory tasks has been demonstrated for varied tasks and species (Gleitman, 1963; Gould, 1986a and 1986b; Grigoryan and Stolberg, 1989; Healy and Krebs, 1992; Hermer and Spelke, 1994). Sp a t i a l memory i s simply the use of remembered information about l o c a t i o n to navigate through the environment. Previously v i s i t e d s i t e s may be found only by dead reckoning (moving between two fi x e d points along a series of remembered vectors) i n some pr i m i t i v e animals (Collett et al. , 1993; Dyer, 1993) but there i s considerable evidence for cognitive maps of the environment i n most higher animals (Gould, 1986a; Menzel, 1973; O'Keefe and Conway, 1980; Olton, 1990). Sp a t i a l memory may be used for almost any ecological function, from foraging for food (Hitchcock and Sherry, 1990; Kamil and Roitblat, 1985; MacDonald and Wilkie, 1990; McQuade et al., 1986), to finding the way home (Holldobler, 1980; Robinson and Dyer, 1993) or to some other location (Morris, 1981; Schenk, 1987; Shettleworth, 1983), to finding mates (Kramer and Weary, 1991) or finding offspring (McCracken, 1993). Learning Processes Why would animals e a s i l y remember locations (on t h e i r own or locations d i r e c t l y associated with response sites) 107 Spatial Association and Spatial Memory but have d i f f i c u l t y learning to associate cues that are displaced from response si t e s with the response s i t e s ? This difference suggests that there may be some underlying p h y s i o l o g i c a l difference i n how these learning processes occur and that these differences may a f f e c t which form of learning i s more advantageous i n s p e c i f i c instances. The best we can say about this i s that the neural bases for these forms of learning are s t i l l speculative. We do have strong evidence that s p a t i a l memory i s a form of long term memory stored at least p a r t l y i n the hippocampus (Ellen, 1980; Kesner, 1980; Okaichi, 1987; O'Keefe and Conway, 1980; Olton, 1990) . Species with superior s p a t i a l memories have a large hippocampus (Sherry et al., 1989), and place c e l l s i n the hippocampus may i n fact correspond to elements of an animal's cognitive map of i t s surroundings (Speakman and O'Keefe, 1989). The hippocampus has been implicated i n various other functions as well. It i s involved i n forming associations between st i m u l i and i n discounting cues when they are no longer valuable or when better predictors of reward become avai l a b l e (Moore and Stickney, 1980). As well, the hippocampus i s involved i n non-mapping types of s p a t i a l behaviour, temporal mapping, and non-spatial learning (Kesner, 1980; Olton, 1990; Speakman and O'Keefe, 1989). The hippocampus may be involved i n monitoring speed and d i r e c t i o n vectors along with the v i s u a l , motor and p a r i e t a l 108 Spatial Association and Spatial Memory-cortex (Olton, 1990). Spatial working memory may also be stored i n the hippocampus (Olton et al., 1980). While long term memories (items stored for an i n d e f i n i t e period) seem to involve actual changes i n which genes are expressed by a neuron, short term memory (items stored for a short period only) seems to involve covalent modifications of pre-existing c e l l u l a r proteins (Barnes, 1988; Goelet et a l . , 1986; Matthies, 1989; Thompson, 1986). Some authors suggest a t h i r d form of memory, working memory, which i s used only while tasks are ongoing. It i s e s s e n t i a l l y non-associative and i s discarded at the end of the current task (Barnes, 1988; Maki, 1987) . The hippocampus plays a key role i n transf e r r i n g items from working memory to long term memory (Wickelgren, 1979) . Most aspects of s p a t i a l memory are long term memory tasks (Nadel and Willner, 1980). It appears that these neural processes are s i m i l a r across a wide variety of species of birds, mammals and possibly other advanced groups of animals (Bingman et al., 1989; Olton, 1985). Differences i n Learning In simple associative learning, s p a t i a l association learning and s p a t i a l memory, the i n i t i a l learning processes may occur s i m i l a r l y as part of working memory. If there i s a processing difference, i t probably occurs at the point of transfer to short term or long term memory. Work by various authors suggests that many cue (associative) tasks 109 Spatial Association and Spatial Memory-are l i m i t e d to short term memory while landmark ( s p a t i a l memory) tasks are transferred d i r e c t l y to long term memory (Barnes, 1988; Kamil and Mauldin, 1975; Kesner, 1980; Nadel and Willner, 1980; Sherry, pers. comm.). Advantages and Disadvantages These differences, i f re a l , suggest that the development of s p a t i a l memory takes longer and i s more involved than dir e c t associative learning. S p a t i a l association learning should f a l l somewhere between the two since i t involves both associative and s p a t i a l learning, but generally w i l l s t i l l be quicker than reliance s o l e l y on s p a t i a l memory. In a si t u a t i o n i n which either s p a t i a l or associative learning would be possible and e f f e c t i v e , s i m p l i c i t y dictates that associative learning should predominate. These physiological differences between associative tasks and s p a t i a l memory tasks should r e s u l t i n differences i n biases towards p a r t i c u l a r types of learning. Another advantage to simple associative learning i s that animals using i t need learn only one thing: the association between cue and response. Spatial memory, on the other hand, requires the development of a set of memories about landmarks, cues, reward s i t e s and t h e i r i n t e r r e l a t i o n s h i p s . This suggests that simple asso c i a t i v e learning should be preferred to s p a t i a l memory when eithe r i s s u f f i c i e n t to complete the task. Again, s p a t i a l association learning should f a l l between simple association 110 Spatial Association and Spatial Memory and pure s p a t i a l memory i n d i f f i c u l t y , since s p a t i a l associations require animals to remember only the s p a t i a l r e l a t i o n s h i p between cue and reward i n addition to the fact that they are associated. Uncertainty and Perception An animal's perception of i t s environment should also influence whether i t uses s p a t i a l memory or association i n a given s i t u a t i o n . If the environment i s stable, the long term development of maps of s p a t i a l l y structured information should be advantageous as they allow e f f i c i e n t and f l e x i b l e exploration and use of the environment. On the other hand, s p a t i a l mapping would be a waste of time and energy i n a highly variable environment, because the s p a t i a l structure of the environment could change enough before they are used s u f f i c i e n t l y to balance the cost of learning them. In t h i s case, short term associative learning would be more of an advantage because i t involves remembering rules that are not affected by changes i n the environment as long as the association remains i n t a c t . Associations between s t i m u l i and responses are "portable" and can be applied i n various locations and times. For example, i f a hummingbird learns the association between red flowers and nectar production, i t can apply that association to any red nectar producing flowers. I f , however, i t uses s p a t i a l memory to learn the s p a t i a l location of a p a r t i c u l a r set of red flowers, the 111 Spatial Association and Spatial Memory memory i s u s e f u l f o r o n l y t h e n e c t a r p r o d u c i n g l i f e s p a n o f t h o s e f l o w e r s . There i s an i m p o r t a n t d i f f e r e n c e between t h e a c t u a l t e m p o r a l v a r i a b i l i t y o f an a n i m a l ' s environment and t h e a n i m a l ' s p e r c e p t i o n o f i t . W h i l e t h e r e w i l l g e n e r a l l y be a s t r o n g s i m i l a r i t y between p e r c e p t i o n and a c t u a l i t y , i t i s not a b s o l u t e . A n i m a l s n o r m a l l y d e v e l o p p e r c e p t i o n s o f t h e i r e n v i r o n m e n t s based on c u r r e n t s e n s o r y i n p u t and memory of p a s t e x p e r i e n c e s (Church and M i l l e r , 1991; V a l o n e and G i r a r d e a u , 1993) . I n Chapter 2 I p r e s e n t e d e v i d e n c e o f t h e e f f e c t s o f e x p e r i e n c e on p e r s i s t e n c e o f s p a t i a l memories. P e r c e i v e d v a r i a b i l i t y r e s u l t s when e x p e c t a t i o n s do not c o r r e s p o n d t o s e n s o r y e v i d e n c e . I n t h i s c a s e , a n i m a l s w i l l t e n d t o reduce p l a n n e d f o r a g i n g and r e l y on e x p l o r a t i o n and s a m p l i n g o f t h e environment (Valone, 1992). I n g a u g i n g t h e v a l u e of p a s t e x p e r i e n c e , a n i m a l s t e n d t o v a l u e t h e most r e c e n t e x p e r i e n c e most h i g h l y (Todd and K a c e l n i k , 1993). T h i s phenomenon may be t h e r e a s o n f o r t h e r e c e n c y e f f e c t , o r improved performance f o r r e c e n t l y l e a r n e d t a s k s ( S h e r r y , 1984) . Animals not o n l y d i s c o u n t p a s t e x p e r i e n c e based on the e l a p s e d time s i n c e t h e y o b t a i n e d a reward, but a l s o based on the amount and p e r c e i v e d v a r i a b i l i t y o f t h e reward (Bowers and Adams-Manson, 1993; Gibbon et a l . , 1988). V a r i a b l e rewards i n c r e a s e t h e amount of i n f o r m a t i o n r e q u i r e d t o r e t r i e v e them. S i n c e a n i m a l s have a l i m i t e d a b i l i t y t o remember p a s t e x p e r i e n c e s , a t some 112 Spatial Association and Spatial Memory p o i n t t h e y w i l l r e a c h t h e i r c a p a c i t y f o r s t o r e d memory, based on a c o m b i n a t i o n of e l a p s e d t i m e , i n d i v i d u a l e x p e r i e n c e and e n v i r o n m e n t a l c o m p l e x i t y , each o f w h i c h i n c r e a s e s t h e amount o f i n f o r m a t i o n t o be p r o c e s s e d ( N i s h i m u r a , 1994). Current Study T h i s s t u d y had two p r i m a r y p u r p o s e s . F i r s t , i t p r o v i d e d an o p p o r t u n i t y t o c o n t r a s t the r o l e s o f e x p e r i e n c e w i t h a s i m p l e p a t t e r n o f r e w a r d i n g f e e d e r s and cue c h a r a c t e r i s t i c s ( i n t h i s case, cue d i s t a n c e ) . I n c h a p t e r 2 I s t u d i e d t h e e f f e c t o f e x p e r i e n c e (measured i n terms o f number o f t r i a l s w i t h a s t a b l e p a t t e r n o f f e e d e r s ) on p e r s i s t e n c e o f v i s i t a t i o n s t o f o r m e r l y r e w a r d i n g f e e d e r s . I n c h a p t e r 3 I l o o k e d a t how d i f f e r i n g p e r c e p t u a l i n f o r m a t i o n a s s i s t e d s p a t i a l l e a r n i n g . I n t h i s s t u d y I examine how t h e s e f a c t o r s i n t e r a c t . A second r e a s o n t o do t h i s s t u d y was t h e p o t e n t i a l t o c o n t r a s t t h e r o l e s o f s p a t i a l a s s o c i a t i o n l e a r n i n g and s p a t i a l memory i n hummingbird f o r a g i n g . I n p r e v i o u s s t u d i e s w i t h r u f o u s hummingbirds, Brown and Thompson b o t h found t h a t cue s e p a r a t i o n from t h e response s i t e hampered l e a r n i n g (G. Brown, 1992; Thompson, 1994). T h i s s t u d y p r o v i d e s a c o n t r a s t between t h e s p a t i a l a s s o c i a t i o n l e a r n i n g examined by Brown and Thompson and t h e s p a t i a l memory examined by m y s e l f and S u t h e r l a n d ( S u t h e r l a n d , 1985). 113 Spatial Association and Spatial Memory This study also continues my exploration of the ro l e of environmental i n s t a b i l i t y i n hummingbird learning. As i n chapter 2, where I found that persistence with a pattern of feeders increased with increasing experience with that pattern, I provide the animals with a stable foraging environment for d i f f e r i n g periods of time followed by a sudden change i n the pattern of rewarding feeders to probe the extent and persistence of th e i r previous learning. There are nine di f f e r e n t treatments i n t h i s set of experiments, consisting of exposures of three d i f f e r e n t durations (30 minutes, 90 minutes and 300 minutes of free access to a pattern of rewarding and non-rewarding feeders) and three d i f f e r e n t cue conditions (close cues: LEDs cueing rewarding feeders at distances of 1 cm; far cues: LEDs at 12 cm; and uncued: no LEDs at a l l ) . For each duration, the exposure i s t i e d not only to the clock but to the number of feeding bouts by the hummingbirds. I expect that shorter durations w i l l tend to favour the use of associated cues, while longer time periods w i l l favour the development of s p a t i a l memory. Uncued treatments w i l l require s p a t i a l memory, and close cues w i l l favour the association aspects of s p a t i a l association learning over a given duration. Far cues should f a l l somewhere between these two extremes, but w i l l also involve s p a t i a l association learning. The combination of these two factors should allow me to explore 114 Spatial Association and Spatial Memory how the interactions between time and cue distance w i l l bias birds towards use of either type of learning. / 115 Spatial Association and Spatial Memory Section I I . Materials and Methods Subjects The s u b j e c t s of these experiments were 12 a d u l t r u f o u s hummingbirds (Selasphorus rufus) : 1 male and 11 females. The b i r d s were c o l l e c t e d i n the w i l d i n May 1991 from the v i c i n i t y of the Rosewall Creek salmon hatchery, Vancouver I s l a n d , B r i t i s h Columbia, and the U n i v e r s i t y of B r i t i s h Columbia r e s e a r c h f o r e s t i n Maple Ridge, B r i t i s h Columbia and had been used i n previous l e a r n i n g experiments. Due to e x c e s s i v e weight l o s s two of the females c o u l d not complete a l l treatments and were each r e p l a c e d f o r t h e i r f i n a l run by d i f f e r e n t b i r d s (both female), b r i n g i n g the t o t a l number to 14. The animals were maintained i n i n d i v i d u a l 0.6 x 0.6 x 0.6 m wire mesh cages f o r s e v e r a l months p r i o r t o t e s t i n g . P hotoperiod mimicked seasonal v a r i a t i o n i n the w i l d . E x c l u d i n g t e s t p e r i o d s , the b i r d s were s u p p l i e d w i t h e i t h e r Roudybush hummingbird d i e t or Nektar Plus hummingbird d i e t supplemented w i t h i s o l a t e d soy p r o t e i n (3% w/w) ad l i b i t u m from s t a n d a r d commercial u n l i m i t e d volume f e e d e r s on weekdays. On weekends, they had 25% sucrose s o l u t i o n w i t h added v i t a m i n s ( A v i t r o n a v i a n v i t a m i n supplement) and m i n e r a l s (Avimin a v i a n mineral supplement). The b i r d s 116 Spatial Association and Spatial Memory-participated i n s e v e r a l f o r a g i n g e x p e r i m e n t s p r i o r t o t h i s s t u d y . Experimental Environment I c o n d u c t e d a l l t r a i n i n g and e x p e r i m e n t s i n 3 e x p e r i m e n t a l rooms, each 1.3 x 2.5 x 2.5 m h i g h w i t h 2 o v e r h e a d 40 w a t t i n c a n d e s c e n t l i g h t b u l b s . W a l l s and c e i l i n g , e x c ept t h e f e e d e r a r r a y , were a u n i f o r m l i g h t g r e e n c o l o u r . The f l o o r was a u n i f o r m sand c o l o u r . A s i n g l e , stand-mounted, 1.5m h i g h p e r c h was l o c a t e d a t t h e c e n t r e o f each room and f i t t e d w i t h a p h o t o c e l l t o s i g n a l a r r i v a l s and d e p a r t u r e s . A f e e d e r a r r a y c o v e r i n g p a r t of one end w a l l c o n s i s t e d o f a m e t a l p a n e l (107 cm wide x 61 cm h i g h ) p a i n t e d a f l a t d a r k g r e e n c o l o u r w i t h a h o r i z o n t a l a r r a y o f e i g h t e v e n l y s paced f e e d e r s . Each f e e d e r was marked by a round 19 mm d i a m e t e r f l u o r e s c e n t orange Avery l a b e l w i t h a 3 mm d i a m e t e r c e n t r a l h o l e . B e h i n d each f e e d e r was an i n f r a r e d p h o t o c e l l w h i c h d e t e c t e d t h e p r e s e n c e of a hummingbird's b i l l . A s m a l l f o o d r e s e r v o i r c o n s i s t i n g o f the p l a s t i c f i t t i n g o f a d i s p o s a b l e 21 gauge hypodermic n e e d l e was a l s o p o s i t i o n e d b e h i n d each f e e d e r . Each s y r i n g e was c o n n e c t e d by f l e x i b l e p l a s t i c t u b i n g t o a computer c o n t r o l l e d , m i n i a t u r e s o l e n o i d v a l v e ( G e n e r a l V a l v e C o r p o r a t i o n , s e r i e s 3 ) . I f t h e f e e d e r was d e s i g n a t e d as r e w a r d i n g d u r i n g a p a r t i c u l a r t i m e p e r i o d , t h e v a l v e r e l e a s e d 2 | i l o f 20% s u c r o s e s o l u t i o n (mass/mass) 117 Spatial Association and Spatial Memory into the reservoir immediately when the b i r d probed the feeder. If the feeder was non-rewarding, the b i r d received no food from that feeder. There were three variations on t h i s basic panel design, with one v a r i a t i o n i n each experimental room. In one, feeders were unmarked except as noted above. In another, a small red l i g h t (4 mm diameter LED) protruded through the panel 1 cm d i r e c t l y above each feeder. In the t h i r d panel design, the l i g h t s were 12 cm above the feeders. These three panels represented the three treatments: uncued, close cues and far cues. When the l i g h t above a feeder was turned on by the c o n t r o l l i n g computer at the s t a r t of a test period, i t sig n a l l e d that the feeder was rewarding. In a l l 3 cases, a buzzer also indicated the st a r t of a test, so even birds using the p l a i n panel were given a signal that a rewarding feeder was present somewhere i n the array. Hummingbirds were allowed free access to the array and a l l areas of the room during experiments, but they could feed successfully only from one rewarding feeder during each exposure period. Training On the day before testing, the feeder i n each bird's home cage was modified to resemble the feeders i n the experimental arrays. Birds quickly learned to use these feeders and they and t h e i r feeders were moved to the experimental rooms i n the late afternoon. These feeders 118 Spatial Association and Spatial Memory-were hung d i r e c t l y i n f r o n t of the c e n t r e s o f t h e e x p e r i m e n t a l a r r a y s , w h i c h were c o v e r e d . The f o l l o w i n g morning, t h e commercial f e e d e r s were removed and one a r r a y f e e d e r was uncovered i n each room and b i r d s were a l l o w e d a c c e s s t o t h e a r r a y u n t i l t h e y were f e e d i n g r e g u l a r l y . T h i s took about 2 hours i n t o t a l . The a r r a y was t h e n r e c o v e r e d f o r a s h o r t p e r i o d (about 2 0 minutes) u n t i l t e s t i n g began. Experimental Procedures Each b i r d e x p e r i e n c e d n i n e d i f f e r e n t e x p e r i m e n t a l c o n d i t i o n s ( e x c e p t i n g the two b i r d s removed from t h e experiment and t h e i r s u b s t i t u t e s ) . The o r d e r o f p r e s e n t a t i o n o f t h e s e c o n d i t i o n s and t h e b i r d s u sed on any g i v e n t e s t day were randomized. The c o n d i t i o n s c o n s i s t e d o f exposure t o each o f t h e 3 e x p e r i m e n t a l a r r a y s (uncued, c l o s e cue and f a r cue) f o r 3 d i f f e r i n g exposure p e r i o d s b e f o r e t h e r e w a r d i n g f e e d e r was s w i t c h e d . The 3 exposure times t o the o r i g i n a l p a t t e r n o f f e e d e r s were s h o r t (30 minutes o r 3 s u c c e s s f u l f e e d s i f t h e b i r d s had not met t h i s r e quirement i n t h e 3 0 minute exposure p e r i o d ) , medium (90 minutes o r 9 s u c c e s s f u l f e e d s ) , and l o n g (300 minutes o r 30 s u c c e s s f u l f e e d s ) . A s u c c e s s f u l f e e d was any r e w a r d i n g v i s i t t o t h e a r r a y f o l l o w e d by a r e t u r n t o t h e p e r c h . One o f t h e f e e d e r s i n t h e 8 f e e d e r a r r a y was r e w a r d i n g f o r t h e e n t i r e exposure p e r i o d and t h e o t h e r s were n o t . 119 Spatial Association and Spatial Memory Rewarding feeders were randomly a s s i g n e d f o r a l l experimental runs, although n e i t h e r end feeder was ever rewarding. End feeders were l e f t empty to prevent b i r d s from u s i n g a simple r u l e of thumb such as v i s i t i n g the feeder n e a r e s t the w a l l , as seen i n pre v i o u s s t u d i e s ( M i l l e r et al., 1984). A s o f t buzzer sounded f o r 0.5 s to i n d i c a t e the be g i n n i n g of t e s t p e r i o d s . In the c l o s e and f a r cue treatments, the cue above the rewarding feeder was l i t d u r i n g t e s t p e r i o d s to i n d i c a t e that i t was rewarding. During the experiment, the rewarding feeder p r o v i d e d 2ul per probe. Each v i s i t to the a r r a y f o l l o w e d by a r e t u r n t o the pe r c h was c o n s i d e r e d to be a s i n g l e f e e d i n g bout no matter how many times the b i r d probed f e e d e r s . The rewarding feeder was changed randomly t o a new l o c a t i o n i n the a r r a y a f t e r the i n i t i a l exposure p e r i o d (at l e a s t 30, 90 or 300 minutes). As i n the i n i t i a l exposure p e r i o d , the two end feeders were never rewarding. The experimental run continued f o r a minimum of t h i r t y minutes longer, o r u n t i l the b i r d made three s u c c e s s f u l f o r a g i n g bouts. At the end of the run, the b i r d was r e t u r n e d t o i t s home cage and the equipment was cleaned and f l u s h e d . 120 Spatial Association and Spatial Memory Section I I I . Results I n i t i a l Learning In a l l cases the birds performed s i g n i f i c a n t l y better than chance within the f i r s t 10 minutes of the test (Table 13). In thi s case, chance performance was 12.5% correct probes. During this i n i t i a l period, the birds showed the poorest performance with the uncued panel (Fig. 18); even so, they averaged over 60% correct v i s i t s i n the f i r s t 30 minutes. Performance i n the medium and long exposure treatments showed continual improvement, reaching nearly perfect performance i n the close cue treatments and exceeding 90% correct performance i n a l l treatments by the end of the long, 300 minute exposure period. Cue Distance Exposure Time Close Far Uncued Short t value p r o b a b i l i t y 9.593 0.000 4.605 0.001 3 .238 0.008 Medium t value pr o b a b i l i t y 16.787 0.000 10.196 0.000 3.336 0 . 007 Long t value p r o b a b i l i t y 6.855 0.000 15.973 0 .000 4.291 0.001 Table 13. Differences between average proportion correct and random v i s i t a t i o n for a l l treatments i n the f i r s t 10 minutes of experimental runs. Analysis i s based on a one sample t test against a random performance l e v e l of 0.125 (one chance out of 8). Terms for cue distance and exposure time are explained i n the methods section. P r o b a b i l i t i e s indicate the l i k e l i h o o d that performance did not d i f f e r from success due so l e l y to random chance. 121 1,00 o <D i _ i _ o O c o o Q. o o o O c o o d o o CD i _ i _ o O c o -f—' l _ o d o 0,25 6 12 18 24 Blocks of 10 Minute Durations 30 36 Figure 18. Proportion of v i s i t s that were to the correct feeder for each of the 9 treatments. Each l i n e represents the average of the 12 birds from each treatment. The X axis i s divided into blocks of 10 minute durations. The top panel shows the 3 long (300 minute) treatments, the middle panel contains the 3 medium (90 minute) treatments and the bottom panel has the 3 short (30 minute) exposure treatments. The feeder switch i s indicated by the v e r t i c a l l i n e through the graphs on the 3 panels. On a l l 3 panels, the s o l i d l i n e shows the close cue treatment, the dashed l i n e i s the far cue treatment and the dotted l i n e i s the uncued treatment. 122 Spatial Association and Spatial Memory-Performance f o l l o w e d t h e p r e d i c t e d o r d e r f o r a l l t h r e e e xposure t i m e s . B i r d s u s i n g c l o s e cues p e r f o r m e d b e s t , f o l l o w e d by b i r d s u s i n g f a r cues, who i n t u r n p e r f o r m e d b e t t e r t h a n b i r d s u s i n g the uncued p a n e l ( F i g . 18). Switch E f f e c t Performance i n the p e r i o d a f t e r t h e s w i t c h a l s o f o l l o w e d t h e p r e d i c t e d o r d e r . B i r d s i n uncued t r e a t m e n t s p e r s i s t e d l o n g e s t i n v i s i t s t o t h e p r e v i o u s l y r e w a r d i n g f e e d e r a f t e r t h e s w i t c h , f o l l o w e d by b i r d s w i t h f a r cues and f i n a l l y b i r d s w i t h c l o s e cues ( F i g . 19) . B i r d s w i t h l o n g p r e - s w i t c h exposure times p e r s i s t e d l o n g e s t , f o l l o w e d by b i r d s w i t h medium exposures and f i n a l l y t h o s e w i t h a s h o r t e xposure t o t h e i n i t i a l f e e d e r p o s i t i o n s . Time, Distance, and the Interaction E f f e c t Two way a n a l y s i s of v a r i a n c e o f t h e e f f e c t o f cue d i s t a n c e and exposure time shows t h a t b o t h f a c t o r s s i g n i f i c a n t l y a f f e c t p o s t - s w i t c h f e e d i n g b e h a v i o u r . T h i s i s most ap p a r e n t i n t h e p e r s i s t e n c e o f t h e b i r d s i n r e t u r n i n g t o t h e f o r m e r l y good f e e d e r . U s i n g t h i s c r i t e r i o n , d i s t a n c e t o t h e cue (F = 19.953, df = 2,99, p « 0.000) and ti m e (F = 8.622, df = 2,99, p « 0.000) a r e b o t h h i g h l y s i g n i f i c a n t , b ut d i s t a n c e i s a s t r o n g e r e f f e c t t h a n t i m e o f expo s u r e . T h i s comparison i s most c l e a r f o r t h e p r o p o r t i o n o f c o r r e c t v i s i t s i n t h e 3 0 minute p e r i o d a f t e r t h e f e e d e r s w i t c h . I n t h i s case, d i s t a n c e t o t h e cue i s s t i l l a h i g h l y 123 80 eede 60 u_ g 40 o 20 CO "35 > 0 o -*—» CO > 80 1 60 g 40 o -»-- 20 CO > 0 UL UM Treatment C L O S E FAR Cue Distance UNCUED LONG MEDIUM Exposure Time SHORT Figure 19. Box plots of number of v i s i t s by birds to the formerly good feeder a f t e r the feeder switch. The top panel shows each treatment, the middle panel i s birds grouped by cue distance and the bottom panel i s grouped by duration of exposure. In each box plot the central horizontal l i n e i s the median, the upper and lower box edges are the f i r s t and t h i r d q u a r t i l e s (the difference between these q u a r t i l e s i s known as the fourth spread), the v e r t i c a l whiskers extend out to 1.5 times the fourth spread, asterisks indicate mild o u t l i e r s (more than 1.5 times the fourth spread), the empty c i r c l e i s an extreme o u t l i e r (more than 3 times the fourth spread), and the notches i n the v e r t i c a l edges of the boxes represent 95% confidence intervals (which may extend beyond the fourth spread causing a folded edge to the box) . Treatment acronyms i n the top panel are based on cue distance (C = close, F = far and U = uncued) and duration of exposure (S = short, M = medium and L = long). 124 Spatial Association and Spatial Memory-significant e f f e c t on b i r d performance (F = 41.472, d f = 2,99, p = 0.000) but t h e e f f e c t o f ti m e on p o s t - s w i t c h p e r formance i s no l o n g e r s i g n i f i c a n t (F = 0.214, d f = 2,99, p = 0.808). Differences i n Persistence A n a l y s e s o f v a r i a n c e f o r the e f f e c t s o f c h a n g i n g t h e r e w a r d i n g f e e d e r s show t h a t i n d i v i d u a l t r e a t m e n t s d i f f e r s i g n i f i c a n t l y i n the performance b i r d s a c h i e v e d . These h i g h l y s i g n i f i c a n t d i f f e r e n c e s can be seen i n t h e number o f f e e d e r (F = 3.803, df = 8,99. p = 0.001), t h e number o f b o u t s u n t i l b i r d s v i s i t e d t he new good f e e d e r as t h e f i r s t v i s i t o f a f e e d i n g bout (F = 4.683, df = 8,99. p = 0.000), and t h e number o f bouts u n t i l t he t h i r d t i m e t h e b i r d v i s i t e d t h e good f e e d e r as i t s f i r s t v i s i t o f a f e e d i n g bout (F = 6.664, df = 8,99. p « 0.000). Treatment New Good Feeder Old Good Feeder Neither Close Far Uncued Close Far Uncued Close Far Uncued Short 7 3 1 2 5 4 3 4 7 Medium 6 1 0 4 5 4 2 8 8 Lonq 4 0 0 5 9 7 3 3 5 T a b l e 14. P o s t - s w i t c h performance of b i r d s i n t h e d i f f e r e n t t r e a t m e n t s . F i g u r e s f o r new good f e e d e r a r e t h e number o f b i r d s who went d i r e c t l y t o t h e new r e w a r d i n g f e e d e r i m m e d i a t e l y f o l l o w i n g t h e f e e d e r s w i t c h . O l d good f e e d e r shows t h e number o f b i r d s who went i m m e d i a t e l y t o t h e f o r m e r l y r e w a r d i n g f e e d e r a f t e r t h e s w i t c h , w h i l e n e i t h e r i s t h e number o f b i r d s who went t o n e i t h e r t h e new o r o l d r e w a r d i n g f e e d e r . 125 Spatial Association and Spatial Memory B i r d s ' behaviour d i f f e r e d d r a m a t i c a l l y among treatments (Table 14). This t a b l e suggests that p e r s i s t e n c e was gre a t e s t i n the uncued array, that s w i t c h i n g occurred most r a p i d l y i n the cl o s e cue array and b i r d s i n the uncued treatments were more l i k e l y , on t h e i r f i r s t v i s i t a f t e r the feeder switch, to choose feeders that had never been rewarding. The only s i g n i f i c a n t d i f f e r e n c e , however, was that fewer b i r d s switched immediately to the new rewarding feeder at greater cue distances (%2 - 19.73 6, df = 2, p = 0.000). A n a l y s i s of the pa i r w i s e d i f f e r e n c e s i s a l s o not c l e a r . Based on a Tukey a n a l y s i s , the order of the treatments i s i n d i c a t i v e of the p r e d i c t e d order, but many of the d i f f e r e n c e s are nob s i g n i f i c a n t ( F i g . 20). 12 6 CL CS CM FS UM FL FM US UL r _ , 1 1 Find New Feeder CS UM CM CL FS FL FM US UL 1 4 i — A Correct First Visit CS CLCM FS f ; UM FM FL US UL 1 * 1 ^ i 3 Correct First Visits • i — i i — • i — • i i i i i i — i . , i 1 1 1 1 ' • 1 1 I 1 I 1 1 1 1 1 1 1 1— 1 I 0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 Number of Bouts to Criterion F i g u r e 20. Tukey h o n e s t l y s i g n i f i c a n t d i f f e r e n c e a n a l y s i s o f d i f f e r e n c e s i n mean p o s t - s w i t c h f o r a g i n g s u c c e s s . L i n e s c o n n e c t i n g t r e a t m e n t s i n d i c a t e t h a t t h e r e was not a s i g n i f i c a n t d i f f e r e n c e i n performance f o r t h e b i r d s i n t h e s e t r e a t m e n t s . 3 i n c r e a s i n g l y demanding c r i t e r i a t o measure new l e a r n i n g by t h e b i r d s a r e shown. The t o p group of d i f f e r e n c e s i s measured by t h e number of b o u ts u n t i l b i r d s found t h e new r e w a r d i n g f e e d e r . The m i d d l e s e t o f f i g u r e s shows t h e number of b o u ts u n t i l b i r d s v i s i t e d t h e new r e w a r d i n g f e e d e r as t h e f i r s t v i s i t o f a f e e d i n g b o u t . The b ottom group shows the number of bouts u n t i l t h e t h i r d t i m e b i r d s v i s i t e d t h e new r e w a r d i n g f e e d e r as t h e f i r s t f e e d e r i n a f e e d i n g b o u t . Treatment acronyms a r e compounded o f cue d i s t a n c e (C = c l o s e , F = f a r and U = uncued) and d u r a t i o n o f e xposure b e f o r e th e f e e d e r s w i t c h (S = s h o r t , M = medium and L = l o n g ) . 127 Spatial Association and Spatial Memory Section IV. Discussion These experiments provide further evidence that hummingbirds e a s i l y learn s p a t i a l associations accurately even when cues are displaced from feeders (Brown, 1994; Brown and Gass, 1993). Hummingbirds learn s p a t i a l associations more slowly and less well as the distance between cue s i t e and reward s i t e increases, corroborating Brown's findings. This i s similar to the r e s u l t s of other studies (Milner et al., 1979; Pinel et al., 1986; S t o l l n i t z and Schrier, 1962). The birds responded s i m i l a r l y to a l l treatments but t h e i r speed of learning and peak performance varied between treatments. The birds i n a l l treatments showed gradual and continual improvement i n performance u n t i l they reached an asymptote that was less than perfect. While some of t h i s lack of perfection was due to errors, birds also may have been sampling to detect changes i n the environment and to search for survival requirements beyond pure c a l o r i e s , as documented by several authors (Brown and Cook, 1986; C a r r o l l and Moore, 1993; C o l l i a s and C o l l i a s , 1968; Draulans, 1988; Forkman, 1991; Gass, 1985; Kramer and Weary, 1991; Smith, 1974; Wilkie and Spetch, 1980; Wilkie et al., 1981). Treatments d i f f e r e d strongly i n birds' responses to a switch i n feeder p r o f i t a b i l i t y . While both duration of experience of s t a t i c patterns and distance between cues and 128 Spatial Association and Spatial Memory feeders produced s i g n i f i c a n t effects, separations between cues and feeders affected behavioural persistence more strongly. This distance relationship i s consistent with the increasing learning d i f f i c u l t y other authors have seen for increasing separation between cues and reward s i t e s (Brown, 1994; Davis, 1974; Pinel et a l . , 1986; Schrier et a l . , 1963; S t o l l n i t z and Schrier, 1962) . The rel a t i o n s h i p between experience and persistence of previously successful behaviour i s consistent with the results of Chapter 2. Association, Spatial Association and Spatial Memory The hummingbirds learned faster with close cues, which encouraged standard associative learning most strongly, although t h i s treatment s t i l l required the use of s p a t i a l memory to orient from cues to t h e i r associated rewarding feeders. Previous studies have suggested that animals learn associative tasks rapidly by using t r i a l unique working memory of cue and response position (memories that are quickly l a i d down and discarded at the end of the task) to increase speed and e f f i c i e n c y i n t h e i r tasks (Barnes, 1988; Kamil and Mauldin, 1975). Spatial memory tasks seem to require the use of long term memory (Goelet et a l . , 1986; Nadel and w i l i n e r , 1980}. Cue Distance The uncued treatments most closely correspond to a pure s p a t i a l memory task. It seems l i k e l y that birds i n the near and far cue treatments are learning both an associative task 129 Spatial Association and Spatial Memory and a s p a t i a l memory one. B i r d s l e a r n e d t h e s p a t i a l memory t a s k (uncued t r e a t m e n t ) s l o w e r than a t a s k b i a s e d towards t h e a s s o c i a t i v e l e a r n i n g component of t h e t a s k ( c l o s e cue t r e a t m e n t ) . Performance i n t h e f a r cue t r e a t m e n t f e l l between t h e s e two extremes; w h i l e t h e r e were cues t o h e l p l o c a t e t h e r e w a r d i n g f e e d e r , t h e i r g r e a t e r d i s t a n c e from t h e rewards made them more d i f f i c u l t t o use and p r o b a b l y b i a s e d t h e b i r d s t o r e l y more on s p a t i a l memory. T h i s may a c c o u n t f o r t h e i n t e r m e d i a t e l e v e l o f performance on t h i s s e t o f t r e a t m e n t s . How a n i m a l s use cues o r landmarks ( i n t h i s c a s e t h e l i t LED, w h i c h a l s o a c t s as a cue t o the p r o f i t a b i l i t y o f i t s a s s o c i a t e d f e e d e r ) t o l o c a t e o b j e c t s i s s t i l l n o t c l e a r . There i s a d e f i n i t e g e o m e t r i c component t o t h e use o f landmarks (Cheng, 1986 and 1989; Cheng and G a l l i s t e l , 1984; Hermer and S p e l k e , 1994), a l t h o u g h i t appears t h a t a s i m p l e a r i t h m e t i c model of v e c t o r a d d i t i o n o f d i s t a n c e s from landmarks t o t h e i r r e l a t e d l o c a t i o n s does not a p p l y (Cheng, 1990; S p e t c h et a l . , 1992). I f the b i r d s l e a r n t o use t h e LEDs t o p o i n t t o t h e d i r e c t i o n o f the r e w a r d i n g f e e d e r , t h e s i m p l e s t r u l e t o l e a r n might be t o go t o t h e f e e d e r n e a r e s t t o t h e l i t LED. Thompson (1994) showed t h a t hummingbirds w i l l use t h i s s t r a t e g y . S e v e r a l s t u d i e s show t h a t a n i m a l s p r e f e r t o use near landmarks over almost any o t h e r landmark o p t i o n i n n a v i g a t i o n (Bennett, 1993; Cheng, 1989; Cheng et al., 1987b; Vander W a l l , 1982). The d i s t a n c e between landmark and reward s i t e may be c a l c u l a t e d m e t r i c a l l y 130 Spatial Association and Spatial Memory (Cheng, 1990; G a l l i s t e l , 1989) or by the s i z e of the landmark's r e t i n a l image (Collett et a l . , 1992; Gould, 1987; Srinivasan et a l . , 1989) although the l a t t e r measure seems to apply i n l i m i t e d cases (Cheng et al., 1987b), and p r i m a r i l y i n invertebrates such as honeybees. The more complex task of developing a vector r e l a t i o n s h i p (distance and direction) between a landmark and reward s i t e i s possible, but may not be necessary i n t h i s case, where a simple rule of thumb such as going to the feeder nearest the cue w i l l s u f f i c e . Certainly, i f a more complex re l a t i o n s h i p than the one i n t h i s experiment occurs, hummingbirds can learn i t . G. Brown (1992) showed that hummingbirds can learn to go to a feeder other than the one closest to the l i t LED. Similarly, i n Thompson's (1994) experiments, hummingbirds used geometric relationships among cues and response s i t e s to obtain a reward. Birds persisted longer i n v i s i t i n g the formerly good feeder (after a switch of both p r o f i t a b i l i t y and cue) i f the cue was further from the feeder. This suggests animals r e l y i n g more on s p a t i a l memory respond less r a p i d l y to change than those r e l y i n g more on the associative components of s p a t i a l association learning (Roberts et al. , 1988). Although birds using the close cue panel had v i s i b l e indicators of a change, those using s p a t i a l memory with the uncued panel had to r e l y t o t a l l y on t r i a l and error to learn the new location of the rewarding feeder. Birds on the cued panels simply had to transfer t h e i r s p a t i a l association to 131 Spatial Association and Spatial Memory the new cue pos i t i o n instead of modifying a cognitive map, and they did thi s more quickly when cues were close to feeders. Duration of Exposure As birds gained experience over time with a stable feeder position, t h e i r performance improved i n a l l treatments. By the end of the 300 minute exposure time, birds were performing well above ninety percent accuracy, on average, on a l l 3 panels. This suggests that i n a stable environment, birds perform as well using s p a t i a l memory as with s p a t i a l association learning, but only a f t e r they have gained s u f f i c i e n t experience i n u t i l i z i n g t h e i r surroundings. It should be noted, of course, that 5 hours of exposure to an environment i s not a long time. Even though s p a t i a l memory developed more slowly than s p a t i a l association, the e f f o r t required to learn a s p a t i a l memory task paid dividends i n a r e l a t i v e l y short time i n t h i s experiment. Advantages and Disadvantages Spatial memory use corresponds to slower learning and longer i n t e r v a l s before responding a f t e r encountering a stimulus (Brown and Cook, 1986), while associations, e s p e c i a l l y those using working memory, can increase the speed of learning a task (Kamil and Mauldin, 1975) . The advantage of learning a simple, contiguous association rather than a s p a t i a l relationship seems e s p e c i a l l y 132 Spatial Association and Spatial Memory-important i n s h o r t term t a s k s o r v a r i a b l e e n v i r o n m e n t s . I n a l o n g term t a s k o r a s t a b l e environment, p e r f o r m a n c e r e l y i n g on s p a t i a l memory can approach t h a t r e l y i n g on a s s o c i a t i v e l e a r n i n g . A s i m i l a r r e l a t i o n s h i p s h o u l d e x i s t f o r s p a t i a l a s s o c i a t i o n l e a r n i n g , w h i c h combines a s s o c i a t i o n l e a r n i n g w i t h s p a t i a l memory, so t h a t a l l t h r e e modes o f l e a r n i n g s h o u l d y i e l d h i g h l e v e l s o f performance i n s t a b l e e n v i r o n m e n t s . A s s o c i a t i o n s between cues and rewards need n ot be t i e d t o p a r t i c u l a r p o i n t s i n space. As a r e s u l t , b i r d s who l e a r n e d an a s s o c i a t i o n between cue and reward c o u l d a p p l y t h i s r e l a t i o n s h i p when b o t h cue and p r o f i t a b l e f e e d e r moved. T h i s p o r t a b i l i t y of e i t h e r c o n t i g u o u s a s s o c i a t i o n s o r t h e s p a t i a l a s s o c i a t i o n s i n my experiment p r o v i d e s a s t r o n g l e a r n i n g advantage i n environments w i t h t h e k i n d o f redundancy t h a t makes p o r t a b i l i t y o f a s s o c i a t i o n s v a l u a b l e . I n t a s k s t h a t a l l o w a s s o c i a t i v e l e a r n i n g , t h e b i r d needs t o l e a r n o n l y t h i s a s s o c i a t i o n , and i s not r e q u i r e d t o l e a r n t h e v a r i o u s g e o m e t r i c r e l a t i o n s h i p s and o t h e r i t e m s n e c e s s a r y f o r s p a t i a l mapping. I n s p a t i a l a s s o c i a t i o n l e a r n i n g , s m a l l e r s e p a r a t i o n s between cue and r e s p o n s e s i t e improve performance, perhaps because t h e s p a t i a l r e l a t i o n s h i p between t h e two i s e a s i e r t o d e f i n e t h a n f o r more d i s t a n t p a i r i n g s o f cue and response s i t e . T h i s i d e a i s c o n s i s t e n t w i t h G e s t a l t p r i n c i p l e s o f s p a t i a l p r o x i m i t y , w h i c h suggest t h a t o b j e c t s w i l l be p e r c e i v e d as s e t s i f t h e y a r e c l o s e r t o each o t h e r than t o o t h e r n e i g h b o u r i n g s t i m u l i 133 Spatial Association and Spatial Memory (Pomerantz, 1981; Wertheimer, 1950). Animals prefer to use near landmarks to navigate (Bennett, 1993; Cheng, 1989; Cheng et al., 1987b; Vander Wall, 1982), perhaps for s i m i l a r reasons. If speed of learning and p o r t a b i l i t y are advantages of associative learning, one of i t s disadvantages i s i t s s u s c e p t i b i l i t y to interference, perhaps due to i t s r e l i a n c e on working- memory to speed up learning (Barnes, 1988). Several studies have .documented the effects of interference on associative learning i n rats and other animals (Olton, 1985; Zentall et a l . , 1990). As well, associative learning i s susceptible to decay when there i s a s i g n i f i c a n t delay between the stimulus and the response, between i n i t i a l t r a i n i n g and testing, or merely between periods when the animal can respond (Kamil and Mauldin, 1975) . Long i n t e r t r i a l periods may be s u f f i c i e n t to reduce performance in laboratory environments. One p o s s i b i l i t y i s that animals are not always able to discriminate between t r i a l and i n t e r t r i a l periods, so that the learned association may be extinguished during non-rewarding i n t e r t r i a l s (Hoffman and Maki, 1986; Maki, 1979). In contrast to associative learning, s p a t i a l memory seems resistan t , i f not immune, to these forms of interference, presumably due to the storage of s p a t i a l relationships i n long term memory (Maki et a l . , 1979) . This immunity to interference may also provide a way to di s t i n g u i s h between the use of cognitive maps by animals and 134 Spatial Association and Spatial Memory-l i s t s of separate locations. L i s t s are subject to interference, as demonstrated with black-capped chickadees (Crystal and Shettleworth, 1994). This shortcoming of s p a t i a l l i s t s suggests an advantage of cognitive maps over s p a t i a l l i s t s . As a result of the resistance to interference, animals using s p a t i a l memory are able to learn c o n f l i c t i n g tasks i n diff e r e n t contexts and perform well i n a l l of them (Beatty and Shavalia, 1980; Maki et a l . , 1979). In previous studies of s p a t i a l association (G. Brown, 1992; Brown, 1994; Brown and Gass, 1993; Thompson, 1994), birds showed no appreciable decline i n performance overnight i n multi-day experiments. Perhaps s p a t i a l association tasks suffer less from temporal declines i n performance than simple associative learning, although i t may be that hummingbirds are resistant to any form of forgetting over t h i s time frame. Sp a t i a l memories can be maintained for long periods of time. Storing birds can remember cache s i t e s f or the duration of a winter or longer (Balda, 1980; Balda and Kamil, 1989 and 1992; Healy and Krebs, 1992; Sherry, 1984; Shettleworth, 1983). Non-storing animals also seem to re t a i n s p a t i a l information for a long time (Balda and Kamil, 1992; Healy and Krebs, 1992; Hitchcock and Sherry, 1990; Menzel, 1991) . In the laboratory, rats have performed s p a t i a l tasks ten months afte r t r a i n i n g and te s t i n g (Bierley et a l . , 1987). Hummingbirds and other species return to the 135 Spatial Association and Spatial Memory same breeding and feeding s i t e s annually (Cole et al., 1982; Colwell, 1974; Gass, 1985; Roberts, 1979) . One of the main disadvantages of s p a t i a l memory i s also due to i t s long term nature. Due to t h e i r storage i n long term memory, s p a t i a l maps are resistant to change and may res u l t i n inappropriate behaviour i n the face of change. There are various examples of animals dodging b a r r i e r s that are no longer present or searching for food or nests i n places that are no longer correct (Collett et al., 1986 and 1993; G a l l i s t e l , 1989; Kamil and Balda, 1985; Speakman and O'Keefe, 1989; Spetch et a l . , 1992; Sutherland and Gass, i n press) . The persistence of birds i n v i s i t i n g incorrect feeders seen i n my experiments i s an example of how s p a t i a l memories can ra p i d l y become inappropriate. While animals r e l y i n g purely on cue associations are subject to interference and loss of r e c a l l a f t e r even short delays (Kamil and Mauldin, 1975), the p o r t a b i l i t y of t h e i r association allows them to respond rapi d l y to changes i n th e i r environment, as long as those changes don't affect the relationship between cue and reward. A l l of the treatments i n my experiments required s p a t i a l memory, although the increasing importance of the associative component of the task i n the far and close cue treatments decreased persistence at formerly rewarding feeders since birds could use the same learned association between cue and reward for the new feeder loca t i o n . 136 Spatial Association and Spatial Memory-Change can cause problems f o r animals u s i n g s p a t i a l memory, but some animals respond to r e g u l a r environmental change by remembering the p a t t e r n of temporal changes. These temporal maps have been documented f o r d a i l y f l u c t u a t i o n s i n the environment (Biebach et al., 1989; Krebs and Biebach, 1989; Olton, 1990). Perhaps animals can a l s o develop temporal maps f o r seasonal change, such as m i g r a t o r y s p e c i e s encounter. The d i f f e r i n g advantages and disadvantages of a s s o c i a t i v e and s p a t i a l l e a r n i n g does not mean t h a t they cannot work i n concert w i t h each other, as s p a t i a l a s s o c i a t i o n demonstrates they can do. In f a c t , t h e r e i s evidence t h a t i n a s t a b l e environment, a. working map of the surroundings may b e n e f i t a s s o c i a t i v e l e a r n i n g as w e l l as f u n c t i o n i n g i n s p a t i a l memory (Spetch and Honig, 1988). There a r e many n a t u r a l examples of the i n t e r a c t i o n o f s p a t i a l and a s s o c i a t i o n l e a r n i n g i n c l u d i n g use of marks on banner p e t a l s t o assess n e c t a r q u a l i t y of fl o w e r s by bees (Go r i , 1989), and the use of c i r c l i n g v u l t u r e s by p r e d a t o r s to l o c a t e prey (Houston, 1983; Rabenold, 1983 and 1987). G. Brown (1992) l i s t s other examples i n c l u d i n g s o c i a l t r a n s m i s s i o n of f o r a g i n g i n f o r m a t i o n . Memory Load M a i n t a i n i n g both s p a t i a l and temporal maps p l a c e s a heavy l o a d on the memory c a p a c i t y of animals. Energy models of hummingbird f o r a g i n g suggest that i n some cases the c o s t s 137 Spatial Association and Spatial Memory o f l o n g t e rm memory of f o r a g i n g environments may o u t w e i g h t h e b e n e f i t s (Armstrong et al., 1987). I n my e x p e r i m e n t s (and o t h e r s , f o r i n s t a n c e S u t h e r l a n d , 1985) c o n t i n u i n g r e v i s i t s t o emptied f e e d e r s s u g g e s t s t h a t t h e b i r d s n e g l e c t e d t o use w o r k i n g memory t o remember v i s i t s t o i n d i v i d u a l l o c a t i o n s . R o b e r t s (1988), a l s o found l i t t l e e v i d e n c e t h a t p i g e o n s r e t a i n e d a w o r k i n g memory o f v i s i t a t i o n s w i t h i n p a t c h e s , and su g g e s t e d t h a t r a t s have s i m i l a r d e f i c i e n c i e s . R e v i s i t a t i o n s d u r i n g b o u t s o f f o r a g i n g i n g i v e n p a t c h e s may i n f a c t be e v i d e n c e t h a t an a n i m a l has l e a r n e d t h e p a t c h b o u n d a r i e s r a t h e r t h a n t h e i n d i v i d u a l components o f the p a t c h ( M e l l g r e n and Roper, 1986) . T h i s would then suggest t h a t t h e a n i m a l s a r e r e d u c i n g memory l o a d by chu n k i n g . Chunking i s a n o t h e r way t o reduce t h e memory l o a d imposed by c o g n i t i v e mapping ( C a p e l l i et al. , 1986). T h i s p r o c e s s o f g e n e r a l i z i n g t h e f e a t u r e s o f t h e environment may be what l e a d s t o h i g h r e v i s i t a t i o n r a t e s under some e x p e r i m e n t a l p r o t o c o l s . The e x p e r i m e n t a l a n i m a l s t o r e s o n l y t h e o v e r a l l f e a t u r e s o f the environment r a t h e r t h a n t h e f i n e g r a i n e d d e t a i l s (Gass, 1985). N i s h i m u r a (1994) suggested t h a t t h e advantages o f l e a r n i n g a r e t i g h t l y t i e d t o the memory c a p a c i t y o f t h e a n i m a l . I f t h e a n i m a l has a l i m i t e d c a p a c i t y , t h e advantages o f l e a r n i n g a r e soon l o s t . T h i s i s e s p e c i a l l y t r u e when r e s o u r c e s a r e depressed, so t h a t t h e a n i m a l must remember more i n f o r m a t i o n f o r each p o t e n t i a l reward. Memory 138 Spatial Association and Spatial Memory load seems to be a s i g n i f i c a n t problem for animals i n some situations, so that they modify t h e i r memory use throughout a prolonged task i n response to th i s load (Cook et al., 1985) . Conclusions These experiments have demonstrated that hummingbirds can learn both s p a t i a l memory tasks and s p a t i a l associations, for which I believe the l a t t e r requires a combination of s p a t i a l memory and associative learning. Hummingbirds learn s p a t i a l association tasks more r a p i d l y than tasks that r e l y solely on s p a t i a l memory, achieving high l e v e l s of performance aft e r a very short time i n t e r v a l . While the s p a t i a l memory tasks I used required a s l i g h t l y longer learning period, the birds eventually achieved performance levels comparable to those for s p a t i a l association tasks. The amount of experience with a s p e c i f i c rewarding pattern a f f e c t s the persistence of the birds' behaviour once the pattern has changed. Generally, the longer the period of s t a b i l i t y before a pattern switch, the longer the animal w i l l r e s i s t changing i t s previously successful foraging behaviour. The effect of exposure time appears to have less influence on s p a t i a l association tasks than s p a t i a l memory ones. The d i f f i c u l t y of forming a s p a t i a l association between a cue and reward s i t e i s strongly dependent on the s p a t i a l 139 Spatial Association and Spatial Memory-separation of the two s i t e s . Greater separations slow the speed of learning, and tend to result i n more re l i a n c e on s p a t i a l memory and greater persistence i n the face of change. Greater separations between cue and reward and longer periods of exposure favour the use of s p a t i a l memory over s p a t i a l association, while the opposite i s true for cues close to the reward and short periods of exposure. 140 Chapter 5 General Discussion Various questions a r i s e out of studies l i k e mine, but Rescorla and Holland (1982) narrowed them down to three basic ones: What conditions produce learning? How i s learning revealed i n performance? What i s learned? A l l three questions deal with external factors and t h e i r r o l e i n learning. I w i l l address the f i r s t two questions b r i e f l y , then expand the t h i r d to ask: What do animals learn about t h e i r environments and how do they learn i t ? What Conditions Produce Learning? In these studies, the birds learned s p a t i a l r e lationships among features of t h e i r foraging environments under a v a r i e t y of conditions. Learning was promoted by the use of v i s u a l and auditory cues and landmarks and by the motivation of the birds to feed. In a l l experiments the birds were provided with v i s u a l cues to feeder locations i n the form of orange rings surrounding the feeders that revealed nothing about t h e i r p r o f i t a b i l i t y . In the experiments described i n chapter 2, feeders offered only t h i s information, so birds had to learn the pattern of rewarding and non-rewarding feeders using p o s i t i o n only, as 141 General Discussion i n the experiments described i n Sutherland and Gass (in press). Most treatments described i n chapter 3 provided additional information i n the form of landmarks. In some cases these landmarks also included information about the p r o f i t a b i l i t y of feeders. In 6 of the 9 treatments of the experiment described i n chapter 4 they could use s p a t i a l l y separated LED cues to rewarding feeders. Aside from the various cues, landmarks and arrays of feeders, the main condition that led to learning was motivation of the birds to feed frequently and t h e i r expectancy of reward from array feeders. I w i l l deal with the importance of each of these factors as part of my consideration of what i s learned. How i s Learning Revealed i n Performance? In these experiments the birds demonstrated learning through t h e i r improving performance over time. I reported t h i s performance only through two measures of f i r s t v i s i t s to feeders i n t r i a l s because birds continued to r e v i s i t locations even a f t e r depleting them. Their f a i l u r e to learn to avoid r e v i s i t i n g depleted feeders suggests that they learned rewarding regions of the array rather than learning i n d i v i d u a l rewarding feeder locations. Indicated by t h e i r f i r s t v i s i t s to locations i n t r i a l s , the birds showed rapid progression to rates of feeding well above chance, revealing that they had begun to learn the locations of rewarding feeders within f i v e minutes of exposure to the arrays (five 142 General Discussion t r i a l s ) . Five minutes of exposure here refers to actual foraging opportunities and excludes i n t e r t r i a l periods when they were unable to see or v i s i t the array but could integrate information from previous v i s i t s . The birds also provided evidence of learning when t h e i r performance dropped a f t e r pattern reversals. In t h i s case, decreased performance demonstrated t h e i r persistence i n v i s i t i n g feeders which had been but were no longer rewarding. The magnitude of t h e i r drop i n performance, as measured by the number of incorrect v i s i t s they made i n the t r i a l s immediately following the reversal, was p o s i t i v e l y r e l a t e d to the duration of exposure to the pattern before the switch. What i s Learned about t h e i r Environments and How? Pattern Learning These experiments reinforced e a r l i e r conclusions that hummingbirds rapidly learn both one and two dimensional patterns of feeders. While th i s work was based p r i m a r i l y on a two dimensional array of feeders divided simply into 4 quarters, hummingbirds learned more complex patterns i n past work (Sutherland and Gass, i n press) . In my studies, not only did the birds learn the patterns of rewarding feeders, but also several kinds of landmarks and cues that s i g n a l l e d the location of rewarding feeders or demarcated patches of feeders. They did t h i s using both s p a t i a l memory and memory of s p a t i a l associations. 143 General Discussion Chunking If the birds learned the pattern of feeders rather than i n d i v i d u a l locations, they were exhibiting chunking, which i s the process of grouping stimuli together into a single mental unit (Olton, 1985). Chunking has been demonstrated i n studies with humans and laboratory animals (Capaldie et al., 1984 and 1986; M i l l e r , 1956), although i t i s d i f f i c u l t to substantiate because remembering a l l of the st i m u l i separately could produce results very s i m i l a r to chunking them into units (Sutherland and Gass, i n press) . If an animal loses the a b i l i t y to distinguish i n d i v i d u a l items i n a group while s t i l l demonstrating knowledge of the grouped structure t h i s may provide evidence for chunking of the separate items into an overall pattern (Olton et a i . , 1980). Animals appear to chunk items together based on t h e i r perception of relationships of various kinds between them. Hummingbirds may be chunking individual feeders into an o v e r a l l pattern i n my array studies. Their tendency to r e v i s i t i n d i v i d u a l feeders, to make most errors on the edges of feeder groups- and to perform better when rewarding feeders are marked with edge landmarks, a l l argue that they are learning a pattern of rewarding feeders (chunking) rather than learning the individual feeders. This evidence i s i n d i r e c t and s t i l l inconclusive, although birds demonstrated i t consistently. 144 General Discussion One of the more prominent results from these studies was that the birds did not learn to avoid r e v i s i t i n g emptied feeder locations. While they e f f e c t i v e l y learned the o v e r a l l pattern of feeders, they showed no improvement i n r e v i s i t a t i o n rates during experiments. Sutherland (1985) also observed a high rate of feeder r e v i s i t a t i o n and no improvement i n h i s work on pattern learning with t h i s same species i n s i m i l a r arrays, Shettleworth and Krebs (1982) found continuing r e v i s i t a t i o n to emptied cache s i t e s i n marsh t i t s , and Roberts (1988) found no evidence for use of working s p a t i a l memory to avoid within patch r e v i s i t a t i o n by pigeons. In a modelling study, Armstrong et al. (1987) predicted a d i f f e r e n t r e s u l t than thi s , suggesting that use of short term memory by hummingbirds to avoid flower r e v i s i t s during foraging bouts i n patches would be energetically b e n e f i c i a l . Brown (1987) found that pigeons could integrate a group of elements into a u n i f i e d pattern i f they were trained on the separate elements, but i f they were trained with a compound group of items, they were unable to dissociate the grouped items to use the separate elements. One possible explanation for continuing r e v i s i t a t i o n i n my study and Sutherland's, despite the theoretical energy benefits suggested by Armstrong et al. 1 s models, i s that once the birds chunked feeders into patterns they were unable to di s s o c i a t e i n d i v i d u a l feeders. 145 General Discussion S p a t i a l Memory In chapter 4, I demonstrated that hummingbirds learn locations of rewarding feeders faster when the p r o f i t a b i l i t y of the in d i v i d u a l feeders i s cued. In the uncued treatments birds had to r e l y only on s p a t i a l memory alone rather than using a s p a t i a l association between, feeder and reward cues. Since birds learned more slowly i n the uncued treatments, t h i s may suggest that s p a t i a l memory requires a longer learning period than s p a t i a l association. At the same time, however, s p a t i a l memory i s resistant to interference learning or distractions (Maki et a l . , 1979). Thus, i t seems that items stored i n s p a t i a l memory by birds are those to be remembered i n the long term, and the experiment described i n chapter 2 suggests the time course over which hummingbirds commit s p a t i a l patterns to long term memory. The importance of long term memory to s p a t i a l learning has been noted i n several studies (Beatty and Shavalia, 1980; Kesner, 1980; Nadel and Willner, 1980). Cognitive Maps The evidence that hummingbirds used cognitive maps i n these experiments i s based on v i s i t a t i o n patterns and the evidence for chunking discussed above. If the birds were dead reckoning, they should show stereotyped approaches to the array and regimented sequences of v i s i t s once they began feeding. Such systematic patterns of feeding have been seen i n insects such as bumblebees, euglossine bees and hawkmoths 146 General Discussion (Dreisig, 1989; Pyke and Cartar, 1992) as well as more advanced animals such as nectar-feeding birds and bats (Kamil, 1978; Pyke, 1978) and i n previous studies with hummingbirds using more complex patterns of feeders (Sutherland, 1985). I found no evidence of systematic foraging i n any of the experiments I conducted. Scholl (1987) suggested that the a b i l i t y of animals to access a l l s i t e s i n a cognitive map with equal ease was one of i t s main advantages over dead reckoning, where the need to follow a series of memorized vectors makes some s i t e s more d i f f i c u l t to access. Landmarks and Cues In the experiments of chapter 3, the birds demonstrated that they can use landmarks to enhance t h e i r learning of s p a t i a l patterns. Edge landmarks that d i f f e r e n t i a t e d rewarding and non-rewarding areas of the array were more useful than c i r c u l a r disks marking the centres of these areas. Since l i n e s have a d i r e c t i o n a l component that c i r c l e s lack, perhaps the birds used t h i s a d d i t i o n a l information to help navigate to rewarding feeders. The l i n e s that marked edges of rewarding groups of feeders were joined into squares, so aside from the possible l e f t - r i g h t or up-down directions birds could derive from them, they could learn that inside two of the squares was rewarding, while outside them (inside the other two squares) was non-rewarding . 147 General Discussion The b i r d s i n a l l o f my exp e r i m e n t s used cues t o l o c a t e t h e f e e d e r s . I n a l l the a r r a y t r e a t m e n t s t h e y had s u r r o u n d i n g orange r i n g s as cues t o f e e d e r l o c a t i o n s t h a t t h e y may o r may not have used as i n f o r m a t i o n . I n t h e c h a p t e r 4 e x p e r i m e n t s t h e y used s p a t i a l l y s e p a r a t e d LEDs t o i d e n t i f y r e w a r d i n g f e e d e r s . I n t h e s t u d i e s o f c h a p t e r 3, t h e y used c o l o u r t o i d e n t i f y r e w a r d i n g groups o f f e e d e r s on t h e a r r a y . T h i s p r o v i d e d some b e n e f i t s t o l e a r n i n g , b u t t h e i n c r e m e n t a l v a l u e was not l a r g e . The b e n e f i t s o f p r o v i d i n g cues t o p r o f i t a b i l i t y were more apparent i n t h e e x p e r i m e n t s o f c h a p t e r 4. I n t h e s e s t u d i e s , t h e a d d i t i o n o f rewar d cues s i g n i f i c a n t l y improved performance. Performance was h i g h e r when cues were c l o s e r t o t h e r e w a r d i n g f e e d e r , w h i c h was a l s o found i n p r e v i o u s s t u d i e s t h a t have s u g g e s t e d t h a t i n c r e a s i n g s e p a r a t i o n between cue and reward i n c r e a s e s t h e l e a r n i n g d i f f i c u l t y (G. Brown, 1992; Brown and Gass, 1993; P i n e l e t a l . , 1986; S t o l l n i t z and S c h r i e r , 1962). I n my experiments b i r d s may a l s o have used cues e x t e r n a l t o t h e a r r a y . I have no d i r e c t e v i d e n c e t h a t t h e b i r d s o r i e n t e d themselves v i a e x t e r n a l v i s u a l cues such as d i s t a n c e t o t h e w a l l s and l i g h t s but I b e l i e v e t h a t t h e y used t h e s e g l o b a l cues when t h e y were f i r s t d e v e l o p i n g c o g n i t i v e maps t o e x p l o i t t h e a r r a y . D i s t a l cues a r e an i m p o r t a n t a s p e c t i n the development o f c o g n i t i v e maps ( E l l e n , 1980; E l l e n e t a l . , 1984; G a l l i s t e l , 1989; M e l l g r e n and Roper, 1986; M i l l e r et al. , 1984; M o r r i s , 1981; S p e t c h 148 General Discussion and Edwards, 1988; Spetch and Honig, 1988; Sutherland and Dyck, 1984; Suzuki et al. , 1980). Even an author who did not accept the idea of cognitive mapping suggested that s p a t i a l learning was a conditioned response to d i s t a l cues (Restle, 1957) . Expectancy and Persistence By showing that birds p e r s i s t i n formerly p r o f i t a b l e patterns of foraging i n the face of sudden environmental s h i f t s that make thi s behaviour unprofitable, a l l of my experiments demonstrated that birds' expectations about the d i s t r i b u t i o n of rewarding feeders was affected by the amount of time they spent using that pattern. As exposure to a pattern increased, so did the birds' persistence i n feeding at the formerly rewarding feeders a f t e r the switch. In laboratory studies, i t appears that the expectancy of reward i s d i r e c t l y t i e d to the past frequency and magnitude of reward (Mellgren et a l . , 1973). Expectancy i s also an increasing function of the number of rewarding t r i a l s (Morris and Capaldie, 1979). Chapter 2 shows that persistent v i s i t a t i o n to formerly p r o f i t a b l e feeders increased only s l i g h t l y with the change from 10 to 20 exposure t r i a l s , presumably because birds' success with the d i s t r i b u t i o n of rewarding feeders was too l i m i t e d i n time to induce a large degree of persistence a f t e r the switch. Persistence at unprofitable feeders then increased r a p i d l y over intermediate numbers of t r i a l s before plateauing a f t e r 149 General Discussion an exposure p e r i o d o f about 40 t r i a l s . P o s s i b l y p e r s i s t e n c e s t o p p e d i n c r e a s i n g because t h e r e i s a l i m i t t o t h e amount of e x p e r i e n c e t h a t i s s t o r e d i n a b i r d ' s memory. T h i s t y p e o f r e s u l t was p r e d i c t e d by s e v e r a l a u t h o r s , who d e v e l o p e d t h e h y p o t h e s i s o f a l i m i t e d and w e i g h t e d memory window t o e x p l a i n l i m i t a t i o n s on a n i m a l l e a r n i n g and memory ( K a c e l n i k e t al., 1987; McNamara and Houston, 1987; McNamara et al., 1989) . The b i r d s i n a l l of my e x periments r e l e a r n e d p a t t e r n s o f r e w a r d i n g f e e d e r s a f t e r the p a t t e r n had been r e v e r s e d . A l t h o u g h I i n t r o d u c e d a complete and sudden r e v e r s a l o f t h e p a t t e r n o f r e w a r d i n g f e e d e r s , t h i s was s t i l l a one t i m e change i n t h e d i s t r i b u t i o n o f f e e d e r s . Perhaps subsequent and r e p e a t e d r e v e r s a l s would have produced enough t e m p o r a l v a r i a b i l i t y t o make l e a r n i n g u n p r o f i t a b l e . I n f i e l d s t u d i e s w i t h b l a c k - c h i n n e d hummingbirds, V a l o n e (1992) found t h a t b i r d s i n s t a b l e environments r e l i e d on p r i o r e x p e r i e n c e t o f i n d f o o d . I n v a r i a b l e environments some b i r d s a d o p t e d a s a m p l i n g approach, but b i r d s u s i n g memory were more s u c c e s s f u l f o r a g e r s . L e a r n i n g i s more, e f f e c t i v e i n c o n s e r v a t i v e environments where change i s l e s s l i k e l y t o r e d u ce t h e p r o f i t a b i l i t y o f b e h a v i o u r based on memory ( N i s h i m u r a , 1994) . A n i m a l s respond t o u n p r e d i c t a b l e v a r i a t i o n by d i s c o u n t i n g t h e v a l u e of h i g h l y u n p r e d i c t a b l e r e s o u r c e s (Bowers and Adams-Manson, 1993). Temporal v a r i a b i l i t y p l a y s 150 General Discussion an important role i n foraging choices for many species (Caraco, 1982; Caraco and Lima, 1987; Gibbon et al. , 1988; Stephens, 1981). Animals as diverse as honeybees and tamarins, for instance, respond to both the mean and variance of food sources and adjust t h e i r foraging choices based on changing energy requirements (Cartar, 1991; Garber, 1988a; Stephens and Paton, 1986). As environmental i n s t a b i l i t y increases, animals reduce extraneous behaviours and focus on maximizing t h e i r short term gains (Forkman, 1991). At some point of increasing environmental i n s t a b i l i t y and unpredictability, individuals should abandon a strategy dependent on learning and memory because i t w i l l lose i t s energetic advantage. Future Studies My studies have l e f t several avenues open that need further exploration. The evidence that hummingbirds synthesize the d i s t r i b u t i o n of rewarding feeders into a single pattern rather than learning i n d i v i d u a l feeder locations i s strongly suggestive but s t i l l not conclusive. Better ways to discriminate between these two p o s s i b i l i t i e s are needed. Work by Brown (1987) might provide an approach to t h i s problem. He suggested that animals who grouped a set of elements into a single unit or pattern could not transfer that learning back to the individual elements; i n the case of hummingbird s p a t i a l memory this would mean that once they 151 General Discussion have l e a r n e d a p a t t e r n they e s s e n t i a l l y throw away t h e memory o f i n d i v i d u a l l o c a t i o n s . I f hummingbirds were t r a i n e d t o use an a r r a y w i t h a s i m p l e but l a r g e p a t t e r n o f r e w a r d i n g and non-rewarding f e e d e r s , and i f t h e y l e a r n a c o h e s i v e p a t t e r n and not j u s t i n d i v i d u a l l o c a t i o n s , t h e y s h o u l d n o t change v i s i t p a t t e r n s t o a s m a l l number o f reward l o c a t i o n s t h a t a r e changed w i t h o u t w a r n i n g t o n o n - r e w a r d i n g , but a r e s t i l l s u rrounded by r e w a r d i n g f e e d e r s . The removal o f s m a l l p i e c e s o f a p a t t e r n o f r e w a r d i n g f e e d e r s (by making f e e d e r s non-rewarding) c o u l d be c o n t i n u e d t o t h e p o i n t where t h e r e was a s i g n i f i c a n t and g r o w i n g drop i n rewards a v a i l a b l e from the p r o f i t a b l e group o f f e e d e r s . At some p o i n t i n t h e c o n t i n u i n g d e t e r i o r a t i o n o f t h e p a t t e r n , b i r d s s h o u l d abandon t h e i r e x p e c t a t i o n s and r e l i a n c e on memory o f reward based on t h e p a t t e r n o f f e e d e r s and change t o e x p l o i t a t i o n o f the a r r a y based e i t h e r on memory o f i n d i v i d u a l l o c a t i o n s ( i f they c o u l d ) o r w i t h o u t r e f e r e n c e t o memory o f p a s t v i s i t s . The r o l e o f t h e s t a b i l i t y of environments c o u l d a l s o be i n v e s t i g a t e d by c a r r y i n g out m u l t i p l e p a t t e r n r e v e r s a l s . I n my e x p e r i m e n t s , b i r d s r e l e a r n e d r e v e r s e d p a t t e r n s , but t h i s might change i f t h e r e v e r s a l s happened more t h a n once. As th e number o r f r e q u e n c y o f p a t t e r n r e v e r s a l s i n c r e a s e d , t h i s e x p e r i m e n t a l p r o t o c o l would b e g i n t o resemble t h e c o n s t a n t s h i f t s i n reward s i t e s seen i n many p s y c h o l o g i c a l e x p e r i m e n t s where a n i m a l s l e a r n t h e a s s o c i a t i o n between 152 General Discussion s t i m u l u s and response and a p p l y t h a t a s s o c i a t i o n i r r e s p e c t i v e o f s p a t i a l p o s i t i o n . I n t h i s s p a t i a l memory ex p e r i m e n t , however, a n i m a l s would l a c k a s i m p l e a s s o c i a t i v e r u l e w h i c h t h e y c o u l d a p p l y . A n o t h e r a r e a t h a t needs f u r t h e r i n v e s t i g a t i o n i s v i s i t a t i o n p a t t e r n s i n n a t u r a l h a b i t a t s t o c o n t r a s t random, s y s t e m a t i c and a r e a r e s t r i c t e d s e a r c h methods. The work t h a t has been done so f a r i n t h i s r e g a r d ( K a m i l , 1978; Wolf and H a i n s w o r t h , 1983; Wolf and H a i n s w o r t h , 1991), i s i n t r i g u i n g and seems t o be c o m p a t i b l e w i t h l a b o r a t o r y s t u d i e s but many q u e s t i o n s remain unanswered. One i t e m t h a t needs d e t a i l e d i n v e s t i g a t i o n i s the degree and e f f e c t o f r e v i s i t a t i o n t o n e c t a r s o u r c e s by n e c t a r - f e e d i n g a n i m a l s . M o d e l l i n g s t u d i e s (Armstrong et a l . , 1987) seem t o c o n t r a d i c t t h e r e s u l t s seen i n l a b o r a t o r y s t u d i e s s uch as mine. The reasons b e h i n d t h i s d i f f e r e n c e need t o be examined. I f t h e e n e r g e t i c arguments r a i s e d by t h e models a r e a c c u r a t e , why do a n i m a l s i n t h e l a b o r a t o r y show c o n t i n u i n g r e v i s i t a t i o n ? I s r e v i s i t a t i o n due t o i n t e g r a t i o n o f f e e d e r l o c a t i o n s i n t o a n o n - d i s s o c i a b l e p a t t e r n ? I s t h i s b e h a v i o u r a l s o seen i n f o r a g i n g b e h a v i o u r i n t h e w i l d ? F i n a l l y , one o f t h e drawbacks t o w o r k i n g w i t h r u f o u s hummingbirds i s t h a t t h e y a r e h i g h l y t e r r i t o r i a l and a n t i s o c i a l . As a r e s u l t , o b s e r v a t i o n a l l e a r n i n g and s o c i a l communication a r e d i f f i c u l t t o e x p l o r e , e s p e c i a l l y i n a l a b o r a t o r y environment, w h i c h reduces t h e g e n e r a l 153 General Discussion a p p l i c a b i l i t y of the results from hummingbird studies to date. 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