Open Collections

UBC Theses and Dissertations

UBC Theses Logo

UBC Theses and Dissertations

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

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

Item Metadata

Download

Media
831-ubc_1995-0105.pdf [ 7.59MB ]
Metadata
JSON: 831-1.0086804.json
JSON-LD: 831-1.0086804-ld.json
RDF/XML (Pretty): 831-1.0086804-rdf.xml
RDF/JSON: 831-1.0086804-rdf.json
Turtle: 831-1.0086804-turtle.txt
N-Triples: 831-1.0086804-rdf-ntriples.txt
Original Record: 831-1.0086804-source.json
Full Text
831-1.0086804-fulltext.txt
Citation
831-1.0086804.ris

Full Text

PATTERN LEARNING AND SPATIAL MEMORY IN RUFOUS HUMMINGBIRDS (Selasphorus rufus) by G o r d o n D. M c l n t y r e B.Sc,  U n i v e r s i t y o f B r i t i s h Columbia V a n c o u v e r , B.C. 1980  A THESIS SUBMITTED I N PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF SCIENCE  in 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 a s c o n f o r m i n g to the required  standard  THE UNIVERSITY OF B R I T I S H COLUMBIA FEBRUARY 1995 © GORDON D. MCINTYRE, 1 9 9 5  In  presenting  degree freely  at  this  the  thesis  in  University of  partial  fulfilment  of  of  department publication  this or of  thesis for by  his  or  agree that  scholarly purposes may be her  representatives.  It  this thesis for financial gain shall not  permission.  Department  of  2°<M-OGy-<  tg^^/tH?  The University of British Columbia Vancouver, Canada  Date  DE-6 (2/88)  requirements  British Columbia, I agree that the  available for reference and study. I further  copying  the  "S7iJ2>'&$  is  an advanced  Library shall make  it  permission for extensive  granted  by the  understood  be  for  that  head  of  copying  my or  allowed without my written  Abstract  In t h i s study rufous  hummingbirds.  hummingbirds rewards. birds  I examined s p a t i a l  rapidly  They u s e d  were  This  laboratory  landmarks  visiting  most  to  find  feeders  patterns  reward  in  sites.  rewarding  i n non-rewarding areas,  subsided  evidence  r a p i d l y once  applicable,  f o l l o w e d r a p i d l y by  patterns.  The  significantly learning.  types  influenced  than  information  central  about  markers, although In  of  one  both  associations  Persistence  was  the  information rate  and  more  landmarks.  I  not  rapidly  They  hummingbirds  rapidly  also  learned  eventually  using used  period,  of edge  colour  kinds  of  than  both  spatial  They l e a r n e d  spatial  spatial  A l t h o u g h s p a t i a l memory t a s k s learning  provided  a strong benefit to l e a r n i n g .  spatial associations.  more  longer  persistence  memory  a c h i e v i n g a h i g h r a t e of performance a f t e r a very interval.  no  l e a r n i n g the a l t e r e d reward  learned  t h i s was  and  reversed.  r e w a r d q u a l i t y embedded i n b o t h  experiment,  memory t a s k s and  behaviour  landmark  Hummingbirds  landmarks  birds'  Once  they p e r s i s t e d  f o r c o g n i t i v e mapping. the  of  areas  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 w e r e  i s strong  longer  memory i n  experiments,  2-dimensional  learned  a v o i d i n g most f e e d e r s i n the  In  l e a r n i n g and  the  c o m p a r a b l e t o t h a t on  birds' spatial  tasks,  short  required a  time  slightly  performance association  was tasks.  The  speed  of  reward s i t e s although  forming  spatial  associations  between  cue  d e p e n d e d s t r o n g l y on t h e d i s t a n c e b e t w e e n  hummingbirds  eventually  achieved  and  them,  comparable  performance regardless of separation. Birds tasks  were  than  between  more  spatial  resistant  t o change  association tasks.  After  Time  the  longer  feeders,  spatial  a s s o c i a t i o n ones.  memories  on  when  the p a t t e r n  longer  spent  using  memory  tasks  in a much  a  more  face  patterns changed.  pattern  formerly pattern  spatial  i n the  rewarding  of s u c c e s s f u l l y using  persisted Time  foraging  persistence  experience  birds  behaviours. influenced  birds'  spent  memory  separations  c u e and r e w a r d r e s u l t e d i n more r e l i a n c e on  change.  affected  spatial  Greater  memory a n d g r e a t e r p e r s i s t e n c e o f t h e s e of  on  of  rewarding of  feeders  than  spatial  Table o f Contents  Abstract Table of Contents L i s t of Tables L i s t of Figures Acknowledgements  i i iv v i i viii x  Chapter 1 . General Introduction Tactics of Survival Learning Components o f L e a r n i n g Memory S p a t i a l Memory R o l e o f L e a r n i n g i n S p a t i a l Memory C o g n i t i v e Maps Cues and Landmarks Cues Landmarks R o l e o f Cues and Landmarks i n L e a r n i n g Outline of Studies Chapter 2 . Pattern Learning and Memory i n R u f o u s H u m m i n g b i r d s  Persistence  1 1 1 2 4 7 9 11 13 15 16 17 18 of  Spatial 19  Section I . Introduction Learning Advantages of Learning Disadvantages of Learning Alternatives to learning Complex environments Mathematical modelling P e r c e p t i o n o f t h e environment Experimental protocols Current study  19 19 20 21 21 22 23 25 27 28  S e c t i o n I I . M a t e r i a l s and Methods Subjects Experimental Environment Training Experimental Procedures  30 30 30 32 33  Section I I I . Results I n i t i a l Performance D u r a t i o n o f Exposure and P a t t e r n R e v e r s a l s V i s i t a t i o n Patterns  37 37 40 45  Section IV. Discussion Advantages of Learning  53 53 iv  Factors A f f e c t i n g Learning Cues Search Techniques Stability Costs of Learning... Sampling Change E x p e c t a t i o n s and P e r s i s t e n c e R e l e a r n i n g A f t e r a Change Conclusions Chapter 3 . Landmark Hummingbirds  Forms  53 53 54 56 57 57 58 59 62 63  and S p a t i a l  Memory  i n Rufous 64  Section I. Introduction S p a t i a l Memory Cues a n d L a n d m a r k s Cues Landmarks R o l e o f Cues a n d Landmarks i n L e a r n i n g Current Study  64 64 64 65 66 66 67  S e c t i o n I I . M a t e r i a l s and Methods Subjects . .. Experimental Environment Experimental Design Training Experimental Procedures  69 69 69 71 75 76  Section I I I . Results Performance I n d i c a t o r s I n i t i a l Learning D i f f e r e n c e s Between Treatments Switch Effect V i s i t a t i o n Patterns  79 79 79 83 89 90  Section IV. Discussion Use o f A r r a y M a r k e r s Lines versus Centres Lines versus Colours C o g n i t i v e Maps Chunking E n v i r o n m e n t a l Change, C o m p l e x i t y a n d t h e S w i t c h Conclusions  93 93 93 95 96 98 E f f e c t . . 99 103  Chapter 4 . S p a t i a l A s s o c i a t i o n a n d S p a t i a l Memory i n R u f o u s Hummingbirds 105 Section I . Introduction S p a t i a l Association Learning S p a t i a l Memory Learning Processes Differences i n Learning  105 105 107 107 109 v  Advantages and Disadvantages U n c e r t a i n t y and Perception Current Study  110 I l l 113  S e c t i o n I I . M a t e r i a l s and Methods Subjects Experimental Environment Training Experimental Procedures  116 116 117 118 119  Section I I I . Results I n i t i a l Learning Switch E f f e c t 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 Differences i n Persistence  121 121 123 123 125  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 a n d 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 L o a d 137 Conclusions 139 Chapter 5. G e n e r a l D i s c u s s i o n What C o n d i t i o n s P r o d u c e L e a r n i n g ? How i s L e a r n i n g R e v e a l e d i n P e r f o r m a n c e ? What i s L e a r n e d a b o u t t h e i r E n v i r o n m e n t s a n d How? Pattern Learning : Chunking S p a t i a l Memory........ C o g n i t i v e Maps L a n d m a r k s a n d Cues Expectancy and P e r s i s t e n c e Future Studies  141 141 142 143 143 144 146 146 147 149 151  Literature Cited  155  vi  L i s t of Tables  Chapter  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 e a c h o f t h e t r e a t m e n t s 37 T a b l e 2. Regression a n a l y s i s of i n i t i a l performance versus n a t u r a l l o g of 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 switch 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 switch 42 T a b l e 5. Comparison of 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 the switch 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 both performance i n d i c a t o r s 43 Chapter  3  Table  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 t h e 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 of 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 regressions 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 f i r s t 50 trials 84 T a b l e 10. R a n k e d means o f t r e a t m e n t s f r o m T u k e y 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 incorrect first 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 the switch 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 switch 91 Chapter  4  Table  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 a n d 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 first 10 m i n u t e s o f e x p e r i m e n t a l r u n s 121 T a b l e 14. P o s t - s w i t c h p e r f o r m a n c e o f b i r d s i n t h e d i f f e r e n t treatments 125  vii  L i s t of F i g u r e s  Chapter 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 for the feeder array 34 F i g u r e 2. 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 c o r r e c t (rewarding) averaged over blocks of 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 treatments 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 e r a g e d 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 of the 4 treatments. 39 F i g u r e 4. A v e r a g e number o f i n c o r r e c t v i s i t s f o r e a c h o f the 4 . exposure treatments 41 F i g u r e 5. A v e r a g e number o f i n c o r r e c t v i s i t s b y b i r d s f o r each of the treatments i n the 5 t r i a l s immediately following the pattern reversal 44 Figure 6. Differences i n number o f i n c o r r e c t visits ( 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 the period following the pattern reversal 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 e a c h 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 o f a l l v i s i t s t o e a c h 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 switch) 49 F i g u r e 9. S a m p l e 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 o n t h e i r f i r s t 10 v i s i t s o f T r i a l 1 51 F i g u r e 1 0 . S a m p l e 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 of T r i a l s 1 - 6 52 Chapter 3 F i g u r e 11. S t y l i z e d representations of the a r r a y markers used f o r the eight treatments described i n the text..72 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 across a l l b i r d s i n each treatment a n d 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 treatments 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 e a c h 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 to rewarding feeders, averaged f o r a l l b i r d s i n each of the 8 treatments 82 F i g u r e 15. Summary o f T u k e y 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 of t h e 8 treatments 86 F i g u r e 1 6 . Summary o f T u k e y 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 treatments 87 viii  Figure 17. T o t a l v i s i t s by a l l b i r d s t o non-rewarding l o c a t i o n s i n t r i a l s 46 - 50 of a l l treatments 92 Chapter 4 F i g u r e 18. Percent o f v i s i t s that were t o the c o r r e c t feeder f o r each of the 9 treatments 122 F i g u r e 19. Box p l o t s of number of v i s i t s by b i r d s t o the formerly good feeder a f t e r the feeder s w i t c h 124 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 of 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 . 127  ix  Acknowledgment 8  I would e s p e c i a l l y l i k e to thank my a d v i s o r , Lee Gass, f o r h i s support and encouragement d u r i n g my t h e s i s work. My r e s e a r c h committee, Don Ludwig, Jamie Smith and Don W i l k i e a l s o p r o v i d e d sound advice and a great d e a l of p a t i e n c e throughout t h i s study. Many people p r o v i d e d t e c h n i c a l support and a s s i s t a n c e that g r e a t l y eased the pains of doing t h i s r e s e a r c h . They a l l deserve my thanks. Don Brandys and Tony Lum p u z z l e d with me over numerous electrical design questions. G r a n v i l l e W i l l i a m s went beyond the c a l l of duty i n p r o d u c i n g cages and o t h e r m a t e r i a l s f o r my experiments and maintenance of the b i r d s . Charles Mathieson and A l a s t a i r B l a t c h f o r d were f o u n t a i n s of computer programming knowledge. Chris Harvey C l a r k , A r t h u r Vanderhorst, and Armin Tepper helped us through numerous d i f f i c u l t i e s w i t h animal c a r e . My f e l l o w staff members i n the Science Department of Vancouver Community C o l l e g e always p r o v i d e d encouragement and support. B i l l Milsom allowed us to borrow l a b equipment at 1:00 a.m. and probably saved s e v e r a l b i r d s ' l i v e s as a r e s u l t . Very s p e c i a l thanks go to my labmates and fellow v e t e r a n s , Mark Roberts and Gayle (one of these days I ' l l get your .name r i g h t ) Brown f o r t h e i r friendship, help and support throughout my work. The rapport between us kept us at l e a s t somewhat sane. I r e s e r v e my f i n a l thank-yous f o r my family. My f i a n c e e L o r r a i n e , my mother Brenda, my b r o t h e r John, and my o t h e r f a m i l y and f r i e n d s p r o v i d e d the moral support (and o c c a s i o n a l needed nagging) t h a t kept me going. T h i s r e s e a r c h was p a r t i a l l y funded by an o p e r a t i n g grant (NSERC) to Lee Gass.  x  1.  Chapter  General  Introduction  T a c t i c s of S u r v i v a l Animals everyday  must  existence  reproduction. and  carry in  order  with  Foraging  a  number  of  to  ensure  their  These i n c l u d e f i n d i n g food,  avoiding predators.  coexist  out  their  has  Schoener, 1987) experimental  in  their  survival  and  s h e l t e r and mates  For s o c i a l animals, f i n d i n g ways to  compatriots  been  tasks  i s another  extensively  important  studied  (see  task.  review  by  perhaps because i t i s easy to q u a n t i f y i n an  setting.  Learning Learning change  i n an  alter  the  i s an animal,  important as  animal's 1978).  nudibranchs  learning  Examples  l e a r n i n g new  languages.  to  sensitization  learning to  a  of  survival.  given  shock  l e a r n i n g can  non-associative is  stimulus,  the such  1  simple as  in  is  that  a  can  circumstances  learning  electric  Generally,  It  experience,  in of  avoid  broad c a t e g o r i e s :  Non-associative  to  result  behaviour  (Hintzman,  i n t o two  a  aid  range  from  to  humans  be  divided  and a s s o c i a t i v e . habituation the  or  nudibranch  General  example the  (Raven a n d J o h n s o n ,  development  1989).  Associative  o f an a s s o c i a t i o n  between a s t i m u l u s  and response.  between Most  learning  such  foraging  and others a r e a s s o c i a t i v e .  There  are  processes. and be  as language  discussed  involved  of  mechanistically  about  .  believe that  found  events  group,  learning  learning  behaviours  should  (Hintzman, boxes.  a task  The  are either  a r e unobservable, or  A second school terms  i n humans.  like  learning  they  are  by  considered  ideas,  thoughts  and both  group  t o t h e thought  i s interested i n  and purposes  approach o f f e r s  offer  considers  the processes of  equivalent  This  neither  o f thought  and t r e a t s  as i f they were  I n my v i e w ,  processes  because  i n humanistic  learning  processes  1978)  about  b y o t h e r w o r k e r s who t a k e a s i m i l a r a p p r o a c h  thebehaviourists.  behaviour  navigation,  o f thought a r e b e h a v i o u r i s m  i n learning  this  or  examples o f complex  theories  of observable  unimportant,  members  mental  of  Behaviourists  processes  considered  animal  two s t i m u l i  E s s e n t i a l l y , they t r e a t animals as b l a c k  internal  some  number  i n terms  learning i s  acquisition, spatial  Two d o m i n a n t s c h o o l s  cognitivism.  1978).  to  a  Introduction  valuable  (Hintzman,  the sole  insights  truth  into the  involved.  Components o f L e a r n i n g P e r h a p s t h e most b a s i c the  linkage  repeatedly  between presented  idea  stimulus with  a  i n associative and response.  stimulus, 2  each  learning i s An  time  animal followed  General  closely will  by  a  link  reward on  the  completion  items  together  of a  into  specific  a  (Damianopoulos, 1989).  association  to be made i s that the stimulus and  be  linked  spatial  i n space  s e p a r a t i o n between  the a b i l i t y of the animal al.,  and  P i n e l et  1988; In  a  few  demonstrate  al.,  reward  Either and  reinforcer temporal  stimulus  to a s s o c i a t e the items  however,  i n the  i t has  absence of  been  (Gibbon  et  possible  to  a  1978).  In most cases, though, reinforcement i s an  element  of  This  linking  frequency  the  animals  and  and  the  stimulus value  carry  the  out  response  the  of  1979).  association.  rewards  yield  by  to  attempt  the to  animal deal  value  can  reduce  assume  rewards  or  (Gleitman,  only  with  the  Low  al.,  et  Cognitivists  that  important  i s affected  (Gibbon  can  (Hintzman,  reinforcement:  learning  actions  two  t o i n t e r n a l m o t i v a t i o n or the i n t r i n s i c  stimulus  Behaviourists behaviours,  degree  the  stimulus-response  and  of  Capaldie,  punishment due of  of  between  i n f r e q u e n t rewards or v a r i a b l e  speed  Morris  of  and  rewards,  association  In  response  create  formation  or  weaken  reinforcement.  some cases the mere c o n t i g u i t y of stimulus and learned  for this  1986).  cases,  learning  requirement  time.  the  response,  stimulus-response  association  closely  One  Introduction  1988; that avoid value 1974) .  observable  e i t h e r i g n o r i n g m o t i v a t i o n , or acknowledging i t s  e x i s t e n c e but t r e a t i n g i t m e c h a n i s t i c a l l y .  3  General  Another aspect that  i n v o l v e s and a f f e c t s m o t i v a t i o n i s  the expectancy of an event o c c u r r i n g . promoted workers  by the c o g n i t i v e propose  that  Introduction  school  animals  T h i s concept has been  (Hintzman,  develop  1978).  These  expectations  rewards and f u t u r e events based on past e x p e r i e n c e .  about None of  these b e h a v i o u r a l processes can occur, however, without the a b i l i t y t o use past experience through memory. Memory "Memory" r e f e r s  t o processes through which e x p e r i e n c e s  and l e a r n i n g a r e r e t a i n e d over time et al., At  1978; G o e l e t  1986), and we a r e j u s t b e g i n n i n g t o understand them.  least  suggested, durable task.  (Hintzman,  three based  different  types  on d u r a b i l i t y  o f these i s working Slightly  of  memory  have  been  of the memory.  The  least  memory that  more permanent  i s short  i s used  during  term memory,  a  that  l a s t s beyond the task at hand but which i s s t i l l measured i n minutes o r hours.  Finally,  long term memory can p e r s i s t f o r  days o r throughout an animal's l i f e t i m e . Working Generally,  memory  i s used  short  term.  the d i f f e r e n c e between working memory and short  term memory i s not w e l l doubt  i n the extreme  understood.  Some authors tend t o  i t s e x i s t e n c e as a separate form of memory from s h o r t  term memory  (van L u i j t e l a a r  may not be d i s t i n c t  et al.,  1989).  processes w i t h d i f f e r i n g  The two may o r physiological  bases, but workers agree the purpose of working memory i s t o retain  only  those  elements  of 4  experience  necessary  to  General  accomplish  t h e immediate task  "throwaways  (Maki,  M  a t hand.  1987) t h a t  Introduction  These memories a r e  are acquired  quickly,  used  immediately and f o r g o t t e n . Short  t e r m memory i n c l u d e s  may  need t o r e c a l l  not  retained  involve  beyond t h e immediate t a s k  indefinitely.  covalent  the activities  (Barnes,  1988; G o e l e t term  indefinitely.  This  modifications  regulate  Long  those items which an animal  o f memory  of existing  o f t h e neurons  e t al.,  memory These  form  includes  memories  e t al.,  (Goelet  1986) .  I f long  proteins,  proteins  and t h e i r  everything  also  involve  synapses.  memory  proteins, but  requires  genes i n  1 9 8 9 ; Thompson,  generation  o f new  d e v e l o p more s l o w l y  this  than  t e r m memory.  d i f f e r e n c e b e t w e e n s h o r t a n d l o n g t e r m memory i s i n  some ways a n a l o g o u s t o t h e d i f f e r e n c e b e t w e e n hormone In  that  retained  of specific  1986; M a t t h i e s ,  l o n g t e r m memories s h o u l d  working o r short The  term  seems t o  1986).  through m o d i f i c a t i o n of the expression neurons  but which a r e  case,  short  term  memory  i s stored  types.  i n ar fashion  similar  t o p r o t e i n b a s e d hormones s u c h a s a d r e n a l i n .  Both  provide  immediate responses that a r e short  term  memory like but  i s stored  i n a fashion  testosterone. can survive Wickelgren  limbic arousal  similar  Here t h e e f f e c t s  lived.  Long  to steroid  take  longer  hormones  t o develop  indefinitely. (197 9)  suggested  that  the  hippocampal,  system plays a key r o l e i n t r a n s f e r r i n g  5  items  General  from  working  altered  memory  neurons  t o long  from  term  memory  continuing  Introduction  by i s o l a t i n g t h e  inputs  while  cellular  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 term memories. While  some  workers  have  suggested  multiple  w o r k i n g memory, i n c l u d i n g a f o r m u s e d s o l e l y of  spatial  relationships  , (Gallistel,  forms  of  f o r remembrance  1990; I n u i ,  1988;  R o b e r t s , 1 9 8 8 ) , o t h e r s s u g g e s t t h a t t h e r e i s no e v i d e n c e f o r multiple  f o r m s o f w o r k i n g memory, a n d t h a t b o t h s p a t i a l a n d  non-spatial short term In  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 (Ennaceur and M e l i a n i ,  the long  differences.  term,  For  1992).  however,  example,  there  Nadel  do  and  Willner  (1980)  that  via  t e r m o r w o r k i n g memory b u t a c o g n i t i v e map o f a n  animal's and  surroundings i s too large  spatial  different  use o f cues.  c a n be used  f o rshort  reference to a cognitive from  memory  t o be  suggested short  some a s p e c t s o f s p a t i a l  seem  term  storage  map i s f u n d a m e n t a l l y  I t should  be  remembered,  h o w e v e r , t h a t a n i m a l s a t t e n d t o many s e n s e s a t o n c e , which involve a t least s l i g h t l y d i f f e r e n t neural least  sensors,  p r o c e s s i n g mechanisms a n d s t o r a g e s i t e s , several  overlapping  brain  areas w i l l  a l l of  pathways,  so that a t  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 a n d m e m o r i e s a r e u n l i k e l y t o b e e n t i r e l y isolated  from  (Squire,  1986).  birds neural  each  other i n single  Many g r o u p s  a n d humans, structures  may s h a r e  locations  o f advanced many  and f u n c t i o n s  6  i n the brain  animals,  o f t h e same (Bingman  including  or  e t al.,  similar 1989;  General  Griffin,  1976;  differences  may  lateralization (Clayton,  MacPhail, be of  1982;  important  spatial  1993; C l a y t o n  and  size  spatial  memory  1989),  but  coupled  Krebs,  1993  and  variation  i s general  such  storing  1982), o r v a r i a t i o n with  Species  1982),  i n food  (Sherry and Vaccarino,  there  1985).  (MacPhail,  memory  p o s s i b l y humans (de Renzio, hippocampal  Olton,  Introduction  as  birds  1994) and i n relative  i n reliance  1989; Sherry  agreement  that  on  et a l . ,  the b a s i c  p r i n c i p l e s a r e widely a p p l i c a b l e .  S p a t i a l Memory "Spatial  memory"  refers  animals  remember l o c a t i o n s  numbers  of  species  v a r i o u s ways. use  spatial  memory  thousand  locate  fruit  with  a r e known  by  environment.  t o use  spatial  which  Growing memory i n  pups  their  (McCracken,  young  bats  i n colonies of  1993), monkeys use i t  three-dimensional  jungle  to  environment  1991), and f i s h l o c a t e nests and d e f i n e t e r r i t o r i e s of s p a t i a l  spatial  territoriality 1981;  i n their  to l o c a t e  in a  the h e l p  birds,  the processes  Among v e r t e b r a t e s f o r i n s t a n c e , female  several  (Menzel,  to  memory  memory is  used  (Warburton, in  both  1990) .  Among  foraging  and  (Balda and Kamil, 1988; Gass and Montgomerie,  Gass and Sutherland, 1985; Shettleworth, 1983), and i s  flexible  enough  (Valone  and  t o cope  Girardeau,  L u i j t e l a a r et al.,  with  rapidly  1993;  changing  Vander  Wall,  conditions 1991;  1989; W i l k i e , 1986b; W i l k i e et al.,  Wunderle and Martinez, 1987; Z e n t a l l et al., 7  1990).  van  1981;  General  Invertebrates combination to  food  also  use s p a t i a l  memory.  o f s p a t i a l memory and o l f a c t o r y  sources  o r nest  Haefner and C r i s t ,  locations  Introduction  Ants  cues t o r e t u r n et al.,  (Collett  1994; H o l l d o b l e r , 1980).  use a  1992;  H o v e r f l i e s use  s p a t i a l memory t o r e t u r n to an unmarked l o c a t i o n  i n mid-air  ( C o l l e t t and Land, 1975). Spatial studied.  memory  i n honeybees  i s well  (Wellington and Cmiralova,  h i v e and t o n a v i g a t e w i t h i n the h i v e  The  such  as may occur  (Dyer,  use o f s p a t i a l  that  using  greater  than  a five-fold  1994). with  search  swarming t o a new nest  and  (Valone, 1991) .  spatial  a  memory  energy  three  searching.  to  advantage five-fold  (Armstrong  arthropods advantages.  limited use  learning  spatial  over  completely  advantage  over  to  gain  that  even  animals  as  desert  such these  energetic  S i m i l a r e n e r g e t i c advantages apply t o d i f f e r e n t  kinds o f organisms performing as t e r r i t o r i a l (Gallistel,  can p r o v i d e  et al., 1987; Benhamou,  abilities  memory  energetic  Modelling studies  t o forage  Benhamou's s t u d i e s a l s o suggest more  t o a l t e r a t i o n s of  memory a f f o r d s d i s t i n c t  suggest  systematic  1991), and i t i s  1993).  and e c o l o g i c a l advantages  random  after  1979), t o f i n d the  (Dyer,  enough t o a l l o w them t o r e o r i e n t  landmarks, location  and  F o r example, they use s p a t i a l memory t o r e t u r n t o  flower patches  plastic  documented  defense,  1990; Gould  similar ecological  nest b u i l d i n g , and Marler,  8  tasks  such  and brood p r o t e c t i o n  1987; Kramer and Weary,  General  1991;  Wolf  e t al.,  differences these  1972).  The p h y s i o l o g i c a l  b e t w e e n s p e c i e s make t h e b r o a d  advantages  cornerstones  remarkable,  Introduction  and e c o l o g i c a l based  and have p r o v i d e d  of behavioural ecology  (Gray,  nature of one o f t h e  1987; Schoener,  1987). Learning enables environments, disappear (Bowers from  animals  although  i f irregular  t o make more e f f e c t i v e  t h e advantages temporal  a n d Adams-Manson,  of spatial  variability  1993; N i s h i m u r a ,  t h e e n e r g e t i c and other p h y s i o l o g i c a l  memories,  i t becomes  variability  increasingly  increases that  the cost  use of learning  i s too great 1994).  Aside  costs of storing  likely  as  temporal  of foraging  (or other  ways o f u s i n g m e m o r i e s ) w i l l be w a s t e d .  Role of Learning i n Spatial Memory If workers of  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 , a s most assume i t t o b e , t h e n 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  remembering a n d u s i n g e x p e r i e n c e s h o u l d be  Especially they  t o the extent  l e a r n about t h e i r  that animals  environments  s h o u l d be a b l e t o use t h e i r  all  red tubular  visiting that  should  flowers  flower  across s i t u a t i o n s ,  of  a  certain  more u s e f u l .  9  learning  shape  difficult  i s rewarding,  they  effectively with a  F o r example,  n o t b e much more  a particular  c a n g e n e r a l i z e what  environments  minimum o f s t o r e d i n f o r m a t i o n .  advantageous.  are  than  that worth  learning  but c l e a r l y  i t  i s  General Several  studies  behaviours  have  elicited  demonstrate natural  in  and  activities  Elsmore,  evidence  laboratory  the use of s p a t i a l  foraging  Mellgren  provided  memory  that  to  are equivalent  to  and  Baum,  Numerous  or  increases  foraging efficiency,  t o f i n d mates  al., and  Dyer,  1993).  The  ability there  food  abilities,  spatial  information  i s not  species  differences.  Animals  learn  are distinct  bird,  the blue  corvid  and  Shettleworth Even variation  parid  reckoning  limited  bird  does  The m a r s h  spatial  memory  not cache  A similar  food,  disparity  r e l a t e d j a y and jackdaw  (Clayton  based  (Balda  and  Kamil,  1989;  1986). oriented  species  there  t o use s p a t i a l  wasps and a n t s  ability  excellent  which  species  i n the a b i l i t y  dead  f o r example,  S i m i l a r r e s u l t s have been found i n o t h e r  i n spatially  as bees,  has  learning tasks.  and Krebs,  such  and marsh t i t s ,  tit,  e x i s t s between t h e c l o s e l y 1994).  1991; Robinson  s p a t i a l memory a b i l i t i e s .  storing  while  Krebs,  t o l o c a t e dens o r h i v e s  to  cannot perform s i m i l a r  and  tool  1991; Menzel,  have g r e a t l y d i f f e r e n t a  i sa  a n d Weary,  as c l o s e l y r e l a t e d a s b l u e t i t s  tit,  have  (Bowers a n d Adams-Manson, 1 9 9 3 ; H a c c o u e t  1991; Kramer  universal;  1991;  studies  d e m o n s t r a t e d t h a t u s e o f s p a t i a l memory i n n a t u r e that  operant  environments  (Dallery  1991) .  Introduction  seem t o r e l y  o n remembered  i s definite  memory. most  landmarks,  Insects  h e a v i l y on with  a  very  t o g e n e r a l i z e a n d p r o d u c e c o g n i t i v e maps o f  10  General  their  surroundings  1993;  Dyer,  (Collett  1991; Dyer,  B i r d s and mammals,  et al.,  Introduction  1992; C o l l e t t  1993; Greggers  et  and Menzel,  on the other hand, o f t e n produce  c o g n i t i v e maps, as evidenced by t h e i r a b i l i t y  al.,  1993). complex  t o f i n d novel  r o u t e s , a v o i d o b s t a c l e s and vary t h e i r behaviour t o respond to  novel  Collett,  environmental 1987; E l l e n  changes  et al.,  (Bingman  et  al.,  1984; E t i e n n e et al.,  1988; 1990;  Gass and Sutherland, 1985; Menzel, 1973; Vander W a l l , 1991) . While reckoning  i t may be p o s s i b l e paths  locations,  of  movement  t h e r e a r e ways t o s i m p l i f y  by b u i l d i n g  vectors)  spatial  based  (Giraudo and Perauch,  on a range , of s t u d i e s ,  (Aadland et al.,  1988), that  between  memory t a s k s  up map-like images of the environment.  do t h i s r e g u l a r l y likely,  (a s e r i e s  f o r animals t o remember dead  Humans  and i t seems  animals do a l s o  1985; Gould, 1985; Maki et al.,  1979; Nadel  and W i l l n e r , 1980; O'Keefe and Conway, 1980; Tolman,  1948).  C o g n i t i v e Maps A c o g n i t i v e map i s an i n t e r n a l i z e d r e p r e s e n t a t i o n of an animal's  environment  between l o c a t i o n s 1990; maps  Gould,  i n that  1986c).  i n animals  including  the geometric  environment  greatly  other  than  humans  advantageous.  cognitive  abilities  flexible,  there  (Gallistel,  1989 and  The evidence f o r the use of c o g n i t i v e  s t o r i n g memories of the environment be  relationships  such  i s ample  as  i s circumstantial,  i n such a f a s h i o n s h o u l d  While  animals  ants  are less  evidence 11  but  that  with  limited  behaviourally  animals  such  as  General  mammals  and b i r d s  go beyond  inertial  r e p e t i t i o n s of past a c t i v i t i e s The  concept  Introduction  reckoning  and simple  (Tolman, 1948) .  o f a c o g n i t i v e map i n any animal  not u n i v e r s a l l y accepted.  is still  In a f a s h i o n s i m i l a r t o the s p l i t  between c o g n i t i v i s t s and b e h a v i o u r i s t s t h e r e a r e two s c h o o l s of thought authors  such  animals  rely  remembered (1986a  on s p a t i a l n a v i g a t i o n . as  Dyer  (1991,  have  suggested  that  o r movement along a s e t of  to navigate.  and 1986c) , argue  paths  1993),  on dead reckoning,  vectors,  One group, championed by  that  Others,  such  the a b i l i t y  and n a v i g a t e w i t h only a subset  as  Gould  to find  novel  of previous  cues and  landmarks p r e c l u d e s the s o l e use of s i m p l i s t i c n a v i g a t i o n a l t o o l s as dead reckoning i n many animals. Cognitive navigational  maps  the environment  advantages.  distance travelled 1990;  of  provide  Monkeys and chimps  t o reward sources  numerous  minimize  the  (MacDonald and W i l k i e ,  Menzel, 1991; Menzel, 1973), g e r b i l s o r i e n t  themselves  i n n o v e l l o c a t i o n s w i t h r e f e r e n c e t o o b j e c t s they c o u l d o n l y be remembering a t the time and  rats  flexible  (Thinus-Blanc and I n g l e s , 1985),  s t o r e m u l t i p l e maps simultaneously, exploitations  of t h e i r  environment  allowing f o r (Maki  et  al.,  1979) . We understand  p o o r l y at best how animals  of t h e i r environments. process  begins  with  s y s t e m a t i c sampling  develop  maps  I b e l i e v e that i t i s l i k e l y t h a t the either  random  sampling  forays and that p r i o r  12  forays  experience  or  likely  General  biases tied  u s e o f t h e s e methods.  to their  e c o l o g i c a l needs  to a b i l i t i e s  gained through  the  trial  original  different  Animals'  search patterns a r e  (Root a n d K a r e i v a , 1 9 8 4 )  evolution  and e r r o r  (Gould,  investigation  portions of the terrain,  an animal  some a n i m a l s c a n n o t move b e y o n d t h i s  know  that  they  1985; as  primates,  these  sets  complex  maps  that  These b i r d s , and o t h e r s ,  allow  Ellen  e t a l . , 1984; S h o l l ,  of  Perhaps  places  into  relationships  i n press;  Sutherland,  along w i t h groups  can apparently  highly  e x p l o i t a t i o n o f t h e i r environments 1993;  sites.  geometric  ( S u t h e r l a n d and Gass,  rodents  can begin t o  s u c h a s h u m m i n g b i r d s , h o w e v e r , we  synthesize  Thompson, 1 9 9 4 ) .  From  stage.  structures that incorporate spatial, among e l e m e n t s  1986c) .  and  of the value of  remember s e t s o f r e w a r d i n g a n d n o n - r e w a r d i n g  In t h e case o f b i r d s  Introduction  flexible  such  generate  movement  and  (Bowers a n d Adams-Manson, 1987).  Cues and Landmarks Part  of  t h e process  environment  involves learning  landmarks.  Without  limited  to  dead  Landmarks,  by t h i s  permanent  items  navigational physical  aids.  item  that  of  developing  the positions  cues o r landmarks reckoning  as  definition, that  an animal  a  map  animals a r e presumably means  can  of navigation.  sense  we t h i n k can e a s i l y  c o u l d be an a r e a o f s p e c i f i c wind 13  of the  of recognizable  a r e any permanent  animals  Typically,  a  and  o r semiuse  o f a landmark  as  as a  s e e ; however, i t  currents or a site  where  General  an  o d o u r , o r a n y o f a number o f o t h e r  maximized.  I t must be c o n s i s t e n t  a n i m a l t o become c o n d i t i o n e d associate  i t with  some  Introduction  s e n s o r y phenomena, i s  enough, h o w e v e r ,  f o r the  t o i t s presence and t o l e a r n t o  specific  reward  or  task  overlap  between  this  in a  p a r t i c u l a r place o r area. There of  i s considerable  a landmark and t h e d e f i n i t i o n  define  a  reward  specifically  cue as an  will  that i s (and i n  i n d i c a t e s an area  containing  one o r  sites.  evidence  environmental that  o f reward  I  one c u e , one r e w a r d ) , a n d a r e w a r d l a n d m a r k a s  a navigational a i d that  The  indicator  cue.  l i n k e d t o t h a t reward i n space and time  a 1:1 r a t i o :  more r e w a r d  o f a reward  definition  hints  information  information  however, t h a t  i s a  that  an  differently,  cue o r a  animal  deals  with  depending on whether  landmark.  In practice,  d i f f e r e n c e i s much more d i f f i c u l t  to discern.  I t may b e u n i m p o r t a n t w h e t h e r we l a b e l a n i t e m a s a l a n d m a r k or a reward cue and.in overlap  between  difficult work  short  b y D.  many c a s e s t h e r e w i l l  them.  Differentiating  of invasive  Sherry  (pers.  be  between  s u r g i c a l techniques,  comm.,  1992) w h i c h  landmarks r e g i s t e r i n areas o f t h e b r a i n used memory w h i l e memory of  cues a r e p r o c e s s e d i n s h o r t  storage  an animal's  although  used  considerable them i s such  suggests  as that  f o r long-term  t e r m memory.  This  d i f f e r e n c e makes s e n s e i f l a n d m a r k s a r e p a r t continuing f o r similar  map  of the world,  purposes  14  while  and o f t e n  cues,  permanent  General  features  o f the landscape,  Introduction  are a s s o c i a t e d w i t h  a transient  reward event. Cues Previous  studies  differentiated provide  s e v e r a l types  directional  reward.  of s p a t i a l  This  type  memory  and l e a r n i n g  of cue i n f o r m a t i o n .  information,  marking  o f cue i s common  have  Cues may  the  site  i n many  of  a  studies i n  which, f o r i n s t a n c e , a l i g h t comes on t o mark the h a l f o f a screen also light  that  contains  provide  et al. ,  (Suzuki  information  provides  quality,  food  about  the most  1980).  profitability.  basic  information  a t the same time marking  one s i d e  Cues may This  about  reward  as o f f e r i n g  p o s i t i v e reward and the other as o f f e r i n g no reward. experiments information site  have  1988),  and Menzel,  (Sherry,  1984).  The  the  to  provide  amount  and  quality  kind  detailed  a  nectar  1968; D r e i s i g ,  o r the type  of  more  information  of food  that  a  Other  items present  of  and C o l l i a s ,  1993),  at a source 1989;  present  could  be  by a cue i s h i g h l y f l e x i b l e and depends as much on  experimenter  as  on  whether the i n f o r m a t i o n of  the  1978; C o l l i a s  Greggers  provided  cues  such as the number of food  (Roberts,  (Bogdany,  used  same  course,  the nature  cues  themselves;  i s a c t u a l l y conveyed t o the animal,  depends on the animal.  which an animal  of  Almost  can be t r a i n e d t o d e t e c t  can be p r o v i d e d by a cue.  any  information  or d i f f e r e n t i a t e  T h i s i n c l u d e s d u r a t i o n o f reward 15  General  periods,  reward v a r i a b i l i t y ,  forms  of  information  Pepperberg, Gaffan,  Introduction  event sequences  (Colwill  1987; R e s c o r l a ,  and  a n d many o t h e r  Rescorla,  1986; R o b e r t s ,  1985;  1988; S e l f and  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 u s e t o n a v i g a t e through t h e i r environments.  Studies  o f landmark use suggest  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. d i s t i n g u i s h landmarks on t h e b a s i s o f s i z e , prefer  t o use large  1993).  Shape,  landmarks  the  accompanying  miss  distance  sets  t h e reward  1990).  effect  Cheng  Animals  also  and  their  ( B e n n e t t , 1993; Cheng e t  1992),  and t h i s  a landmark  information i s  causes  b y t h e same d i s t a n c e  animals t o  as t h e s h i f t i n  1986 a n d 1 9 8 8 ; T i n b e r g e n , 1 9 3 2 ;  1938; Vander  t h e landmarks  i n. learning  landmarks  Wall,  Angular d i r e c t i o n t o locations  Tengo e t al.,  landmarks  1991).  about  sites  Moving  (Cheng,  and Kruyt,  moving  similar  site  (Bennett,  information  by animals  Wall,  between  o f reward  location  Tinbergen  and  Vander  to navigation.  landmark  and used  C o l l e t e t al.,  1987b;  vital  1987a;  f o r example, and  f o r navigation  and o t h e r s i m i l a r  i s remembered  remember  al.,  colour  e t al.,  (Cheng  landmarks  They  used  o n assumed  1982; Warburton,  i s also  remembered  i n t r i a n g u l a t i o n may h a v e a  reward  location  (Cheng, 1 9 8 9 ;  1990) . and  as  others  have  navigational  suggested aids 16  by  that  animals  calculating  use  vectors  General  between This  the landmark  hypothesis  and the reward  does  animals use landmarks play  a  role  not account  (Cheng,  1988) .  f o r a l l the ways  et al.,  (Spetch  i n landmark  site  Introduction  that  1992), but may  navigation  where  still  landmarks  and  rewards a r e c l o s e l y a s s o c i a t e d and there are few confounding objects.  Role of Cues and Animals  i n Learning  La^HmaT-Trg  use landmark  and cue i n f o r m a t i o n  c o g n i t i v e maps of t h e i r surroundings, Tolman i n 1948. that  of  I n i t i a l sampling forays p r o v i d e  the animal  obtains  during  dead  learns  these  reckoning,  landmarks,  more  as f i r s t  to associate  forays. but as  flexible  with  to  develop  suggested by information  the rewards i t  E a r l y n a v i g a t i o n may c o n s i s t an  animal  learns  and e f f e c t i v e  to  identify  approaches  t o the  reward s i t e s become p o s s i b l e and as i t l e a r n s the cues  there  it  sites  can  ignore  altogether.  non-rewarding  Eventually,  or  i t may  less  rewarding  t i e together  information  about i n d i v i d u a l reward l o c a t i o n s i n t o p a t t e r n s t h a t r e q u i r e l e s s i n f o r m a t i o n storage and l e s s time t o l o c a t e and e x p l o i t repeatedly. spatial  This  information  process  of  about  their  chunking  or  environments  generalizing (cognitive  mapping) i s found i n a number of v e r t e b r a t e s p e c i e s and may be  found  Olton,  i n i n v e r t e b r a t e s as w e l l  1985; S h i f f r i n et al.,  1976).  17  (McNamara et al.,  1989;  General  Introduction  Outline o f Studies In  this  thesis  memory and i t s r o l e {Selasphorus  I examine  several  i n foraging  rufus).  aspects  using  These b i r d s  rufous  have  studies.  their  requirements  maintained second  s i z e and space without  advantage  metabolic  rate,  excessive i s that  and r e q u i r e  high  feeding  learning  abilities,  learning  experiments  rates,  space  allow  have  food  often.  compounded  in a  the short  them  t o be  requirements.  they  allows  advantages  One advantage i s that  an  This  their  completion  high  ensures  foraging  with  period  Their  extremely  they a r e h i g h l y motivated to l e a r n v a r i o u s Their  spatial  hummingbirds  several  f o r l e a r n i n g and b e h a v i o u r a l small  of  of  of time  that  tasks.  advanced complex and w i t h  r e l a t i v e l y short t r a i n i n g requirements. The  first  experience  s e t of experiments  i n spatial  pattern  examines  learning,  f u n c t i o n o f environmental i n s t a b i l i t y . experiments spatial different  I study  pattern kinds  how v i s i b l e  learning  cues  the r o l e  especially  of  as a  In my second s e t of and landmarks a f f e c t  and the r e l a t i v e  importance  of v i s u a l c h a r a c t e r i s t i c s t o l e a r n i n g .  of The  f i n a l s e t o f experiments examines the c o n t r a s t i n g e f f e c t s of s p a t i a l memory and s p a t i a l a s s o c i a t i o n memory.  18  Chapter 2  Pattern Learning and Persistence of Spatial Memory i n Rufous HnmrnHnqVi-i rriff  Section I.  Introduction  Learning Learning Estes  (1994)  alternate  aids  effective  described  courses  use of a v a i l a b l e  an i n d i v i d u a l as a c t i v e l y  of a c t i o n ,  generating  resources. sampling  expectations  and  s e l e c t i n g those most l i k e l y t o succeed. In the l a b o r a t o r y , many l e a r n i n g experiments have d e a l t with  simple  maze,  environments, i n which r a t s choose one arm o f a  o r pigeons  r e c e i v e a reward Colwill  tasks  a  (Bolhuis  and Dickinson,  1986a). that  .learn  pecking  et al.,  protocol  i n order  1987; Bond et al.,  1980; Spetch  et al.,  to  1981;  1992; W i l k i e ,  In these experiments i t i s o f t e n the case not o n l y  the environment required  i s simplified  of the animal  but t h a t  the l e a r n i n g  are straightforward.  This  approach s i m p l i f i e s  and c o n t r o l s the v a r i a b l e s p r e s e n t e d  the  in  study  animal  p a r t i c u l a r aspect  order  to  of l e a r n i n g .  19  better  understand  to  some  Pattern  In such  natural a  environments,  clean  characteristics change  with  weather.  and of a  however,  refuge of  1989).  Food  change c o l o u r , daily  basis  1985;  Wolf  conditions,  and  subsequent and  visits  may  such  change  a c t i v i t y and  1 9 7 1 a a n d 1971b;  a n d Waser,  1994; Lawrence,  such  as hummingbirds  be  1987; Gass  1991) .  Food  absent,  richer  1976; Weis,  unpredictably i n natural this  consequence  of  these  careful  extrapolating  i n their  available  results  but they  environments,  simple  studies t o t h ebehaviour of animals i n the w i l d Stoddard,  on  1983; Wunderle  researchers of  from  o r poorer  decision-making.  complexities,  on a  and Sutherland,  N o t o n l y do t h i n g s c h a n g e ,  a n i m a l s must t o l e r a t e  i n  as shape,  (Dawkins,  e t al.,  (Gass  M a r t i n e z , 1987) .  often  e t al.,  and Hainsworth, sources  The  shape and e n e r g e t i c p r o f i t a b i l i t y  (Armstrong  particular  affair.  day, l i g h t i n g  f o r nectarivores  size,  i s seldom  may  1 9 9 3 ; Dukas  sites  learning  environment  characteristics  and E l l n e r ,  Persistence  or foraging  l o c a t i o n v a r y i n almost a l l cases Dukas  and  straightforward  t h e time  Prey  Learning  and As a  must  be  laboratory (Beecher and  1990) .  Advantages of Learning In  many  situations  characteristics  of  i t benefits  their  animals  environments,  t h a t most a f f e c t  obvious  t h i n g s as t h e h a b i t s o f predators, s i t e s  locations  of food  fitness.  especially  factors  and  their  to learn the  (Krebs and D a v i e s ,  20  These i n c l u d e  1984) .  those such  of refuge, In stable  Pattern.  environments,  Learning  i n d i v i d u a l s of a given  and  species  Persistence  who  l e a r n are  more f i t (Benhamou, 1994; Valone, 1992) .  Disadvantages of Learning The energy  disadvantages spent  of  sampling  learning  the  Valone, 1992) and p r o c e s s i n g 1990;  M.  found  Brown,  that  learning)  environment information  1992; Brown  foraging  include  with  the  time  (Forkman,  1986) .  One  no  expectation  t o guide e x p l o r a t i o n was only 4 p e r cent  (Vander Wall,  study (i.e.  effective  1991) so the e x p l o r a t i o n r e q u i r e d f o r l e a r n i n g  i s expensive. remembering  1991;  (Blough and Blough,  and Cook, prior  and  Another disadvantage i s the e n e r g e t i c  cost of  et al. , 1986;  Miller,  (Bullock,  1993; C a p e l l i  1956).  Alternatives to learning Animals advantages. resource is a  presumably  Other f o r a g i n g  poor o r unstable  less prevalent. simpler  strategies rules (1983  use l e a r n i n g  strategy include  o f thumb and  hummingbirds  s t r a t e g i e s may  be p r e f e r r e d i n  environments, where t h i s advantage  S i m i l a r l y , l e a r n i n g need not be used i f will  produce s u c c e s s f u l  random  foraging,  t o govern  1991)  due t o i t s e n e r g e t i c  found  foraging  o r the use o f  behaviour. no  in  Wolf  evidence  resource  foraging.  of  Such simple  and Hainsworth memory  limited  use  by  environments.  Under c o n d i t i o n s of heavy competition,  random behaviour that  cannot  be  may  (Bryant  and Church, 1974).  predicted  by  competitors  be  Bees t a k i n g n e c t a r 21  advantageous from  flowers  Pattern  Learning  and  Persistence  o f t e n s t a r t at the bottom of the p l a n t and g i v e up when they encounter a poor blossom, foraging  pattern  C a r t a r , 1992) .  (Dreisig,  for a  host  1983) .  Such  rules  theorem,  environments including  for a  fixed  Pyke,  1978;  time  which  states  then  1980;  animals  maximize  the use of p r i o r (Bond,  that  their  knowledge Charnov,  Pyke  (Torymus give  of thumb are the b a s i s  i n ways that  advantageous  1989;  P a r a s i t i c wasp-like i n s e c t s  search  value  demonstrating a simple s y s t e m a t i c and capite) up  (Weis,  of the m a r g i n a l should use rates  of  their  return,  (learning) when i t i s  1976;  Krebs  and Davies,  1984) .  Complex environments Learning situations. only  learn  is  advantageous  In p e r f e c t l y once;  for  stable  however,  many  animals  environments  learning  in  many  animals  need  consolidated  over  p e r i o d of time tends to be l e s s f l e x i b l e than newly tasks to  (Gould, 1986c).  a  stable  In extreme  environment  can  a  learned  cases, long term exposure lead  to  canalization  or  automation of behaviour (Gass, 1985; Tierney, 1986) . Learning  can a l s o  unpredictable  be  a response to r a p i d l y  environments  unpredictability,  (Tierney,  changing,  1986).  Too  however, can negate the v a l u e of  much  learning  by r e d u c i n g the e f f e c t i v e n e s s of memories (Bowers and AdamsManson,  1993;  Nishimura,  1994).  Thus,  the  reliance  of  animals on l e a r n i n g and memory v a r i e s w i t h the c o m p l e x i t y of the environment  (Bond et al.,  1981; 22  Killeen  and  Fetterman,  Pattern  1988; that  Warburton,  1990),  animals p r e f e r  1975).  Learning  environments  and  there  complex,  seems  and  Persistence  i s experimental evidence  changing environments  to  be  (Gleitman,  surroundings are f a m i l i a r  Learning  enhanced  1963),  in  such  especially  to the animal  (Denny, complex if  (Biederman  the al.,  et  1973). D e s p i t e the importance of understanding the e f f e c t s predictability important  factor  Papaj, 1988), of  on  learning, has  partly  creating  been  Testing  of  et  patch q u a l i t y al..  1987;  unpredictability  some  Regelmann,  of  these  variance  1986)  i n the  level  of  the  theories  has  i n reward  and Lea, 1987;  1985).  Other  examined  reward  1988;  in  Dow  have been  this  difficulties  environments  levels  Kacelnik  factors  i n the  i n c l u d e p e r s i s t e n c e i n patches (Lima, 1983, to  study  (Eisenberger,  as v a r i a t i o n s  (Caraco, 1982;  that  to  of the p r a c t i c a l  variable  c o n c e n t r a t e d on such changes or  ability  limited  because  precisely  laboratory.  our  of  in  laboratory  1984), responses  (Stephens  and s c h e d u l i n g of r e t u r n s to cached food  and  Paton,  (Gill,  1988;  Sherry, 1985) .  Mathematical modelling Mathematical m o d e l l i n g has been developing environments 1974;  Fagan  theories  about  (Booth, 1986;  an  learning  in  Caraco and  and Young, 1978;  Laming  McNamara, 1982; McNamara and Houston, 23  important t o o l f o r complex,  Lima,  and  1987;  changing Colwell,  Scheiwiller,  1985b, 1987).  1985;  The use  Pattern  of  such models has allowed  tasks  that  Learning  researchers  are d i f f i c u l t  to d u p l i c a t e  and  Persistence  t o examine  complex  i n the l a b o r a t o r y  (Cahoon, 1984; Cain,  1985; Haefner and C r i s t ,  1994).  modelling  have  insight  exercises  provided  n a t u r a l l e a r n i n g processes  us  with  These into  that can be a p p l i e d 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 t e s t the f e a s i b i l i t y of our l e a r n i n g theories  (Devi  and  Sarma,  1986;  Faris  and M a i j e r ,  1988;  Fuchs and Haken, 1988a and 1988b; Haken, 1988; Hobbs, 1986; Park,  1985;  Selfridge  experimentally  and  Nesser,  i n t e r n a l processes  combination  tested  al.  (1987)  suggested  the  environment  by  has been t o examine  of l e a r n i n g and memory.  of modelling  and experimentation,  that a  animals  means  that  exponentially  weighted  moving  McNamara  Houston  (1985b)  and  or  (Stephens and Paton, 1986).  One use of mathematical m o d e l l i n g the  1960)  Kacelnik  store t h e i r can be  memory  Based on a  memories of  modelled  window.  suggested  that  as  or  overcome by l a r g e inputs  a  then memory can be  of new and v a r i e d  T h i s t h e o r e t i c a l e x p e c t a t i o n was c o r r o b o r a t e d by Nishimura The suggest  an  Similarly, weighted  moving memory window i s an accurate model of l e a r n i n g . memory window models are v a l i d ,  et  If  swamped  experience.  experimentally  (1994).  ideas  proposed  t h a t experience  in  these  memory  of an environment  (both  i n an environment and number of experiences) what and how much an animal  l e a r n s about  24  window time  models spent  contributes to  i t s surroundings.  Pattern  Retention since or  o f a memory,  then,  rewards were o b t a i n e d  intertrial  confirmed Capaldie  e t al.,  Mauldin,  1975) .  affect  This  depend  authors  (Capaldie  Increasing to learn  1953; L a v e r t y ,  Persistence  on b o t h  has  and M i l l e r ,  Hulse,  been 1988;  1978; K a m i l and  complexity  could  a n d remember  1994) s i n c e  time  and i n t e r v e n i n g  expectation  1987a a n d 1987b;  the a b i l i t y  McAlister,  should  and  (reinforcement)  experience.  by s e v e r a l  Learning  adversely  (Hochberg  i t provides  and more  t h i n g s t o remember, swamping a memory window.  Perception of the environment The under  a d a p t i v e s i g n i f i c a n c e o f l e a r n i n g has been examined  various  Denning, Dukas  but limited  1989; Draulans,  a n d Waser,  1980) .  conditions  (Damianopolous, 1989;  1 9 8 8 ; Dukas  and V i s s c h e r , 1994;  1994; G l e i t m a n ,  When s h o u l d  an animal  et  1963; Johannson  l e a r n about  al.  ,  i t s environment  a n d when s h o u l d i t f o r a g e r a n d o m l y o r b y some s i m p l e r u l e o f thumb?  I f t h e environment  learning  the locations of individual  energy Most  and f o r a g i n g time  food  storing  seasonal  experience changes relevant,  (Bond,  b i r d s who r e l y  r e l o c a t e food caches, in  i n their  are irrelevant are  often  food  predictable,  sources  1980; Vander  will  Wall,  save  1982).  o n l e a r n i n g a n d memory t o  f o r instance, a r e t e r r i t o r i a l and l i v e  environments change  i s sufficiently  (Roberts,  1979) .  environments  to their predictable  c o n s i s t e n t environments favour l e a r n i n g , 25  b u t many  foraging and  These  birds of the  and even  consistent.  when If  t h e q u e s t i o n c a n be  Pattern  refined  t o a s k how  l e a r n i n g about  Learning  consistent  and  environments  Persistence  must  them t o be a d v a n t a g e o u s .  Discussions considerations  of of  energetic  optimal  advantages  foraging,  often  which  1 9 7 6 ; McNamara a n d H o u s t o n ,  Tamm a n d G a s s , do  things  concepts 1985;  that  are not easily  e t al.,  optimize  efficient  1988; R o b e r t s ,  their  efforts  approaches which s t i l l  a  30 y e a r s now  1985a; R o b e r t s , 1991;  explained  maximization  to  been  I t i s apparent, however, t h a t  such as energy  Maier  always  1986).  lead  has  d o m i n a n t theme i n b e h a v i o u r a l s t u d i e s f o r a b o u t (Charnov,  be f o r  by  optimality  (Forkman,  1991; Gass,  1991).  but  animals  They  instead  do n o t  adopt  meet t h e i r n e e d s  less  (Stephens,  1981) . It  i s important  context  t o place behaviours  o f the animals' various  into  activities  the larger  when  examining  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 one  activity  other  with  activities  S m i t h , 1974) . is (Bond,  coupled  i t s associated (Getty  with  of their  rules  o f thumb  rates  begin  and i t s e f f e c t s  and P u l l i a m ,  1993; Lima,  on  1984;  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 information-processing  1980; Todd  knowledge  costs  from  and  Kacelnik,  environments  such  t o drop.  1993) .  Animals  are not l i m i t e d  as l e a v i n g  a patch  Learning i n these  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  hypotheses  making.  26  when  with  t o simple  food  intake  situations  allows  Pattern  Learning  and  Persistence  What i s optimal to do at any moment can depend on what an  animal  often  has  done  displays  learning intend  can be m o d i f i e d  to  explore  learning,  sources  is  survival.  a  selection  role  since  of  the  structure. of  ability  which  In  turn,  consistency.  predictability to  requirement  suggests  ability  maps of  to  in  for  I  spatial  return  to  many  the  to  honeybees  1988a  environment.  food  animals'  1988b;  et al.,  1990;  and Bitterman, study,  1973).  there  and  is  of  conditions,  strong  food  Spatial  the  sites  memory  has  ranging  from  et  al.,  1985;  et  al.,  1989;  Spetch and Edwards, 1986;  Woodard  to  and  that  learn patterns  i n many animals  Shettleworth  i n my  the  learning,  f o r the  studied  Garber,  spatial  by p e r c e p t i o n s  fundamental  of  spatial  goldfish  i t s environment,  The need to forage s u c c e s s f u l l y , coupled w i t h  advantages  been  l e a r n about  recognizable  pattern  and  to  humans Gould,  (Aadland 1987;  Jue  Rufous hummingbirds, the s p e c i e s used  can l e a r n s p a t i a l p a t t e r n s , as demonstrated  by  S u t h e r l a n d and Gass ( i n p r e s s ) . Experimental  protocols  Sutherland to  (1985) s t u d i e d the  l e a r n p a t t e r n s of rewarding  dimensional  array. a  He  feeders  over  reversed  the p a t t e r n ,  series  non-rewarding and of  a  learned  allowed  so  of  of  hummingbirds  feeders d i s t r i b u t e d  in a  two  b i r d s to l e a r n a p a t t e r n of  30  trials  and  that a l l rewarding  v i c e versa.  pattern  ability  Complete and  produced 27  a  then  suddenly  feeders  became  sudden r e v e r s a l  significant  drop  in  Pattern  performance chance). patterns cent  He  repeated  of feeders  feeder this  on  included either  "quarters" quarter  procedure  Persistence  dropped  with  four  different  each p r o v i d i n g  random feeder  below  a 50 p e r  visitation.  The  "halves" where the rewarding feeders  the l e f t  where  of  and  visitations  on the array,  chance of reward w i t h  patterns all  (successful  Learning  the  the  or r i g h t top  array  left  were  hand  side  quarter  rewarding  were  of the array,  and  bottom  right  (or  vice  versa),  "checkerboard" where the array c o n s i s t e d of e i g h t groups of four  rewarding  eight  groups  squares,  feeders of  four  the s t a r t  all  unrewarding  runs) .  From had  alternated  feeders  this  learned  feeders  were  in  located  presented  run remained the same f o r  study  he  concluded  the p a t t e r n  that  the  of rewarding  feeders  of experience  on the  expected the p a t t e r n to p e r s i s t . Current In  study  order  persistence  t o examine the e f f e c t  of behaviours  that  rely  on  spatial  memory  performed s i m i l a r experiments u s i n g the "quarters" but  with  arranged  (although the random p a t t e r n  of the experimental  hummingbirds and  i n squares  and "random" where rewarding  randomly on the a r r a y at  arranged  varying  the number of t r i a l s  I  pattern,  b i r d s were exposed t o the  p a t t e r n of feeders before a sudden and complete r e v e r s a l of the  pattern.  memory  o r the  s t r e n g t h of r e l i a n c e on i t develops with  experience,  i n the  sense  the  of  that  I f the s t r e n g t h  it  persists  of  longer 28  spatial  in  face  no  Pattern  reinforcement, drop  Learning  and  Persistence  then as the p r e - s w i t c h exposure i n c r e a s e s the  i n performance  after  the switch  magnitude o r d u r a t i o n .  29  should  increase i n  Pattern  Section I I .  Learning  and  Persistence  Materials and Methods  Subjects In  this  experiment (Selasphorus  hummingbirds, The  birds  I  were  used rufus):  captured  in  north  individual t o two  of  0.6  x  Maple 0.6  x  months p r i o r t o  m  were  at  Nektar  Plus  with  B.C.)  minerals  near  Rosewall  U.B.C.  research  maintained  ad  avian  in  for  one  photoperiod  periods,  the  hummingbird  libitum  avian  mineral  the  test  Roudybush  diet  (Avitron  (Avimin  females.  and  captivity  Excluding  either  hummingbird  vitamins  8  (10  2 i n the  w e e k e n d s , b i r d s w e r e p r o v i d e d w i t h 25% added  and  rufous  testing.  14L:10D.  supplied  adult  f i b r e g l a s s mesh c a g e s  Throughout the p e r i o d of maintained  field  and  Ridge, 1.0  naive, 4 males  the  C r e e k , V a n c o u v e r I s l a n d , B.C., forest  12  on sucrose  vitamin  birds  diet  or  weekdays.  On  solution with  supplement)  supplement).  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  was  At  a l l  and times  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 x  2.6  lights. uniform colour.  x  2.6m  high  Walls light A  and  with  overhead  ceiling,  full-spectrum  except the  g r e e n c o l o u r and  single,  e x p e r i m e n t s i n a room  the  stand-mounted,  30  feeder  f l o o r was 1.7  m  high  1.1  fluorescent  a r r a y , were a uniform perch  a  sand  was.  at  Pattern  the  c e n t r e of  the  room,  fitted  Learning  with  and  Persistence  a p h o t o c e l l to  signal  a r r i v a l s and departures to a computer m o n i t o r i n g the room. On metal  one  end  panel  into  this  spaced  w a l l of the  extended  panel  at 10.5  consisted  of  from  were  64  room a 1.0  just  below  feeders  in a  x  1.0  the  m dark  ceiling.  square  a  2.0  cm  length  of  1.67  mm  end.  I.D.  The  array-  Each  and  bent  resulting  tube resembled a small smoker's pipe, whose bowl was 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 The  stem of  the  feeder  drilled  f l u s h w i t h the f r o n t of the p a n e l . by an orange 19 mm  to  feeder an open  corolla.  photodarlington  panel and was  6 mm  hole  a  and  surrounded  4 mm  through  photodetector  was  a  extended  feeder  Intramedic  p o l y e t h y l e n e t u b i n g which had been flame heated form a t e r m i n a l r e s e r v o i r at one  Inset  8 x 8  cm v e r t i c a l l y and h o r i z o n t a l l y .  green  i n the  metal  array  Each h o l e  Avery l a b e l punched w i t h a  centre hole. A  computer  durations signals  f o r the  from  the  about 10 ms. with  2 ]il  trials  22%  normal  used  Carpenter  by  et al.,  the  and  each  photocells.  sucrose  dispenser  the  species  perch  arrivals,  Before each t r i a l  of  repeating within  recorded  array  range of rufous 1983; was  individual  Recording  was  and  visit  feeder,  using  accurate  I s u p p l i e d rewarding  solution  (Hamilton  departures,  (weight/weight)  PB-600-1).  n e c t a r volumes hummingbirds  Gass and covered  Roberts, by  31  a  feeders from  This  volume  found  in  (Armstrong, 1992).  beige  roller  to  a is  floral 1986; Between blind  Pattern  operated  from  outside  Learning  the experimental  and  Persistence  chamber  by a  pull  cord. Training E a c h b i r d was t r a i n e d to  testing.  For the f i r s t  f o r t h r e e days i m m e d i a t e l y two d a y s  birds  lived  c a g e s b u t w e r e f e d m a i n t e n a n c e f o o d ad libitum marked i d e n t i c a l l y t o those  the t r a i n i n g  feeders  experimental  chamber  blind) .  day o f t r a i n i n g ,  (the feeder  array  the  As t h e b i r d  height  i n t h e room was r a i s e d  became a c c u s t o m e d  was g r a d u a l l y d e c r e a s e d  centre  of  the feeder  was  directly fed with  moved  i n front  regularly.  from  Next,  After  i t s position  o f t h e covered  solution,  refilled, was  feeders.  minimal  levels  visiting of  positional  bias  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 32  the bird  t h e home c a g e  the panel,  was  the ceiling  covered,  to  again  provided  f e e d e r was  the bird  a n d a new t r a i n i n g t r i a l was b e g u n .  consistently  the height of  l o c a t i o n s were  The a r r a y was t h e n  perch  arrangement, t h e  near  r e m o v e d , a n d t h e a r r a y was u n c o v e r e d u n t i l several  this  the bird  array u n t i l  a l l 64 a r r a y  2 u l o f 22% sucrose  i n front of this  t o 1.7 m,  i n this  by t h e  to a height  to using  array.  accustomed t o t h e feeder and p e r c h feeder  b i r d s and  was c o v e r e d  o f 2.4 m a n d t h e f e e d e r was p l a c e d d i r e c t l y  its  chamber.  f r o m t h e i r home c a g e s w e r e moved t o t h e  The s o l e p e r c h  perch.  i n their  from a feeder  i n the experimental  On t h e m o r n i n g o f t h e t h i r d  prior  f e d from  the feeders Once t h e b i r d  and  showed  (based  on  no  or  informal  for specific portions  Pattern  of t h e feeder covering  a r r a y and i f necessary  areas  of the array  foraging outside of until caused  foraging  through  a  series  that  and  Persistence  enforced  by t e m p o r a r i l y  the bird  had n o t been  the blocking of preferred  t o become  more  o f 10-20 sham  l o c a t i o n s rewarding 5 minute  Learning  widespread) trials  feeders  i t was p u t  with  a l l feeder  t o accustom i t t o t h e 1 minute t r i a l and  intertrial  periods  t o be used  during  testing the  f o l l o w i n g day. E x p e r i m e n t a l Procedures On t h e d a y o f t e s t i n g of  t w o m i r r o r image q u a r t e r s  rewarding cases,  feeders,  feeders  (weight/weight)  m a k i n g 64 u l o f n e c t a r twice  bird  used  exposed  2 ]il  of rufous  bird  to  one  was  orientation.  pattern  with  of  of  o f the treatments  i t soriginal  In  pattern  both  22% sucrose  o f each  trial,  approximately under  The t r e a t m e n t a n d  by a  schedule  the pre-switch  I n each  and non-  hummingbirds  (Diamond e t a l . , 1 9 8 6 ) .  o n a n y d a y was d e t e r m i n e d  each  w i t h one  ( F i g . 1) .  contained  size  The o r d e r  trials.  randomly  a v a i l a b l e each t r i a l :  treatments.  presented  of rewarding  at the beginning  t h e p r e f e r r e d meal  normal c o n d i t i o n s  patterns  selected  rewarding  solution  its  e a c h b i r d was p r e s e n t e d  that  exposure  was r a n d o m i s e d , a s  treatment  a  f o ra fixed  Then t h e p a t t e r n was s u d d e n l y s w i t c h e d  bird  was  number o f (changed t o  m i r r o r image) b e t w e e n two t r i a l s , s o t h a t a l l p r e v i o u s l y  rewarding  array  l o c a t i o n s were  now n o n - r e w a r d i n g  33  and  vice  OOOOttft OOOOitii  oooottti ooooitti •••toooo ••••oooo ••••oooo ••••oooo  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 of one q u a r t e r s p a t t e r n f o r the feeder a r r a y (not to s c a l e ) . Each c i r c l e r e p r e s e n t s one feeder. Solid black circles represent rewarding feeders, and open c i r c l e s are empty feeder l o c a t i o n s .  34  Pattern  versa.  The  four  exposures of 10, The immediately lasted the  30 and 40 bird  preceding  one  perch  treatments  20,  subject  minute, at  any  time.  studies nectar this any  by  from the  reason,  of  pre-switch  fasted  test  for  period. stop  I ignored  15-2 0 Although  feeding any  minutes  and  trial  return  (Sutherland,  have  shown that  1985)  as  well  hummingbirds  as  revisits  to  as c o r r e c t v i s i t s . feeders  feeders  performance and  as  remove a l l  d u r i n g any  the  After  an  intertrial  visits  and  for  feeders to  ignored  determining  emptied and  flushed a l l feeders.  feeders  the feeder a r r a y  period  exposure p e r i o d , I covered  feeder  trial  feeders which the b i r d had  the i n i t i a l  reversed  visits  I covered  uncovered the a r r a y and began the next  rewarding  to  f o r a g i n g success.  rewarding  trial.  given  For  For a n a l y s i s of  I treated f i r s t  incorrect  At the end of each t r i a l refilled  pilot  subsequent v i s i t s  feeder d u r i n g a t r i a l as non-rewarding.  non-rewarding  the  feeders when a volume of 2ul i s used.  I t r e a t e d a l l second and  each t r i a l  to  i n which  r e s u l t s I t r e a t e d only the f i r s t v i s i t s to rewarding in  trials  the feeder p a n e l .  studies  myself  Persistence  trials.  was  the  and  consisted  birds could  s u b j e c t d i d not v i s i t Previous  Learning  and  carried  pattern.  At  out the  35  emptied d u r i n g  of  trial. the  5  minutes  At the end  feeder a r r a y  I then f i l l e d  of  the  I of and  the 32 newly  40 more t r i a l s end  and  with  this  experimental  Pattern  run,  t h e b i r d was r e t u r n e d  Learning  and  Persistence  t o i t s home c a g e a n d a l l f e e d e r s  were emptied and f l u s h e d .  36  Pattern  Section III.  Initial  Persistence  Results  i n a l l four treatments  (Fig.  2).  then  improved  Initially,  I  their  rapidly  a b o u t 20 t r i a l s .  day  (Fig. 3).  food  array  curves;  however,  feeding  rate  approximately  consumption  There  was n e a r  explained  rates  chance,  curves.  the applicability  that.birds  constant  f e d from  rate during the  i s considerable v a r i a b i l i t y  birds  (amount half  to test  and found  at a relatively  d i d not s i g n i f i c a n t l y of sucrose  consumed  o f the treatments  f e e d i n g r a t e s throughout poorly  performance  at similar  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  two p e r f o r m a n c e i n d i c a t o r s feeder  improved  These a r e d e c e l e r a t i n g monotonic  examined  the  by  t h e course  t h e number  c o n s i s t e n t p a t t e r n o f rewarding r^  and  Performance  Birds  of  Learning  i n these  change  every  (Table 1 ) .  trial)  in  Changes i n  o f t h e experiments  of t r i a l s  their  spent  were  with  a  f e e d e r s , a s shown b y t h e l o w  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 T r i a l s 2 F P 4.317 0.071 0.350 3 .585 0.075 0.166 9.688 0.004 0.257 7.969 0.008 0.173 r  Switch Switch Switch Switch  10 20 30 40  Post-switch T r i a l s 2 F P 3 .287 0.078 0.079 5.101 0.03 0 0.118 9 .832 0.003 0.205 0.014 0.907 0.000 r  All Trials F P 8.450 0.006 9 .244 0.004 2.253 0.138 8.920 0.004  r  2  0.150 0.138 0.036 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 o f 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 h e a s s u m p t i o n 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 . T r e a t m e n t names r e f e r t o t h e number o f t r i a l s before r e v e r s a l o f the p a t t e r n o f rewarding feeders. 37  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 per t r i a l that were c o r r e c t (rewarding) averaged over b l o c k s of 5 t r i a l s and a l l b i r d s i n each treatment f o r each of the 4 treatments. Curves i n the l e f t panel are performance b e f o r e the p a t t e r n r e v e r s a l and curves i n the r i g h t panel are performance a f t e r the r e v e r s a l . Blocks of 5 t r i a l s a f t e r the p a t t e r n r e v e r s a l are numbered from 1 t o s t a n d a r d i z e 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 b i r d s when the p a t t e r n was switched a f t e r 10 t r i a l s , the s o l i d b o l d l i n e r e p r e s e n t s b i r d s switched a f t e r 20 t r i a l s , the d o t t e d 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  F i g u r e 3. Number of c o r r e c t v i s i t s p e r t r i a l (averaged over 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 treatment) f o r each of the 4 treatments. Curves i n the l e f t panel are performance b e f o r e the p a t t e r n r e v e r s a l and curves i n the r i g h t p a n e l a r e performance a f t e r the r e v e r s a l . B l o c k s of 5 t r i a l s a f t e r the p a t t e r n r e v e r s a l a r e numbered from 1 t o s t a n d a r d i z e alignment of curves from each treatment. The solid light l i n e i s the performance of b i r d s when the p a t t e r n was switched a f t e r 10 t r i a l s , the s o l i d b o l d l i n e r e p r e s e n t s b i r d s switched a f t e r 20 t r i a l s , the d o t t e d 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 . 39  Pattern  Learning  and  Persistence  P r o p o r t i o n c o r r e c t i s t h e most w i d e l y u s e d i n d i c a t o r o f performance  (Fig. 2).  Since  t h e number o f c o r r e c t  s t a y e d r e l a t i v e l y constant throughout I was c o n c e r n e d of  the experimental  than  total  incorrect  (first)  As a consequence, I have p r e s e n t e d  there i sa difference.  The a v e r a g e s  to  i n each  the array  runs,  t h a t p r o p o r t i o n c o r r e c t may b e a w e a k e r  performance  trial.  visits  by b i r d s  visits  per  both values  when  of the incorrect  treatment  test  visits  are presented i n  F i g u r e 4. Birds initial  improved  i n performance d u r i n g t h e  l e a r n i n g p e r i o d i n a l l treatments Proportion F value 27 .799 8.356 92.064 8.393  Treatment Switch Switch Switch Switch  significantly  10 20 30 40  Correct probability 0.001 0.010 0.000 0.006  (Table 2 ) .  Incorrect F value 8.358 2 .108 54.303 37 .589  Visits probability 0.020 0 .164 0 .000 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 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 natural l o g of trial ( t o improve linearity of regressions). Values f o r both performance i n d i c a t o r s are given. T r e a t m e n t names r e f e r t o t h e number o f t r i a l s before the reversal of the p a t t e r n of rewarding feeders. P r o b a b i l i t i e s a r e t h e c h a n c e o f no d i f f e r e n c e .  Duration of Exposure and Pattern Reversals • Performance immediately reversed. the  after  treatments  the quarters  pattern  dropped of  immediately  immediately  after  before (Table  40  the switch 3).  sharply  feeders  P e r f o r m a n c e was s t r o n g l y s i g n i f i c a n t l y  5 trials  trials  for a l l 4  was  better i n  than  i n the 5  As w e l l ,  birds i n  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 of the 4 exposure treatments. Curves i n the l e f t p a n e l are performance b e f o r e the p a t t e r n r e v e r s a l and curves i n the r i g h t p a n e l are performance a f t e r the r e v e r s a l . B l o c k s of 5 t r i a l s a f t e r the p a t t e r n r e v e r s a l are numbered from 1 t o s t a n d a r d i z e alignment of curves from each treatment. The solid light l i n e i s the performance of b i r d s when the p a t t e r n was switched a f t e r 10 t r i a l s , the s o l i d b o l d l i n e r e p r e s e n t s b i r d s switched a f t e r 20 t r i a l s , the d o t t e d 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  treatments w i t h g r e a t e r numbers of t r i a l s (30 and 40 t r i a l to  Treatment Switch 10 Switch 20 Switch 30 Switch 40  Persistence  b e f o r e the s w i t c h  treatments) r e q u i r e d more v i s i t s  o b t a i n the amount  which remained  and  of n e c t a r  they  required  per t r i a l (Table  4) ,  r e l a t i v e l y constant (Table 5 ) . probability 0 .000 0.001 . 0 .000 0.000  t value 5.022 4.102 7 .160 6.208  Table 3. Comparison of performance b e f o r e and a f t e r the switch. F i g u r e s are based on the average p r o p o r t i o n c o r r e c t f o r a l l b i r d s i n each treatment f o r the 5 t r i a l s immediately b e f o r e and the 5 t r i a l s immediately a f t e r the r e v e r s a l . Treatment names r e f e r t o the number of t r i a l s b e f o r e the r e v e r s a l of the p a t t e r n o f rewarding feeders. P r o b a b i l i t i e s are the chance of no d i f f e r e n c e . Treatment Switch 10 Switch 2 0 Switch 3 0 Switch 40  probability 0.203 0 .118 0.023 0.037  t value -1.522 1.989 3 .595 3.066  T a b l e 4. Comparison of t o t a l v i s i t s b e f o r e and a f t e r the switch. F i g u r e s are based on the average number of v i s i t s p e r t r i a l f o r a l l b i r d s i n each treatment f o r the 5 t r i a l s b e f o r e and the 5 t r i a l s a f t e r the r e v e r s a l . Treatment names r e f e r t o the number of t r i a l s b e f o r e 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 d i f f e r e n c e . Treatment Switch 10 Switch 20 Switch 30 Switch 40  probability 0 .005 0.099 0.096 1.000  t value -5.573 -2.173 -2.166 0.000  Table 5. Comparison of 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 the s w i t c h . F i g u r e s are based on the average number of c o r r e c t v i s i t s per t r i a l f o r a l l b i r d s i n each treatment f o r the 5 t r i a l s immediately p r e c e d i n g the p a t t e r n r e v e r s a l and the 5 t r i a l s immediately f o l l o w i n g the r e v e r s a l . Treatment names r e f e r t o the number of t r i a l s b e f o r e the r e v e r s a l of the p a t t e r n of rewarding feeders. P r o b a b i l i t i e s are the chance of no d i f f e r e n c e . 42  Pattern  Performance trials  until  improved  switch.  strongly  significant  measure,  showing  trials  over  i t was a t o r n e a r  pattern  new p a t t e r n s  again  Learning  Improvement  the next  the level following  i n a l l cases using  that  birds  o f rewarding  and  just  during  five  toten  before the  the switch  either  i n a l l treatments  feeders  Persistence  was  performance learned the  t h e 40 p o s t - s w i t c h  (Table 6 ) . Incorrect F value 56.698 13.530 38.850 57.516  Treatment S w i t c h 10 Switch 2 0 Switch 3 0 S w i t c h 40  Visits probability 0.000 • 0.001 0.000 0.000  Proportion F value 55.550 30.744 53.234 66.127  Correct probability 0 .000 0.000 0.000 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 o f i m p r o v e m e n t i n p o s t - s w i t c h p e r f o r m a n c e 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 performance o f a l l b i r d s i n a treatment. T r e a t m e n t 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 o f t h e p a t t e r n o f rewarding feeders. As  predicted,  the  intensity  and  duration  of the  p e r f o r m a n c e d r o p was r e l a t e d t o t h e d u r a t i o n o f e x p o s u r e t o the p a t t e r n before  the switch  ( F i g . 5 ) . Drop i n p e r f o r m a n c e  after  increased  i n magnitude  the switch  exposure fitted  increased  (positively  to the 5 t r i a l  F = 42.280, excluding  r = 0.811,  t h e zero  averages  sloped of total  as  linear  regression  visits:  r e s i d u a l d f = 22, p = 0.000).  point,  analysis  t h e r e l a t i o n s h i p between  excluding  43  the  of  regression  incorrect  performance and exposure i s s t r o n g l y s i g n i f i c a n t sloped  duration  Even bird  (positively zero  point:  F i g u r e 5. Average number of i n c o r r e c t v i s i t s p e r t r i a l byb i r d s f o r each o f the treatments i n the 5 t r i a l s immediately f o l l o w i n g the p a t t e r n r e v e r s a l (the maximum i n c o r r e c t v i s i t s p o s s i b l e i s 32) . The X a x i s shows the number o f t r i a l s b i r d s experienced b e f o r e the switch. The l i n e passes through the average performance f o r each treatment. I n d i v i d u a l p o i n t s show the r e s u l t s f o r each b i r d (3 p e r treatment, and 12 f o r the zero p o i n t ) . The b e g i n n i n g of each experimental run exposes b i r d s to a novel p a t t e r n w i t h no previous exposure t o a s i m i l a r p a t t e r n , so i t i s e q u i v a l e n t t o a s w i t c h a f t e r a zero t r i a l exposure t o the p a t t e r n , p r o v i d i n g the f i f t h p o i n t . I n s e t s show sample performances f o r b i r d s i n i n d i v i d u a l treatments (shaded c i r c l e s surround these v a l u e s ) . 44  Pattern  F =23.914,  Learning  and  Persistence  r = 0.840, r e s i d u a l df = 10, p = 0.001).  While  the r e l a t i o n s h i p does not appear l i n e a r , a n o n - l i n e a r  f i t to  this  line  will  be  underestimates  even  the  strength  positive  relationship  rewarding  behaviour  not  l i n e a r , but  below 20 trials,  but  The  and  of  of  since  this  between  sigmoid;  trials  stronger,  a  straight  relationship.  persistence  previous  rewarding  of  experience  and  experience  little  i n c r e a s e d markedly between 20 and  greater  drop  i n performance by  This  formerly  persistence increased l i t t l e  initial  line  was  i f any  beyond  30  30 trials.  birds with  longer  exposures to the p a t t e r n produced a range of e r r o r s between treatments greatest  that  was  between  initially  the  and  T h i s d i f f e r e n c e i n response by (measured  by  t o any  remaining treatment  typically pre-switch  following  the  switch  the b i r d s . t o  incorrect v i s i t s )  decreases d u r i n g the 40 p o s t - s w i t c h due  was  trial  (Fig.  reversal  immediately  40  in  pattern  period  trial  and  treatments 6).  the  10  large  the  gradually  t r i a l s until differences  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. Visitation  Patterns  Several results out  potential  sources  of  s i m i l a r to those I found.  error First,  could  produce  I needed to  the p o s s i b i l i t y of unplanned cues to rewarding  rule  feeders.  There c o u l d c o n c e i v a b l y be v i s u a l t r a c e s of n e c t a r , marks on the such  array  or  any  cues were  of  a number of  a v a i l a b l e and  other  birds 45  possibilities.  knew how  to  use  If them,  20  D i f  0  1  0  1  1  1  10  20  30  1  40  Trials after switch  Figure 6. Differences i n number o f i n c o r r e c t visits ( e r r o r s ) by b i r d s i n each of the treatments i n t h e p e r i o d following the pattern r e v e r s a l . The l i n e r e p r e s e n t s t h e maximum range of d i f f e r e n c e s i n the number.of e r r o r s between the 4 treatments. This range i s g r e a t e s t immediately f o l l o w i n g t h e switch, and decreases throughout the course of the remaining t r i a l s . 46  Pattern  they  should  correct)  visit  on  the  statistically  more rewarding  first  trial,  but  and  feeders  than  the  from random v i s i t a t i o n  mean d i f f e r e n c e = 0.066, p <= for  Learning  Persistence  chance  (50%  b i r d s d i d not  differ  (t = 1.494, df  =  0.163), p r o v i d i n g no  11,  evidence  i n i t i a l use of e x t e r n a l cues. P o s i t i o n a l biases  visitation were  not  nature  patterns a major  of  protocol.  enough to a f f e c t  concern  the  presentation  of  the  ensured  b i a s e s would s t i l l non-rewarding Birds  due  quarters  These two  pattern),  (which i n some p r o t o c o l s c o u l d  two  to  performance measures)  the  diagonally  pattern  and  versions  of  birds  with  encounter equal  the  the  f a c t o r s (randomisation  that  symmetric randomised  pattern and  horizontal  a  significantly  or  vertical  numbers of rewarding  show some p o s i t i o n a l preferred  feeders  bias higher  ( F i g . 7) . . in  distribution:  Maximum  d i f f e r e n c e = 0.391,  There  vertical  and  as  uniformity: of  visits  both well  (Fig.  (K-S  versus  towards  the  test  biases  of  versus  visits  a  room  uniform  p = 0.000).  horizontal  horizontal p = 0.001).  higher  8), although  in Figure  and  They  in  visit  vertical  Maximum d i f f e r e n c e =0.59, p = 0.004, K-S  d i f f e r e n c e = 0.63, biased  my  symmetric  (Kolmogorov-Smirnov t e s t of observed v i s i t s versus  patterns  in  feeders.  did  were  alter  feeders  uniformity: Birds  during  were the  test  Maximum most  first  10  heavily trials  t h i s b i a s d i d decrease over time as  7.  47  seen  F i g u r e 7. T o t a l of a l l v i s i t s to each feeder ( a l l b i r d s on a l l treatments, b e f o r e and a f t e r s w i t c h ) . I f no p o s i t i o n a l b i a s o c c u r r e d 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 s u r f a c e . This figure was produced u s i n g a step-smoothing a l g o r i t h m . As a r e s u l t , each feeder l o c a t i o n i s represented by 16 g r i d u n i t s . 48  F i g u r e 8. T o t a l 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 b i r d s on a l l treatments) . I f no p o s i t i o n a l b i a s o c c u r r e d 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 s u r f a c e . This figure was produced u s i n g a step-smoothing a l g o r i t h m . As a r e s u l t , each feeder l o c a t i o n i s represented by 16 g r i d u n i t s . 49  Pattern  While  birds  explorations predictable ordered. after  (Fig.  of the a r r a y  and  positional bias, (on the f i r s t  Persistence  their  trial)  initial were not  ( F i g . 9), and d i d not appear t o be s y s t e m a t i c Birds  their  systematic  exhibited  Learning  began t o explore  initial and  visits,  consistent  but  a l l areas they  visitation  10) .  50  of the  showed patterns  no  or  array  obvious  over  time  oo  ooooo ooooo ooo oooo o$oo oooo o ooooo (fcooo o o o o ®ooo oooo oooo oooo oooooooo o^aooooo o<$d® o o o o 0(S^f-4oOOO  ooeooooo oooooooo oooooooo oooooooo ooo oooo oooo ooooo oooooo oooooooo oooooooo oooooooo  <$>o® o o o o o  oooooooo 0-e-fe.O\O^e)o  o o o otefo o o oooooooo oooooooo oooo oooo  0,0 0 0 0 0 0 0  oooooooo oooooooo oooooooo oooooooo oooooooo ooooo ooooo oooooooo ooooo oooooooo oooooooo oooooooo oooooooo  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 of 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 o f T r i a l 1. Each box r e p r e s e n t s the feeder a r r a y and i l l u s t r a t e s a d i f f e r e n t b i r d . In a l l cases shown, the top r i g h t and bottom l e f t q u a r t e r s o f the a r r a y were rewarding. The s o l i d l i n e marking each a r r a y shows the visitation sequence d u r i n g the t r i a l . The arrow head r e p r e s e n t s t h e d i r e c t i o n o f t r a v e l and b l a c k dots r e p r e s e n t feeders v i s i t e d d u r i n g the t r i a l .  0(p(^® o o o o 0Jb olht) o o o  oooooooo oooooooo oooooooo oooooooo 2 oooooooo oooooooo ooooooi® oooooooo ooooooo* oooooooo OOOOOOOf) oooooooo 00(^)0000  o o o V eo o o oooooooo o o o <s> o o o 3 o o ooo o 00000(^0  O^t^OOO O^ffOOOO 00^0000  4oo oo oo oo oo oo oo oo oooooooo oooooooo oooooooo  o o o o ®-® ^ oooooooo oooooooo oooooooo  OOOOOOM  5  oooooooo oooooooo  6  oooooooo oooooooo  Of^OOOOO MOOOOOO 0-4)0000 0 0 GOOOOOOO  6^ o o o o o o  oooooooo oooooooo oooooooo  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 the f i r s t 10 v i s i t s o f T r i a l s 1 - 6. Each box r e p r e s e n t s t h e feeder a r r a y and i l l u s t r a t e s a d i f f e r e n t t r i a l . The t o p l e f t and bottom r i g h t q u a r t e r s o f the a r r a y were rewarding.' T r i a l numbers a r e t o the l e f t o f each box. The s o l i d l i n e marking each a r r a y shows the v i s i t a t i o n sequence d u r i n g t h e t r i a l . The arrow head represents the d i r e c t i o n o f t r a v e l and b l a c k dots r e p r e s e n t feeders v i s i t e d d u r i n g the t r i a l . 52  Pattern  Section IV.  The in  a  birds  very  success  i n this  short  after  learning  reward  learned  consistently  ten trials.  performance suggests that patterns  r e s u l t s of Sutherland  and  Persistence  Discussion  experiment  time,  about  Learning  a simple  achieving  Their  i n a novel right  pattern over  rapidly  improving  environment they  away,  80%  begin  corroborating  the  (1985).  Advantages of Learning Modelling times  studies  f o r hidden  performance  indicate learning  objects  (Benhamou,  to at least  1994).  Since  can reduce  one t h i r d  the rewarding  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 energy  spent  on f o r a g i n g .  learning  i s an e f f i c i e n t  through  increased  provides  more  reduced  efficient  and food  Bunnell,  experience  foraging  i s located  a  naive  feeders  environment,  to foraging.  in  of  a means t o r e d u c e  In a predictable approach  search  stable  Learning environment  because  search  time i s  more  rapidly  (Gillingham and  that  global  1989) .  Factors A f f e c t i n g Learning Cues Past  studies  have  beyond  those  presented  source  of information  shown  intentionally f o r foraging 53  and d i s t a l  c a n be an animals  cues  important  (Olton, 1990;  Pattern  Spetch  and  Luijtelaar  Edwards, et al.,  1988;  1989).  b i r d s used such things nectar  to i n i t i a l l y  towards array or  high  Learning  Suzuki  and  al.  et  There was  no  Persistence  ,  1980;  evidence here  as odours or small v i s i b l e  l o c a t e rewarding feeders,  feeders  indicates  that  cues  but  gravity)  play  some  role  in  uncued,  the  that  traces their  outside  of  bias  of  (such as the arrangement of c e i l i n g and w a l l s ,  even  van  the  echoes,  their  spatial  explorations. Since feeders  profitability  on  position  the  i n the  learning. specific and  combined  room, should  Using  distal  with  have played  cues  to  1988).  In my  arrangement  distal  experiment,  cues  of  such  as  a primary r o l e i n  locate  l o c a l cues i s harder than u s i n g  Edwards,  cued  array,  was  rewards  local feeder  (by a surrounding orange ring) but not  without  cues  (Spetch  position  was  feeder q u a l i t y .  Search Techniques In error flight  learning  feeder  exploration  quality,  during  initial  t r a j e c t o r i e s ( F i g s . 8 and  e x p l o r a t i o n was systematic  not  search  the  random, but  birds  used  trials. 10)  feeding  that  initial  suggest  series  and  Early  I c o u l d f i n d no  (stereotyped  trial  of  evidence f o r visits  with  p r e d i c t a b l e r u l e s about d i r e c t i o n , number of v i s i t s or  other  characteristics  In  study  on  Hainsworth, restricted  of  the  visit)  hummingbird 1991), search;  to t h e i r  foraging  in  hummingbirds that  is,  they 54  explorations.  the  used  wild random  showed  no  (Wolf but  a  and area  predictable  Pattern sequence  o f movements y e t s t i l l  located  the e n t i r e p a t c h .  rewarding  and  Persistence  remained w i t h i n a r e s t r i c t e d  a r e a of a p a t c h on a g i v e n bout throughout  Learning  rather  than moving  In my experiments,  feeders they  tended  freely  once b i r d s  to return  t o those  l o c a t i o n s w i t h i n and between bouts and sample areas those s i t e s .  When these searches were not rewarding,  might  s e a r c h nearby  areas  t o see i f more  might  be  Trial  and  better.  restricted badgers  tactics  s e a r c h has a l s o  error  been  (Mellgren and Roper,  (Menzel,  around  combined  seen  1983).  area  such  1986) and Japanese  Systematic  places  with  i n species  1991) and i n models s i m u l a t i n g (Ollason,  distant  birds  as  monkeys  efficient  foraging  s e a r c h p a t t e r n s have  a l s o been seen, e s p e c i a l l y i n i n s e c t s such as bumblebees and honeybees search  (Dreisig,  techniques  1989; Menzel, are t i e d  s p e c i e s and t o the s i t u a t i o n  1985).  I t appears  t o the unique  needs  of  that each  (Root and K a r e i v a , 1984) .  Some times my b i r d s q u i c k l y found one rewarding q u a r t e r of  the a r r a y  one.  but were extremely  I selected  intertrial  slow  to locate  p e r i o d s and reward  the other amounts so  b i r d s c o u l d e a s i l y maintain t h e i r weight throughout t h e day, that  may  longer  reduced  intertrial  decreasing forced  have  their  periods  the amount  motivation  (e.g. Sutherland,  or quality  greater exploration  t o feed.  o f rewards  of the array,  Using  1985) could  or have  but I chose  to  minimize r i s k t o the animals, s i n c e I was a l r e a d y concerned about t h e i r o v e r a l l h e a l t h .  55  Pattern  Learning  and  Persistence  Stability Learning  is  most  (Nishimura,  1994).  Nutcrackers  have  characteristics l e a r n and  Caching  Balda  food,  can  and  Kamil,  as  Clark's  retain  time.  similar  These b i r d s  Animals  have b e t t e r  memory  abilities  and  abilities  species  periods,  the  the  sources  in  to  stable  biases  them  during  feeding  not  in  remember  least  4  to  bouts.  of  cache weeks  do  a  broad  the  to  dealing  continual  Thus,  renewal of  they  al.,  appear  locations  in  the  et  tasks  items.  individual  When  As  must d e a l w i t h  food  of  unpredictable  remember  months  remember  (Bond  1993).  similar  stored  days  to  also  environments  l e a r n and  change  over  (Balda,  consequence  value  c o n t i n u a l d e p l e t i o n and  nectar  who  for species  s t a b l e items than animals who  caching  at  a  Adams-Manson,  animals  unpredictable  for  are  of resources discount  (Bowers  Chickadees,  can  1990).  learning  generalization,  1992).  cache  normal d i s t r i b u t i o n  and  of  environments  such  that  f o r long p e r i o d s  retain  Spatial  with  stable  birds  surroundings  (Hitchcock and Sherry,  resources  in  remember food caches f o r at l e a s t 6 months  1980;  1981) .  effective  while  for  long  hummingbird  same l o c a t i o n  flower show  qualities  evidence  of  f o r a g i n g memory w i t h i n bouts i n a patch they u s u a l l y e x h i b i t win-shift locations seen  in  behaviour, (Cole other  et  al.,  avoiding. 1982).  nectariv'orous  previously Similar results  species  56  such  as  successful have  been  bananaquits  Pattern (Wunderle nectar  and Martinez,  feeding  learning  animals  abilities  Learning  1987) . have  but that  This  does  inferior they  and  Persistence  not mean  spatial  learn  that  memory o r  and remember  items  that a r e l i a b l e t o remain s t a b l e such as c h a r a c t e r i s t i c s o f rewarding  f l o w e r types.  Their  evident at coarser s p a t i a l the q u a l i t y Cole  spatial  scales,  memories  as they c l e a r l y  o f patches o f flowers (Armstrong  et al., 1982; Gass  are also  and Sutherland,  et al.,  1992;  1987;  1985; M i t c h e l l ,  1989; Valone, 1992), and whole f o r a g i n g h a b i t a t s 19?.; Gass, 1978b; Sutherland et a l . ,  remember  (Armstrong,  Tamm, 1987).  Costs o f L e a r n i n g Sampling Once the b i r d s l e a r n e d the g e n e r a l p a t t e r n o f rewarding feeders, but  t h e number o f i n c o r r e c t  continuing  choices sampling  were  amount.  probably  While errors,  o f t h e environment  d e t e c t changes (Draulans,  visits most  1987; W i l k i e et al.,  by the b i r d  incorrect  probably  ongoing  i n an attempt t o  as seen i n o t h e r animals  1985; Kramer and Weary,  1981).  t o a small  o f these  some were  i n reward l o c a t i o n ,  1988; Gass,  dropped  1991; Tamm,  Sampling and mistakes cannot be  d i s t i n g u i s h e d i n most p r o t o c o l s , i n c l u d i n g mine. Sampling its  i s a way f o r an animal t o c o n t i n u e e x p l o r i n g  environment  novel  items  surroundings  and t e s t  f o r change,  by r a t s  t o improve  (Pinel  et al. , 1986);  i n c r e a s e s greatly>  their  as ' i n e x p l o r a t i o n o f knowledge  however,  of t h e i r  i f uncertainty  animals e x p l o r e l e s s and spend more time 57  Pattern  exploiting  known  a d d i t i o n a l ones  resources  (Forkman,  Learning  instead  and  of  Persistence  searching  for  1991).  Change Learning  c a n be a d i s a d v a n t a g e  changes i n an animal's surroundings, complete  reversal  Performance reversal the  dropped  first  few t r i a l s  birds  instead  explore  experiment. after the  i t dropped below chance f o r  the switch  t o forage  what  (typically  3 - 5  that  they  directly  had learned  changing  their  reflected before  constant, i n ways  the switch  reflecting  that  1984),  provide  the  behaviour t o  W h i l e t h e number o f c o r r e c t  (Tooze a n d Gass, before  a cost  of immediately  relatively  tendencies  trials  with  t h e new p a t t e r n .  remained  intakes  after  incurred  persistence  switch  this  During t h i s short p e r i o d o f poor performance a f t e r  switch,  their  in  and s i g n i f i c a n t l y  pattern;  o f major  such as t h e sudden and  the pattern  strongly  o f t h e feeder  trials). the  of  i n t h e face  visits  hummingbirds' constant  energy  b i r d s who e x p e r i e n c e d  r e q u i r e d more v i s i t s  more  per t r i a l to  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 . Before reduced  the switch,  foraging  stability. the  pattern  incur  effort  during  I n an extremely of  unpredictably, to  l e a r n i n g was a d v a n t a g e o u s b e c a u s e i t  variable  profitability  r e l i a n c e on s p a t i a l  costs  environments  the period  with  and h i g h l y  each  change.  environment changed  Both  pattern i n which  often  l e a r n i n g would  v a r i a b l e environments  58  of  and  continue  resource  poor  c a n overcome  Pattern  the  value  of  persistence costs and  learning  i n the face  was s e e n  Learning  (Nishimura, o f change w i t h  Persistence  1994) .  Similar  similar  associated  i n r u f o u s hummingbirds by S u t h e r l a n d  i n Anna's hummingbirds by C o l l i a s  drop  and  i n performance  seen i n g o l d f i s h  and i n c r e a s e  (Warburton,  and C o l l i a s  (1985)  (1968).  A  i n e x p l o r a t i o n was a l s o  1990) a n d c h i p m u n k s  (Kramer a n d  Weary, 1991) . E x p e c t a t i o n s and P e r s i s t e n c e As  experience  performance Animals and  with  following  use past  1983).  t h e r e was n o r e a s o n  bouts. to  learned that  reversal  increased,  dropped  t o gauge f u t u r e r e t u r n s Until  t o discount  t h e unexpected  their  and reduce  however,  hummingbirds weight as  design,  my  their  result  past  experience  foraging  h a d n o way  persistence with strongly  experience  in  reversed  the value of  the birds  their  more. (Bowers  t h e p a t t e r n was  for the birds  my e x p e r i m e n t a l  behaviours;  heavily  pattern  s p a t i a l memory o f t h e p a t t e r n t o g u i d e  Given  expect  stable  the pattern  experience  Adams-Manson,  using their  the  stable  suggests  increasingly environments  increases. Animals most  a c t as i f t h e i r  important  (Haccou Kacelnik,  f o r t h e purposes  e t al., 1993),  1991; Haefner  intervening  experience  of guiding and C r i s t ,  and d i s c o u n t  f u n c t i o n o f t h e time of  most r e c e n t  less  future  i s the choices  1994; Todd a n d  recent  events  as  a  s i n c e t h e y w e r e l e a r n e d a n d t h e number  experiences  (McHose  59  and  Peters,  1975;  Pattern  et  McNamara into  al.,  1989).  These  t h e memory window m o d e l s  authors  (Kacelnik  1985b),  but  preference (MacPhail,  et  al.,  from  were  Shettleworth,  1994; G a f f a n ,  incorporated  acquired  early  effect,  most  sets of Houston,  effect, i n  training  recently  (Crystal  and  1994; K e s n e r e t  1994; W r i g h t ,  1994).  Other  m o d e l s 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 since  learning  memory  guided  behaviours  W i l k i e a n d Kennedy, 1 9 8 7 ; W i l k i e e t al.,  1990;  The (Fig. to  affects  sigmoid  shape o f t h e curve  exhibit  persistence  profitability trials  o f rewarding  feeders.  of  changes  Over  begun  i n the  t h e next  thirty  maximum c h a n g e i n b i r d 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  may c o r r e s p o n d treated  t o a d u r a t i o n o f exposure a t which t h e b i r d s  the learned patterns  T h i s p o i n t may c o r r e s p o n d window f o r t h i s  patterns  because  as i f they  roughly  they  longer could  had always e x i s t e d .  t o t h e s i z e o f t h e memory  kind of learning task  interpretation,  consistent effect  experiment  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  this  1990).  b i r d s had already  i n the face  time  (Spetch,  seen i n t h i s  5) i m p l i e s t h a t b y t e n t r i a l s ,  a  a preference f o r  1992; G a f f a n ,  1 9 8 5 ; Reed,  and  t h e primacy  and t h e recency  acquired  1994; O l t o n ,  concepts  Persistence  suggested by s e v e r a l  f o r information  information  al.,  and  1 9 8 7 ; McNamara  are distinct  1982),  Learning  f o r these  durations  not produce  had exceeded  memory w i n d o w s o f t h e a n i m a l s .  a  In  exposure  to  larger  the size  Further,  60  of  birds.  surprise  of the working  the i n i t i a l  level  Pattern  Learning  and  Persistence  p o r t i o n of the curve would correspond to a p e r i o d when, f o r the  animals,  new  and  had  the  of  rewarding  not been f u l l y l e a r n e d .  persistence represent  patterns  near  the  inflection  feeders  The  point  were  still  rapidly increasing of  the  curve  a p e r i o d of r a p i d l y i n c r e a s i n g e x p e c t a t i o n s  may about  s t a b i l i t y of the p a t t e r n . This past and  general  experience,  strategy strong but  of  rapidly learning  w i l l be  and  i f i t realizes  that  before  i t i s c e r t a i n of  predictability  of  food  the  sources.  familiar  s i t u a t i o n when i t experiences  behaviours, Generally, to  be  success;  or behavioural  flexible, are  of  i s , the inertia,  behaviours based on  more  experiences  that  while  less flexible  stereotyping i t s  i t s environment  strength  response)  which  of  an  persistence  of  he  believed  term experiences  consolidated (Gould,  between  61  tend  memories  1986c).  increased  reinforcement.  learned  makes e c o l o g i c a l sense.  short  association  in a  minor v a r i a t i o n s i n  Hull  a p p l i e d a s i m i l a r p r i n c i p l e when he d e s c r i b e d h a b i t (the  new,  Alternatively, i t i s  to abandon i t s p e r c e p t i o n  foraging  animal i n a  l o c a t i o n , abundance,  unlikely  its  An  i t s situation is  u n l i k e l y to r i s k wasting energy by  foraging  on  responses makes  sense f o r animals i n a n a t u r a l environment. situation,  rely  ephemeral r e s i s t a n c e to change,  more r a p i d abandonment of newly l e a r n e d  novel  to  (1943)  strength  stimulus  with  and  and  increasing  Pattern  Learning  and  Persistence  T h e s e 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 w i n d o w hypothesis. less  In a variable  likely  change, with  t o remain  habitat,  valid  a n d we know t h a t  information  1990) .  In  reliance  a  information i s  due t o o n g o i n g  t h e temporal and s p a t i a l  (Warburton,  older  environmental  on s p a t i a l  memory  varies  complexity of t h e environment  complex  environment,  c a n o v e r l o a d memory c a p a c i t y  too  much  ( 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  and  Bransfield,  Orians,  1983; G i l l  (George, of  1987; Ewald  by i n t r u d e r  1979),  (Gass  myriad  of  other  (Ewald  e t a l . , 1976),  and  new n e c t a r p r o d u c t i o n  1 9 8 0 ) , m a t u r a t i o n o f new f l o w e r s  o l d blooms  birds  and C a r p e n t e r , 1978; Ewald  and Wolf,  of whole patches of flowers a  raids  and d e t e r i o r a t i o n  changes  i n the quality  (Gass a n d S u t h e r l a n d , 1 9 8 5 ) , o r  items.  Given  a  limited  ability  to  remember p a s t e v e n t s , more r e c e n t i t e m s s h o u l d a l s o b e g i v e n h i g h e r w e i g h t i n g t o r e d u c e t h e i m p a c t o f memory f a d i n g t i m e , w h i c h i s a common p r o b l e m can  lead  al.,  to increasing  errors  over  ( A r o n s o h n e t al., 1978) t h a t i n spatial  tasks  1987; S p e t c h , 1990; S t r i j k s t r a and B o l h u i s ,  (Bolhuis et 1987).  R e l e a r n i n g A f t e r a Change The pattern foraging which  reduction reversal  in  foraging  eventually  behaviour, v i s i t i n g  they  had been  success  induced  l e d to the birds previously  avoiding.  This  time, o c c u r r i n g over f i v e t o t e n t r i a l s 62  changing  unrewarding change  by  took  the their  feeders a  short  ( o r 30 t o 60 m i n u t e s  Pattern  of  actual  visit  time) .  the  feeders  feeder  and  feeders,  exploration  ten  none of  period,  visited  of  the  this  one  after  them  array  pattern,  above 80%  the  and  or  two  immediately  for  changes  switch,  eventually  Persistence  some b i r d s  or fed r e p e a t e d l y  non-rewarding feeders.  trials  feeder  array,  then gave up,  but  formerly  During  Learning  did  formerly  began  intensive  in profitability  birds  returning  good  at non-rewarding  Over the course of the  not  learned  of  five the  to performance  to new  levels  correct.  Conclusions These that  experiments  hummingbirds  (Sutherland,  have  learn  1985).  corroborated  2-dimensional  More  importantly,  p e r s i s t e n c e of l e a r n e d p a t t e r n s as a f u n c t i o n of experience This  persistence  under  the  learning  patterns  quickly  they  pressure  spite  demonstrate  i n the face of sudden change  of s t a b i l i t y b e f o r e  of  severely  the  change.  (in this  reduced  case  foraging  the b i r d s soon l e a r n the a l t e r e d reward  Hummingbirds seem disposed in  findings  d i s s i p a t e s r a p i d l y , however  p r o f i t a b i l i t y ) , and pattern.  earlier  of  or  perhaps  imposed by u n p r e d i c t a b i l i t y .  63  to a s t r a t e g y o f r a p i d  because  of  the  problems  Chapter 3  Landmark Forms and Spatial Memory i n Rufous Hummingbirds.  Section I. Introduction  Spatial Memory Spatial  memory i s the process by which animals remember  l o c a t i o n s i n t h e i r environment. memory  i s used  defending  f o r tasks  territories  Among b i r d s p e c i e s ,  such as n a v i g a t i n g ,  (Balda  and  Montgomerie, 1981; Shettleworth, Spatial ecological  memory advantages using  greater  than  a five-fold  random  search  systematic  and  searching  spatial  a  1991).  memory  energy  three  1988;  distinct  (Valone,  that  f o r a g i n g and Gass  and  1983).  affords  suggest  Kamil,  spatial  energetic Modelling  t o forage  advantage  to  five-fold  (Armstrong  et  al.,  over  can  and  studies provide  completely  advantage  over  1987; Benhamou,  1994) .  Cues and Landmarks One  component of developing  a map of the environment i s  to l e a r n the p o s i t i o n s of r e c o g n i z a b l e landmarks and cues t o  64  Landmark  Forms  a s s o c i a t e items i n t h e environment w i t h expected r e s u l t s . will  define  indicator  a reward  o f reward that  space and time (hereinafter  termed  many  overlap  unclear; site.  cases  areas  i s difficult  generally  groups  features  will  be  considerable because t h e  locations only  may  be  one p o t e n t i a l  t h e s e ways o f r e l a t i n g t o t h e  not only  o r a cue.  i n practice,  a  F o r my p u r p o s e s ,  because  given  I  will  the features  I intended  not i n d i v i d u a l  contain  but i n  to label  to describe  arrays,  of feeders,  do, however,  considered  sites.  may c o n t a i n  u s e t h e term landmark  i n my e x p e r i m e n t a l  delimit  a i d that  I t may b e u n i m p o r t a n t w h e t h e r  as a landmark  reward i n  as a n a v i g a t i o n a l  and s p e c i f i c  an area  as an  landmark  there  D i f f e r e n t i a t i n g between  object  that  t h e s e two a i d s t o l o c a t i n g f o o d ,  f o r example  principle.  with  "cue")  and a reward  c o n t a i n i n g reward  between  environment  used  "landmark")  foraging  between  difference  i s associated  ( a n d i n a 1:1 r a t i o ) ,  i n d i c a t e s an area In  cue ( h e r e i n a f t e r termed  I  them t o  feeders.  information  that  o f cues.  Distal  I  These  could  be  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 separated  b y some v a r i a b l e  distance  from  (Brown,  1 9 9 4 ; Brown a n d G a s s , 1 9 9 3 ; S c h e n k ,  e t al.,  1987).  and  Edwards,  (Brown  and Gass,  t h e reward  c o n t i g u o u s cues  1993; P i n e l  e t al., 65  adjoin  site  1987; S u t h e r l a n d  L o c a l cues a r e near t h e reward s i t e  1988),  cues a r e  (Spetch  t h e reward  site  1986), and g l o b a l  cues  Landmark h a v e a more t e n u o u s 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 (Spetch  and  distal call  E d w a r d s , 1988).  cues)  include  landmarks.  setting  Global  many  Examples  items of  i n c l u d e p o s i t i o n s of  cues  that  global  (and  reward  site  i n some c a s e s  other cues  Forms  authors  in  a  would  laboratory  the w a l l s , overhead  lights  and  doors.  Landmarks I use  have d e f i n e d  to  locate  reward). these  patches tree  reward  This  aids. as  I defined centre  navigational aids  (food  is  only  suggests at l e a s t  landmarks  landmarks. by  i n the  In  middle  nature,  nectar-producing  item.  surrounding  A  second type  A stream at the a  vegetable  of  one  two  berry  of  ways t o  use  both  be  bushes, i n the  landmark d e f i n e s  could  foraging  could  edge o f a t e r r i t o r y  garden  animals kind  of  this  s t a l k of a f l o w e r i n g p l a n t , or a rock  of a t e r r i t o r y . o f an  as  sites  definition  surrounded  central  landmarks  the  middle  the  or a  serve  a  edge fence  as  edge  landmarks.  Role of Cues and Animals cognitive  Landmarks i n Learning  use  maps  landmark of  their  t h i s r e q u i r e s the use spatial species  learning  tasks  information  is  not  universal;  The  levels.  there 66  is  1948),  are  Various  a  develop  ability  there  i n c l u d i n g primates,  which  to  (Tolman,  o f s p a t i a l memory.  animals, in  cue  surroundings  differences in s k i l l  suggested that learning  and  use  distinct  studies  have  spatial  to  and  have  difficulty separation  Landmark between reward hummingbirds,  sites  and reward  however,  cues  regularly  (Pinel  Forms  et a i . , 1986);  use landmarks  and cues t o  n a v i g a t e towards reward s i t e s that a r e s e p a r a t e d from reward cues, and t h i s behaviour can be d u p l i c a t e d environment  (Brown and Gass,  i n a laboratory  1993).  C u r r e n t Study The a b i l i t y has  been  (G.  Brown,  1968; et  of hummingbirds t o use s p a t i a l  demonstrated 1992; Cole  and f i e l d  experiments  et al. , 1982; C o l l i a s  and C o l l i a s ,  Gass, 1978a and 1978b; Gass and Sutherland, 1985; Gass  al., 1976; M i l l e r  Thompson, 1994) . of  i n laboratory  information  spatial  and Gass,  One recent  memory  use by  suggested p o s s i b l e  failure  (Wolf and Hainsworth, this  experiment  study f a i l e d  foraging  authors  In  1985; M i l l e r  et a l . , 1984;  to f i n d  hummingbirds,  m e t h o d o l o g i c a l reasons  I examine how  rufous  information  types  of  f o r the  hummingbirds  i n a s p a t i a l memory t a s k .  expect b i r d s t o l e a r n f a s t e r w i t h edge landmarks Both  but the  1991).  use edge and c e n t r e landmarks  landmarks.  evidence  landmark  to f i n d p r o f i t a b l e  provide  feeders,  I  than c e n t r e navigational  but edge  landmarks  a l s o d e l i m i t groups of rewarding feeders and can be used f o r t r i a n g u l a t i o n due t o the shape of the l i n e s  I use f o r edge  landmarks. Of  special  these landmarks sources  interest  i s the i n f o r m a t i o n  provided  that h e l p s animals t o l o c a t e p o t e n t i a l  and assess  their  quality. 67  In some  by food  treatments I  Landmark  provide  cues  to profitability  t h e s e cues t o f u r t h e r speed Chapter use  of  changes.  memory  that  are  profitability  profitability profitability  of  more  Here  and  t o environmental  I again suddenly  distributions  of  feeders  to  change probe  I n one t r e a t m e n t I move c u e s t o f e e d e r  simultaneously  with  the  change  i n  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 .  expect b i r d s  recover  learning  By c h a n g i n g t h e e n v i r o n m e n t , we c a n e s t i m a t e t h e  l e a r n i n g a n d memory.  I  hummingbird  sensitive  d e g r e e o f r e l i a n c e o n memory. the  and expect  learning.  2 demonstrated  spatial  i n t h e landmarks  Forms  t o be l e s s  rapidly  from  surprised this  reversals.  68  by t h i s  reversal  than  treatment and from  uncued  Landmark  Forms  Section I I . Materials and Methods  Subjects In  this  hummingbirds, the in  Rosewall May  1991  experiment  I  (Selasphorus  rufus)  Creek  used  6  adult,  captured  salmon h a t c h e r y ,  and maintained  i n individual  time  they  were  used  i n other  rufous  i n the f i e l d  Vancouver 0.6  w i r e mesh c a g e s f o r s e v e r a l months p r i o r which  female  Island, x 0.6  B.C.  x 0.6  to testing,  learning  near  m  during  experiments.  Due t o p o o r 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 of  the treatment  b i r d s t o seven  sequence,  bringing  the t o t a l  on a  schedule  that  under  conditions i n the wild.  birds  were  or Nektar  supplied with  Excluding  P l u s hummingbird d i e t  avian  avian mineral  vitamin  the photoperiod  mimicked  either  w e e k e n d s , t h e y h a d 25% s u c r o s e (Avitron  of  ( a l l female).  Throughout t h e p e r i o d o f c a p t i v i t y maintained  number  seasonal test  variation  periods, the  Roudybush hummingbird a d libitum  on weekdays.  s o l u t i o n w i t h added  supplement)  and  was  minerals  diet On  vitamins (Avimin  supplement).  Experimental Environment I  conducted  a l l training  and experiments  i n two rooms,  e a c h 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 spectrum f l u o r e s c e n t l i g h t s .  Walls  69  and c e i l i n g ,  except  fullthe  Landmark feeder floor 1.7  array, was  m  Each and  a  were  a  uniform  high  perch  perch  was  uniform  sand  was  light  colour.  A  l o c a t e d at  fitted  with  a  green  colour  single,  the  and  of  each  signal  room.  arrivals  departures. On  metal  one  end  panel  into  this  spaced  at  extended  10.5 of  polyethylene form a  w a l l of  panel  consisted  from  were cm  a  e a c h room a 1.0  64  just  below  feeders  in  vertically  2.0  cm  and  length  t u b i n g w h i c h had  terminal reservoir  x  1.0  the  a  m  dark  ceiling.  square  1.67  been  a t one  mm  flame  end.  array  Each  I.D.  feeder  Intramedic  heated  The  Inset  8 x 8  horizontally. of  green,  and  bent  resulting  t u b e r e s e m b l e d a s m a l l smoker's p i p e , whose b o w l was nectar The  reservoir  stem  of  and  the  whose stem s e r v e d  feeder  extended  photodetector  which b r i d g e d  array panel.  The  of  the  stand-mounted,  centre  p h o t o c e l l to  Forms  the  Avery  panel.  t i p of the  Each h o l e  which  and  recorded  feeder  arrivals,  accurate  t o about  rewarding  feeder  a  Hamilton  array  10  2  hole  centre  ul  of  PB-600-1 r e p e a t i n g  photodarlington  by  an  used  by  rufous  metal  the  front  orange  19  mm  hole. led  and  to  a  visit  sucrose  computer  durations,  I supplied  each  (weight/weight)  dispenser.  hummingbirds  70  corolla.  i n the  This  i s w i t h i n t h e normal range of n e c t a r volumes found species  open  a  each t r i a l 22%  an  floral  flush with  photocells  Before  feeder  a  drilled  surrounded  departures,  ms.  with  through  f e e d e r was  l a b e l p u n c h e d w i t h a 6 mm Perch  from  was  a 4mm  as  to  in  (Armstrong  volume floral 1986;  Landmark Carpenter  et  al.,  rewarding  feeders  1983; were  left  showed t h a t b i r d s b e h a v e d filled  w i t h water  trials  the  operated  was  and  as  a  1992).  Non-  previous  study  t h e same i f f e e d e r s and Gass,  covered  outside  Roberts,  empty,  (Sutherland  array  from  Gass  by  a  w e r e empty o r  i n press). beige  the experimental  Forms  Between  roller  chamber  blind  by  a  pull  cord. In control to  s e v e r a l cases,  videocamera,  c a b l e s were a l s o p r e s e n t  videotape  about  an 8 mm  the session  and  i t stripod  and  i n t h e chamber t o a l l o w  obtain  anecdotal  me  information  performance.  E x p e r i m e n t a l Design Treatments were d e s i g n e d and  centre  evaluate these  landmarks  about  utility  differently  disks  the energetic  i n rewarding  of l i n e s  combined  throughout  edge a n d c e n t r e  examined profitable  that the  provided effects  of  information moving  feeders.  71  (edge  and  groups  to  coloured of the  the array. but  landmarks  Two  provided  Finally,  about  of  landmarks)  sectors  landmarks  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 t w o . treatment  of  were e i t h e r  and non-rewarding colour  learning  quality  ( c e n t r e s ) , and t h e y  o r were a u n i f o r m  treatments  pattern  o f edge  of providing information i n  Landmarks were p a t t e r n s  coloured  array  i n spatial  the additional  feeders. or  landmarks  t o compare t h e u t i l i t y  i n one  quality, along  I with  o o o o  o o o o  ooo o 00 oo 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 0o oo o o #  o o o o  o o o o  o o oo o o o o #  #  #  o o o o  o oo oooo oo oo ooo o  o o o o o  o o o oo o o o o o o oo o o o  o o o oo o oo o oo oo o o o  o o o o  #  o o o o  #  oooo  o o o o  #  O OO 0 o oo 0 O OO 0  o o o o  o o oo o o oo 0o o o o o o 0  o o o oo o o o o o o oo o o o o oo o o oo o o o o oo o o o oooo oooo o ooo oooo  0o o o o o 00 0o 0o 00o o oooo oo oo o oo o o o oo  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 of the a r r a y markers used f o r the e i g h t treatments d e s c r i b e d i n the t e x t (not t o scale). In each diagram the u n f i l l e d c i r c l e s r e p r e s e n t feeder l o c a t i o n s marked by orange l a b e l s . Top l e f t : Plain 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 c e n t r e landmarks.  72  Landmark The b a s i c  forms  representations  f o r these  treatments  i n Figure  11.  below t o represent of  the results  experiment were over s i x t y 1.  in 2.  The  i n t h e graphs  eight  ( i n expected order  listed  and t a b l e s  treatments  for this  of i n c r e a s i n g performance  trials):  Plain. only  a r e shown i n s t y l i z e d  I use t h e acronyms  the treatments  section.  Forms  A p l a i n array  with  t h e orange  a l l treatments  P l a i n Centres the  centre  All  four  i n which a l l feeders feeder  (top l e f t  stickers  were  present  diagram i n F i g . 1 1 ) .  A 1 inch c i r c u l a r Avery l a b e l i n  (Plctr).  o f each o f t h e four labels  that  were marked  were  quadrants  t h e same  colour  of the array. ( F i g . 11,  top  right). 3.  4.  Coloured  Centres  (Clctr).  Same a s P l c t r ,  in  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  in  non-rewarding sectors  Plain  Lines  surrounding  Lines sectors  s q u a r e s w e r e o f one c o l o u r 5.  Coloured sectors  Lines  (Cline).  were marked w i t h  rewarding sectors  colour  than  those  drafting  tape  (Fig. 11, top r i g h t ) .  (Pline). the four  but the labels  of  6  mm  of the array.  ( F i g . 11, bottom Same a s P l i n e a different  ( F i g . 11, bottom  73  A l l four left).  but rewarding  colour  left).  than non-  Landmark 6.  Plain  Centres  one  colour surrounding  two  c o l o u r s marking rewarding 11,  (Fig. 7.  Lines with Coloured  bottom  Coloured one  Lines  colour  in  the  (Plcct).  with  Plain  each  Centres  quarter  with  squares  quarters  ( F i g . 11,  right).  bottom  Switch  (Clnsw).  squares marking the rewarding 11,  (Fig.  bottom  profitability  quarters  of  and  left).  feeders,  and  Labels  of  associated with  different  Differently  coloured  non-rewarding  quarters  When I also  rewarding  of  non-rewarding  I  reversed  reversed  the  p a t t e r n so t h a t t h e c o l o u r e d s q u a r e s t h a t h a d been  of  (Clpct).  rewarding  Line  labels  right).  differentiating  Coloured  of  non-rewarding  colours  8.  Squares  four sectors, with and  Forms  feeders  the  landmark  previously  maintained  this  association. Global  other  room  p a r a p h e r n a l i a c a n n o t be  e l i m i n a t e d from the experiment,  even  in  and  to  a control them,  landmarks  situation,  they  will  measures  of  constant  across  in  my  cancel  always  performance.  walls,  to the add  extent  some  Since  floor  and  that birds  underlying  these  features  treatments  attend  noise  to  remained  (differences  rooms s h o u l d h a v e b e e n c a n c e l l e d o u t  o f room u s e  analysis,  as  a l l experimental  between e x p e r i m e n t a l randomisation  such  assuming  across that  treatments),  any  out. 74  systematic  I ignored effects  by  them would  Landmark In  each  treatment  pattern continued switched  the original  f o r 50 t r i a l s ,  reward  and  rewarding  and  v i c e versa.  the  pattern  the  persistence with  landmark  t h e n t h e r e w a r d p a t t e r n was  t o i t s m i r r o r image f o r 10 more t r i a l s  previously  Forms  so t h a t a l l  a r r a y l o c a t i o n s w e r e now n o n - r e w a r d i n g  The t e n t r i a l p e r i o d a f t e r  o f rewarding  feeders  which  the reversal of  indicates differences i n  birds  used  previously  learned  k n o w l e d g e a n d 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 eight  i n t h e experiment  treatments.  The  randomized f o r each b i r d post-switch  patterns,  landmark c o l o u r s  was e x p o s e d t o e a c h o f t h e  order  of  these  treatments  was  a s was t h e a r r a n g e m e n t o f p r e - a n d  the experimental  room  used,  and t h e  seen.  Training E a c h b i r d was t r a i n e d to  testing.  but  For the f i r s t  was f e d ad libitum  volume  feeder  experimental  f o r t h r e e days i m m e d i a t e l y  two d a y s a b i r d l i v e d i n i t s c a g e  from a standard  marked  identically  moved  commercial u n l i m i t e d to  t o an  experimental  chamber  with  (the e x p e r i m e n t a l  covered  The s o l e  directly this  by t h e b l i n d ) . to a  height  i n front  perch  in  day o f t r a i n i n g ,  f e e d e r f r o m i t s home c a g e  raised  those  the  chambers.  On t h e m o r n i n g o f t h e t h i r d was  prior  o f 2.4  of this  normally,  m  the  i n t h e room  When t h e b i r d  gradually 75  training  f e e d e r a r r a y was  and t h e f e e d e r  perch.  i t was  perch  the bird  lowered  was was  was  placed using  t o 1.7  m,  level the  with  bird  the centre  was u s i n g  of the covered  both  feeder  Landmark  Forms  feeding array.  When  and perch,  the f e e d e r  moved d i r e c t l y  i n f r o n t of the centre of the covered  Once  was again  the b i r d  feeding  2 u l of 22% sucrose  the  removed,  home  cage  uncovered u n t i l  the b i r d had f e d from s e v e r a l f e e d e r s .  The  array  covered,  trial  the feeders  was begun.  and  solution, was  training  was  array  the array  was then  feeder  array.  r e g u l a r l y , a l l 64  l o c a t i o n s were p r o v i d e d with  was  refilled,  Once the b i r d  and a new  was c o n s i s t e n t l y  v i s i t i n g the panel, and showed minimal o r no p o s i t i o n a l b i a s (based for  on i n f o r m a l  estimation  of any u n t r a i n e d  preference  s p e c i f i c p o r t i o n s of the feeder a r r a y and i f necessary-  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 areas of the a r r a y t h a t the 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 h e b l o c k i n g o f p r e f e r r e d feeders caused f o r a g i n g t o become more widespread) it  was put through a s e r i e s  of 10-20 sham t r i a l s  with a l l  feeder l o c a t i o n s p r o f i t a b l e i n order t o accustom i t t o the 1 minute  trial  and 5 minute  intertrial  periods  t o be  used  d u r i n g t e s t i n g the f o l l o w i n g day. Experimental On of and of  Procedures  the day of 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  two randomly s e l e c t e d m i r r o r image p a t t e r n s o f rewarding non-rewarding feeders the s e t s  (Figure  11) .  portions  of  of markings In  each  the a r r a y  (Figure 1 i n Chapter 1) w i t h one described case, were  i n Experimental  feeders filled 76  i n the with  2 pi  Design  rewarding of  22%  Landmark (weight/weight) trial. taken  sucrose  solution  at  This provided a potential i n each t r i a l  and  the  beginning  Forms  of  each  f o r 64 \il o f n e c t a r t o  be  exceeded the p r e f e r r e d meal s i z e  of  r u f o u s h u m m i n g b i r d s u n d e r n o r m a l c o n d i t i o n s (Diamond e t 1986)  to minimize  s t r e s s to the  L i m e g r e e n and treatments; In  both  treatments  light  randomly assigned. associated was  with  assigned Each  trials  landmarks were used  one  When b o t h  rewarding  colour,  five  to  p e r c h a t any  as  run  f o r the  consisted intertrial  the  birds  experimental  to  run.  time.  of  first  sixty  maintain Although  minutes, I  was  the  one  50  trials  one  minute  t o see  t h e a r r a y and  the  during first  the  any  their  trials  was  weight were  one  return to  the  feeder  o f f e r e d the  only  a r r a y m a r k i n g s as  well  Emptied rewarding  intertrial  trial,  This  period, the  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  refilled  preceding  panel.  blue  periods.  During the i n t e r t r i a l  the only opportunity to feed.  were  or  c o l o u r s were p r e s e n t ,  sectors  minute  allow  the  opportunity  green  green  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  a r r a y was  for a l l  randomly.  with  throughout  blue  only  experimental  intended  birds.  c o n t r a s t e d w e l l w i t h the dark  using  al.,  period.  t h e s u b j e c t was  feeders  Immediately  fasted for  15-20  i n which the s u b j e c t d i d not  visit  or 2 t o 3 normal meals. i g n o r e d any  trial  the f e e d e r p a n e l , imposed the normal i n t e r t r i a l continued  as b e f o r e .  Previous  s t u d i e s by  77  interval  Sutherland  and  (1985)  Landmark and from  myself the  have shown t h a t hummingbirds feeders  reason,  I  when a volume of  treated  a l l second  feeders d u r i n g t r i a l s At  the  end  of  2ul  and  remove a l l n e c t a r i s used.  subsequent  For  one  to  halted  the  as non-rewarding. fifty  trials,  I temporarily  f i l l e d a l l p r e v i o u s l y non-rewarding f e e d e r s . treatment  Treatment 8 the with  lines  rewarding but  left  array  markings  so  that  feeders was  i n the  the still  opposite  p e r i o d of the p r e v i o u s  colour  unchanged.  formerly  50 t r i a l s .  of  the  Once I had  In  I changed associated  associated with  quarters  feeders  In a l l but  (the c o l o u r e d l i n e switch treatment),  landmark  feeders  I  this  visits  experiment, emptied, f l u s h e d and d r i e d a l l rewarding and  Forms  rewarding  array  to  the  completed  the  a p p r o p r i a t e changes I r e s t a r t e d the experiment; t h i s u s u a l l y took 5 to 10 minutes. A f t e r these trials  using  trials. home  changes, I continued  the  same  A f t e r the  cage,  flushed  last  procedures trial,  f o r an a d d i t i o n a l ten  as  in  I returned  a l l feeders,  markings.  78  and  the the  removed  first bird the  fifty to i t s array  Section I I I .  Landmark  Forms  of c o r r e c t  first  Results  Performance Indicators I measured l e a r n i n g by visits  in  each  feeders  and  by  trial the  the p r o p o r t i o n  out  total  of  the  incorrect f i r s t  In Chapter 2 I emphasized that stronger  indicator  satiate  themselves  however,  birds  than  not  maintain  their  weight  increased  their  feeding  the  course  treatments  of  the  always  (total  t h i s was  visits  correct In  obtain  throughout  visits  to to  filled feeders.  i n c o r r e c t v i s i t s was  trials.  when b i r d s  this  sixty  runs  six  can  food  trials.  first  in  a  experiment,  sufficient  correct  experimental  ( F i g . 12);  e i g h t treatments  total  proportion  during  could  total  Birds  visits) out  to  of  over eight  s i g n i f i c a n t f o r four  of  the  (see Table 7 f o r summary s t a t i s t i c s ) .  I n i t i a l Learning As as  i n Chapter 2,  decelerating  differences (initial rates  curves  between treatments  were not  indicator  monotonic  slope) and  l e a r n i n g by  l e a r n i n g proceeded f o r a l l treatments (Figs.  l i e i n the  i n peak performance.  constant,  13  I tested  the  and  rate  the  natural  log  79  of  The  of  learning  Since the  learning  s i g n i f i c a n c e of  l i n e a r r e g r e s s i o n of the a p p r o p r i a t e on  14).  the  the  performance  trial  number.  24  18 CO "CO  >  •4—•  o ©  12  i_  o O  -PLINE ••• P L C T R • P L C C T — PLAIN -C L P C T — C L N S W —C U N E •- C L C T R  0  J  3  4  6  Blocks of 10 Trials 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 per t r i a l (averaged a c r o s s a l l b i r d s i n each treatment and across b l o c k s of 10 t r i a l s ) f o r a l l treatments. The X a x i s i s d i v i d e d i n t o b l o c k s of 10 trials. The p a t t e r n was r e v e r s e d a f t e r b l o c k 5 ( t r i a l 50). Acronyms i n the legend correspond to the d e s c r i p t i o n s of treatments i n Methods. Pline = plain lines. Plctr = plain centres. 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 . Plain = p l a i n array. 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 . Clnsw = c o l o u r e d l i n e markers switched a f t e r the p a t t e r n reversal. C l i n e = coloured lines. Clctr = coloured centres. 80  Trial  Trial  F i g u r e 13. Number of i n c o r r e c t f i r s t v i s i t s per t r i a l averaged f o r a l l b i r d s i n each of the 8 treatments. Two treatments a r e shown i n each p a n e l . Acronyms f o r treatments are 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 switched a f t e r the 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 . Cline = coloured lines. 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 . Pline = plain lines. C l c t r = coloured centres. Plctr = plain centres. P l a i n = p l a i n array. 81  00  1  0  1  1  10  L  20  -—  1  30  1  40  1  50  o.o  60  0-10  20  Trial  30 40 Trial  50  60  50  60  CLNSW CLPCT 10  20  30  40  50  60  0  10  20  30  40  Trial  Trial  F i g u r e 14. 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 to rewarding feeders, averaged f o r a l l b i r d s i n each o f t h e 8 treatments. Two treatments a r e shown i n each p a n e l . Acronyms f o r treatments a r e f u l l y d e s c r i b e d i n t h e methods section. Clnsw = c o l o u r e d l i n e markers switched a f t e r the pattern reversal. 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 . Cline = coloured 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 centres. Pline = plain lines. 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  Probability 0.000 0.000 0.043 0.000 0.652 0.664 0 .758 0.493  F value 17 .899 35.107 4.302 102.399 0.206 0 .190 0.096 0.476  Treatment 1. P l a i n 2. P l c t r 3. C l c t r 4. P l i n e 5. P l c c t 6. C l i n e 7. C l p c t 8. Clnsw  Y intercept 12.142 11.387 15.699 6.52 18.422 18.452 20.853 18.612  Forms  Slope 0.072 0.076 0.044 0 .174 0.000 0.01 -0.007 0.014  Table 7. Linear regressions (since the r e l a t i o n s h i p i s assumed t o be l i n e a r and f l a t ) of t o t a l c o r r e c t f i r s t visits on t r i a l number f o r the f i r s t 50 trials. Acronyms f o r treatments are 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 switched 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 centres. C l i n e = coloured l i n e s . Plcct = plain l i n e s and c o l o u r e d c e n t r e s . Pline = plain l i n e s . Clctr = coloured centres. P l c t r = p l a i n centres. Plain = p l a i n array. Improvement i n performance was s t r o n g l y s i g n i f i c a n t 8  treatments  trials.  using  proportion  correct  Measuring performance by t o t a l  f o r the f i r s t  improvement f o r b i r d s i n 7 out o f 8  with  i n the p l a i n  insignificant  improvement  line  50  incorrect indicated  significant birds  for a l l  treatment  treatments,  showing  the lone  (Tables 8 and 9 ) .  D i f f e r e n c e s Between Treatments Birds  learned  the p a t t e r n s  treatments  ( F i g . 13 and 14) ;  proportion  correct  measures  using  was s t r o n g l y  p = 0.000.  differently  repeated  5 trial  measures  blocks  significant:  in  as t h e  F(7,40  the 8  ANOVA o f repeated  d f ) = 13.875,  Differences i n total incorrect f i r s t  v i s i t s were  similarly highly significant  (repeated measures ANOVA o f the  first  blocks:  50 t r i a l s  for 5 trial  p « 0.000) . 83  F  (7,40 df) = 5.289,  Landmark Treatment 1. P l a i n 2. P l c t r 3. C l c t r 4. P l i n e 5. P l c c t 6. C l i n e 7. C l p c t 8. Clnsw  F value 68.599 13 .215 134.565 42.581 463.101 279.550 170.072 199.572  Probability 0.000 0.001 0.000 0.000 0 .000 0.000 0.000 0.000  Y intercept 0 .628 0.738 0 .573 0.676 0 .596 0.644 0.642 0.618  Forms  Slope 0.058 0.028 0.078 0.064 0 .101 0.094 0.096 0 .102  Table 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 n a t u r a l l o g of t r i a l number f o r the f i r s t 50 trials. Acronyms f o r treatments 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 switched a f t e r the p a t t e r n r e v e r s a l . Clpct = coloured 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 . Plcct = p l a i n l i n e s and coloured c e n t r e s . Pline = plain lines. Clctr = coloured c e n t r e s . Plctr = plain centres. Plain = p l a i n array. Treatment 1. P l a i n 2. P l c t r 3. C l c t r 4. P l i n e 5. P l c c t 6. C l i n e 7. C l p c t 8. Clnsw  F value 21.736 6.894 32 .463 0.749 245.653 198.277 143.252 182 .978  Probability 0.000 0.012 0 .000 0.391 0 .000 0 .000 A V  AAA  • \J \J V  0.000  Y intercept 6.453 4.468 8.030 1.961 9 .502 7 .428 8.487 8.733  Slope -0.835 -0.387 -1.229 -0.120 -2 .358 -1.926 -2 .256 -2 .326  Table 9. 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 n a t u r a l l o g of t r i a l number f o r the f i r s t 50 t r i a l s . Acronyms f o r treatments a r e f u l l y described 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 switched a f t e r the 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 centres. C l i n e = coloured l i n e s . Plcct = plain l i n e s and c o l o u r e d c e n t r e s . Pline = plain lines. Clctr = coloured centres. P l c t r = p l a i n centres. Plain = p l a i n array. Since performance significant individual  the ANOVAs  showed  between treatments difference  significant  differences i n  I conducted  Tukey  analyses  to  contrast  d i f f e r e n c e s i n both measures ( F i g s .  84  honestly pairs  of  15 and 16).  Landmark In  general,  there  performance increasing the  significant  (based on treatment  pattern  -  few  switch  after  reached  50,  the  significantly  the  better  trial  tests  on  in  50.  Differences  show  arrays  but  p e r i o d l e a d i n g up  a maximum i n t r i a l s  Tukey  differences  means) i n e a r l y t r i a l s ,  d i f f e r e n c e s throughout  treatments 40  were  Forms  30  - 40.  that  marked  to  between  From  trial  performance  with  lines  was  than  on  p l a i n a r r a y s o r those marked o n l y with c e n t r e s .  Immediately  after  significant  the  switch  differences more  trial  during  i n the  56  were  i n performance,  rapidly  appeared  there  to  this  initial  trial  60  but  again the  period  few  differences  of  relearning  l e a r n i n g phase. reveals  a  reappeared than  they  Performance  number  of  from  significantly  d i f f e r e n t responses to the p a t t e r n switch. Tukey  analyses  show  2-tailed  differences  only.  I  compared s e t s of these p a i r w i s e d i f f e r e n c e s to i n d i c a t e the order  of d i f f i c u l t y  cases  the  of the  resulting  predictions. performance  For would  treatments  ranks the  correspond  first  increase  50  in  coloured  centres,  plain  coloured  centres,  coloured  lines  array  with  marked  observed  the with  best  lines  I  and  and  plain  birds  lines line  with switch  visiting centres.  rankings d i f f e r only i n the poor performance of  b i r d s on the c o l o u r e d centres p a t t e r n .  85  my  plain,  plain  plain  with  that  coloured  from  In most  expected  order:  lines,  performance  coloured  closely  trials,  the  centres,  (tied),  (Table 10) .  an The the  14  3 6  12 H  io H 7' 5' 3i 1  2H  5 2  1 . 2"  8 4  5" 6.  4 . 5!  11  16  6" 21  ?:  3. 2a 14-  6  26  31  3' 2| B  7 6 5 "I  3-1  5. 4'  5"  8"  2i  1, 3 2.  7  8 4  4-i  36  T 41  ~~1  46  51  56  Trial Number  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 treatments. R e s u l t s along the x a x i s a r e grouped i n t o b l o c k s of 5 t r i a l s , w i t h a x i s numbers i n d i c a t i n g which t r i a l begins t h e 5 t r i a l b l o c k . The switch o c c u r r e d immediately b e f o r e t r i a l 51. L i n e s connecting treatments 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 the b i r d s i n these treatments d u r i n g the i n d i c a t e d b l o c k . Numbers r e f e r t o 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 c o l o u r e d centres, 6 = c o l o u r e d l i n e s , 7 = c o l o u r e d l i n e s and p l a i n centres, 8 = c o l o u r e d l i n e markers switched a f t e r the p a t t e r n r e v e r s a l . 86  0.95 p  r o  P 0  0.85 -  r t  0.8 -  1  0.75 -  o n  C o r r e c  t  87" 6-  • 0.7 - 16 7 Am B  4"  fil  8' 5'  4-  3.  4 •  3 •  67»  1  1'  1  3"  2" 1-  7 5 " 6  3 .  1  7  1"  2'  3  4-  0.85 -  6. 4 6 . 8" 5" 5. 2 •  25-  2'  76  B B  7 •  0.9 -  6 . 87 6 • 8 575 •  J:  1  1-  3  2  13"  7. 5•  58"  0.6 2  I  0.55 H 0.5 0.45  "1 11  I 16  I 21  1 28  1 31  1 -r36 41  46  51  56  Trial Number  F i g u r e 16. Summary of Tukey a n a l y s i s of 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 that were c o r r e c t , averaged f o r a l l b i r d s i n each of the 8 treatments. R e s u l t s along the x a x i s a r e grouped i n t o 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 b l o c k . The s w i t c h o c c u r r e d immediately before t r i a l 51. Lines connecting treatments i n d i c a t e that there was not a significant d i f f e r e n c e i n performance f o r the b i r d s i n these treatments d u r i n g the i n d i c a t e d group of t r i a l s . Numbers r e f e r t o the d i f f e r e n t treatments: 1 = p l a i n array, 2 = p l a i n c e n t r e s , 3 = c o l o u r e d c e n t r e s , 4 = p l a i n l i n e s , 5 = 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 , 6 = coloured l i n e s , 7 = 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 , 8 = c o l o u r e d l i n e markers switched a f t e r the pattern reversal. 87  Landmark Treatment  1. 2. 3. 4. 5. 6. 7. 8.  Plain Plctr Clctr Pline Plcct Cline Clpct Clnsw  Pre- Switch Only Comb Prop Tot Inc Rank Corr 1 1.5 2 3 3 3 1.5 1 2 5 4 4 5 5 4 7 6.5 7.5 6 8 8 6.5 7.5 6  Post--Switch Prop Tot Inc Corr 2.5 2 2.5 3 1 1 5 4 5.5 7.5 4 5.5 6 7 7.5 8  Forms  Complete Run Prop Tot Comb Corr Inc Rank 2 2 2 3 3 3 1 1 1 4 4.5 5 5 4.5 4 6.5 6 6 8 7 6.5 7 8 8  Only Comb Rank 2 3 1 4 6.5 5 6.5 8  T a b l e 1 0 . R a n k e d means o f t r e a t m e n t s f r o m T u k e y a n a l y s i s . In t h i s t a b l e a rank o f 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 treatment performed b e t t e r than b i r d s i n any other treatment, while a rank o f 1 i n d i c a t e s t h e worst performance o f any group o f b i r d s . Prop. Corr. 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 . Tot. Inc. = 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 = A v e r a g e o f t h e 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 ranks 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 c o l u m n shows a v e r a g e s f r o m t r i a l s 51 - 60. C o m p l e t e r u n d a t a a r e a v e r a g e s 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 t h e methods s e c t i o n . Clnsw = coloured line markers switched after the pattern reversal. C l p c t = coloured l i n e s and p l a i n c e n t r e s . Cline = coloured lines. Plcct = plain l i n e s and coloured centres. Pline = plain lines. Clctr = coloured centres. Plctr = plain centres. Plain = plain array. After  t h e p a t t e r n r e v e r s a l I expected  of performance as i n t h e f i r s t the  coloured  other  line  treatment.  w e l l w i t h these treatment with  plain  expectations.  performed  good r e c o v e r y  t h e observed  and coloured  from t h e p a t t e r n  rankings  those  poorly  centres reversal.  88  again, showed  i n any  corresponded  Birds i n the coloured  surprisingly  order  but with birds i n  switch pattern outperforming Again,  lines  50 t r i a l s ,  a similar  while  centres those  surprisingly  Landmark Overall, plain,  I  plain  expected  centres,  lines with coloured with plain rankings  centres  followed  the order  coloured  of performance  centres,  centres, coloured and c o l o u r e d these  line  plain  Forms t o be  lines,  plain  lines,  coloured  lines  switch.  The  predictions with  observed  the exception  of  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 p e r f o r m a n c e was p o o r e s t . Switch  Effect  Birds  i n t h e 8 treatments  responded  differently  p a t t e r n r e v e r s a l a s shown g r a p h i c a l l y ( F i g s . by  Tukey a n a l y s i s (Table  bird  performance  than  before  after  13 a n d 14) a n d  1 0 ; F i g s . 15 a n d 1 6 ) . the pattern  the reversal.  Rankings o f  r e v e r s a l were  Birds  using  to a  different  arrays  with  both  l i n e s a n d c e n t r e s p e r f o r m e d 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 switch  (compared t o o t h e r t r e a t m e n t s )  The  most  reversals  obvious  was b e t w e e n  difference coloured  switch  treatments,  which  effect  of  reversals  rewarding line  pattern  treatment. followed  line  I used  treatment When  but  the coloured  t h e movement  specifically  on  learning.  not  when  feeders  feeders in  switched  s t a y e d t h e same). 89  to test I  moved  line the the  i n the coloured  the  indicator  of profitable  were  to pattern  and t h e c o l o u r e d  markedly fewer e r r o r s a f t e r t h e s w i t c h pattern  before.  i n responses  colours w i t h the rewarding  switch  than  coloured  of  feeders,  line  profitability birds  made  ( c o m p a r e d t o t h e same but landmark  patterns  Landmark Birds  i n a l l treatments  rewarding  feeders  regressions number  as  learned  shown  o f performance  by  on  the  t h e new  pattern of  significant  the natural  Forms  linear  l o g of  trial  ( T a b l e s 11 a n d 1 2 ) .  Treatment 1. P l a i n 2. P l c t r 3. C l c t r 4. P l i n e 5. P l c c t 6. C l i n e 7. C l p c t 8. C l n s w  F value 89.780 20.590 24.413 36.071 14.579 34.356 14.569 44.806  Slope -57 .790 -50.358 -70.625 -66.603 -58.853 -99.362 -69 .648 -70 .246  Y intercept 240.096 210.157 292 .914 274.380 240.830 406.061 285.390 286.374  Probability 0.002 0.002 0.001 0.000 0.005 0.000 0.005 0.000  Table 11. Linear regressions of total incorrect first v i s i t s o n 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 after the switch. 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 markers switched a f t e r the p a t t e r n r e v e r s a l . Clpct = 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 . Cline = coloured lines. 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 . Pline = plain lines. C l c t r = coloured centres. P l c t r = p l a i n centres. Plain = plain array.  V i s i t a t i o n Patterns When b i r d s h a d g a i n e d pattern  of rewarding  feeders  most e r r o r s t o n o n - r e w a r d i n g rewarding feeders average,  feeders  beside than  (0.096 v e r s u s  (trials  - 50) ,  Birds visited  feeders  visited  46  they  made  feeders b o r d e r i n g t h e groups of  ( F i g . 17) .  rewarding they  considerable experience w i t h the  four times  other  0.025 t i m e s p e r t r i a l ,  90  non-rewarding more o f t e n , o n  non-rewarding respectively).  locations  Treatment 1. P l a i n 2. P l c t r 3. C l c t r 4. P l i n e 5. P l c c t 6. C l i n e 7 . Clpct 8. Clnsw  Probability 0.000 0.003 0.001 0.000 0.006 0.001 0.009 0 .000  F value 33.616 17.391 24.826 41.334 13.752 24.297 11.946 81.525  Landmark  Y intercept -9.740 -7 .129 -12.989 -11.212 -9 .722 -13 .897 -9.046 -8.513  Forms  Slope 2 .588 1.940 3 .388 2 .962 2 .616 3.643 2 .448 2 .327  Table 12. 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 c o r r e c t on n a t u r a l l o g o f t r i a l number f o r the 10 t r i a l s a f t e r the switch. Acronyms f o r treatments 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 switched a f t e r the p a t t e r n r e v e r s a l . Clpct = coloured 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 . Plcct = p l a i n l i n e s and coloured c e n t r e s . Pline = plain lines. C l c t r = coloured centres. Plctr = plain centres. P l a i n = p l a i n array. B i r d s can remember rewarding l o c a t i o n s , as demonstrated by  their  continued Even  in  high  performance  to r e v i s i t the  final  on  first  unrewarding 5  trials  revisited  feeders  regularly,  rewarding  l o c a t i o n per t r i a l .  feeders  before averaging Thus,  " c o r r e c t " v i s i t s were rewarding.  91  visits,  but  during  the 4.84 only  they  a  trial.  switch,  birds  revisits about  per  20% of  F i g u r e 17. T o t a l v i s i t s by a l l b i r d s to non-rewarding l o c a t i o n s i n t r i a l s 46 - 50 of a l l treatments. V i s i t s to rewarding l o c a t i o n s are not shown. T h i s f i g u r e was produced u s i n g a step smoothing a l g o r i t h m . As a r e s u l t , each f e e d e r l o c a t i o n i s represented by 16 g r i d u n i t s . 92  Landmark  Forms  S e c t i o n IV. D i s c u s s i o n  Use o f A r r a y Markers The  hummingbirds l e a r n e d the d i s t r i b u t i o n  feeders  under  a l l sets  of experimental  similar  shapes  of the i n i t i a l  of rewarding  conditions.  performance  curves  The  for a l l 8  treatments suggests that the b i r d s used s i m i l a r p r o c e s s e s t o learn  a l l o f the treatments.  differences  between  usefulness Adding  the  of v i s u a l  markers  Given  curves  aids  i n locating  t o the p l a i n  of  array  providing  the  relative  rewarding  feeders.  sped  up  treatments  indicate  l o c a t o r s of patches a  colour  learning  asymptotic  and achieved a h i g h e r asymptote.  the d i f f e r e n t  more u s e f u l  the s i g n i f i c a n t  represent  a r r a y ; b i r d s more r a p i d l y approached w i t h markers,  this,  that  the  performance The r a n k i n g s  edge markers a r e  than c e n t r e marks and t h a t  indicator  to  profitability  i n the  landmarks p r o v i d e s some l e a r n i n g b e n e f i t s t o the b i r d s . L i n e s v e r s u s Centres The s t r o n g e s t and most obvious d i f f e r e n c e between these treatments  i s that  lines  were much more e f f e c t i v e  aids to  l e a r n i n g than c e n t r a l marks, which were l i t t l e b e t t e r than a plain  array.  superiority hummingbirds, foraging,  Among of  lines,  perhaps  several the  possible  most  because  feasible  of  information delimiting 93  reasons  how  they  the edges  is  f o r the that  move  for  during  of patches i s  Landmark more  useful  Geometry 1986; My  than  is  an  important  Cheng and  indicating  aspect  Gallistel,  1984;  Birds  that could  spatial  have  used  and  or  rules  landmarks.  rewarding  1989  edge  or  up-down movement  near  and  surrounding  non-rewarding.  relation  to  to  to  centre  f a r feeders  1990) .  develop  based on  orientations in relation  about  (Cheng,  and  landmarks  in  centres.  use  i n t o 4 squares  a r r a y s marked only w i t h  either  a  the  set  of  squares.  landmarks  in relation  could to  the  A l t e r n a t i v e l y , they c o u l d use v e c t o r o r i e n t a t i o n  from e i t h e r type fashion  these  landmark  thumb about p r o f i t a b i l i t y  in-out  Birds using form  a l l either  r u l e s of  left-right lines,  were  of  their  Gallistel,  edge landmarks were arranged  feeders  a  information  Forms  of landmark to f i n d p r o f i t a b l e  similar  to  that  1990).  T h i s v e c t o r sum  though,  especially  suggested  by  Cheng  model of o r i e n t a t i o n has  in relation  to  diagonal  animals seem to have more d i f f i c u l t y  feeders,  in  (1989  and  some  vectors,  flaws which  using.  Another p o s s i b l e e x p l a n a t i o n f o r the d i f f e r e n c e between edge  and  total  centre amount  (centres = 20.3  landmarks of  colour  cm^,  second p o s s i b i l i t y .  Cheng,  near  1989) .  differences to  cm^)  There may  was  rewards  line  over  form of  94  in  the  be some t r u t h to  others  array  the  array  sufficient  In general, animals p r e f e r to use  their The  the  added  l i n e s = 566.4  make the l i n e s more u s e f u l .  landmarks  i s that  (Bennett,  mark may  to this  large 1993;  provide  a  Landmark Forms l a r g e l a n d m a r k t h a t i s more u s e f u l t o a f o r a g i n g h u m m i n g b i r d 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. L i n e s v e r s u s Colours T h e r e was a s t r o n g d i f f e r e n c e b e t w e e n t h e u s e f u l n e s s o f both kinds  o f l a n d m a r k s , per  information. forms or  T h e r e was a much s t r o n g e r  (lines versus  absence  coloured  of  centres)  reward  markers).  profitability the  se, a n d l a n d m a r k s w i t h  d i f f e r e n c e between  t h a n t h e r e was b e t w e e n p r e s e n c e  information Adding  (contrasting  colour  d i d not s i g n i f i c a n t l y  as  an  The  several  significant  possible  demonstrated  that  stimuli  once  at  Montgomerie, 1963;  Roberts 1984;  Various  can attend  Krebs,  1981; Giraudo  and  Perauch,  1987; O l t o n ,  The b i r d s  i n this  of information  1994;  provided  with  the combination  about p r o f i t a b i l i t y What  do  ecologically?  these Various  importance of colour  also  o f landmarks  differences authors  i n hummingbird  95  Gass  array in  have  of and  Gleitman,  1987;  1986; Sherry,  and Z a n f o r l i n , attended  performed  than w i t h uniform  have  types  1988;  and Tversky,  they  have  authors  1990; R e s c o r l a ,  experiment  a t once;  could  to several  and  e t a l . , 1988; S a t t a t h  of  a benefit to  effect  S p e t c h a n d E d w a r d s , 1988; V a l l o r t i g a r a  1989) . types  interaction  (Clayton  Gould and M a r l e r ,  same  increase performance but  meanings. animals  or  indicator  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  learning.  reward  and  t o two  better  when  information  markers. usefulness demonstrated  foraging.  Collias  mean the and  Landmark Collias  (1968)  feeders  used  in  outdoor  t o show that Anna's hummingbirds use c o l o u r  cues i n  choosing feeders and  Wheeler  important  simple  preference  of d i f f e r e n t q u a l i t y .  (1980)  visual  also  cue  tests  Forms  M i l l e r et al. (1984)  demonstrated  that  colour  f o r hummingbirds.  i s an  A l l of  these  s t u d i e s , however, demonstrated that c o l o u r i s l e s s important than  positional  overshadowed  cues.  i n my  The  study,  effect  of  i n this  colour  case  by  was  also  the type  of  marker. Cognitive  Maps  I believe forms  as  an  integral  environments. boundaries,  that b i r d s w i l l use these d i f f e r i n g part  of a  cognitive  Edge landmarks may help  e s p e c i a l l y during  birds  a period  map  landmark of  their  delimit  patch  of area r e s t r i c t e d  s e a r c h a f t e r a reward s i t e has been l o c a t e d and e x p l o i t e d by techniques of  such as random search.  the edge  Information presumably  landmarks may about another  the  also  have  quality  component  The l a r g e r o v e r a l l area facilitated  of  food  necessary  learning.  locations  is  for a  successful  been  challenged  c o g n i t i v e map. The  cognitive  repeatedly al.,  concept  i n the l i t e r a t u r e  1986;  Restle,  map  Collett  et  al.,  has  (M. Brown, 1993;  Dyer,  1991  et  and 1993;  1957) but has gained wide acceptance by many authors  (de Renzio, 1982; E l l e n , 1980; G a l l i s t e l , Perauch,  1992; C o l l e t t  1988; Gould  and Marler, 96  1989; Giraudo and  1987; Nadel  and W i l l n e r ,  Landmark 1980;  O k a i c h i , 1987;  Sholl,  1987;  1989;  Spetch  Sutherland  1985) .  O'Keefe and Conway, 1980; and  and  Skeptics  Honig,  Dyck,  1988;  1984;  suggest  Olton,  Srinivasan  Thinus-Blanc  that  at  least  Forms  et  and  some  1990; al.,  Ingle,  groups  of  animals, e s p e c i a l l y i n v e r t e b r a t e s , r e l y on dead r e c k o n i n g to navigate  rather  environment  than  and  a  argue  remembered that  the  mapping i s weak ( C o l l e t t et a l . , alternative list  of  to  cognitive  specific  geometric  organization  each o t h e r (M. Brown, Map-using animals  of  evidence  1993;  mapping  locations  r e p r e s e n t a t i o n of  these  Dyer,  i s the  with  for  no  cognitive  1991).  Another  maintenance reference  locations  with  lists,  Gould  and  Marler,  1980;  Schenk, 1987;  and I n g l e , 1985) in  a  should be  Morris,  1987;  experiment  finding  a goal s i t e  Menzel,  1984;  to  adaptable  1991;  from  Nadel  and  Olton,  1986c;  1990).  a novel  Willner,  landmarks  Kramer and The  1989;  Thinus-Blanc  or n a v i g a t i n g without u s i n g l o c a l (Gould,  those  Gallistel,  Sutherland and Dyck, 1984;  1981;  the  respect  capable of more  ( E l l e n et a l . ,  stereotyped fashion  1991;  a  1992).  including  environmental p o s i t i o n  of  to  movement p a t t e r n s than those u s i n g dead r e c k o n i n g or checking  the  birds  Weary, in  my  were not c o n s t r a i n e d to approach the f e e d e r a r r a y  from a n o v e l p o s i t i o n ,  ( n a v i g a t i o n through a known landscape  from  is a  there  a  novel p o s i t i o n was  no  evidence  common t e s t  for  repeated,  97  f o r mapping) , but stereotyped  or  Landmark Forms systematic use  movements w i t h i n t h e a r r a y  o f dead  (an i n d i c a t i o n o f t h e  reckoning).  Chunking Learning  a pattern  of feeders  i s an i m p o r t a n t  t h e d e v e l o p m e n t o f a n o v e r a l l c o g n i t i v e map. a  spatial  p a t t e r n of rewarding  feeders  step i n  I f birds  rather  than  learn  learning  a s e t o f i n d i v i d u a l rewarding l o c a t i o n s , they could gain the advantage process  o f reduced involves  characteristics chunking. and  grouping  into  units  Suzuki  et al.,  1989).  The  this  e t al. , 1 9 7 6 ) , animal  1980; V a l l o r t i g a r a of  as  ( F i s k and L l o y d ,  i n several  process  i n memory.  such  i n memory;  1978; S h i f f r i n  described  stored  items  Humans do t h i s  Palmer,  been  information  components  as  demonstrated  i n hummingbirds  i s known  as  and i t has a l s o (Olton,  1985;  a n d Z a n f o r l i n , 1987 a n d a  an by  environmental  1 9 8 8 ; Hemenway  species  learning  distributed  This  group  overall  of  spatially  pattern  Sutherland  and  was  Gass ( i n  press) . T o l m a n , who s u g g e s t e d t h e c o n c e p t o f c o g n i t i v e maps i n 1948,  believed  were  t h e norm,  that  broadly  and t h a t  applicable  narrowly  a n d i n c l u s i v e maps  defined  maps  or sets  i n s t r u c t i o n s were t h e r e s u l t o f inadequate cues, training, this  or strong motivations.  experiment  feeders,  but also  might  I f this  include  not  of  restricted  i s t r u e , a map i n  only  t h e l o c a t i o n and d i s t a n c e  the pattern from  of  the perch  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 the  experimental  the  importance  (Bennett, 1988;  chamber. of  such  Several studies global  cues  Forms  have  suggested  i n spatial  learning  1993; Spetch and Edwards, 1988; Spetch and Honig,  Suzuki et a l . ,  1980).  Environmental Change, Complexity and t h e Switch E f f e c t I n f o r m a t i o n about an  important  temporal  aspect  of  changes  cognitive  mapping  f o r a g i n g i n g e n e r a l (Biebach et a l . , however,  the s c a l e  examining 1981;  i t s effects  Gass  experiments the  of  course  and  temporal (Gass,  Roberts,  d i d not l e a r n of a t r i a l ,  i n reward  sites i s  and  effective  1989; G a l l i s t e l ,  change  i s important  1985; Gass  1992).  1989); in  and Montgomerie,  Hummingbirds  in  my  to avoid depleted feeders during  but l e a r n e d t o a v o i d empty  feeders  a c r o s s a s e r i e s of t r i a l s . The  tendency  environment  i t .  For  instance,  more r a p i d l y  in  when  many f o r a g i n g (Mitchell, rapidly  or  sample  the  surrounding  they  sites  1989).  change  quality  and the animal's memories and p e r c e p t i o n s  strategies reward  explore  i s s t r o n g l y a f f e c t e d both by the a c t u a l  of t h e environment of  to  animals  change  i n response  possess  their  t o temporal  i n f o r m a t i o n about  foraging variations several  than i f they know o n l y one food  Animals their  with  such  behaviour  or  source  r e s t r i c t e d information  only  if  there  is  an  environmental change and they possess s u f f i c i e n t i n f o r m a t i o n about  t h e environment.  99  The  switch  hummingbird  in  spatial  this  experiment  memory  i s resistant  Landmark  Forms  demonstrated  that  to  sudden  change.  As Chapter 2 demonstrated, t h i s r e s i s t a n c e i s r e l a t e d t o the number of t r i a l s in  i n which a b i r d has  i t s environment.  array  markings  The  also  results  suggest  experienced  stability  from t h i s  experiment  into  (although not  strongly)  that  when b i r d s l e a r n more about t h e i r environment  and have more  visual  cues p r o v i d i n g unchanging i n f o r m a t i o n ,  they a r e  likely  t o change t h e i r behaviour i n the face of sudden  unpredictable  change,  as shown by  less and  the c o m p a r a t i v e l y p o o r e r  performance of b i r d s i n treatments w i t h both edge and c e n t r e landmarks. If  the cues  demonstrated  in their  environment  i n the movement  of  change,  coloured  however  lines  after  s w i t c h i n one treatment), they are l e s s r e s i s t a n t (Roberts  et  treatment  where  the  al.,  rewarding  1988).  Performance  array  markers  feeders  showed  that  the  birds  birds  on t h i s p a t t e r n a f t e r the switch was  associate and  result  the c o l o u r  indicates of a r r a y  f o l l o w e d the c o l o u r cues  memory of feeder l o c a t i o n s . and  reward,  which was  markers.  that  The  the  markers  in  the  moved w i t h are  able  to  performance  of  better  birds  with  the  t o change  birds  lines)  changes  This  array  (coloured  track  other.  i n the  by  (as  learned  feeder  i n s t e a d of r e l y i n g  than  on  any to  quality spatial  The a s s o c i a t i o n between c o l o u r  "portable",  was  balanced against  s p a t i a l memory of past reward l o c a t i o n s .  100  the  The b i r d s i n t h i s  Landmark treatment switch  showed  but  a  small  recovered  treatment.  drop  in  more r a p i d l y  performance than  Forms  after  b i r d s i n any  T h e i r use of s p a t i a l memory was  the other  flexible  enough  to r a p i d l y adapt to rearrangement of groups of f e e d e r s . Responses to the switch r e v e a l no apply  to  little after all  a l l treatments.  effect the  on  the  switch.  treatments  indicators  level  to  of  which after  array  followed  the  switch  the  dropping  in  markings  performance  (excepting the treatment  which were s t a t i s t i c a l l y the  type  Immediately  performed s i m i l a r l y ,  By  The  simple p a t t e r n s t h a t  switch,  where  feeder  dropped birds in  profitability profitability)  to l e v e l s of f o r a g i n g  indistinguishable  second b l o c k of 5 t r i a l s  after  success  from each  the  switch,  other.  however,  b i r d s r e t u r n e d to the p r e - s w i t c h order of performance, birds  using  arrays  with  edge  landmarks  had  performing  with  better  than those w i t h p l a i n a r r a y s or centre landmarks o n l y . In  a  Fetterman  review  of  the  timing  (1988) suggested  that  of  behaviour,  the  r i c h n e s s or  of the environment a f f e c t s animals'  foraging.  various  similar  animals  environmental exploratory  have  shown  r i c h n e s s and behaviour  use  systematic  linear  foraging.  based  r i c h n e s s of the environment  a  on  the  Killeen  and  complexity  Studies link  with  between  Chipmunks v a r y  their  predictability  (Kramer and Weary; 1991) .  f o r a g i n g when food i s e a s i l y  and Rats  visible,  but become s e l e c t i v e i n t h e i r search when the food i s hidden (Ilersich  et  a l . , 1988).  G e r b i l s reduce  101  exploration  and  Landmark become  short  increases temporal  term  energy  (Forkman, and  Nor  i s this  fragmented  sites  by  random  Chipmunks  temporal  and  o t h e r t a s k s such  1987;  suggests  that  Menzel,  forests  may  as  appear  to  Warren  adjust  search  their  conditions both  and  animals for  (Gibb,  Warren,  begin food  sources,  criteria  as t i m e i n a p a t c h i n c r e a s e s .  rewarding  site  random s e a r c h f o r a g e r may and  has for a  then  animal's  been  found  limited  restrict itself  Hainsworth,  depends  an  on  the  environment  1991),  i n foraging  and  (Mitchell,  Guilford Heller patch  using  broadening  their  step i n a Once  foraging c r i t e r i a ) ,  the  this  knowledge  1989),  its  step of  r a n d o m s e a r c h h e l p s l o c a t e new  factors  the  (Weiss,  and  surrounding (Forkman,  (Kramer and  food sources, area  102  (Wolf  i s variable  motivation  and  other  a by  1991)  of  (1980)  (perhaps  the v a r i a b i l i t y of the environment number  and  by  exploited  1991),  a  Weary,  to search around t h a t s i t e  although  animal's  al., to  environment.  and  set of  et  techniques  V a r i o u s f o r m s o f s e a r c h a r e l i k e l y an i n i t i a l e x p l o r a t i o n of  breeding  (Haila  1961;  foraging i n a  criteria  to foraging.  (Kramer and  1973).  limited  naive  sources  l o c a t e new sites  species  the  1985).  s e a r c h i n g f o r a mate  other  to  n a t u r a l food  for suitable  environmental  Dawkins,  unpredictability  f o r a g i n g i s adapted  p a t t e r n s of t h e i r  search  1993).  may  when  v a r i a b i l i t y in' search l i m i t e d  in  as  Bee  P l o w r i g h t , 1988;  Birds  1991),  1991).  spatial  ( L a v e r t y and  maximizers  Forms  Weary,  1983).  If  restricted  Landmark  Forms  s e a r c h i s an e f f e c t i v e way  to d e f i n e the boundaries of food  sources.  experiments may  sector  The  of  birds  the  inflorescence patch.  i n my  array  in a  o r a bush  similar  or  be  fashion  treating  to  some o t h e r form  a  of  compound restricted  Once b i r d s had experienced a number of t r i a l s  made most e r r o r s  (first visits  to non-rewarding  f e e d e r s a d j o i n i n g the rewarding f e e d e r s .  one  they  f e e d e r s ) at  T h i s may  be due t o  u n c e r t a i n t y about the edges of the rewarding p a t c h o r may sampling changes  of  areas  around  the  rewarding  patch  detect  in profitability.  Eventually  the animal w i l l  learn  the reward  v a l u e s of the rewards i n i t s environment. values  to  be  of  cognitive sites,  the  rewards  should be  In  to  map.  however,  landmarks (Cheng,  and 1986;  Krebs, 1986). provided  order  the  cues  animal to  must  1989  and  The l o c a t i o n s  and  major  return  navigate  Gallistel,  a  sites  to use  portion  the  known  its  1990;  to  assist  in  from  environment  S h e t t l e w o r t h and  The markers p r o v i d e d on the a r r a y  information  reward  information  through  and  of i t s  this  presumably  step  in  map  hummingbirds  use  formation. Conclusions This landmarks landmarks  experiment  demonstrates  to  reward  locate  that  sites.  The  i s important, and hummingbirds  rewarding  feeders  landmarks  than  more  with  rapidly  central  and  learn  better  landmarks. 103  form  of  these  patterns using  They  also  of  edge use  Landmark information these  about  markers,  reward q u a l i t y  although  the  conveyed by  effect  of  the  reward  Forms  colour  of  information  does not p r o v i d e a very strong b e n e f i t to l e a r n i n g . Once persist evidence of  birds  i n using  have  learned  their  t h i s knowledge u n t i l  they  have  p e r s i s t e n c e may  in.  foraging.  be r e l a t e d  The  i n t h e i r environment before a change. memories  indicating  can  be  strength  to the success  reduced  t h a t a change has  by  occurred.  104  they  sufficient  t h a t t h e i r memories are no longer a v a l u a b l e  information  spatial  surroundings,  of  they have  source this  achieved  P e r s i s t e n c e of use providing  of  information  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  Section I.  In of  this  spatial  period  experiment association  Introduction  I examined and s p a t i a l  o f exposure t o a p a t t e r n  spatial  separation  f e e d e r and t h a t together  the contrasting  between  feeder.  a  This  some o f t h e a s p e c t s  memory  effects  by v a r y i n g  the  of rewarding feeders and t h e cue  to profitability  of  a  s t u d y was a l s o i n t e n d e d t o t i e of spatial  learning  discussed  i n C h a p t e r s 2 a n d 3. S p a t i a l A s s o c i a t i o n Learning Simple associating examples pressing  of  associative a  contiguous simple  the correct  learning  is  the  cue and response  associative bar i n a  learning group  site.  of bars  a  food  reward  Hoffmann and Maki, these  (Bond  as  the stimulus.  learns  to obtain  a  a r m o f a maze  1983; M a k i ,  1985;  1979).  In  t o r e s p o n d a t t h e same  In other 105  a rat  a l . , 1981; C o l w i l l ,  1986; M a c k i n t o s h ,  s i t u a t i o n s , the animal  location  et  of  Typical  include  r e w a r d 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 with  process  situations,  however,  Spatial  Association  t h e r e may be a displacement and In  t h e response such  cases,  o r reward  and Spatial  i n space between sites  many animals  have  1963;  (Davis,  1974; P i n e l  Stollnitz  this  study  I  difficulty  l e a r n i n g the  and l e n g t h y t r a i n i n g  et a l . , 1986; S c h r i e r  and S c h r i e r ,  define  the s t i m u l u s  (Rumbaugh et al., 1989).  t a s k without s p e c i a l t r a i n i n g p r o t o c o l s periods  1962).  spatial  Memory  et a l . ,  F o r the purposes o f  association  learning  as the  p r o c e s s o f a s s o c i a t i n g a s p a t i a l l y s e p a r a t e d cue and reward (Bowe,  1984; Brown  learning,  laboratory  al.,  1993).  Simple  associative  i n which the reward and cue a r e contiguous,  much s i m p l e r  instance  and Gass,  task f o r animals t o l e a r n  isa  i n both n a t u r a l and  environments and has been h e a v i l y documented  Aadland e t al., 1985; Balda  (for  e t al., 1986; Bond e t  1981; Bruce and Herman, 1987; C l a y t o n and Krebs, 1993  and  1994; C o l e  Baum,  e t al., 1982; C o l w i l l ,  1991; Dawkins,  Gillingham  1971a and  and Bunnell,  In  nature,  animals  learning  or reward s i t e .  1985; D a l l e r y  1971b;  Gallistel,  and  1989;  1989; Fuchs and Haken, 1988a).  however,  there  to associate  are various  a separated  examples  of  cue and response  The 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 o f flowers by bees  (Gori, 1989), and t h e use  of  to locate  circling  1983;  vultures  by p r e d a t o r s  prey  (Houston,  Rabenold, 1983 and 1987) a r e both examples o f s p a t i a l  association  learning.  Brown and Gass  (1993)  demonstrated  the a b i l i t y of hummingbirds t o c a r r y out s p a t i a l a s s o c i a t i o n  106  Spatial  learning  Association  and  Spatial  Memory-  t a s k s i n a l a b o r a t o r y environment a f t e r a s h o r t  and  simple t r a i n i n g p e r i o d . S p a t i a l Memory Similarly, demonstrated  f a c i l i t y w i t h s p a t i a l memory t a s k s has  f o r v a r i e d tasks  and  species  Gould, 1986a and  1986b; Grigoryan and  and  Hermer and  Krebs,  1992;  is  simply  to  navigate  sites two  the use  may  fixed  found  the  animals  a  dead  1973;  i n most  O'Keefe  memory may foraging  series  and  1985;  1986),  finding  and  to  Dyer,  1993)  Schenk, 1987;  Why own  or  S p a t i a l memory  Previously  any and  (moving  al. , 1993;  et  1980;  or  to  home  between  Dyer,  (Gould, Olton,  1986a;  1990).  in  1993)  ecological Sherry,  location  f u n c t i o n , from  1990;  Kamil  and  McQuade et  al.,  Robinson  (Morris,  1983), to f i n d i n g mates  or f i n d i n g o f f s p r i n g  Menzel, Spatial  ( H o l l d o b l e r , 1980;  some other  visited  f o r c o g n i t i v e maps of the  MacDonald and W i l k i e , 1990; the way  location  remembered v e c t o r s )  animals  (Hitchcock  Shettleworth,  and Weary, 1991) Learning  higher Conway,  food  Roitblat,  Healy  1994).  of  (Collett  be used f o r almost for  S t o l b e r g , 1989;  reckoning  but t h e r e i s c o n s i d e r a b l e evidence environment  1963;  environment.  only by  p o i n t s along  some p r i m i t i v e  (Gleitman,  of remembered i n f o r m a t i o n about  through  be  Spelke,  been  1981;  (Kramer  (McCracken, 1993).  Processes would animals  easily  locations directly  remember l o c a t i o n s (on  associated with  107  response  their sites)  Spatial but  have  difficulty  Association  learning  to  and Spatial  associate  cues  Memory that  are  d i s p l a c e d from response s i t e s w i t h the response s i t e s ? difference  suggests  physiological occur  and  learning best  difference  that  can  say  about  evidence that  memory  stored  at  Kesner, 1980; 1990) .  be  these  processes  a f f e c t which  that  still  underlying  learning  in specific  is  partly  Okaichi,  the  instances. neural  We  may  the  1987;  for  do  have  long  term  hippocampus  O'Keefe and  of The  bases  speculative.  in  form  (Ellen,  Conway,  1980;  w i t h s u p e r i o r s p a t i a l memories have a  (Sherry in  cognitive  some  s p a t i a l memory i s a form of  Species  hippocampus  animal's  this  least  l a r g e hippocampus the  how  l e a r n i n g are  strong  Olton,  in  may  these d i f f e r e n c e s may  forms of  1980;  there  i s more advantageous  we  these  that  This  et al., fact  map  of  1989), and  correspond  place  to  cells  elements  i t s surroundings  of  (Speakman  in an and  O'Keefe, 1989). The  hippocampus  functions between longer  implicated  It i s involved  s t i m u l i and  i n discounting  available  (Moore  and  is  behaviour,  temporal 1980;  i n various  i n forming cues  Stickney,  involved  d i r e c t i o n vectors  may  1990; be  along  and  Speakman  involved  in  types  and  are  no  reward become well, of  non-spatial  motor and  the  spatial learning  O'Keefe,  monitoring  w i t h the v i s u a l ,  108  they  As  non-mapping  mapping,  Olton,  hippocampus  in  1980).  of  other  associations  when  or when b e t t e r p r e d i c t o r s  hippocampus  The  been  as w e l l .  valuable  (Kesner,  has  1989).  speed  and  parietal  Spatial cortex  (Olton,  1990).  indefinite  long  term  period)  memories  seem t o i n v o l v e  f o r a short  modifications 1988;  Goelet  a l s o be  (Olton et al., 1980).  genes a r e expressed by a neuron, stored  and Spatial Memory-  S p a t i a l working memory may  s t o r e d i n the hippocampus While  Association  period  only)  of p r e - e x i s t i n g  (items  stored  f o r an  actual  changes  i n which  short  term memory  seems t o i n v o l v e cellular  et a l . , 1986; Matthies,  (items  covalent  proteins  (Barnes,  1989; Thompson,  1986).  Some authors suggest a t h i r d form of memory, working memory, which  i s used  essentially the  only  while  non-associative  current  hippocampus  task plays  tasks  ongoing.  and i s d i s c a r d e d  (Barnes, a  are  1988;  key r o l e  Maki,  It i s  a t t h e end of 1987) .  i n transferring  The  items  from  working memory t o long term memory (Wickelgren, 1979) .  Most  a s p e c t s o f s p a t i a l memory a r e long term memory tasks and  Willner,  1980).  are  similar  across  mammals  and  I t appears that these n e u r a l a wide  possibly  variety  other  advanced  (Bingman et al., 1989; Olton, Differences In  simple  of s p e c i e s groups  various  of b i r d s , of  animals  i n Learning associative  learning,  spatial  association  learning processes  may occur s i m i l a r l y as p a r t of working memory.  transfer  processes  1985).  l e a r n i n g and s p a t i a l memory, the i n i t i a l  a processing  (Nadel  I f there i s  d i f f e r e n c e , i t probably occurs a t t h e p o i n t of  t o short authors  term  suggests  or long that 109  term  memory.  Work  many cue ( a s s o c i a t i v e )  by tasks  are  limited  Spatial  Association  term  memory w h i l e  t o short  memory) t a s k s a r e t r a n s f e r r e d  Willner,  landmark  d i r e c t l y t o long  (Barnes, 1988; Kamil and Mauldin, and  and Spatial Memory(spatial  term memory  1975; Kesner,  1980; Nadel  1980; Sherry, p e r s . comm.).  Advantages and Disadvantages These  differences,  development involved  of  spatial  than  association  real,  memory  direct  learning  if  suggest  takes  associative  should  fall  longer  that and  the  i s more  learning.  Spatial  somewhere between  t h e two  s i n c e i t i n v o l v e s both 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 , but generally  will  still  s p a t i a l memory. associative  be  than  reliance  In a s i t u a t i o n i n which e i t h e r  learning  simplicity  quicker  would  dictates  predominate.  be  that  These  possible  associative  physiological  and  solely  on  s p a t i a l or effective,  learning  differences  should 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  Another that  the  advantage  animals  association other  memories  using  between hand,  about  is  t o simple  i t need  landmarks,  association  to  learning  only  This  one  cues,  reward  suggests  that  complete  learning thing:  Spatial  the development  should be p r e f e r r e d  sufficient  learn  associative  cue and response.  requires  interrelationships. learning  towards p a r t i c u l a r types of l e a r n i n g .  of  sites simple  should f a l l 110  task.  a  s e t of  and  their  associative  Again,  between simple  the  memory, on  to s p a t i a l memory when the  is  either spatial  association  Spatial and  pure  spatial  associations  Association  memory  require  in  animals  and Spatial  difficulty,  Memory  since  to remember only  spatial  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 a d d i t i o n  t o the f a c t  t h a t they a r e a s s o c i a t e d . Uncertainty An  and P e r c e p t i o n  animal's p e r c e p t i o n  i n f l u e n c e whether given  should  also  i t uses s p a t i a l memory o r a s s o c i a t i o n  ina  situation.  term development  I f the environment  spatial highly of  as they a l l o w e f f i c i e n t  and use of the environment.  mapping would variable  be a waste  environment,  the environment  could  case,  term a s s o c i a t i v e  association and  it  remains  association can apply  flowers. spatial  structure  them.  would  Associations  In t h i s  be more o f an  as  long  as the  between  stimuli  and can be a p p l i e d  F o r example,  association  i n various  i f a hummingbird  between r e d flowers  that  in a  remembering r u l e s t h a t a r e not  intact.  and times.  and energy  of l e a r n i n g  i n the environment  responses a r e "portable"  locations the  changes  and f l e x i b l e  the s p a t i a l  learning  advantage because i t i n v o l v e s by  information  change enough b e f o r e they a r e used  t o balance the cost  short  the long  On the o t h e r hand,  of time  because  sufficiently  affected  i s stable,  of maps of s p a t i a l l y s t r u c t u r e d  should be advantageous exploration  of i t s environment  and n e c t a r  learns  production,  to any r e d n e c t a r  producing  I f , however, i t uses s p a t i a l memory t o l e a r n t h e location  of a p a r t i c u l a r  111  s e t of r e d flowers,  the  Spatial memory i s u s e f u l  Association  and  Spatial  f o r only the nectar producing  Memory  lifespan  of  those f l o w e r s . There temporal  an  of  similarity  environments  based  Girardeau, effects  of  experience variability  correspond  to sensory  tend t o reduce sampling  to  value  the  Kacelnik,  tasks  1993).  effect,  experience reward,  but  variability  of  1984) .  of past  Valone of  and the  memories. do  not  animals  will  e x p l o r a t i o n and  1992).  experience, most be  animals  highly  tend  (Todd  and  f o r the  performance f o r r e c e n t l y  learned  not time  also  based  on  the  reward  (Bowers  have a l i m i t e d a b i l i t y  of  the reason  elapsed  the  only  discount  since they amount  and  and  retrieve  a  perceived  Adams-Manson,  them.  past  obtained  V a r i a b l e rewards i n c r e a s e the  information required to  a  their  memory  spatial  on  the  i t is  evidence  case,  rely  experience  Animals  the  1991;  In t h i s  (Valone,  and  expectations  T h i s phenomenon may  Gibbon et a l . , 1988). of  when  f o r a g i n g and  recent  b a s e d on  and  actuality,  2 I presented  evidence.  o r improved  (Sherry,  Miller,  results  the value  most  actual  g e n e r a l l y be  input  p e r s i s t e n c e of  of the environment gauging  there w i l l  sensory  and  on  planned  In  recency  current  In Chapter  Perceived  environment  p e r c e p t i o n and  (Church  1993) .  the  normally develop p e r c e p t i o n s of  on  experiences  between  animal's While  between  Animals  difference  an  p e r c e p t i o n of i t .  not a b s o l u t e .  past  important  variability  animal's strong  is  Since  1993; amount animals  t o remember p a s t e x p e r i e n c e s , a t some  112  Spatial  point  they  based  on  a  experience  reach  the  (Nishimura,  their  combination  and  increases  Current  will  Association  capacity  of  of  Spatial  time,  complexity,  information  study  had  two  simple  of  persistence In  pattern (inthis  studied the effect  number  trials  primary  information  of  processed  purposes.  3  a  stable  assisted  A second  reason  the roles  at  spatial  e x a m i n e how t h e s e f a c t o r s  how  of  and cue  In chapter 2 i n terms o f feeders)  rewarding  differing  learning.  feeders.  perceptual  In this  study  spatial  association  learning  s e p a r a t i o n from t h e response  contrast by  1992;  Thompson,  between  1994).  the spatial  B r o w n a n d Thompson  that  s i t e h a m p e r e d l e a r n i n g (G. This  study  association  and t h e s p a t i a l  m y s e l f a n d S u t h e r l a n d ( S u t h e r l a n d , 1985).  113  and  In previous studies  w i t h r u f o u s h u m m i n g b i r d s , Brown a n d Thompson b o t h f o u n d  Brown,  I  s t u d y was t h e p o t e n t i a l t o  s p a t i a l memory i n h u m m i n g b i r d f o r a g i n g .  cue  on  interact.  t o do t h i s of  (measured  pattern  i t  of experience  feeders  t o formerly  looked  First,  cue d i s t a n c e ) .  of experience  with  I  rewarding  case,  of visitations  chapter  contrast  which  1994).  characteristics I  of  be  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 t h e r o l e s a  individual  each  to  memory,  Study  This  with  Memory  f o r stored  elapsed  environmental amount  and  provides  learning  memory  a  examined  examined by  Spatial  Association  and Spatial  Memory  T h i s study a l s o continues my e x p l o r a t i o n o f t h e r o l e of environmental  instability  i n hummingbird  learning.  As i n  chapter 2, where I found that p e r s i s t e n c e w i t h a p a t t e r n of feeders  increased  pattern,  I  with  provide  environment  increasing  the animals  for differing  experience  with  periods  a  stable  of time  sudden change i n the p a t t e r n of rewarding  a r e nine  experiments, durations access  different  consisting  (30 minutes,  of  treatments  exposures  90 minutes  t o a p a t t e r n of rewarding  foraging  followed  i n this  of  three  and 300 minutes  and non-rewarding  no LEDs at a l l ) .  s e t of  different of free feeders)  LEDs c u e i n g  feeders at d i s t a n c e s of 1 cm; f a r cues:  12 cm; and uncued:  by a  learning.  and t h r e e d i f f e r e n t cue c o n d i t i o n s (close cues: rewarding  that  f e e d e r s t o probe  the extent and p e r s i s t e n c e of t h e i r p r e v i o u s There  with  LEDs at  F o r each d u r a t i o n , t h e  exposure i s t i e d not only to the c l o c k but t o the number of feeding  bouts  durations while  will  longer  spatial  by the hummingbirds. tend time  memory.  t o favour periods  Uncued  of s p a t i a l cues  should  will  also  combination  that  shorter  the use of a s s o c i a t e d  will  favour  treatments  memory, and c l o s e cues w i l l  I expect  the development o f  will  require  spatial  favour the a s s o c i a t i o n  aspects  a s s o c i a t i o n l e a r n i n g over a g i v e n d u r a t i o n . fall  somewhere between these  involve  spatial  cues,  association  Far  two extremes, but learning.  The  o f these two f a c t o r s should a l l o w me t o e x p l o r e  114  Spatial how  Association  and Spatial  Memory  the i n t e r a c t i o n s between time and cue d i s t a n c e w i l l  b i r d s towards use of e i t h e r type of /  115  learning.  bias  Spatial Section I I .  Association  and Spatial  Memory  M a t e r i a l s and Methods  Subjects The  s u b j e c t s of  birds  vicinity Island,  had  the  been used  different 14. 0.6  The  forest  loss  (both  animals  Photoperiod test  Roudybush  hummingbird  added  with  the  11  Ridge,  the  diet  isolated  birds or soy  weekends,  (Avimin  they  (Avitron avian  were  avian mineral  116  final  Plus  25%  by  number  to  0.6  0.6  sucrose  x  to  testing.  in  the  (3% w/w)  vitamin  x  wild. either  hummingbird  volume  to  run  supplied with  protein  had  Due  complete  total  variation  unlimited  British Columbia  c o u l d not  in individual  Nektar  of  British  b r i n g i n g the  the  Vancouver  experiments.  females  seasonal  from  hatchery,  University  rufous  females.  1991  f o r s e v e r a l months p r i o r  commercial  vitamins  minerals  of  adult  and  i n May  learning  female),  periods,  standard On  two  mimicked  Excluding  weekdays.  i n Maple  were m a i n t a i n e d  m w i r e mesh c a g e s  from  the  12  and were e a c h r e p l a c e d f o r t h e i r  birds  supplemented  1 male  salmon  and  i n previous  were  wild  Creek  Columbia,  research  treatments  i n the  Rosewall  e x c e s s i v e weight all  rufus) :  collected  British  Columbia and  were of  experiments  (Selasphorus  hummingbirds The  these  ad  diet  libitum  feeders  on  solution  with  supplement)  and  supplement).  The  birds  Spatial participated  i n several  Association  foraging  and  Spatial Memory-  experiments  prior  to  this  study.  E x p e r i m e n t a l Environment I  conducted  a l l  experimental  rooms,  overhead  watt  40  ceiling,  The  each  and  x  2.5  experiments  x  2.5  light  m  floor  was  a  uniform  bulbs.  sand  h i g h p e r c h was  in  high  with  Walls  f e e d e r a r r a y , were a u n i f o r m  s t a n d - m o u n t e d , 1.5m e a c h room a n d  1.3  incandescent  except the  colour.  training  light  colour.  A  3 2 and  green  single,  l o c a t e d at the centre  f i t t e d with a photocell to s i g n a l a r r i v a l s  of and  departures. A of  feeder  array covering part  a metal panel  dark  green  spaced  (107  colour  feeders.  cm  with Each  wide x a  o f one 61  cm  end  was  consisted  high) p a i n t e d  horizontal array  feeder  wall  marked  of by  eight a  hole.  which  detected  small  food  disposable behind  was  the  21  tubing  (General  designated  the v a l v e  presence  of  a  r e s e r v o i r c o n s i s t i n g of  an  infrared  the p l a s t i c  mm  diameter  bill.  fitting  also  19  A of  a  positioned  c o n n e c t e d by  flexible  t o a computer c o n t r o l l e d , m i n i a t u r e  solenoid  Valve  E a c h s y r i n g e was  was  evenly  photocell  hummingbird's  gauge h y p o d e r m i c n e e d l e  each feeder.  plastic valve  B e h i n d e a c h f e e d e r was  flat  round  d i a m e t e r f l u o r e s c e n t o r a n g e A v e r y l a b e l w i t h a 3 mm central  a  Corporation,  as r e w a r d i n g  released 2 |il  of  series 3).  I f the  feeder  during a p a r t i c u l a r time period, 20% 117  sucrose  solution  (mass/mass)  Spatial into  the  Association  r e s e r v o i r immediately  feeder.  I f the  feeder was  no food from that  and Spatial  when  the  bird  Memory  probed  non-rewarding, the b i r d  received  feeder.  There were three v a r i a t i o n s on t h i s b a s i c panel with  one  variation  in  each  experimental  feeders were unmarked except small  red  panel  1 cm  design, three  light  (4 mm  directly  the  diameter  were  LED)  12 cm  represented  c l o s e cues and  as noted  above  the  f a r cues.  three  design,  room.  above.  third  a the  panel  feeders.  These  treatments:  When the l i g h t  one,  through  In the the  In  In another,  protruded  above each feeder.  lights  panels  the  uncued,  above a f e e d e r  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 t e s t period, 3  i t s i g n a l l e d that the feeder was  cases,  a buzzer  also  i n d i c a t e d the  rewarding.  start  of  a  In a l l test,  even b i r d s u s i n g the p l a i n panel were given a s i g n a l rewarding  feeder was  present  areas  of  the  that a  somewhere i n the a r r a y .  Hummingbirds were allowed all  so  f r e e access  room d u r i n g  to the a r r a y  experiments,  feed s u c c e s s f u l l y only from one  rewarding  but  they  and  could  feeder d u r i n g each  exposure p e r i o d . Training On home  the  cage  day was  before modified  experimental  arrays.  feeders  they  and  rooms  in  and  experimental  testing, to  resemble  Birds  quickly  their the  the  feeders  late 118  feeder the  i n each b i r d ' s feeders  learned were  afternoon.  to  in  use  the these  moved  to  the  These  feeders  Spatial were  hung  directly  experimental The  in  following  were  feeding array  front  of  and Spatial the  Memory-  centres  of  the  a r r a y s , w h i c h were c o v e r e d . morning,  r e m o v e d a n d one a r r a y birds  Association  allowed  regularly. was  then  minutes) u n t i l  the  feeder  testing  to  the  array  until  took about 2 hours  recovered  feeders  were  was u n c o v e r e d i n e a c h room a n d  access This  commercial  for a  short  they  were  in total.  The  period  (about  20  began.  E x p e r i m e n t a l Procedures Each  bird  experienced  conditions  (excepting  experiment  and  presentation given  nine  the  their  two  different birds  removed  substitutes) .  of these conditions  experimental  The  and t h e b i r d s  from  the  order  of  used  t e s t day were randomized. The  conditions  experimental differing switched. feeders  arrays  c o n s i s t e d of exposure (uncued,  exposure periods  close  before  The 3 e x p o s u r e t i m e s  were s h o r t  (30  t o each o f t h e 3  cue and  f a r cue)  the rewarding to the o r i g i n a l  minutes or 3 s u c c e s s f u l  p e r i o d ) , medium (90  any  m i n u t e s o r 30 rewarding v i s i t  for 3  feeder pattern  feeds  b i r d s h a d n o t met t h i s r e q u i r e m e n t i n t h e 3 0 m i n u t e  (300  on any  to the array  of  i f the  exposure  minutes o r 9 s u c c e s s f u l f e e d s ) , and successful feeds).  was  A successful feed  long was  f o l l o w e d by a r e t u r n t o t h e  perch. One o f t h e f e e d e r s for  the  entire  exposure  i n the 8 feeder period 119  and  a r r a y was  the others  rewarding were n o t .  Spatial Rewarding  feeders  experimental rewarding. using  a  nearest al.,  simple  beginning  buzzer  test  periods  t h e experiment,  probe.  Each v i s i t  The location least  period,  t h e two  bouts.  feeder  end  was  ever  birds  from  the  feeder  (Miller  et  and  f a r cue  feeder  i t was  was l i t rewarding.  feeder provided  f e e d i n g bout  no m a t t e r  feeders. changed  the i n i t i a l  randomly  to  As i n t h e i n i t i a l were  made  never  three  A t t h e end o f t h e r u n , t h e b i r d  a  new  exposure p e r i o d (at  f o r a minimum  exposure  rewarding. of t h i r t y  successful  The minutes  foraging  was r e t u r n e d  home c a g e a n d t h e equipment was c l e a n e d a n d f l u s h e d .  120  2ul p e r  f o l l o w e d by a r e t u r n t o t h e  was  feeders  the b i r d  close  that  t o be a s i n g l e  run continued  or until  the  the rewarding  90 o r 300 m i n u t e s ) .  experimental longer,  indicate  i n the array after  30,  studies  the rewarding  the b i r d probed  rewarding  as v i s i t i n g  In  to the array  was c o n s i d e r e d  how many t i m e s  such  for a l l  feeder  empty t o p r e v e n t  Memory  sounded f o r 0.5 s t o i n d i c a t e t h e  above to  end  i n previous  periods.  t h e cue  test  seen  assigned  neither  o f thumb  as  A soft  of  treatments,  perch  although  rule  and Spatial  randomly  E n d f e e d e r s were l e f t  1984).  During  were  runs,  the wall,  during  Association  to i t s  Spatial  Association  Section I I I .  and Spatial  Memory  Results  I n i t i a l Learning In than  a l l cases the b i r d s  chance  (Table 13). correct showed (Fig. the  within In t h i s  probes. the  the  first  case,  During  poorest  performed 10  minutes  chance  this  significantly  performance  initial  performance  of  with  period, the  better  the  test  was  12.5%  the  birds  uncued  panel  18); even so, they averaged over 60% c o r r e c t v i s i t s i n first  exposure  30 minutes.  Performance  treatments showed  n e a r l y p e r f e c t performance exceeding  90% c o r r e c t  i n the medium and long  continual  improvement,  i n the c l o s e  performance  reaching  cue treatments and  i n a l l treatments by the  end o f the long, 300 minute exposure p e r i o d .  Exposure Time Short t value probability Medium t value probability Long t value probability  Close 9.593 0.000 16.787 0.000 6.855 0.000  Cue D i s t a n c e Far Uncued 4.605 3 .238 0.001 0.008 10.196 3.336 0.000 0 . 007 15.973 4.291 0 .000 0.001  Table 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 treatments i n the f i r s t 10 minutes of experimental runs. A n a l y s i s i s based on a one sample t t e s t a g a i n s t a random performance l e v e l o f 0.125 (one chance out of 8 ) . Terms f o r cue d i s t a n c e and exposure time a r e e x p l a i n e d i n the methods s e c t i o n . P r o b a b i l i t i e s i n d i c a t e the l i k e l i h o o d t h a t performance d i d not d i f f e r from success due s o l e l y t o 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  30  36  Blocks of 10 Minute Durations F i g u r e 18. P r o p o r t i o n of v i s i t s that were t o the c o r r e c t f e e d e r f o r each of the 9 treatments. Each l i n e r e p r e s e n t s the average o f the 12 b i r d s from each treatment. The X a x i s i s d i v i d e d i n t o b l o c k s of 10 minute d u r a t i o n s . The top panel shows the 3 long (300 minute) treatments, the middle panel c o n t a i n s the 3 medium (90 minute) treatments and the bottom panel has the 3 short (30 minute) exposure treatments. The feeder switch i s i n d i c a t e d by the v e r t i c a l l i n e through the graphs on the 3 p a n e l s . On a l l 3 p a n e l s , the s o l i d l i n e shows the c l o s e cue treatment, the dashed l i n e i s the f a r cue treatment and the d o t t e d l i n e i s the uncued treatment. 122  Spatial Performance  Association  and Spatial Memory-  followed the predicted order  exposure  times.  Birds  followed  by b i r d s  using  using  close  f a r cues,  cues who  followed  feeder  i n the period  the predicted  persisted  longest  order.  ( F i g . 18).  after  Birds  i n visits  birds with  pre-switch  close  exposure  the  i n uncued  ( F i g . 19) .  persisted  also  treatments rewarding  w i t h medium e x p o s u r e s a n d f i n a l l y  Two distance  way  of variance  exposure  time  long  followed  those  with  a  by  short  i n the persistence  t h e f o r m e r l y good f e e d e r .  Effect  of the effect  shows  s i g n i f i c a n t l y affect post-switch most a p p a r e n t  with  feeder p o s i t i o n s .  analysis  and  Birds  longest,  Time, D i s t a n c e , and the I n t e r a c t i o n  that  o f cue  both  factors  feeding behaviour.  This i s  of the birds  distance  t h e c u e (F = 19.953, d f = 2,99, p « 0.000)  and time  df  significant,  but distance  exposure.  This  =  p  «  0.000)  i sa stronger  are both effect  highly  than time o f  c o m p a r i s o n i s most c l e a r f o r t h e p r o p o r t i o n  correct v i s i t s  switch.  2,99,  Using  i n returning  this criterion,  (F = 8.622,  of  switch  to the previously  cues  times  exposure t o t h e i n i t i a l  to  performed  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  finally  to  best,  Effect  Performance  birds  performed  i n turn  b e t t e r t h a n b i r d s u s i n g t h e uncued p a n e l Switch  f o r a l l three  i n t h e 3 0 minute p e r i o d  I n t h i s case,  after  the feeder  d i s t a n c e t o t h e cue i s s t i l l  123  a highly  eede  80  u_  g o CO  "35 >  60 40 20 0 UL  UM  Treatment  1  g  o -»--  CO  >  80 60 40 20 0 CLOSE  FAR  UNCUED  Cue Distance  o -*—»  CO  >  LONG  MEDIUM  SHORT  Exposure Time  F i g u r e 19. Box p l o t s of number of v i s i t s by b i r d s t o the f o r m e r l y good feeder a f t e r the feeder s w i t c h . The top p a n e l shows each treatment, the middle panel i s b i r d s grouped by cue d i s t a n c e and the bottom panel i s grouped by d u r a t i o n of exposure. In each box p l o t the c e n t r a l h o r i z o n t a l 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 d i f f e r e n c e between these q u a r t i l e s i s known as the f o u r t h spread), the v e r t i c a l whiskers extend out t o 1.5 times the f o u r t h spread, a s t e r i s k s i n d i c a t e m i l d o u t l i e r s (more than 1.5 times the f o u r t h 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 f o u r t h spread), and the notches i n the v e r t i c a l edges of the boxes r e p r e s e n t 95% c o n f i d e n c e i n t e r v a l s (which may extend beyond the f o u r t h spread c a u s i n g a f o l d e d edge t o the box) . Treatment acronyms i n the top panel are based on 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 of exposure (S = short, M = medium and L = l o n g ) . 124  Spatial significant  effect  on  Association  bird  and Spatial  performance  (F  =  Memory41.472,  d f = 2,99, p = 0.000) b u t t h e e f f e c t  of time  p e r f o r m a n c e i s no l o n g e r  (F = 0.214, d f = 2,99,  significant  on p o s t - s w i t c h  p = 0.808). Differences i n Persistence Analyses rewarding  of variance  feeders  significantly highly  and  d f = 8,99.  birds visited  o f a f e e d i n g bout t h e number  visited  individual birds  of changing the  treatments  differ  achieved.  These  d i f f e r e n c e s c a n be s e e n i n t h e number o f  (F = 3.803,  bouts u n t i l  that  i n the performance  significant  feeder  visit  show  f o r the effects  p  = 0.001),  t h e new g o o d  t h e number o f  feeder  as t h e f i r s t  (F = 4.683, d f = 8,99. p = 0.000),  of bouts  until  the t h i r d  t h e good f e e d e r as i t s f i r s t  visit  time  the  bird  of a feeding  bout  (F = 6.664, d f = 8,99. p « 0.000).  Treatment  Short Medium Lonq  New  Good  Feeder  Old  Good  Feeder  Neither  Close  Far  Uncued  Close  Far  Uncued  Close  Far  Uncued  7 6 4  3 1 0  1 0 0  2 4 5  5 5 9  4 4 7  3 2 3  4 8 3  7 8 5  T a b l e 14. P o s t - s w i t c h p e r f o r m a n c e o f b i r d s i n t h e d i f f e r e n t treatments. F i g u r e s f o r new g o o d 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 feeder immediately f o l l o w i n g the feeder switch. O l d good f e e d e r shows t h e number o f b i r d s who w e n t i m m e d i a t e l y t o the formerly rewarding feeder a f t e r the switch, 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 ' b e h a v i o u r d i f f e r e d d r a m a t i c a l l y among t r e a t m e n t s (Table greatest rapidly  14).  This  table  suggests  i n t h e uncued a r r a y , i n the close  that  cue a r r a y  that  persistence  switching  and b i r d s  t r e a t m e n t s were more l i k e l y ,  on t h e i r f i r s t  feeder  feeders  switch,  rewarding. that  to  choose  The o n l y  significant  fewer b i r d s s w i t c h e d  feeder  at greater  that  most  i n t h e uncued visit had  a f t e r the  never  been  d i f f e r e n c e , however, was  i m m e d i a t e l y t o t h e new r e w a r d i n g  cue d i s t a n c e s  (%2  of the pairwise  -  19.73 6,  d f = 2,  differences  i s also  p = 0.000).  Analysis  not  Based on a Tukey a n a l y s i s ,  clear.  occurred  was  the order  of the  t r e a t m e n t s i s i n d i c a t i v e o f t h e p r e d i c t e d o r d e r , b u t many o f the d i f f e r e n c e s a r e nob s i g n i f i c a n t  12 6  (Fig. 20).  CL CS CM FS UM  FL  r  FM US _  UL  ,  1  1  Find New Feeder  CS CM CL  FS  FL  1  UM  FM  i  US  UL  4  —  A  Correct First Visit  CS  CLCM  FS  UM FM FL  f  ;  1  US  UL  ^  i  1 *  i  1  3 Correct First Visits • 1  0  1 2  1  i—i  1  3  'i — •  4  •  5  1  6  i — •  7  Ii  1  8  N u m b e r of  1i  9  Ii  1i  1i  1i — i  1  1.  1,  1  1—  1  10 11 12 13 14 15 16 17 18 19  B o u t s to  I  20  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 difference analysis 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 . Lines connecting treatments indicate that there 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 the b i r d s i n these treatments. 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 top group of d i f f e r e n c e s i s m e a s u r e d by t h e number o f b o u t s u n t i l b i r d s f o u n d 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 o f b o u t s u n t i l b i r d s v i s i t e d the 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 o t t o m g r o u p shows t h e number o f b o u t s 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 feeding bout. T r e a t m e n t a c r o n y m s 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 = u n c u e d ) and d u r a t i o n o f e x p o s u r e b e f o r e t h e f e e d e r s w i t c h (S = s h o r t , M = medium a n d L = long). 127  Spatial  Association  S e c t i o n IV.  These  experiments  hummingbirds even  when  Brown  cues  and  are  cue  more site  (Milner  and S c h r i e r , The  et al.,  associations  from  and  reward  This  evidence  feeders  less site  well  that  accurately  (Brown,  Hummingbirds  slowly  Brown's f i n d i n g s . studies  displaced  and  further  spatial  1993).  Memory  Discussion  provide  learn  Gass,  associations between  easily  and Spatial  1994;  learn  spatial  the  distance  as  increases,  corroborating  i s s i m i l a r to the r e s u l t s of o t h e r 1979;  P i n e l et al.,  1986;  Stollnitz  1962).  birds  responded  similarly  to  a l l treatments  but  t h e i r speed of l e a r n i n g and peak performance v a r i e d between treatments.  The b i r d s i n a l l treatments showed g r a d u a l and  continual  improvement  asymptote  that  was  i n performance  less  lack  of p e r f e c t i o n was  been  sampling t o detect  search  for survival  until  than p e r f e c t . due  to e r r o r s ,  changes  they reached  While birds  some of t h i s also  may  i n the environment  requirements beyond  pure  Forkman,  1991;  C o l l i a s and C o l l i a s , Gass,  1985;  Kramer and  1974; W i l k i e and Spetch, 1980; W i l k i e Treatments switch  in  d i f f e r e d strongly  feeder  1968;  to  calories,  as  profitability.  experience of s t a t i c p a t t e r n s  et al.,  in birds' While  and d i s t a n c e  128  Carroll  Draulans,  Weary,  have  and  documented by s e v e r a l authors (Brown and Cook, 1986; and Moore, 1993;  an  1991;  1988; Smith,  1981). responses t o a  both  duration  of  between cues  and  Spatial feeders cues  produced  and  feeders  affected  This distance  increasing  learning  increasing  separation  behavioural  and  difficulty  persistence  other authors have  The  persistence  although  standard  of  increase Kamil  relationship  previously  faster with close  associative  from  tasks  still cues  rapidly  learning  required to t h e i r  by  cue and response  between  successful  cues,  most  trial  position  the use of long  Nadel and w i l i n e r ,  unique  (memories  strongly,  rewarding learn  working that  are  at the end of the task) t o  speed and e f f i c i e n c y i n t h e i r tasks 1975).  which  the use o f s p a t i a l associated  using  l a i d down and d i s c a r d e d  and Mauldin,  require  et a l . , 1963;  Previous s t u d i e s have suggested that animals  associative  quickly  (Brown,  w i t h the r e s u l t s o f Chapter 2.  treatment  to orient  memory  seen f o r  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  this  feeders.  The of  hummingbirds learned  encouraged  memory  1962) .  more  w i t h the  between cues and reward s i t e s  behaviour i s c o n s i s t e n t Association,  between  relationship i s consistent  and S c h r i e r ,  experience  Memory  separations  Davis, 1974; P i n e l et a l . , 1986; S c h r i e r  Stollnitz  Spatial  memory  term memory  (Goelet  (Barnes, 1988; tasks  seem t o  et a l . , 1986;  1980}.  Cue  Distance  The  uncued treatments most c l o s e l y correspond t o a pure  s p a t i a l memory task. and  and Spatial  significant effects,  strongly.  1994;  Association  I t seems l i k e l y that b i r d s i n t h e near  f a r cue treatments are l e a r n i n g both an a s s o c i a t i v e 129  task  Spatial and  a s p a t i a l memory one.  task the  (uncued  treatment)  Spatial  Memory  Birds learned  the  spatial  memory  than  a s s o c i a t i v e l e a r n i n g component Performance  between  two  these  locate the  the  the  account  animals  which  intermediate  is  (Cheng, 1986 Spelke,  arithmetic  model  landmarks to t h e i r Spetch  LEDs t o p o i n t simplest the  will  as  to  definite  Hermer and  1990;  spatial  level  of  cues o r landmarks  feeder) a  landmarks  use  also acts  associated There  the  were  to  towards  (close  treatment  greater  difficult  b i r d s t o r e l y more on  task  cue  there  their  biased  the  far  while  them more  task  of  the  feeder,  a  cues  fell  to  help  distance  use  and  cue  from  probably  memory.  This  performance  on  may this  treatments.  How LED,  made  for  set of  in  extremes;  rewarding  rewards  biased  a  cue  to  locate  of  objects  this  and  Cheng and  1989;  vector  Thompson  strategy.  i n navigation  and  to  addition  I f the the  t o go  (1994)  reward  Wall, site  clear.  the  use  simple from  (Cheng,  b i r d s l e a r n t o use rewarding to the  studies  1993;  apply  of 1984;  distances  feeder,  feeder  that  Cheng,  the the  nearest  hummingbirds  show t h a t  n e a r l a n d m a r k s o v e r a l m o s t any  Vander  not  Gallistel,  of  showed  Several  (Bennett,  of i t s  i t appears that a  to the d i r e c t i o n of  option  landmark  still  r e l a t e d l o c a t i o n s does not  t o use  1987b;  is  component  r u l e t o l e a r n m i g h t be  use  profitability  geometric  et a l . , 1992).  l i t LED.  ( i n t h i s case the l i t  the  1994), a l t h o u g h  prefer  al.,  and  slower  treatment) .  to  Association  other 1989;  landmark Cheng  et  1982).  The  may  calculated metrically  130  be  distance  animals  between  Spatial (Cheng,  1990;  Gallistel,  Association 1989)  or  and Spatial by  the  size  landmark's r e t i n a l image ( C o l l e t t et a l . , 1992; Srinivasan  et a l . , 1989)  to  in  apply  limited  although the cases  p r i m a r i l y i n invertebrates The  more  relationship reward case,  site where  a  and  simple  feeder nearest  the  Gould,  1987;  et  al.,  1987b),  and  of  developing  a  vector  d i r e c t i o n ) between a landmark but  rule  cue  the  l a t t e r measure seems  (Cheng  task  i s possible,  of  such as honeybees.  complex  (distance  Memory  may  of  will  not  be  thumb  necessary  such  suffice.  as  in  going  Certainly,  and this  to  the  i f a more  complex r e l a t i o n s h i p than the one  i n t h i s experiment o c c u r s ,  hummingbirds  Brown  can  learn  hummingbirds can closest  to  the  it.  l e a r n to go l i t LED.  G.  (1992)  showed  that  to a feeder o t h e r than the  Similarly,  in  Thompson's  one  (1994)  experiments, hummingbirds used geometric r e l a t i o n s h i p s among cues and  response s i t e s to o b t a i n a reward.  Birds feeder cue  persisted  longer  in visiting  the  formerly  ( a f t e r a switch of both p r o f i t a b i l i t y and  was  further  relying  more  from  on  the  spatial  feeder. memory  This respond  cue)  suggests less  spatial  Although  association  birds  using  learning the  (Roberts  close  i n d i c a t o r s of a change, those u s i n g uncued p a n e l had the new panels  cue  panel  to r e l y t o t a l l y on t r i a l and  to  transfer 131  animals to  components  al. , had  1988). visible  s p a t i a l memory w i t h  l o c a t i o n of the rewarding feeder. simply had  et  i f the  rapidly  change than those r e l y i n g more on the a s s o c i a t i v e of  good  e r r o r to  B i r d s on the  the  learn cued  their spatial association  to  Spatial the new cue p o s i t i o n and  they  d i d this  Association  and Spatial  i n s t e a d of modifying more q u i c k l y  Memory  a c o g n i t i v e map,  when  cues  were  close to  over  time  with  a  feeders. D u r a t i o n o f Exposure As  birds  feeder  gained  position,  treatments.  experience  their  performance  improved  By the end of the 300 minute  stable in a l l  exposure  time,  b i r d s were performing w e l l above n i n e t y percent accuracy, on average,  on a l l 3 panels.  T h i s suggests  environment, b i r d s perform  sufficient  surroundings. of  exposure  though  t o an environment  association, task  paid  experience  in  memory  the e f f o r t  dividends  of course,  more  slowly  required to learn  in a  they have  utilizing  relatively  time. than  a spatial  short  their  t h a t 5 hours  i s not a long  developed  stable  memory as  but o n l y a f t e r  I t should be noted,  spatial  in a  as w e l l u s i n g s p a t i a l  with s p a t i a l association learning, gained  that  time  Even spatial memory  i n this  experiment. Advantages and Disadvantages Spatial longer  intervals  stimulus  (Brown  especially speed  those  of l e a r n i n g  advantage rather  memory use corresponds  of  than  before and using  a  responding  Cook,  a  spatial  after  1986),  working  a task  learning  t o slower  (Kamil  can i n c r e a s e the  contiguous  relationship  a  associations,  and Mauldin,  simple,  132  encountering  while  memory,  l e a r n i n g and  seems  1975) .  The  association especially  Spatial important a  i n short  long  term  relying  on  term tasks  task  or  spatial  associative  Association  a  learning.  Memory-  or v a r i a b l e environments.  stable  memory  and Spatial  environment,  can approach  In  performance  that  relying  A s i m i l a r r e l a t i o n s h i p should  on  exist  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 learning  with  spatial  learning  should  memory,  yield  high  so t h a t  a l l three  modes o f  l e v e l s of performance  i n stable  environments. Associations to  between cues and rewards need n o t be  p a r t i c u l a r points  learned  i n space.  an a s s o c i a t i o n  between  As  a  result,  cue and r e w a r d  birds could  tied who apply  t h i s r e l a t i o n s h i p when b o t h c u e a n d p r o f i t a b l e f e e d e r  moved.  This  or the  portability  spatial  of e i t h e r  associations  learning  advantage  contiguous  i n my in  experiment  environments  r e d u n d a n c y t h a t makes p o r t a b i l i t y In tasks learn the  that  only  this  various  necessary  allow  provides with  association,  geometric  learning,  smaller  improve  performance,  consistent  mapping.  In  and  because  t h e two i s e a s i e r  to learn items  association  than t o other 133  site  the  spatial  to define  than f o r  site.  Gestalt principles of spatial  c l o s e r t o each other  needs t o  between cue and r e s p o n s e  perhaps  of  valuable.  other  spatial  w h i c h s u g g e s t 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 are  strong  kind  and i s not r e q u i r e d  relationships  separations  between  with  the  of associations  more d i s t a n t p a i r i n g s o f c u e a n d r e s p o n s e is  a  associative learning, the b i r d  for spatial  relationship  associations  This  idea  proximity,  as s e t s  i f they  neighbouring  stimuli  Spatial  Association  and Spatial  (Pomerantz, 1981; Wertheimer, 1950). near  landmarks  t o navigate  Memory  Animals p r e f e r  (Bennett,  t o use  1993; Cheng,  1989;  Cheng et al., 1987b; Vander Wall, 1982), perhaps f o r s i m i l a r reasons. If  speed of l e a r n i n g  associative  learning,  susceptibility on  on  is  studies  learning  susceptible  animal  and t e s t i n g , can  intertrial  respond  up  i n rats  and  learning  and other  As w e l l ,  o r merely (Kamil  able  periods,  extinguished  (Barnes,  1988).  during  to  animals  and  (Olton,  associative  learning  i s a significant  the response,  environments.  always  intertrial  isi t s  perhaps due t o i t s r e l i a n c e  between  between periods  Mauldin,  p e r i o d s may be s u f f i c i e n t  laboratory not  i t s disadvantages  t o decay when there  the stimulus  training  are  t o speed  Z e n t a l l et a l . , 1990).  between  in  of  have .documented the e f f e c t s of i n t e r f e r e n c e  associative  1985;  one  to interference,  working- memory  Several  and p o r t a b i l i t y a r e advantages of  initial when the  1975) .  t o reduce  so that  between  the learned  non-rewarding  animals  trial  association  intertrials  Long  performance  One p o s s i b i l i t y i s that discriminate  delay  and  may be  (Hoffman and  Maki, 1986; Maki, 1979). In seems  contrast resistant,  interference,  to associative if  not  presumably  learning,  immune,  due  to  to  spatial these  the storage  memory  forms of  spatial  r e l a t i o n s h i p s i n long term memory (Maki et a l . , 1979) . immunity  to  interference  may  also  provide  a  of  way  This to  d i s t i n g u i s h between the use of c o g n i t i v e maps by animals and 134  Spatial lists  of  separate  Association  locations.  interference,  as demonstrated  (Crystal  Shettleworth,  spatial  and lists  spatial  Lists  As  a  are  subject  w i t h black-capped 1994).  This  suggests an advantage  lists.  and Spatial Memory-  result  to  chickadees  shortcoming  of  of c o g n i t i v e maps over of  the  resistance  to  i n t e r f e r e n c e , animals u s i n g s p a t i a l memory a r e a b l e t o l e a r n conflicting all  tasks i n d i f f e r e n t  contexts and perform w e l l i n  o f them (Beatty and S h a v a l i a , 1980; Maki et a l . , In  1992;  previous studies Brown,  of s p a t i a l  1994; Brown and Gass,  association  1979).  (G. Brown,  1993; Thompson,  1994),  b i r d s showed no a p p r e c i a b l e d e c l i n e i n performance o v e r n i g h t i n m u l t i - d a y experiments. suffer  less  simple  associative  hummingbirds t h i s time  from  Perhaps s p a t i a l a s s o c i a t i o n t a s k s  temporal  declines  learning,  are r e s i s t a n t  i n performance  although  t o any form  i t may  than  be  that  of f o r g e t t i n g  over  frame.  S p a t i a l memories can be maintained f o r l o n g p e r i o d s of time.  Storing  duration Kamil,  birds  of a winter  can remember o r longer  cache  (Balda,  1989 and 1992; Healy and Krebs,  Shettleworth,  1983).  Non-storing  Healy  Menzel,  and Krebs,  1991) .  1980; Balda  animals  also  al.,  1987).  and  seem  to  (Balda and Kamil,  1992; Hitchcock and Sherry, 1990;  In the l a b o r a t o r y ,  rats  have  s p a t i a l t a s k s t e n months a f t e r t r a i n i n g and t e s t i n g et  f o r the  1992; Sherry, 1984;  r e t a i n s p a t i a l i n f o r m a t i o n f o r a long time 1992;  sites  performed (Bierley  Hummingbirds and other s p e c i e s r e t u r n t o the  135  Spatial same b r e e d i n g Colwell, One due  spatial  There a r e v a r i o u s  places 1993;  (Cole et al., 1982;  1979) .  longer  Due t o t h e i r  maps a r e r e s i s t a n t  i n inappropriate  no  Memory  of the main disadvantages of s p a t i a l memory i s a l s o  t o i t s long term nature.  result  and Spatial  and f e e d i n g s i t e s a n n u a l l y  1974; Gass, 1985; Roberts,  term memory,  are  Association  behaviour  i n long  t o change and may  i n the face  of change.  examples of animals dodging b a r r i e r s t h a t  present  o r searching  t h a t a r e no longer c o r r e c t Gallistel,  storage  f o r food  (Collett  1989; Kamil and Balda,  or nests i n  et al., 1986 and  1985; Speakman and  O'Keefe, 1989; Spetch et a l . , 1992; Sutherland  and Gass, i n  press) . The  p e r s i s t e n c e of b i r d s 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  r a p i d l y become i n a p p r o p r i a t e .  purely loss  While  on cue a s s o c i a t i o n s are s u b j e c t  of r e c a l l  1975),  after  even short  the p o r t a b i l i t y  of t h e i r  animals  relying  t o i n t e r f e r e n c e and  delays  (Kamil  and Mauldin,  a s s o c i a t i o n allows  them t o  respond r a p i d l y t o changes i n t h e i r environment, as l o n g as those  changes don't a f f e c t  reward. spatial  the r e l a t i o n s h i p between cue and  A l l of the treatments memory,  although  i n my  required  the i n c r e a s i n g importance  associative  component of the task  treatments  decreased  feeders  experiments  persistence  of the  i n the f a r and c l o s e cue at  formerly  rewarding  s i n c e b i r d s c o u l d use the same l e a r n e d a s s o c i a t i o n  between cue and reward f o r the new feeder  136  location.  Spatial Change memory,  can  cause  b u t some  change  by  These  temporal  Association  problems  animals  remembering maps  pattern  have  been  and  1989; O l t o n ,  of  1990).  Perhaps  encounter.  cannot  and  work  association evidence  in  banner (Gori,  benefit  i n spatial  a r e many  spatial  to  may  natural  does  G. Brown  prey (1992)  lists  In  learning  (Spetch of  and the  including  1983; other  they  there i s map  of the  well  Honig,  as  1988).  interaction  of  u s e o f marks  on  o f f l o w e r s by  Rabenold,  of  spatial  as  vultures  examples  that  fact,  associative  nectar quality  (Houston,  can a l s o  as  a. w o r k i n g  1989), a n d t h e u s e o f c i r c l i n g  locate  other,  environment,  learning  Krebs  such as m i g r a t o r y  n o t mean  c a n do.  examples  t o assess  daily  disadvantages  each  memory  and a s s o c i a t i o n petals  with they  i n a stable  surroundings  There  concert  for  animals  and  learning  demonstrates  that  functioning  advantages  spatial  changes.  ( B i e b a c h e t al., 1989;  species  associative  environmental  documented  t e m p o r a l maps f o r s e a s o n a l change,  differing  spatial  temporal  develop  The  using  to regular  the  i n t h e environment  Biebach,  f o r animals  respond  fluctuations  and Spatial Memory-  bees  by p r e d a t o r s  1983  and  including  1987). social  transmission of foraging information.  Memory Load Maintaining heavy l o a d  both  spatial  and  temporal  on t h e memory c a p a c i t y o f a n i m a l s .  of hummingbird  foraging  suggest  137  that  maps  places  Energy  a  models  i n some c a s e s t h e c o s t s  Spatial of  long  the  t e r m memory  benefits  (and  revisits  emptied  to  individual  use  that  working  visitations  within  deficiencies.  foraging  i n given  has  individual 1986) . reducing  This  would  the  found  working  of  the patch  that  then  suggest  that  the  little  rats  of have  bouts  rather  (Mellgren  to  memory  during  boundaries  birds  visits  i n f a c t be e v i d e n c e  i s another  way  to  reduce  (Capelli  process of generalizing the features what  leads  experimental the o v e r a l l  to  high  protocols.  of  that than  and  an the  Roper,  animals  are  t h e memory  load  e t al. , 1986).  This  of t h e environment  may  revisitation The e x p e r i m e n t a l  rates  under  some  animal stores  only  f e a t u r e s o f t h e environment r a t h e r than t h e f i n e  details  Nishimura learning  continuing  and suggested  imposed by c o g n i t i v e mapping  grained  1985)  memory l o a d b y c h u n k i n g .  Chunking  be  experiments  that  Revisitations  outweigh  I n my  remember  a  Memory  may  (1988), a l s o  the patch  components  to  retained  p a t c h e s may  learned  1987).  memory  patches,  similar  environments  suggests  Roberts  pigeons  and Spatial  Sutherland,  feeders  locations.  evidence  animal  e t al.,  f o r instance  to  neglected  of foraging  (Armstrong  others,  Association  ( G a s s , 1985). (1994)  are tightly the  suggested tied  If  advantages  o f l e a r n i n g a r e soon  has  a  advantages  capacity  limited  lost.  a r e depressed,  remember more i n f o r m a t i o n  the  t o t h e memory  animal.  t r u e when r e s o u r c e s  animal  that  so t h a t  the  i s especially  the animal  f o r each p o t e n t i a l reward. 138  of the  capacity,  This  of  must  Memory  Spatial  load  and  Spatial  Memory  seems t o be a s i g n i f i c a n t problem f o r animals  situations, a  Association  so that  prolonged  task  i n some  they modify t h e i r memory use throughout  i n response  to t h i s  load  et  (Cook  al.,  1985) . Conclusions These can  experiments  learn  both  associations, combination Hummingbirds than  tasks  high  spatial  f o r which of  spatial  learn that  memory  I believe memory  tasks  solely  and  learning  performance association The pattern  period,  levels  behaviour. influence  birds  comparable  of experience  a f f e c t s the p e r s i s t e n c e  resist  I used  the  has changed.  more  those  rapidly  achieving  time  required  a  learning.  interval.  a  eventually  to  changing  with  slightly achieved  for  spatial  a  specific  rewarding  of the b i r d s ' behaviour once  Generally,  of s t a b i l i t y b e f o r e a p a t t e r n will  requires  associative tasks  spatial  tasks.  amount  pattern  and  on s p a t i a l memory,  t h e s p a t i a l memory tasks  longer  hummingbirds  the l a t t e r  spatial association  rely  that  l e v e l s of performance a f t e r a very short  While  the  have demonstrated  the longer  the p e r i o d  the longer  t h e animal  switch,  i t s previously  successful  foraging  The e f f e c t of exposure time appears t o have l e s s on s p a t i a l a s s o c i a t i o n  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 a s s o c i a t i o n between  a cue and reward s i t e  i s strongly 139  dependent on the s p a t i a l  Spatial separation  Association  o f the two s i t e s .  speed o f l e a r n i n g , and tend spatial  memory  and  Greater to result  greater  and Spatial Memoryseparations  slow the  i n more r e l i a n c e on  persistence  i n the  face  of  change. Greater  s e p a r a t i o n s between cue and reward and l o n g e r  periods  o f exposure  favour  spatial  a s s o c i a t i o n , while  the use of s p a t i a l the opposite  memory  i s true  c l o s e t o the reward and short p e r i o d s of exposure.  140  over  f o r cues  Chapter 5  General  Various Rescorla basic  questions  and H o l l a n d  ones:  learning  What  revealed  three questions learning.  Discussion  a r i s e out o f s t u d i e s  like  (1982)  down  narrowed  conditions  them  produce  i n performance?  mine, but to  learning?  What  three  How i s  i s learned?  All  d e a l w i t h e x t e r n a l f a c t o r s and t h e i r r o l e i n  I will  address the f i r s t  then expand the t h i r d  t o ask:  two q u e s t i o n s  briefly,  What do animals l e a r n about  t h e i r environments and how do they l e a r n i t ? What C o n d i t i o n s Produce In  these  relationships  Learning?  studies,  the  among f e a t u r e s of t h e i r  under a v a r i e t y of c o n d i t i o n s . use  of visual  motivation  birds  and a u d i t o r y  of the b i r d s  learned  foraging  environments  Learning was promoted by the  cues  t o feed.  and landmarks  and by the  In a l l experiments the  b i r d s were p r o v i d e d w i t h v i s u a l cues t o feeder the  form  revealed  of  nothing  experiments this  orange  about  described  information,  rings  surrounding  their  i n chapter  so b i r d s  spatial  the  locations i n feeders  profitability. 2,  feeders  had t o l e a r n  that  In  offered  the p a t t e r n  the only of  rewarding and non-rewarding feeders u s i n g p o s i t i o n only, as 141  General in  the  experiments  press).  Most  additional cases  experiment  LED  Aside  also  form of  included  chapter  i n chapter  Gass 3  In  information  4 they  (in  provided  landmarks.  In 6 of the  the  the  various  main  of  the  cues,  some  about  the  9 treatments o f  the  could  use  importance  of  landmarks  spatially  and  condition  that  led  birds  feed  frequently  to  expectancy of reward from a r r a y the  in  and  cues to rewarding f e e d e r s .  from  motivation  Sutherland  described  of f e e d e r s .  described  in  i n the  landmarks  profitability  feeders,  treatments  information  these  separated  described  Discussion  each  of  to  feeders.  these  arrays  learning and  I will  factors  as  of was  their  deal  part  with  of  my  c o n s i d e r a t i o n of what i s learned. How  i s L e a r n i n g Revealed i n Performance? In  these  experiments  through t h e i r this to  improving  performance o n l y feeders  in  trials  the  birds  performance over time. through two because  measures of  birds  l o c a t i o n s even a f t e r d e p l e t i n g them. to  avoid  revisiting  depleted  l e a r n e d rewarding regions individual first  rewarding  visits  demonstrated  learning  I  reported  first  continued  to  visits revisit  T h e i r f a i l u r e to l e a r n  feeders  suggests  that  they  of the a r r a y r a t h e r than l e a r n i n g  feeder  locations.  to locations i n t r i a l s ,  I n d i c a t e d by  their  the b i r d s showed r a p i d  p r o g r e s s i o n t o r a t e s of f e e d i n g w e l l above chance, r e v e a l i n g that  they  had  begun  to  learn  the  locations  of  rewarding  f e e d e r s w i t h i n f i v e minutes of exposure to the a r r a y s 142  (five  General trials).  Five  minutes  of  exposure  f o r a g i n g o p p o r t u n i t i e s and  excludes  they  or  were  unable  to  see  here  refers  intertrial  visit  i n t e g r a t e i n f o r m a t i o n from previous  the  visiting  feeders  demonstrated  which  had  array  their  been  the number of i n c o r r e c t v i s i t s  related  to  the  following  duration  of  the  could  In t h i s  case,  persistence were  measured by  the  magnitude of t h e i r  but  The  immediately  but  of l e a r n i n g when t h e i r  rewarding.  trials  actual  p e r i o d s when  performance dropped a f t e r p a t t e r n r e v e r s a l s . performance  to  visits.  The b i r d s a l s o p r o v i d e d evidence  decreased  Discussion  no  in  longer  drop i n performance,  they made i n the  r e v e r s a l , was  exposure  to  as  the  positively  pattern  before  switch.  What i s Learned about t h e i r Environments and How? Pattern These  Learning  experiments  hummingbirds  rapidly  p a t t e r n s of f e e d e r s . a  two  dimensional  reinforced earlier learn  both  one  and  While t h i s work was  array  of  feeders  conclusions two  that  dimensional  based p r i m a r i l y on  divided  simply  into  4  q u a r t e r s , hummingbirds learned more complex p a t t e r n s i n past work  (Sutherland  and  Gass,  i n press) .  In my  studies,  o n l y d i d the b i r d s l e a r n the p a t t e r n s of rewarding but  a l s o s e v e r a l kinds of landmarks and  the  l o c a t i o n of rewarding  feeders.  feeders  cues t h a t  not  feeders, signalled  or demarcated patches  of  They d i d t h i s u s i n g both s p a t i a l memory and memory  of s p a t i a l a s s o c i a t i o n s . 143  General  Discussion  Chunking I f the b i r d s l e a r n e d the p a t t e r n of feeders r a t h e r than individual is  they were e x h i b i t i n g  t h e p r o c e s s o f grouping  mental in  locations,  unit  (Olton,  stimuli  1985).  together i n t o  Chunking  1984 and 1986; M i l l e r ,  to  s u b s t a n t i a t e because  separately them  into  animal a group  results  while s t i l l  structure  this  ( C a p a l d i e et  although i t i s d i f f i c u l t  very  a l l of  the  similar  provide  stimuli  t o chunking  i n press) .  to d i s t i n g u i s h i n d i v i d u a l  demonstrating  may  single  animals  (Sutherland and Gass,  l o s e s the a b i l i t y  a  demonstrated  remembering  c o u l d produce units  1956),  which  has been  s t u d i e s w i t h humans and l a b o r a t o r y  al.,  chunking,  I f an items i n  knowledge of the grouped  evidence  f o r chunking  o f the  separate items i n t o an o v e r a l l p a t t e r n (Olton et a i . , Animals perception  appear  t o chunk items  of r e l a t i o n s h i p s  Hummingbirds  may  be  together based  on t h e i r  of v a r i o u s kinds between  chunking  an  tendency  to  revisit  i n d i v i d u a l feeders, t o make most e r r o r s on the edges groups-  and  to perform  better  f e e d e r s a r e marked w i t h edge landmarks, are  learning  a  pattern  of  indirect  demonstrated  and  still  144  feeders  feeders.  inconclusive,  i t consistently.  when  a l l argue  rewarding  r a t h e r than l e a r n i n g the i n d i v i d u a l is  Their  into  p a t t e r n i n my  feeder  studies.  feeders  them.  overall  of  array  individual  1980).  rewarding that  they  (chunking)  T h i s evidence  although  birds  General One was  of  the  more prominent  results  from  Discussion  these  studies  t h a t the b i r d s d i d not l e a r n to a v o i d r e v i s i t i n g  feeder  locations.  overall  pattern  revisitation also  of  rates  observed  a  While  they  effectively  feeders,  they  showed no  during  high  experiments.  rate  of  feeder  improvement  i n h i s work on p a t t e r n  species  similar  found  in  continuing  marsh t i t s ,  and  arrays,  Roberts  to  learned  the  improvement  in  Sutherland  (1985)  revisitation  learning with  Shettleworth  revisitation  emptied  and  emptied  (1988) found no  and  this  Krebs  cache  evidence  no same  (1982)  sites  in  f o r use  of  working s p a t i a l memory t o a v o i d w i t h i n p a t c h r e v i s i t a t i o n  by  pigeons. In a m o d e l l i n g a different  result  study,  Armstrong et al.  than t h i s ,  suggesting  (1987) p r e d i c t e d  that  term memory by hummingbirds to a v o i d flower  use  of  revisits  short during  f o r a g i n g bouts i n patches would be e n e r g e t i c a l l y b e n e f i c i a l . Brown  (1987) found t h a t pigeons c o u l d  i n t e g r a t e a group  elements i n t o a u n i f i e d p a t t e r n i f they were t r a i n e d on separate  elements, but  group of  items,  items  to  use  explanation  birds  by  chunked  separate  continuing  despite  feeders  dissociate individual  et into  One  revisitation  the  Armstrong  elements. in  theoretical al. s models, 1  patterns  feeders.  145  my  energy i s that  they  were  the  a compound  were unable to d i s s o c i a t e the  the  for  Sutherland's, suggested  they  i f they were t r a i n e d w i t h  of  grouped possible  study  and  benefits once unable  the to  General  Discussion  S p a t i a l Memory In  chapter  4,  I demonstrated  that  hummingbirds  learn  l o c a t i o n s of rewarding feeders f a s t e r when the p r o f i t a b i l i t y of the i n d i v i d u a l feeders i s cued. b i r d s had t o r e l y  In the uncued treatments  o n l y on s p a t i a l memory alone r a t h e r  u s i n g a s p a t i a l a s s o c i a t i o n between, feeder and reward Since this  birds may  learned  suggest  more s l o w l y i n the uncued  that  spatial  memory  however,  spatial  learning  memory  or distractions  is  a  longer  At t h e same time,  resistant  (Maki  cues.  treatments,  requires  l e a r n i n g p e r i o d than s p a t i a l a s s o c i a t i o n .  than  to  interference  et a l . , 1979).  Thus, i t  seems that items s t o r e d i n s p a t i a l memory by b i r d s a r e those to  be  remembered  described  commit  importance  been noted Kesner,  term,  and  the  experiment  i n chapter 2 suggests the time course over  hummingbirds The  i n the long  spatial  p a t t e r n s t o l o n g term  of long term memory t o s p a t i a l  i n several  studies  memory.  l e a r n i n g has  (Beatty and S h a v a l i a ,  1980; Nadel and W i l l n e r ,  which  1980;  1980).  C o g n i t i v e Maps The these  experiments  evidence dead  evidence that  hummingbirds  i s based  f o r chunking  used  on v i s i t a t i o n  d i s c u s s e d above.  cognitive  maps i n  p a t t e r n s and the I f the b i r d s  were  reckoning, they should show s t e r e o t y p e d approaches  the a r r a y and regimented sequences feeding.  to  of v i s i t s once they began  Such systematic p a t t e r n s of f e e d i n g have been seen  i n i n s e c t s such as bumblebees, e u g l o s s i n e bees and hawkmoths 146  General (Dreisig,  1989;  advanced  Pyke  animals  (Kamil,  1978;  and  such  Pyke,  Cartar,  as  and  complex  using  more  (Sutherland,  1985).  I  i n any  of  (1987) suggested  the  that  advantages  found  in  well  previous  as  more  and  bats  studies  with  patterns  no  evidence  experiments  the a b i l i t y  s i t e s i n a c o g n i t i v e map  as  nectar-feeding birds  1978)  hummingbirds  foraging  1992)  Discussion  I  of of  feeders  systematic  conducted.  of animals  w i t h equal ease was  Scholl  t o access a l l one of i t s main  over dead reckoning, where the need t o f o l l o w  s e r i e s of memorized v e c t o r s makes some s i t e s more  a  difficult  to a c c e s s . Landmarks and Cues In the experiments that  they  spatial  can  and  than  areas.  lines joined or  to  disks  lines  have  perhaps help  to  enhance  landmarks areas  a  the  that  of  marking  their  the the  navigate  to  into  learn  squares,  centres  used  directions that  birds  inside  w h i l e o u t s i d e them  two  this  the  squares  rewarding .  147  more these that  The  of f e e d e r s were  the p o s s i b l e  ( i n s i d e the other two  of  additional  feeders.  c o u l d d e r i v e from of  of  component  rewarding  so a s i d e from  learning  a r r a y were  directional birds  demonstrated  differentiated  that marked edges of rewarding groups  up-down  could  circular  lack,  information  Edge  non-rewarding  Since  circles  landmarks  patterns.  rewarding useful  use  of chapter 3, the b i r d s  left-right them,  was  squares)  they  rewarding, was  non-  General  the  The b i r d s  in all  feeders.  In  surrounding they  may  orange  o r may  o f my e x p e r i m e n t s u s e d c u e s t o l o c a t e a l l the  rings  array  as cues  n o t have  used  treatments  rewarding feeders.  they used c o l o u r t o i d e n t i f y the array.  as  information.  o f c h a p t e r 4.  when  cues  also  found  o f f e e d e r s on  birds  used  (G. Brown,  have  1992;  and l i g h t s  cues  when  to exploit  aspect  1980;  may  in  Ellen  1986;  the  suggested  Miller  have  visual  1993;  used  cues  first  the array.  Distal  development  of  148  that  cues  evidence that the  were  Gallistel,  e t al. , 1984;  was  increases the  but I b e l i e v e  they  e t a l . , 1984;  which  1962).  also  themselves v i a e x t e r n a l  global  maps  birds  cues  higher  Brown a n d G a s s ,  I h a v e no d i r e c t  to the walls  Roper,  that  feeder,  between cue and reward  experiments  oriented  (Ellen,  to the rewarding  to the array.  important  P e r f o r m a n c e was  1986; S t o l l n i t z a n d S c h r i e r ,  my  cognitive  and  separation  these  the a d d i t i o n of reward  i n previous studies  et a l . ,  distance  The b e n e f i t s o f p r o v i d i n g  w e r e more a p p a r e n t i n t h e e x p e r i m e n t s  closer  difficulty  external  s e p a r a t e d LEDs t o  rewarding groups  improved performance.  were  increasing  In  In the  o f c h a p t e r 3,  In these studies,  significantly  Pinel  that  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  to profitability  learning  had  In the studies  i n c r e m e n t a l v a l u e was n o t l a r g e . cues  they  to feeder locations  chapter 4 experiments they used s p a t i a l l y identify  Discussion  such as  that  developing cues  a r e an  cognitive 1989;  Morris,  they  maps  Mellgren  1981;  Spetch  General and  Edwards,  Dyck, not  1988;  1984;  Suzuki  accept  spatial  Spetch  the  and  Honig,  Sutherland  and  Even an  author who  did  mapping  suggested  that  response to d i s t a l  cues  et al. , 1980).  idea  l e a r n i n g was  of  cognitive  a conditioned  1988;  Discussion  ( R e s t l e , 1957) . Expectancy and By  showing  patterns shifts  of  Persistence  that  birds  foraging  that  make  in  this  persist  the  face  behaviour  in of  formerly sudden  profitable  environmental  unprofitable,  a l l of  experiments demonstrated that b i r d s ' e x p e c t a t i o n s d i s t r i b u t i o n of rewarding feeders was of  time  they  spent  pattern  increased,  at  formerly  the  using  that  pattern.  feeders  the  a f f e c t e d by the amount As  exposure  so d i d the b i r d s ' p e r s i s t e n c e rewarding  about  my  after  the  in  to  a  feeding  switch.  In  l a b o r a t o r y s t u d i e s , i t appears that the expectancy of reward is  directly  reward  tied  to  the  (Mellgren  et  a l . , 1973).  increasing (Morris  function  and  persistent  of  Capaldie, visitation  increased  only  slightly  exposure t r i a l s ,  past  the  frequency  to  the  a  large  Persistence  at  2  of  unprofitable  change  from  numbers of t r i a l s  149  of an  trials  profitable  that  feeders  10  to  with  20 the  too l i m i t e d i n time to  persistence feeders  also  shows  presumably because b i r d s ' success  degree  over i n t e r m e d i a t e  is  rewarding  Chapter  d i s t r i b u t i o n of rewarding feeders was induce  of  formerly  with  magnitude  Expectancy  number  1979).  and  after  then before  the  switch.  increased  rapidly  plateauing  after  General an  exposure p e r i o d  o f a b o u t 40  trials.  stopped i n c r e a s i n g because there experience that result  was  i s stored  predicted  hypothesis  of  a  by  l i m i t a t i o n s on  et  1987;  al.,  1989)  Houston,  type  of the  window  memory  1987;  of  developed  memory  a n i m a l l e a r n i n g and  McNamara and  This  who  weighted  amount  to  (Kacelnik  McNamara  et  al.,  . The  of  and  authors,  persistence  to the  i n a b i r d ' s memory.  limited  explain  Possibly  is a limit  several  Discussion  birds  rewarding  i n a l l of feeders  my  experiments  after  the  relearned  pattern  had  patterns  been  reversed.  Although I introduced  a c o m p l e t e and  sudden r e v e r s a l  pattern  feeders,  was  change and  of  rewarding  i n the  repeated  variability with  reversals  i n stable food.  sampling  In  conservative reduce  the  environments  discounting (Bowers and  on  environments  but  birds  foragers.  (1992)  time  temporal studies  found  that  p r i o r experience some b i r d s  using  memory more,  where  change  is  of  the  subsequent  In f i e l d  is  profitability  one  enough  Learning  environments  behaviour  adopted were  based  likely on  a  more  effective  less  to  in to  memory  .  respond the  Valone  relied  a  Perhaps  would have p r o d u c e d  variable  ( N i s h i m u r a , 1994) Animals  feeders.  hummingbirds,  approach,  successful  still  t o make l e a r n i n g u n p r o f i t a b l e .  black-chinned  birds find  d i s t r i b u t i o n of  this  of  value  to of  unpredictable highly  Adams-Manson, 1993).  150  variation  unpredictable  by  resources  Temporal v a r i a b i l i t y  plays  General an  important  (Caraco,  role  i n foraging  choices  1982; Caraco and Lima,  Stephens,  1981).  tamarins,  f o r instance,  variance  Animals  o f food  diverse  respond  to  sources and adjust  Stephens  instability and  and  Paton,  increases,  focus  At  some  both  honeybees  and  the mean  and  foraging  point  As  short  of  choices  (Cartar, 1991; Garber,  1986).  their  species  et al. , 1988;  environmental  animals reduce extraneous  on maximizing  1991).  as  their  based on changing energy requirements 1988a;  f o r many  1987; Gibbon  as  Discussion  term  behaviours  gains  increasing  (Forkman,  environmental  i n s t a b i l i t y and u n p r e d i c t a b i l i t y , i n d i v i d u a l s should  abandon  a s t r a t e g y dependent on l e a r n i n g and memory because i t w i l l lose i t s energetic Future  advantage.  Studies  My  studies  further  left  exploration.  synthesize single  have  The  avenues  evidence  rather  i s strongly  than  learning  suggestive  open  that  the d i s t r i b u t i o n of rewarding  pattern  locations  several  that  hummingbirds  feeders  into  individual  but s t i l l  need  a  feeder  not c o n c l u s i v e .  B e t t e r ways t o d i s c r i m i n a t e between these two p o s s i b i l i t i e s are needed. Work by Brown (1987) might provide problem. elements that  He suggested  that  into a single unit  animals  an approach t o t h i s  who  or pattern  grouped could  l e a r n i n g back t o the i n d i v i d u a l elements;  a s e t of  not t r a n s f e r i n the case  of hummingbird s p a t i a l memory t h i s would mean t h a t once they 151  General have  learned  a  pattern  individual  they  memory  of  trained  t o u s e an a r r a y w i t h  rewarding cohesive should  locations.  and non-rewarding pattern  essentially If  The feeders  individual  At  rewards some  pattern,  locations,  in  birds  the  should  of a pattern  of rewarding  non-rewarding) c o u l d be  continuing abandon  continued  and growing of  deterioration  their  change  memory  of  expectations  t o e x p l o i t a t i o n of the array  of individual  reference The  locations  t o memory o f p a s t  ( i f they  based could)  either or  without  reversed  patterns,  t h 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 ,  reward  in  experiments  where  would begin sites  seen  animals  learn  152  t o resemble in  many  the  In  but t h i s  c h a n g e i f t h e r e v e r s a l s h a p p e n e d more t h a n o n c e .  shifts  on  o f e n v i r o n m e n t s c o u l d a l s o be  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  protocol  and  visits.  role of the s t a b i l i t y  experimental  the  feeders  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 .  might  drop  feeders.  r e l i a n c e o n memory o f r e w a r d b a s e d o n t h e p a t t e r n o f and  they  feeders.  a v a i l a b l e from t h e p r o f i t a b l e group  point  a  warning t o non-rewarding,  t o t h e p o i n t w h e r e t h e r e was a s i g n i f i c a n t in  learn  t o a s m a l l number o f r e w a r d  pieces  (by m a k i n g f e e d e r s  were  and i f they  and not j u s t  of small  hummingbirds  feeders,  surrounded by rewarding  removal  away t h e  but large pattern of  n o t change v i s i t p a t t e r n s  are s t i l l  throw  a simple  l o c a t i o n s t h a t a r e changed w i t h o u t but  Discussion  As this  constant  psychological  the association  between  General stimulus  and  irrespective  response of  spatial  and  apply  position.  Discussion  that  In  this  association spatial  e x 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 r u l e which they could Another  area  patterns  systematic  and  t h a t has and  1983;  Wolf  and  seems  s t u d i e s but  many q u e s t i o n s  detailed  revisitation  to  nectar  studies  contradict  the  The  examined. are  of  behind  by  1978;  Wolf  in  hummingbirds antisocial. communication  one  of  is  that  As  al.,  laboratory  this  One  arguments in  drawbacks  seem  they  to which  153  as  to  be  the  models  laboratory  working  Is  reduces  this  wild? with  rufous  territorial  l e a r n i n g and  explore,  show  to i n t e g r a t i o n  pattern?  highly  observational  difficult  environment,  are  to  such  need  r a i s e d by  to  of  animals.  studies  the  that  effect  foraging behaviour i n the the  item  and  difference  is  laboratory  1987)  I s r e v i s i t a t i o n due  a result, are  with  degree  locations into a non-dissociable  Finally,  1991),  nectar-feeding  et  animals  revisitation?  b e h a v i o u r a l s o seen i n  laboratory  sources  do  (Kamil,  remain unanswered.  energetic  why  work  Hainsworth,  the  random, The  compatible  (Armstrong  reasons  accurate,  feeder  be  r e s u l t s seen  I f the  continuing  and  contrast  is  methods.  regard  investigation is  Modelling  mine.  to  investigation to  search  far in this  intriguing  needs  further  restricted  b e e n done so  Hainsworth,  needs  i n natural habitats  area  associative  apply.  that  visitation  memory  especially the  and social in  a  general  General applicability date.  of  These two  the  results  from  1976;  Haefner and C r i s t ,  food-storing (Baker  birds  et  al. ,  such  and  Observational  learning  (Valone on  as  1988;  Shettleworth  adjuncts  studies  forms of l e a r n i n g p l a y a s i g n i f i c a n t  i n f o r a g i n g by more s o c i a l animals Galef,  hummingbird  Discussion  1994;  Rabenold, 1983)  nutcrackers,  Roberts,  Krebs,  (Bryant and Church,  1986;  and  1979; Vander  communication  jays  and  Sasvari, Wall, are  dealing  Girardeau, with  1993)  and  environmental  their ameliorating  uncertainty  deserve i n v e s t i g a t i o n .  154  and  role 1974;  and  by  others 1979; 1982).  important  to s p a t i a l memory and v i s u a l cues i n s o c i a l and  to  species effects  instability  Literature Cited  Aadland, Jan, W i l l i a m W. Beatty and Ruth H. Maki. 1985. S p a t i a l memory of c h i l d r e n and a d u l t s a s s e s s e d i n a r a d i a l maze. Developmental Psvchobiolocrv 18(2): 163 172 . Armstrong, Doug P. 1986. Some aspects of the economics of t e r r i t o r i a l i t y i n North American hummingbirds. M. Sc. thesis. U n i v e r s i t y of B r i t i s h Columbia, Vancouver. Armstrong, Doug P. 1987. Economics of t e r r i t o r i a l i t y i n male c a l l i o p e hummingbirds. 242 - 253.  breeding Auk 104:  Armstrong, Doug P., Clifton Lee Gass, and Glenn D. Sutherland. 1987. Should f o r a g e r s remember where they've been? E x p l o r a t i o n s of a s i m u l a t i o n model based on the behavior and energetics of territorial hummingbirds. In F o r a g i n g Behavior. A l a n C. Kamil, John R. Krebs and H. Ronald Pulliam, e d i t o r s . Plenum Press, New York. Aronsohn, S., 0. C a s t i l l o , and T. Pinto-Hamuy. Fading procedure effects on a visual d i s c r i m i n a t i o n r e v e r s a l i n the a l b i n o r a t . L e a r n i n g and Behavior 6 (1): 72 - 76.  1978. pattern Animal  Baker, Myron C h a r l e s , E r i c Stone, Ann E i l e e n M i l l e r Baker, Robert J . Sheldon, P a t r i c i a S k i l l i c o r n and Mark D. Mantych. 1988. Evidence against observational l e a r n i n g i n storage and recovery of seeds by b l a c k capped chickadees. Auk 105: 492 - 497. Balda, R u s s e l l P. 1980. Recovery of captive Nucifraga caryocatactes. T i e r p s v c h o l o g i e 52(4): 331 - 346.  cached seeds by a Zeitschrift fur  Balda, R u s s e l l P. and A l a n C. Kamil. 1988. The s p a t i a l memory of C l a r k ' s n u t c r a c k e r s [Nucifraga columbiana) i n an analogue of the r a d i a l arm maze. Animal L e a r n i n g and Behaviour 16(2): 116 - 122. Balda, R u s s e l l P. and A l a n C. Kamil. 1989. A comparative study of cache recovery by three c o r v i d species. Animal Behaviour 38: '486 - 495. Balda, R u s s e l l P. and A l a n C. Kamil. 1992. Long term spatial memory in Clark's nutcracker, Nucifraga columbiana. Animal Behaviour 44: 761 - 769. 155  B a l d a , R u s s e l l P., A l a n C. K a m i l a n d K r i s t i e G r i m . 1986. R e v i s i t s t o emptied cache s i t e s by C l a r k ' s n u t c r a c k e r s (Nucifraga columbiana). A n i m a l B e h a v i o u r 34: 1289 1298. B a r n e s , C. A. 1988. S p a t i a l l e a r n i n g a n d memory: The s e a r c h f o r n e u r o b i o l o g i c a l mechanisms i n r a t s . Trends i n N e u r o s c i e n c e s 11(4): 163 - 169. B e a t t y , W i l l i a m W. a n d D a v i d A. S h a v a l i a . 1980. Rat s p a t i a l memory: R e s i s t a n c e t o r e t r o a c t i v e i n t e r f e r e n c e at long retention intervals. Animal L e a r n i n g and B e h a v i o r 8 ( 4 ) : 550 - 552. B e e c h e r , M i c h a e l D. a n d P h i l i p K. S t o d d a r d . 1990. The r o l e of b i r d song and c a l l s i n individual recognition: Contrasting field and l a b o r a t o r y p e r s p e c t i v e s . In Comparative P e r c e p t i o n . Volume I I : Complex s i g n a l s . W i l l i a m C. S t e b b i n s a n d Mark A. B e r k l e y , e d i t o r s . John W i l e y and Sons, T o r o n t o . Benhamou, S i m o n . 1994. S p a t i a l memory a n d s e a r c h i n g efficiency. A n i m a l B e h a v i o u r 47(6): 1423 - 1433. B e n n e t t , A n d r e w T. D. 1993. S p a t i a l memory i n a f o o d storing corvid. J o u r n a l o f Comparative Physiology A 173 (2) : 193 - 207. B i e b a c h , H e r b e r t , M a r i j k e G o r d i j n a n d J o h n R. K r e b s . Time-and-place learning by garden w a r b l e r s , borin. A n i m a l B e h a v i o u r 37: 353-360.  1989. Sylvia  B i e d e r m a n , I r v i n g , A r n o l d L. G l a s s a n d E. Webb S t a c e y , J r . 1973. Searching f o r objects i n real world scenes. J o u r n a l o f E x p e r i m e n t a l P s y c h o l o g y 97(1): 22 - 27. B i e r l e y , R e x A., G l o r i a J . R i x e n , A l e x a n d e r I . T r o s t e r a n d W i l l i a m W. B e a t t y . 1987. P r e s e r v e d s p a t i a l memory i n old rats survives t e n months without training. B e h a v i o r a l a n d N e u r a l B i o l o g y 45(2): 223 - 229. B i n g m a n , V e r n e r P., P a o l o B a g n o l i , P a o l o I o a l e , a n d G i o v a n n i Casini. 1989. B e h a v i o r a l and a n a t o m i c a l s t u d i e s o f t h e a v i a n h i p p o c a m p u s . In The h i p p o c a m p u s - new v i s t a s . V i c t o r i a Chan-Palay and C h r i s t e r K o l e r , e d i t o r s . Alan R. L i s s , I n c . , New Y o r k . B i n g m a n , V e r n e r P., P a o l o I o a l e , G i o v a n n i C a s i n i , a n d P a o l o Bagnoli. 1988. Hippocampal a b l a t i o n s don't change spatial r e f e r e n c e memory b u t do a f f e c t homing i n pigeons. B e h a v i o u r a n d B r a i n R e s e a r c h 27(2): 179 187.  156  B l o u g h , D o n a l d S. and P a t r i c i a M. B l o u g h . 1990. Reaction time assessments of v i s u a l p e r c e p t i o n i n pigeons. In Comparative Perception. Volume I I : Complex s i g n a l s , e d i t o r s W i l l i a m C. S t e b b i n s and Mark A. B e r k l e y . John W i l e y and Sons, T o r o n t o . Bogdany, F r a n z J o s e f . 1978. honeybee orientation. S o c i o b i o l o g v 3: 323 -  L i n k i n g of l e a r n i n g s i g n a l s i n Behavioral Ecology and 336.  Bolhuis, J. J., S. Biljsma and P. Ansmink. 1987. E x p o n e n t i a l d e c a y o f s p a t i a l memory o f r a t s i n a r a d i a l maze. B e h a v i o r a l and N e u r a l B i o l o g y 46(2): 115 122. Bond, A l a n B. 1980. Optimal foraging i n a uniform The s e a r c h mechanism o f t h e g r e e n l a c e w i n g . Behaviour 28(1): 10 - 19. Bond,  habitat: Animal  A l a n B., R o b e r t G. Cook and M a r v i n R. Lamb. 1981. S p a t i a l memory and t h e p e r f o r m a n c e o f r a t s and p i g e o n s i n t h e r a d i a l - a r m maze. A n i m a l L e a r n i n g and Behavior  9(4):  575  -  580.  Booth, Thomas E. 1986. Monte C a r l o learning experiment with integer random numbers. S c i e n c e and E n g i n e e r i n g 92(3): 465 481.  biasing Nuclear  Bowe, C r a i g A. 1984. S p a t i a l r e l a t i o n s i n animal l e a r n i n g and b e h a v i o u r . P s y c h o l o g i c a l R e c o r d 34: 181 209. Bowers, Michael A. and Robert H. Adams-Manson. 1993. I n f o r m a t i o n and p a t c h e x p l o i t a t i o n s t r a t e g i e s o f the eastern chipmunk, Tamias striatus (Rodentia: Sciuridae). E t h o l o g y 95: 299 308. Brown, Gayle S. 1992. Factors affecting a s s o c i a t i o n l e a r n i n g bv h u m m i n g b i r d s . Ph. D. U n i v e r s i t y of B r i t i s h Columbia, Vancouver.  spatial Thesis.  Brown, G a y l e S. 1994. Spatial association learning by r u f o u s hummingbirds (Selasphorus rufus): Effects of r e l a t i v e s p a c i n g among s t i m u l i . J o u r n a l o f C o m p a r a t i v e P s y c h o l o g y . 1 0 8 ( 1 ) : 29 - 35. Brown, G a y l e S. and C l i f t o n L. G a s s . a s s o c i a t i o n l e a r n i n g by h u m m i n g b i r d s .  46(3):  487  -  497.  Brown, Michael F. 1987. components by pigeons. P s y c h o l o g y A 13(1): 80 -  157  1993. Animal  Dissociation Journal of 91.  Spatial Behaviour  of stimulus Experimental  Brown, M i c h a e l F. 1992. in the r a d i a l - a r m Psychology A 18(1):  Does a c o g n i t i v e map guide c h o i c e s maze? J o u r n a l of Experimental 56 - 66.  Brown, M i c h a e l F. and Robert G. Cook. 1986. Within-trial dynamics of r a d i a l arm maze performance i n rats. L e a r n i n g and M o t i v a t i o n 17: 190 - 205. Bruce, P a t r i c i a R. and James M. Herman. 1987. A d u l t age differences in spatial memory: Effects of d i s t i n c t i v e n e s s and repeated experience. J o u r n a l of Gerontology 41(6): 774 - 777. Bryant, Donna and determinants of Behaviour 2 ( 4 ) :  Russell M. Church. random c h o i c e . Animal 245 - 248.  1974. Learning  The and  B u l l o c k , Theodore H. 1993. How are more complex b r a i n s different? One view and an agenda f o r comparative n e u r o b i o l o g y . B r a i n , Behaviour and E v o l u t i o n 41: 88 96. Cahoon, P e t e r . 1984. D e t e c t i n g and e l i m i n a t i n g s p a t i a l b i a s when t r a c k i n g f o r a g i n g behavior i n a l a b o r a t o r y environment. M. Sc. T h e s i s . U n i v e r s i t y of B r i t i s h Columbia, Vancouver. Cain,  Michael insects: 888.  L. 1985. Random A s i m u l a t i o n model.  search by h e r b i v o r o u s Ecology 66(3): 876 -  C a p a l d i e , E. J . and D a n i e l J . M i l l e r . 1988. The r a t ' s simultaneous a n t i c i p a t i o n of remote events and c u r r e n t events can be s u s t a i n e d by event memories alone. Animal L e a r n i n g and Behavior 16(1): 1-7. C a p a l d i e , E. J . , D a n i e l J . M i l l e r and Timothy M. Nawrocki. 1987a. R e t e n t i o n i n t e r v a l and i n t e r t r i a l i n t e r v a l i n a serial learning or delayed discrimination task. J o u r n a l of Experimental Psychology A 12(1): 59 - 68. C a p a l d i e , E. J . , Timothy M. Nawrocki, D a n i e l J . M i l l e r and Donna R. V e r r y . 1986. Grouping, chunking, memory and learning. Q u a r t e r l y J o u r n a l of Experimental Psychology B 38(1): 53-80. C a p a l d i e , E. J . , Timothy M. Nawrocki, D a n i e l J . M i l l e r and Donna R. V e r r y . 1987b. Time between events as a retrieval cue: Recall and temporal similarities between storage and r e t r i e v a l i n t e r v a l . J o u r n a l of Experimental Psychology A 12(3): 258 - 269.  158  C a p a l d i e , E . J . , Donna R. V e r r y , T i m o t h y M. N a w r o c k i and Daniel J. Miller. 1984. Serial learning, interitem associations, phrasing, cues, interference, o v e r s h a d o w i n g , c h u n k i n g , memory and e x t i n c t i o n . Animal L e a r n i n g and B e h a v i o r 12: 7 - 20. Capelli, Amedeo, Gianni Caracoglia and Lorenzo Moretti. 1986. Chunking Mechanism for a knowledge r e p r e s e n t a t i o n system. C y b e r n e t i c s and S y s t e m s : An I n t e r n a t i o n a l J o u r n a l 17: 277 - 287. Caraco, Thomas. 1982. Risk groups. E c o l o g y 62(3): 527  sensitivity - 531.  and  foraging  C a r a c o , Thomas and S t e v e n Lima. 1987. S u r v i v o r s h i p , energy b u d g e t s and f o r a g i n g r i s k . In S i x t h A n n u a l Harvard Symposium on t h e Q u a n t i t a t i v e A n a l y s i s o f B e h a v i o r . M i c h a e l L. Common, S a r a J . S h e t t l e w o r t h , and A l e j a n d r o Kacelnik, editors. Erlbaum, New Y o r k . C a r p e n t e r , F. Lynn, D a v i d C. P a t o n and Mark A. H i x o n . 1983. W e i g h t g a i n and a d j u s t m e n t o f f e e d i n g t e r r i t o r y s i z e i n migrant hummingbirds. Proceedings of the National Academy o f S c i e n c e , U. S. A. 80: 7259. Carroll, S c o t t P. and L a u r e l Moore. 1993. t a k e t h e i r v i t a m i n s . A n i m a l B e h a v i o u r 46: C a r t a r , R a l p h V. 1991. i n w i l d bumble b e e s .  A  Hummingbirds 817 - 820.  t e s t of r i s k - s e n s i t i v e f o r a g i n g E c o l o g y 72(3): 888 - 895.  Charnov, E r i c L. 1976. Optimal foraging: The m a r g i n a l v a l u e theorem. T h e o r e t i c a l P o p u l a t i o n B i o l o g y 9: 129  -  136.  Cheng, Ken. spatial  1986. A p u r e l y g e o m e t r i c module i n t h e r a t ' s representation. C o g n i t i o n 23: 149 - 178.  Cheng, Ken. 1988. o f landmarks.  815  -  Some p s y c h o p h y s i c s o f t h e p i g e o n ' s u s e J o u r n a l o f C o m p a r a t i v e P h y s i o l o g y A 162:  826.  Cheng, Ken. 1989. The v e c t o r sum model o f p i g e o n l a n d m a r k use. J o u r n a l of E x p e r i m e n t a l P s y c h o l o g y A 15(4): 366  -  375.  Cheng, Ken. 1990. of landmarks.  857  -  More p s y c h o p h y s i c s o f t h e p i g e o n ' s u s e J o u r n a l o f C o m p a r a t i v e P h y s i o l o g y A 166:  863.  159  Cheng, Ken, and Charles R. G a l l i s t e l . 1984. T e s t i n g the geometric power of an animal's s p a t i a l r e p r e s e n t a t i o n . In Animal C o g n i t i o n . Herbert L. R o i t b l a t , T. G. Bever and H. S. Terrace, e d i t o r s . Erlbaum, H i l l s d a l e , New Jersey. Cheng, Ken, T. S. C o l l e t t and R. Wehner. 1987a. Honeybees l e a r n the c o l o u r s of landmarks. J o u r n a l of Comparative P h y s i o l o g y A 159(1): 69 - 73. Cheng, Ken, T. S. C o l l e t t , A. P i c k h a r d and R. Wehner. 1987b. The use of v i s u a l landmarks by honeybees: Bees weight landmarks a c c o r d i n g to t h e i r d i s t a n c e from the goal. J o u r n a l of Comparative P h y s i o l o g y A 161: 469 475. Church, R u s s e l l M. and Kevin D. M i l l e r . 1991. Symmetrical and asymmetrical sources of v a r i a n c e i n temporal generalization. Animal L e a r n i n g and Behavior 19(3): 207 - 214. C l a y t o n , Nicky S. 1993. L a t e r a l i z a t i o n and t r a n s f e r of s p a t i a l memory i n marsh t i t s . Comparative Physiology A 171: 799 - 806.  unilateral J o u r n a l of  C l a y t o n , N i c k y S. and John R. Krebs. 1993. Lateralization i n Paridae: Comparison of a s t o r i n g and a n o n - s t o r i n g species on a one-trial associative memory task. J o u r n a l of Comparative Physiology A 171: 807 - 815. C l a y t o n , Nicky S. and John R. Krebs. 1994. Memory f o r s p a t i a l and o b j e c t - s p e c i f i c cues i n f o o d - s t o r i n g and non-storing birds. J o u r n a l of Comparative P h y s i o l o g y A 174: 371 - 379. Cole,  Susan, Reed Hainsworth, A l a n C. Kamil, T e r r y M e r c i e r and L a r r y L. Wolf. 1982. S p a t i a l l e a r n i n g as an a d a p t a t i o n i n hummingbirds. Science 217: 655 - 657.  C o l l e t t , T. S. 1987. The use of v i s u a l landmarks by gerbils: Reaching a goal when landmarks are d i s p l a c e d . J o u r n a l of Comparative Physiology A 160(1): 109 - 113. C o l l e t t , T. S. and M. F. Land. 1975. V i s u a l s p a t i a l memory in a hoverfly. J o u r n a l of Comparative P h y s i o l o g y 100 (1) : 59 - 84. C o l l e t t , T. S., B. A. C a r t w r i g h t and B. A. Smith. 1986. Landmark learning and visuo-spatial memories in gerbils. J o u r n a l of Comparative P h y s i o l o g y A 158(6): 835 - 851.  160  C o l l e t t , T. S., E. D i l l m a n n , A. G i g e r a n d R. Wehner. 1 9 9 2 . V i s u a l landmarks and r o u t e f o l l o w i n g i n d e s e r t a n t s . J o u r n a l o f C o m p a r a t i v e P h y s i o l o g y A 170:' 435 - 4 4 2 . C o l l e t t , T. S., S. N. F r y a n d R. Wehner. learning by honeybees. Journal P h y s i o l o g y A 1 7 2 : 693 - 7 0 6 .  1993. Sequence of Comparative  C o l l i a s , N i c h o l a s E. a n d E l s i e C. C o l l i a s . 1968. Anna's Hummingbirds t r a i n e d t o s e l e c t d i f f e r e n t colors i n feeding. Condor 7 0 ( 3 ) : 273 - 2 7 4 . C o l w e l l , R o b e r t K. 1974. C o m p e t i t i o n a n d c o e x i s t e n c e i n a simple tropical community. American Naturalist 107 (958) : 737 - 7 6 0 . C o l w i l l , R u t h M. 1985. E f f e c t o f a s s o c i a t i v e l y s i g n i f i c a n t post-trial stimulation on learning and memory. Q u a r t e r l y Journal of Experimental Psychology B 37(2): 101 - 1 1 9 . C o l w i l l , R u t h M. a n d A n t h o n y D i c k i n s o n . 1980. Short-term r e t e n t i o n o f " s u r p r i s i n g " events following different training conditions. Animal L e a r n i n g and Behaviour 8 ( 4 ) : 561 - 566. Colwill, Ruth M. and Robert A. Rescorla. 1985. Postconditioning devaluation of a reinforcer affects instrumental response. Journal of Experimental Psychology A 11(1): 120 - 1 3 2 . Cook,  Robert G., M i c h a e l F. Brown a n d D o n a l d A. R i l e y . 1985. F l e x i b l e memory p r o c e s s i n g b y r a t s : Use o f p r o s p e c t i v e and r e t r o s p e c t i v e i n f o r m a t i o n i n t h e r a d i a l maze. J o u r n a l o f E x p e r i m e n t a l P s y c h o l o g y A 1 1 ( 3 ) : 453 - 469.  Crystal, J o n a t h o n D. a n d S a r a J . S h e t t l e w o r t h . 1994. Spatial list l e a r n i n g i n black-capped chickadees. Animal L e a r n i n g and Behavior 22(1): 77 - 8 3 . D a l l e r y , J e s s e a n d W i l l i a m M. Baum. 1 9 9 1 . The f u n c t i o n a l e q u i v a l e n c e o f operant b e h a v i o r and f o r a g i n g . Animal L e a r n i n g and Behavior 19(2): 146 - 1 5 2 . D a m i a n o p o u l o s , E r n e s t N. 1989. Biological constraints revisited: A critique. Animal L e a r n i n g and Behavior 17(2): 234 - 2 4 2 . D a v i s , R o g e r T. 1974. S p a t i a l D i s c o n t i g u i t y . In P r i m a t e B e h a v i o r . V o l u m e 3. Monkeys a s P e r c e i v e r s . R o g e r T. Davis, editor. A c a d e m i c P r e s s , New Y o r k .  161  Dawkins, M a r i a n . 1971a. P e r c e p t u a l changes i n A n o t h e r l o o k a t t h e " s e a r c h image" c o n c e p t . Behaviour 19: 566 - 574.  chicks: Animal  Dawkins, M a r i a n . 1971b. S h i f t s of " a t t e n t i o n " i n c h i c k s d u r i n g f e e d i n g . Animal Behaviour 19: 575 - 582. Denning, Peter J . 1989. S c i e n t i s t 7 7 ( 2 ) : 216 -  Bayesian 218.  Learning.  American  Denny, M i c h a e l S. 1975. The r a t ' s l o n g t e r m p r e f e r e n c e f o r c o m p l e x i t y i n i t s environment. A n i m a l L e a r n i n g and B e h a v i o u r 3 ( 3 ) : 245 - 249. de R e n z i o , E n n i o . 1982. D i s o r d e r s of space e x p l o r a t i o n cognition. John W i l e y and Sons, T o r o n t o . Devi,  and  B a r a t h a B. a n d V. V. S. Sarma. 1986. Fuzzy approximation schedules for sequence learning in pattern recognition. IEEE T r a n s a c t i o n s on Systems, Man a n d C y b e r n e t i c s 1 6 ( 5 ) : 668 - 679.  D i a m o n d , J a r e d M., Duong Phan a n d F. L y n n C a r p e n t e r . 1986. Hummingbird d i g e s t i v e physiology, a determinant of f o r a g i n g b o u t f r e q u e n c y . N a t u r e 320: 62 - 63. Dow,  S. M. a n d L e a , S. E. G. 1987. Sampling of schedule p a r a m e t e r s by p i g e o n s : Tests of o p t i m i z i n g t h e o r y . A n i m a l B e h a v i o u r 3 5 ( 1 ) : 102 - 114.  Draulans, Dirk. starlings: 287 - 288.  1988. The u s e o f c o m p l e x c u e s b y f o r a g i n g An e x p e r i m e n t . Animal Behaviour 36(1):  D r e i s i g , Hans. 1989. Nectar d i s t r i b u t i o n assessment by bumblebees f o r a g i n g a t v e r t i c a l i n f l o r e s c e n c e s . Oikos 55: 239 - 249. Dukas, Reuven and Stephen Ellner. p r o c e s s i n g and p r e y d e t e c t i o n . 1346.  1993. Information Ecology 74(5): 1337 -  Dukas, Reuven and P. Kirk Visscher. 1994. Lifetime l e a r n i n g by f o r a g i n g h o n e y b e e s . A n i m a l B e h a v i o u r 48: 1007 - 1012. D u k a s , R e u v e n a n d N i c k o l a s M. Waser. 1994. Categorization of food types enhances foraging performance of b u m b l e b e e s . A n i m a l B e h a v i o u r 48: 1001 - 1006. Dyer,  F r e d C. 1991. Bees a c q u i r e r o u t e - b a s e d m e m o r i e s b u t n o t c o g n i t i v e maps i n a f a m i l i a r l a n d s c a p e . Animal B e h a v i o u r 4 1 ( 2 ) : 239 - 246. 162  Dyer,  F r e d C. 1993. How h o n e y b e e s f i n d f a m i l i a r sites after changing nesting sites with a Animal Behaviour 46(4): 813 - 816.  feeding swarm.  Eisenberger, Robert. 1988. P e r c e p t i o n and learning in self-control. B e h a v i o r a l and B r a i n S c i e n c e s 11(4): 682 - 683. Ellen, Paul. 1980. C o g n i t i v e Maps a n d P h y s i o l o g i c a l Psychology 8(2): 168 -  the Hippocampus. 174.  Ellen, P a u l , B. J . S o t e r e s and C h a r l e n e Wages. 1984. Problem s o l v i n g i n the r a t : Piecemeal a c q u i s i t i o n of c o g n i t i v e maps. A n i m a l L e a r n i n g and B e h a v i o r 12(2): 232 - 237. E n n a c e u r , A b d e l k a d e r and Kamel M e l i a n i . 1992. A new onet r i a l t e s t f o r n e u r o b i o l o g i c a l s t u d i e s o f memory i n rats. III. S p a t i a l v s . n o n - s p a t i a l w o r k i n g memory. B e h a v i o u r a l B r a i n R e s e a r c h 51: 83 - 92. E s t e s , W i l l i a m K. 1994. Toward a s t a t i s t i c a l t h e o r y learning. P s y c h o l o g i c a l Review 101(2): 282 - 289.  of  E t i e n n e , A r i a n e S., Evelyne Teroni, Catherine Hurni and Veronique Portenier. 1990. The e f f e c t o f a s i n g l e l i g h t cue on h o m i n g b e h a v i o u r o f t h e g o l d e n h a m s t e r . A n i m a l B e h a v i o u r 39: 17 - 4 1 . E w a l d , P a u l W. a n d Raymond J . B r a n s f i e l d . 1987. Territory quality and t e r r i t o r i a l behavior i n two sympatric species of hummingbirds. Behavioral Ecology and S o c i o b i o l o g v 20: 285 - 293. E w a l d , P a u l W. and F. L y n n C a r p e n t e r . 1978. responses to energy manipulations in hummingbird. O e c o l o g i a 31: 277 - 292.  Territorial the Anna  E w a l d , P a u l W. and G o r d o n H. O r i a n s . 1983. E f f e c t s of r e s o u r c e d e p r e s s i o n on u s e o f i n e x p e n s i v e a n d e s c a l a t e d aggressive behavior: Experimental t e s t s u s i n g Anna h u m m i n g b i r d s . . B e h a v i o r a l E c o l o g y and S o c i o b i o l o g v 12: 95 - 101. F a g a n , R o b e r t M. and D o n a l d Y. Y o u n g . 1978. Temporal p a t t e r n s of behaviors: Durations, i n t e r v a l s , latencies and sequences. In Quantitative Ethology. P. W. Colgan, e d i t o r . J o h n W i l e y and S o n s , New York. Faris, W. G. and R. S. M a i j e r . a n a l y s i s of a l e a r n i n g m a t r i x . P r o b a b i l i t y 20(4): 695 - 705.  163  1988. Probabilistic Advances i n A p p l i e d  Fisk,  A r t h u r D. and S h i r l e y J . L l o y d . 1988. Stimulus t o r u l e c o n s i s t e n c y i n l e a r n i n g r a p i d a p p l i c a t i o n s of spatial rules. Human F a c t o r s 30(1): 35 - 49.  Forkman, B j o r n . 1991. Some problems w i t h c u r r e n t p a t c h c h o i c e theory: a study on the Mongolian gerbil. Behaviour 117(3-4): 243 - 254. Fuchs, A. and Hermann Haken. 1988a. Pattern recognition and a s s o c i a t i v e memory as dynamical p r o c e s s e s i n a s y n e r g e t i c system: I . T r a n s l a t i o n a l , i n v a r i a n c e and selective attention and decomposition of scenes. B i o l o g i c a l C y b e r n e t i c s 60(1): 17 - 22. Fuchs, A. and Hermann Haken. 1988b. Pattern recognition and a s s o c i a t i v e memory as dynamical p r o c e s s e s i n a s y n e r g e t i c system: II. Decomposition o f complex scenes, simultaneous invariance in respect to translation, rotation and scaling. Biological C y b e r n e t i c s 60(2): 107 - 110. Gaffan, E. A. 1992. Primacy, recency, and the v a r i a b i l i t y of data i n s t u d i e s of animals' working memory. Animal L e a r n i n g and Behavior 20(3): 240 - 252. Gaffan, E. A. Artifacts. 232.  1994. Primacy i n animals' working memory: Animal Learning and Behavior 22(2): 231 -  G a l e f , Bennett G., J r . 1976..,.] S o c i a l t r a n s m i s s i o n of a c q u i r e d behaviour: A d i s c u s s i o n o f t r a d i t i o n and s o c i a l l e a r n i n g i n v e r t e b r a t e s . Advances i n the Study of Behavior 6: 77 - 100. Gallistel, C h a r l e s R. 1989. Animal Cognition: The r e p r e s e n t a t i o n of space, time and number. Annual Review o f Psychology 40: 155 - 189. G a l l i s t e l , C h a r l e s R. 1990. The O r g a n i z a t i o n of L e a r n i n g . MIT Press, Cambridge, Massachusetts. Garber, Paul A. 1988a. f e e d i n g by tamarins.  Foraging d e c i s i o n s d u r i n g n e c t a r B i o t r o p i c a 20(2): 100 - 106.  Garber, Paul A. 1988b. The r o l e of s p a t i a l memory i n tamarin f o r a g i n g . American J o u r n a l of Anthropology 75(2) : 211 - 212. Gass, C l i f t o n Lee. 1978a. Experimental s t u d i e s o f f o r a g i n g i n complex l a b o r a t o r y experiments. American Z o o l o g i s t 18: 729 - 738. 1  164  Gass,  C l i f t o n Lee. 1978b. Rufous hummingbird feeding territoriality i n a suboptimal habitat. Canadian J o u r n a l of Zoology 56(7): 1535 - 1539.  Gass,  Clifton Lee. 1985. Behavioral foundations of adaptation. In P e r s p e c t i v e s i n Ethology. Volume 6. Paul P. G. Bateson and Peter H. K l o p f e r , editors. Plenum Press, New York.  Gass,  C l i f t o n Lee, George Angehr and J a n i c e Centa. 1976. R e g u l a t i o n of food supply by f e e d i n g t e r r i t o r i a l i t y i n the rufous hummingbird. Canadian J o u r n a l of Zoology 54 (12) : 2046 - 2054.  Gass,  Clifton Lee and Robert D. Montgomerie. 1981. Hummingbird f o r a g i n g behavior: Decision-making and energy r e g u l a t i o n . In Foraging Behavior: Ecological, e t h o l o g i c a l and p s y c h o l o g i c a l approaches. Alan C. Kamil and Theodore D. Sargent, e d i t o r s . Garland STDM Press, New York.  Gass, C l i f t o n Lee and W. Mark Roberts. 1992. The problem of temporal s c a l e i n o p t i m i z a t i o n : Three c o n t r a s t i n g views of hummingbird v i s i t s to f l o w e r s . The American N a t u r a l i s t 140(5): 829 - 853. Gass,  Clifton Lee and Glenn D. Sutherland. 1985. Specialization by territorial hummingbirds on e x p e r i m e n t a l l y e n r i c h e d patches of f l o w e r s : Energetic profitability and learning. Canadian Journal of Zoology 63: 2125 - 2133.  George, Mary Wissink.  at Malvaviscus -  794.  1980.  arboreus  Hummingbird f o r a g i n g  v a r . drummondii.  Getty, Thomas and H. Ronald P u l l i a m . d e t e c t i o n by f o r a g i n g sparrows. 742.  Auk  behavior  97:  1993. Search and prey Ecology 74(3): 734 -  Gibb, John A. 1961. L. T i n b e r g e n s hypothesis of the of s p e c i f i c search images. I b i s 104: 106 - 111. 1  790  role  Gibbon, John, R u s s e l l M. Church, Stephen F a i r h u r s t and Alejandro Kacelnik. 1988. S c a l a r expectancy theory and c h o i c e between delayed rewards. Psychological Review 95 (1) : 102 - 114. Gill,  Frank B. 1988. T r a p l i n e f o r a g i n g by hermit hummingbirds: Competition f o r an undefended, renewable resource. Ecology 69(6): 1933 - 1942.  165  Gill,  Frank B. and L a r r y L. Wolf. 1979. golden-winged s u n b i r d s t o c o m p e t i t o r s . 461.  N e c t a r l o s s by Auk 96: 448 -  G i l l i n g h a m , M i c h a e l P. and Bunnell, F r e d L. 1989. Effects of l e a r n i n g on food s e l e c t i o n and s e a r c h i n g behaviour of deer. Canadian J o u r n a l of Zoology 67(1): 24 - 32. Giraudo, Marie-Dominique and Patrick Perauch. 1988. Spatio-temporal aspects of the mental r e p r e s e n t a t i o n of urban space. J o u r n a l of Experimental Psychology 8: 9 - 17. Gleitman, Henry. 1963. Place-learning. American 209(4): 116 - 122.  Scientific  Gleitman, Henry. 1974. G e t t i n g animals to understand experimenter's instructions. Animal Learning Behaviour 2 ( 1 ) : 1 - 5.  the and  G o e l e t , P h i l i p , V i n c e n t F. C a s t e l l u c c i , Samuel Schacher and E r i c R. Kandel. 1986. The long and the s h o r t of l o n g term memory - a molecular framework. Nature 332: 419 - 422. Gori,  David F. 1989. F l o r a l c o l o r change i n Lupinus argenteus (Fabaceae): Why should p l a n t s a d v e r t i s e the location of unrewarding flowers to pollinators? E v o l u t i o n 43: 870 - 881.  Gould, James L. 1985. S c i e n c e 227(4752):  How bees remember 1492 - 1494.  flower  shapes.  Gould, James L. 1986a. L o c a l e maps of bees: Do i n s e c t s have c o g n i t i v e maps? Science 232(4752): 861 - 863. Gould, James L. 1986b. Animal Behaviour 34:  Pattern learning 990 - 997.  Gould, James L. 1986c. The Review of Psychology 37: Gould, James L. 1987. Animal Behaviour 35:  by  honeybees.  b i o l o g y of l e a r n i n g . 163 - 192.  Landmark 26 - 34.  learning  by  Annual  honeybees.  Gould, James L. and Peter M a r l e r . 1987. Learning Instinct. S c i e n t i f i c American 256: 74 - 85.  by  Gray, R u s s e l l D. 1987. F a i t h and f o r a g i n g : A c r i t i q u e of the "Paradigm argument from d e s i g n " . In F o r a g i n g Behavior. A l a n C. Kamil, John R. Krebs and H. Ronald Pulliam, editors. Plenum Press, New York.  166  G r e g g e r s , Uwe and R a n d o l f M e n z e l . 1993. Memory d y n a m i c s and foraging strategies of honeybees. Behavioral E c o l o g y a n d S o c i o b i o l o g v 32: 17 - 29. G r i f f i n , D o n a l d R. 1976. A p o s s i b l e window on t h e m i n d s o f animals. A m e r i c a n S c i e n t i s t 64: 530 - 535. G r i g o r y a n , G. E. and A. M. S t o l b e r g . 1989. Characteristics o f s p a t i a l memory p a r t i c i p a t i o n i n c h o i c e r e a c t i o n s o f white rats. Z h u r n a l V v s s i k a l e N e r o b i o l o g i e 39(2): 259 - 266. G u i l f o r d , T i m and M a r i a n S. D a w k i n s . 1987. Search not proven: A r e a p p r a i s a l of recent evidence. B e h a v i o u r 35: 1838 - 1845.  images Animal  H a c c o u , P a t s y , S a k e J . de V l a s , J a c q u e s J.M. v a n A l p h e n a n d M a r c e l E. V i s s e r . 1991. I n f o r m a t i o n p r o c e s s i n g by foragers: E f f e c t s o f i n t r a - p a t c h e x p e r i e n c e on the l e a v i n g t e n d e n c y o f Leptopilina heterotopia. J o u r n a l of A n i m a l E c o l o g y 60: 93 - 106. H a e f n e r , James W. and Thomas 0. C r i s t . 1994. S p a t i a l model of movement and foraging in harvester ants (Pogonomyrmex) (I) : The roles of memory and communication. J o u r n a l of T h e o r e t i c a l B i o l o g y 166: 299 - 313. Haila, Yrjo, Ilpo K. Hanski and Suvi Raivio. 1993. Turnover of breeding b i r d s i n small f o r e s t fragments: The "sampling" c o l o n i z a t i o n hypothesis c o r r o b o r a t e d . Ecology 74(3): 714 - 725. H a k e n , Hermann. 1988. Learning i n s y n e r g e t i c systems f o r pattern recognition and associative action. Z e i t s c h r i f t f u r Phvsik B 71(4): 521 - 526. H e a l y , S u s a n D. and J o h n R. K r e b s . 1992. Comparing s p a t i a l memory i n two s p e c i e s o f t i t : R e c a l l i n g a single positive location. A n i m a l L e a r n i n g and B e h a v i o r 2 0 ( 2 ) : 121 - 126. Heller, Rolf. environment. 214.  1980. On optimal diet in a T h e o r e t i c a l P o p u l a t i o n B i o l o g y 17:  patchy 201 -  Hemenway, Kathleen and Stephen E. Palmer. 1978. Organizational factors i n perceived dimensionality. J o u r n a l of Experimental Psychology: Human P e r c e p t i o n a n d P e r f o r m a n c e 4 ( 3 ) : 388 - 396. H e r m e r , L i n d a a n d E l i z a b e t h S. S p e l k e . process f o r s p a t i a l reorientation N a t u r e 370: 57 - 59. 167  1994. A i n young  geometric children.  H i t c h c o c k , C h r i s t i n e L. and D a v i d F. S h e r r y . 1990. Longterm memory f o r cache sites i n the black-capped chickadee. A n i m a l B e h a v i o u r 40: 701 - 712. H i n t z m a n , D o u g l a s L. 1978. The P s y c h o l o g y o f L e a r n i n g a n d Memory. W. H. Freeman a n d Company, San F r a n c i s c o . Hobbs, Benjamin F. 1986. What c a n we learn from experiments i n m u l t i o b j e c t i v e d e c i s i o n a n a l y s i s ? IEEE T r a n s a c t i o n s on Systems. Man a n d C y b e r n e t i c s 1 6 ( 3 ) :  384 - 394.  Hochberg, Julian and Edward McAlister. 1953. A q u a n t i t a t i v e approach t o f i g u r a l "goodness". Journal o f E x p e r i m e n t a l P s y c h o l o g y 46(5): 361 - 364. Hoffman, Norman a n d W i l l i a m S. M a k i . 1986. Two s o u r c e s o f proactive interference i n spatial working memory: Multiple effects of repeated t r i a l s on r a d i a l maze performance by r a t s . Animal L e a r n i n g and B e h a v i o r  14(1) :  65 - 72 .  Holldobler, Bert. 1980. Canopy o r i e n t a t i o n : A new k i n d o f o r i e n t a t i o n i n ants. S c i e n c e 210: 86 - 88. H o u s t o n , D a v i d C. 1983. The a d a p t i v e r a d i a t i o n o f t h e griffon vultures. In V u l t u r e B i o l o g y a n d Management. Sanford R. W i l b u r a n d Jerome A. J a c k s o n , editors. U n i v e r s i t y of C a l i f o r n i a Press, Berkeley. Hull,  C l a r k L. 1943. Principles Introduction t o Behavior Theory. C r o f t s , New Y o r k .  of  Behavior: An Appleton-Century-  H u l s e , S t e w a r t H. 1978. C o g n i t i v e s t r u c t u r e and s e r i a l p a t t e r n l e a r n i n g by r a t s . In C o g n i t i v e P r o c e s s e s i n Animal B e h a v i o r . S t e w a r t H. H u l s e , H a r r y F o w l e r a n d W e r n e r K. H o n i g , editors. Erlbaum, Hillsdale, New Jersey. Ilersich, Tamara J . , Dwight S. Mazmanian a n d W i l l i a m A. Roberts. 1988. F o r a g i n g f o r c o v e r e d and uncovered f o o d on a r a d i a l maze. Animal L e a r n i n g and B e h a v i o r  16 (4) :  Inui,  388 - 394.  T. 1988. P r o p e r t i e s o f human v i s u a l memory f o r b l o c k patterns. B i o l o g i c a l C y b e r n e t i c s 59(3): 179 - 187.  Johansson, 1980.  31:  Gunnar, C l a e s v o n H o f s t e n Event p e r c e p t i o n . Annual  27 - 63.  168  a n d Gunnar Jansson. review of Psychology  Jue,  D., K. J . Meador, D. W. L o r i n g a n d M. A l l e n . 1989. Horizontal and vertical deviation errors in visuospatial memory o f h e a l t h y a d u l t s . Annals of N e u r o l o g y 26(1); 12 6.  K a c e l n i k , A l e j a n d r o , J o h n R. K r e b s and E n s , . 1987. In The Q u a n t i t a t i v e A n a l y s i s o f B e h a v i o u r . Volume 6. Michael L. Common, S a r a J . S h e t t l e w o r t h a n d A l e j a n d r o K a c e l n i k , editors. E r l b a u m , New Y o r k . K a m i l , A l a n C. 1978. Systematic f o r a g i n g by a n e c t a r f e e d i n g b i r d , t h e a m a k i h i (Loxops virens) . Journal of Comparative and P h y s i o l o g i c a l Psychology 92: 388 -  396.  K a m i l , A l a n C. a n d R u s s e l l C. B a l d a . 1985. Cache r e c o v e r y a n d s p a t i a l memory i n C l a r k ' s N u t c r a c k e r s (Nucifraga columbiana). Journal of Experimental Psychology A  11(1):  95 - 111.  K a m i l , A l a n C. a n d J o h n E . M a u l d i n . 1975. Intraproblem retention during learning-set acquisition i n bluejays (Cyanocitta cristata) . Animal L e a r n i n g and Behaviour  3(2):  125 - 130.  K a m i l , A l a n C. a n d H e r b e r t L. R o i t b l a t . 1985. The e c o l o g y of foraging behaviour: Implications f o r animal l e a r n i n g a n d memory. A n n u a l Review o f P s y c h o l o g y 36:  141 - 169.  K e s n e r , Raymond P. 1980. An a t t r i b u t e a n a l y s i s The r o l e o f t h e h i p p o c a m p u s . Physiological  8(2) :  189 - 197.  o f memory: Psychology  Kesner, Raymond P., A n d r e a A. C h i b a a n d Pamela JacksonSmith. 1994. R a t s do show p r i m a c y a n d r e c e n c y e f f e c t s i n memory f o r l i s t s o f s p a t i a l l o c a t i o n s : A reply to Gaffan. A n i m a l L e a r n i n g and B e h a v i o r 2 2 ( 2 ) : 214 -  218.  Killeen, Peter behavioral  95 (2) :  R. a n d J . G r e g o r Fetterman. 1988. A theory of timing. P s y c h o l o g i c a l Review  274 - 295.  Kramer, D o n a l d L . a n d D a n i e l M. Weary. 1991. Exploration versus exploitation: A f i e l d study o f time a l l o c a t i o n to environmental tracking by foraging chipmunks. A n i m a l B e h a v i o u r 41(3): 443 - 449. K r e b s , J o h n R. a n d H e r b e r t B i e b a c h . 1989. Time-and-place l e a r n i n g b y g a r d e n w a r b l e r s {Sylvia borin): Route o r map? E t h o l o g y 83: 248 - 256.  169  K r e b s , J o h n R. a n d N. B. D a v i e s . Behavioural Ecology. P u b l i c a t i o n s , Oxford.  1984. An I n t r o d u c t i o n t o Blackwell Scientific  Laming, Donald and P e t e r S c h e i w i l l e r . 1985. R e t e n t i o n i n p e r c e p t u a l memory: A review o f models and d a t a . P e r c e p t i o n and Psvchophvsics 3 7 ( 3 ) : 189 - 1 9 7 . L a v e r t y , Terence morphology.  M. 1994. Bumble b e e l e a r n i n g a n d f l o w e r A n i m a l B e h a v i o u r 4 7 : 531 - 5 4 5 .  L a v e r t y , T e r e n c e M. a n d R.C. P l o w r i g h t . h a n d l i n g by bumblebees: A comparison and g e n e r a l i s t s . A n i m a l B e h a v i o u r 36:  1988. Flower of specialists 733 - 7 4 0 .  L a w r e n c e , E. S i m o n . 1989. Why b l a c k b i r d s o v e r l o o k c r y p t i c prey: S e a r c h r a t e o r s e a r c h image? Animal Behaviour 37: 157 - 164. Lima,  Steven L. 1983. Downy woodpecker (Picoides pubescens) foraging behavior: Foraging by e x p e c t a t i o n and energy i n t a k e r a t e . Oecologia 58(2): 232 - 2 3 7 .  Lima,  S t e v e n L. 1984. Downy w o o d p e c k e r f o r a g i n g b e h a v i o r : E f f i c i e n t sampling i n s t o c h a s t i c environments. Ecology 6 5 ( 1 ) : 166 - 174.  M a c D o n a l d , S u z a n n e E. a n d D o n a l d M. W i l k i e . 1990. Y e l l o w nosed monkeys' (Cercopithecus ascanius whitesidei) s p a t i a l memory i n a s i m u l a t e d f o r a g i n g environment. J o u r n a l o f Comparative Psychology 104(4): 382 - 3 8 7 . M a c k i n t o s h , N i c h o l a s J . 1983. C o n d i t i o n i n g and A s s o c i a t i v e Learning. Clarendon Press, Oxford. MacPhail, E v a n M. 1982. B r a i n and I n t e l l i g e n c e Vertebrates. C l a r e n d o n P r e s s , New Y o r k .  in  M a i e r , S u s a n E., P a u l V a n d e n h o f f a n d D o u g l a s P. C r o w e . 1988. M u l t i v a r i a t e a n a l y s i s o f p u t a t i v e measures o f a c t i v i t y , e x p l o r a t i o n e m o t i o n a l i t y and s p a t i a l b e h a v i o r i n t h e hooded r a t (Rattus n o r v e g i c u s ) . Journal of Comparative Psychology 102(4): 378 - 3 8 7 . Maki,  W i l l i a m S. 1979. Pigeons' s h o r t term memories f o r surprising vs. expected reinforcement and nonreinforcement. Animal L e a r n i n g and B e h a v i o r 7(1) : 31 - 3 7 .  Maki,  W i l l i a m S. 1987. On t h e n o n - a s s o c i a t i v e n a t u r e o f w o r k i n g memory. L e a r n i n g a n d M o t i v a t i o n 1 8 : 99 - 1 1 7 .  170  Maki,  W i l l i a m S., Susan Brokofsky and Bruce Berg. 1979. S p a t i a l memory i n r a t s : Resistance to r e t r o a c t i v e i n t e r f e r e n c e . Animal Learning and Behavior 7 ( 1 ) : 23 30.  M a t t h i e s , H. 1989. N e u r o b i o l o g i c a l a s p e c t s of l e a r n i n g and memory: A review. Annual Review of Psychology 40: 381 - 404. McCracken, Gary F. 1993. L o c a t i o n a l memory and female-pup reunions i n Mexican f r e e - t a i l e d bat m a t e r n i t y c o l o n i e s . Animal Behaviour 45: 811 - 813. McHose, James H. and Douglas P. P e t e r s . 1975. Partial reward, t h e n e g a t i v e c o n t r a s t e f f e c t , and i n c e n t i v e averaging. Animal Learning and Behavior 3 ( 3 ) : 239 244. McNamara, John M. environment. 269 - 288.  1982. Optimal p a t c h use i n a s t o c h a s t i c T h e o r e t i c a l P o p u l a t i o n B i o l o g y 21(2):  McNamara, John M. and A l a s d a i r I . Houston. 1985a. Optimal f o r a g i n g and l e a r n i n g . Journal of T h e o r e t i c a l Biology 117(2): 231 - 249. McNamara, John M. and A l a s d a i r I . Houston. 1985b. A s i m p l e model of information use i n the e x p l o i t a t i o n of p a t c h i l y d i s t r i b u t e d food. Animal Behaviour 3 3 ( 2 ) : 553 - 560. McNamara, Timothy P:, James K. Hardy and Stephen C. H i r t i e . 1989. Subjective hierarchies i n spatial memory. J o u r n a l o f Experimental Psychology: L e a r n i n g . Memory and C o g n i t i o n 15(2): 211 - 227. McQuade, Denise B., Ernest H. W i l l i a m s and Howard B. Eichenbaum. 1986. Cues used f o r l o c a l i z i n g food by the gray s q u i r r e l (Sciurus carolinensis). E t h o l o g y 72: 22-30. Mellgren, Roger L. and Timothy F. Elsmore. 1991. E x t i n c t i o n of Operant Behavior: An a n a l y s i s based on foraging considerations. Animal L e a r n i n g and B e h a v i o r 19 (4) : 317 - 325. M e l l g r e n , Roger L., John P. Lombardo, Dan M. Wrather and Robert F. Weiss. 1973. P a r t i a l reinforcement e f f e c t : The expectancy of reward on nonreward t r i a l s . Animal L e a r n i n g and Behavior 1 ( 2 ) : 105 - 108.  171  M e l l g r e n , R o g e r L. and T . J . R o p e r . 1986. Spatial learning and d i s c r i m i n a t i o n of food p a t c h e s i n t h e European b a d g e r {Meles meles L . ) . A n i m a l B e h a v i o u r 34: 1129 1134. M e n z e l , C h a r l e s R. 1991. Cognitive aspects of foraging i n J a p a n e s e monkeys. A n i m a l B e h a v i o u r 4 1 ( 3 ) : 397 - 402. Menzel, Emil W. organization.  1973. Chimpanzee spatial S c i e n c e 182: 943 - 945.  Menzel, Randolf. 1985. Learning i n e c o l o g i c a l and b e h a v i o u r a l c o n t e x t . Zooloqie 31: 55 - 74. M i l l e r , G e o r g e A. two: Some information.  memory  h o n e y b e e s i n an F o r t s c h r i t t e der  1956. M a g i c number s e v e n , p l u s o r m i n u s limits on o u r c a p a c i t y for processing P s y c h o l o g i c a l R e v i e w 63: 81-97.  Miller, Richard S. and Clifton Lee Gass. 1985. S u r v i v o r s h i p i n hummingbirds: Is predation important? Auk 1 0 2 ( 1 ) : 175 - 178. M i l l e r , R i c h a r d S., S t a f f a n Tamm, G l e n n D. S u t h e r l a n d a n d C l i f t o n Lee Gass. 1984. Cues f o r o r i e n t a t i o n i n hummingbird f o r a g i n g : C o l o r and p o s i t i o n . Canadian J o u r n a l o f Z o o l o g y 63: 18 - 2 1 . Milner, A. Donald, M e l v y n A. Goodale, and M a r g a r e t C. Morton. 1979. V i s u a l sampling a f t e r l e s i o n s of the superior colliculus i n rats. Journal of Comparative a n d P h y s i o l o g i c a l P s y c h o l o g y 93: 1015 - 1023. M i t c h e l l , W i l l i a m A. 1989. I n f o r m a t i o n a l c o n s t r a i n t s on o p t i m a l l y f o r a g i n g hummingbirds. O i k o s 55: 145 - 154. M o o r e , J o h n W. a n d K e n n e t h J . S t i c k n e y . 1980. Formation of a t t e n t i o n a l - a s s o c i a t i v e networks i n r e a l time: Role of t h e hippocampus and implications for conditioning. P h y s i o l o g i c a l P s y c h o l o g y 8 ( 2 ) : 207 - 217. M o r r i s , M i c h a e l D. and E. J . C a p a l d i e . 1979. Extinction responding following partial reinforcement: The e f f e c t s o f number o f r e w a r d e d t r i a l s a n d m a g n i t u d e o f reward. A n i m a l L e a r n i n g and B e h a v i o r 7 ( 4 ) : 509 - 513. M o r r i s , R i c h a r d G. M. 1981. S p a t i a l l o c a l i z a t i o n does r e q u i r e the presence of l o c a l cues. Learning M o t i v a t i o n 12: 239 - 260. Nadel, Lynn and J e f f r e y W i l l n e r . conditioning: A place for P s y c h o l o g y 8 ( 2 ) : 218 - 228. 172  1980. space.  not and  Context and Physiological  Nishimura, Kinya. 1994. D e c i s i o n m a k i n g o f a s i t - a n d - w a i t f o r a g e r i n an u n c e r t a i n environment: L e a r n i n g and memory l o a d . A m e r i c a n N a t u r a l i s t 1 4 3 ( 4 ) : 656 - 6 7 6 . Okaichi, Hiroshige. 1987. Performance and dominant s t r a t e g i e s on p l a c e and cue t a s k s f o l l o w i n g h i p p o c a m p a l lesion i n rats. Psvchobioloqy 15(1): 58 - 6 3 . O ' K e e f e , J o h n a n d D u l c i H. Conway. 1 9 8 0 . On t h e t r a i l o f t h e h i p p o c a m p a l engram. P h y s i o l o g i c a l P s y c h o l o g y 8 ( 2 ) : 229 - 2 3 8 . O l l a s o n , J . G. 1983. B e h a v i o u r a l consequences o f h u n t i n g by expectation: A simulation study of foraging tactics. T h e o r e t i c a l P o p u l a t i o n B i o l o g y 23: 323 346. O l t o n , D a v i d S. 1985. The t e m p o r a l c o n t e x t memory. Philosophical Transactions of S o c i e t y o f London B 308(1135): 79 - 86.  of s p a t i a l the Royal  O l t o n , D a v i d S. 1990. S p a t i a l p e r c e p t i o n : B e h a v i o r a l and neural analyses. In C o m p a r a t i v e P e r c e p t i o n , Volume II: C o m p l e x s i g n a l s . W i l l i a m C. S t e b b i n s a n d M a r k A. B e r k l e y , e d i t o r s . John W i l e y and Sons, T o r o n t o . O l t o n , D a v i d S., James T. B e c k e r , a n d G a i l E. H a n d e l m a n n . 1980. Hippocampal function: Working memory or c o g n i t i v e mapping? P h y s i o l o g i c a l Psychology 8(2): 239 - 246. P a p a j , D a n i e l R. 1988. G e n e t i c d i f f e r e n c e s a n d p h e n o t y p i c p l a s t i c i t y as causes o f v a r i a t i o n i n a n i m a l s : An environmental v a r i a b i l i t y hypothesis f o r the e v o l u t i o n of l e a r n i n g . Behaviour Genetics 18(6): 727 - 7 2 8 . Park,  K y u n g S. 1 9 8 5 . Human r e l i a b i l i t y w i t h p r o b a b i l i s t i c learning in discrete and continuous tasks: C o n c e p t u a l i z a t i o n and m o d e l i n g . M i c r o e l e c t r o n i c s and R e l i a b i l i t y 25(1): 157 - 166.  P e p p e r b e r g , I r e n e M. 1987. A c q u i s i t i o n o f c o n c e p t s by parrots: L e a r n i n g w i t h r e s p e c t t o c o l o u r , shape and material. Animal L e a r n i n g and Behaviour 1 5 ( 4 ) : 423 432 . P i n e l , J o h n P. J . , M i c h a e l J . Mana a n d D o n a l d M. W i l k i e . 1986. P o s t s h o c k l e a r n i n g and c o n d i t i o n e d defensive burying. Animal L e a r n i n g and Behavior 1 4 ( 3 ) : 301 304.  173  Pomerantz, James R. 1981. Perceptual o r g a n i z a t i o n i n information processing. In P e r c e p t u a l Organization. Michael Kubovy and James R. Pomerantz, editors. Lawrence Erlbaum A s s o c i a t e s , New York. Pyke,  Graham H. 1978. Are animals Animal Behaviour 26: 241 - 250.  efficient  harvesters?  Pyke,  Graham H. and Ralph V. C a r t a r . 1992. The flight d i r e c t i o n a l i t y of bumblebees: Do they remember where they came from? Oikos 65: 321. - 327.  Rabenold, P a t r i c i a P. 1983. The communal r o o s t i n b l a c k and turkey v u l t u r e s -- An i n f o r m a t i o n c e n t e r ? In V u l t u r e B i o l o g y and Management. Sanford R. W i l b u r and Jerome A. Jackson, e d i t o r s . U n i v e r s i t y of C a l i f o r n i a Press, Berkeley. Rabenold, P a t r i c i a P. 1987. Recruitment f o r food i n b l a c k vultures: Evidence f o r f o l l o w i n g from communal r o o s t s . Animal Behaviour 35: 1775 - 1785. Raven, Peter H. and George B. Johnson. 1989. Biology. Times Mirror/Mosby C o l l e g e P u b l i s h i n g , S a i n t L o u i s . Reed, P h i l . 1994. Less than expected v a r i a n c e i n s t u d i e s of s e r i a l p o s i t i o n e f f e c t s i s not a s u f f i c i e n t reason for caution. Animal Learning and Behavior 22(2): 224 - 230. Regelmann, Klaus. 1985. s e n s i t i v e foraging. 110(2) : 217 - 222 .  A remark on the theory of r i s k J o u r n a l of T h e o r e t i c a l B i o l o g y  R e s c o r l a , Robert A. 1986. w i t h i n event l e a r n i n g . 14(4): 387 - 392.  Two p e r c e p t i o n v a r i a b i l i t y i n Animal L e a r n i n g and Behavior  R e s c o r l a , Robert A. and Holland, Peter. 1982. Behavioral s t u d i e s of a s s o c i a t i v e l e a r n i n g i n animals. Annual Review of Psychology 33: 265 - 308. R e s t l e , Frank. 1957. D i s c r i m i n a t i o n of cues i n mazes: A resolution of the "place vs. response" question. P s y c h o l o g i c a l Review 64: 217 -228. Roberts, A. C , T. W. Robbins and B. J . E v e r i t t . 1988. The e f f e c t of i n t r a - and extra-dimensional s h i f t s of v i s u a l discrimination learning in humans and primates. Q u a r t e r l y J o u r n a l of Experimental Psychology B 40(4): 321 - 342.  174  Roberts, Robert C. 1979. The e v o l u t i o n of a v i a n s t o r i n g behavior. American N a t u r a l i s t 114(3): 438. Roberts, W i l l i a m A. 1988. pigeons. J o u r n a l of 108 - 117.  food418 -  Foraging and s p a t i a l memory i n Comparative Psychology 102(2):  Roberts, W i l l i a m A. 1991. T e s t i n g optimal f o r a g i n g theory on the r a d i a l maze: The r o l e of l e a r n i n g i n p a t c h sampling. Animal Learning and Behavior 19(4): 305 316. Robinson, Gene E. and Fred C. Dyer. 1993. P l a s t i c i t y of s p a t i a l memory i n honey bees: Reorientation following colony f i s s i o n . Animal Behaviour 46: 311 - 320. Root,  R i c h a r d B. and Peter M. K a r e i v a . 19.84. The s e a r c h f o r resources by cabbage b u t t e r f l i e s (Pieris rapae): E c o l o g i c a l consequences and adaptive s i g n i f i c a n c e o f markovian movements i n a patchy environment. Ecology 65(1) : 147 - 165.  Rumbaugh, Duane M., W. K i r k Richardson, David A. Washburn, E. Sue Savage-Rumbaugh, and W i l l i a m D. Hopkins. 1989. Rhesus monkeys (Macaca mulatta), video tasks, and i m p l i c a t i o n s f o r stimulus-response s p a t i a l c o n t i g u i t y . J o u r n a l of Comparative Psychology 103: 32 - 38. Sasvari, Lajos. 197 9. Blue and Marsh t i t s .  O b s e r v a t i o n a l l e a r n i n g i n Great, Animal Behaviour 27: 767 - 771.  S a t t a t h , Shmuel and Amos Tversky. 1987. On the between common and distinctive feature P s y c h o l o g i c a l Review 94(1): 16 - 22.  relation models.  Schenk, F r a n c o i s e . 1987. Comparison of s p a t i a l l e a r n i n g i n woodmice (Apodemus sylvaticus) and hooded r a t s (.Rattus norvegicus). J o u r n a l of Comparative Psychology 101(2): 150 - 158. Schoener, Thomas W. 1987. A b r i e f h i s t o r y of o p t i m a l f o r a g i n g ecology. In Foraging Behavior. Alan C. Kamil, John R. Krebs and H. Ronald P u l l i a m , e d i t o r s . Plenum Press, New York. S c h r i e r , A l l a n M., Fred S t o l l n i t z and Kenneth F. Green. 1963. Titration of spatial S-R separation in d i s c r i m i n a t i o n by monkeys (Macaca mulatta). J o u r n a l of Comparative and P h y s i o l o g i c a l Psychology 56: 848 851.  175  S e l f , Roland and E. A. Gaffan. p a t t e r n l e a r n i n g by r a t s . 11(1): 10-18.  1983. An a n a l y s i s of s e r i a l Animal L e a r n i n g and Behavior  S e l f r i d g e , O l i v e r G. and U l r i c Nesser. 1960. Pattern r e c o g n i t i o n by machine. S c i e n t i f i c American 203: 60 68. Sherry, David F. 1984. What f o o d - s t o r i n g b i r d s remember. Canadian J o u r n a l of Psychology 38(2): 304 - 321. Sherry, David F. 1985. Food storage by b i r d s and mammals. In Advances i n the Study of Behavior. Volume 15. J a y S. Rosenblatt, C o l i n Beer, Marie C l a i r e Busnel and Peter J . B. S l a t e r , e d i t o r s . Academic Press, Orlando. Sherry, David F. and Anthony L. V a c c a r i n o . 1989. Hippocampus and memory f o r food caches i n black-capped chickadees. Behavioural Neurobiology 103(2): 308 318. Sherry, David F., Anthony L. Vaccarino, Karen Buckenham and Rachel S. Herz. 1989. The hippocampal complex o f food-storing birds. B r a i n , Behavior and E v o l u t i o n 34: 308 - 317. S h e t t l e w o r t h , Sara J . 1983. Memory i n food-hoarding S c i e n t i f i c American 247: 102 - 110.  birds.  S h e t t l e w o r t h , Sara J . and John R. Krebs. 1982. How marsh t i t s f i n d t h e i r hoards: The r o l e s of s i t e p r e f e r e n c e and spatial memory. Journal of Experimental Psychology A 8: 354 - 375. S h e t t l e w o r t h , Sara J . and John R. Krebs. 1986. S t o r e d and encountered seeds: Comparison of two s p a t i a l memory tasks i n marsh-tits and chickadees. J o u r n a l of Experimental Psychology A 12(3): 248 - 257. S h e t t l e w o r t h , Sara J . , John R. Krebs, Susan D. Healy and C y n t h i a M. Thomas. 1990. S p a t i a l memory o f foodstoring tits (Parus ater and P. atricapillus) : Comparison of s t o r i n g and n o n s t o r i n g t a s k s . J o u r n a l of Comparative Psychology 104(1): 71 - 81. S h i f f r i n , R i c h a r d M., D. P. McKay and W. 0. S h a f f e r . 1976. A t t e n d i n g t o f o r t y - n i n e s p a t i a l p o s i t i o n s a t once. J o u r n a l of Experimental Psychology: Human P e r c e p t i o n and Performance 2 ( 1 ) : 14 - 22. S h o l l , M. Jeanne. 1987. C o g n i t i v e maps as o r i e n t i n g schemata. J o u r n a l of Experimental Psychology A 13(4): 615 - 628. 176  S m i t h , James N. M. 1974. The f o o d s e a r c h i n g b e h a v i o u r o f two E u r o p e a n t h r u s h e s . I I : The a d a p t i v e n e s s o f t h e s e a r c h p a t t e r n s . B e h a v i o u r 49: 1 - 5 9 . Speakman, A. a n d J . O ' K e e f e . 1989. Hippocampal p l a c e c e l l s and hippocampal theories. In The h i p p o c a m p u s - new vistas. Victoria Chan-Palay and Christer Koler, editors. A l a n R. L i s s , I n c . , New Y o r k . S p e t c h , M a r c i a L. 1990. Further studies of pigeons' s p a t i a l w o r k i n g memory i n t h e o p e n - f i e l d t a s k . Animal L e a r n i n g and B e h a v i o r 1 8 ( 3 ) : 332 - 3 4 0 . S p e t c h , M a r c i a L. a n d C h a r l e s A. E d w a r d s . 1986. Spatial memory i n p i g e o n s i n a n o p e n f i e l d f e e d i n g e x p e r i m e n t . J o u r n a l o f Comparative Psychology 100(3): 266 - 2 7 8 . S p e t c h , M a r c i a L. a n d C h a r l e s A. E d w a r d s . 1988. Pigeons' Columbia livia, use of g l o b a l and l o c a l cues f o r s p a t i a l memory. A n i m a l B e h a v i o u r 3 6 ( 1 ) : 293 - 2 9 5 . Spetch, Marcia L. and Werner K. Honig. 1988. C h a r a c t e r i s t i c s o f p i g e o n s ' s p a t i a l w o r k i n g memory i n an o p e n - f i e l d t a s k . Animal Learning and Behavior 16(2): 123 - 1 3 1 . S p e t c h , M a r c i a L., Ken Cheng a n d M i c h a e l V. M o n d l o c h . 1 9 9 2 . Landmark u s e by p i g e o n s i n a touch-screen spatial search task. A n i m a l L e a r n i n g a n d B e h a v i o r 2 0 ( 3 ) : 281 - 292. S q u i r e , L a r r y R. 1 9 8 6 . 1612 - 1 6 1 9 .  M e c h a n i s m s o f Memory.  S c i e n c e 232:  Srinivasan, M. V., M. L e h r e r , S. W. Zhang a n d G. A. Horridge. 1989. How h o n e y b e e s m e a s u r e t h e i r d i s t a n c e f r o m o b j e c t s o f unknown s i z e . J o u r n a l of Comparative Physiology A 165(5): 605 - 6 1 3 . Stephens, D a v i d W. 1981. The foraging preferences. Animal 629.  logic of Behaviour  risk-sensitive 29(2): 628 -  S t e p h e n s , D a v i d W. a n d S t e v e n R. P a t o n . 1 9 8 6 . How c o n s t a n t i s t h e c o n s t a n t o f r i s k a v e r s i o n ? A n i m a l B e h a v i o u r 34: 1659 - 1 6 6 7 . S t o l l n i t z , F r e d a n d S c h r i e r , A l l a n M. 1962. D i s c r i m i n a t i o n l e a r n i n g b y monkeys w i t h s p a t i a l s e p a r a t i o n o f c u e a n d response. P s y c h o l o g i c a l R e v i e w 7 2 : 247 - 2 6 1 .  177  S t r i j k s t r a , A. M., and J . J . B o l h u i s . 1987. Memory p e r s i s t e n c e o f r a t s i n a r a d i a l maze v a r i e s w i t h t r a i n i n g procedure. B e h a v i o r a l and Neural Biology 47(2): 158 - 166. Sutherland, Glenn D. 1985. The r o l e o f s p a t i a l learning i n hummingbird foraging. M.Sc. U n i v e r s i t y o f B r i t i s h Columbia, Vancouver.  pattern thesis,  Sutherland, Glenn D. and C l i f t o n Lee Gass. In p r e s s . Learning and remembering of s p a t i a l p a t t e r n s by hummingbirds. Animal Behaviour Sutherland, Glenn D., C l i f t o n Lee Gass, Peter A. Thompson and Kenneth P. Lertzman. 1992. Feeding t e r r i t o r i a l i t y i n migrant rufous hummingbirds: Defense o f y e l l o w b e l l i e d sapsucker (Sphyrapicus varius) feeding s i t e s . Canadian J o u r n a l o f Zoology 60(9): 2046 - 2050. Sutherland, Robert J . , G. L. Chew, J . C. Baker and R. C. Linggard. 1987. Some l i m i t a t i o n s on the use o f d i s t a l cues i n p l a c e n a v i g a t i o n by r a t s . Psvchobiolocrv 15(1) : 48 - 57. S u t h e r l a n d Robert J . and R i c h a r d H. Dyck. 1984. Place n a v i g a t i o n by r a t s i n a swimming p o o l . Canadian J o u r n a l of Psychology 38(2): 322 - 347. Suzuki, Shinya, Gerda Augerinos and Abraham H. B l a c k . 1980. Stimulus c o n t r o l o f s p a t i a l behavior on t h e e i g h t arm maze i n r a t s . Learning and M o t i v a t i o n 11: 1 - 1 8 . Tamm, S t a f f a n . 1987. T r a c k i n g v a r y i n g h a b i t a t s : Sampling by hummingbirds. Animal Behaviour 35: 1725 - 1734. Tamm, S t a f f a n and C l i f t o n Lee Gass. 1986. Energy i n t a k e rates and nectar concentration preferences by hummingbirds. Oecologia 70: 20-23. Tengo, Jan, Hermann Schone and J e r z y Chmurzynski. 1990. Homing i n the d i g g e r wasp Bembix rostrata (Hymenoptera, Sphecidae) i n r e l a t i o n t o sex and stage. E t h o l o g y 86: 47 - 56. Thinus-Blanc, C a t h e r i n e and David I n g l e . 1985. b e h a v i o r i n g e r b i l s (Meriones unguiculatus) . of Comparative Psychology 99(3): 311 - 315.  Spatial Journal  Thompson, James. 1994. Do hummingbirds use c o n t e x t u a l i n f o r m a t i o n when performing s p a t i a l a s s o c i a t i o n t a s k s ? M. Sc. T h e s i s . U n i v e r s i t y of B r i t i s h Columbia, Vancouver.  178  Thompson, R i c h a r d F. 1986. The neurobiology o f l e a r n i n g and memory. Science 233(4767): 941 - 947. T i e r n e y , Ann J . 1986. The e v o l u t i o n of l e a r n e d and i n n a t e behavior: C o n t r i b u t i o n s from g e n e t i c s and n e u r o b i o l o g y t o a theory o f b e h a v i o r a l e v o l u t i o n . Animal L e a r n i n g and Behavior 14(4): 339 - 348. Tinbergen, Niko. 1932. Ueber d i e O r i e n t i e r u n g des Bienenwolfes (Philanthus triangulxxm Fabr.). Z e i t s c h r i f t f u r Vergleichende P h v s i o l o g i e 16: 305 334. Tinbergen, Niko and W. Kruyt. 1938. Ueber d i e O r i e n t i e r u n g des Bienenwolfes (Philanthus triangulum Fabr.) I I I . Die Bevorzugung bestimmter Wegmarken. Z e i t s c h c r i f t f u r V e r g l e i c h e n d e P h v s i o l o g i e 25: 292 - 334. Todd,  Ian A. and A l e j a n d r o K a c e l n i k . 1993. Psychological mechanisms and the marginal value theorem: Dynamics o f s c a l a r memory f o r t r a v e l time. Animal Behaviour 46(4) : 765 - 775.  Tolman, Edward C. 1948. C o g n i t i v e maps i n mice and men. P s y c h o l o g i c a l Review 55(4): 189 - 208. Tooze, Zena J . and C l i f t o n Lee Gass. 1984. Responses of rufous hummingbirds t o midday f a s t s . Canadian J o u r n a l of Zoology 63: 2249 - 2253. Vallortigara, Giorgio and Mario Zanforlin. 1987. Simultaneous discrimination learning in chicks: Spatial representations and o b j e c t characteristics. Ethology 79: 248 - 256. V a l l o r t i g a r a , G i o r g i o and Mario Z a n f o r l i n . 1989. Place and o b j e c t l e a r n i n g i n Chicks (Gallus domesticus). Journal of Comparative Psychology 103(2): 201 - 209. Valone, Thomas J . 1991. Bayesian Foraging with pre-harvest Behaviour 41(4): 569 - 577.  and p r e s c i e n t assessment: information. Animal  Valone, Thomas J . 1992. Information f o r patch assessment: A f i e l d i n v e s t i g a t i o n w i t h b l a c k - c h i n n e d hummingbirds. B e h a v i o r a l Ecology 3(3): 211 - 222. Valone, Thomas J . and L u c - A l a i n Girardeau. 1993. Patch e s t i m a t i o n by group f o r a g e r s : What i n f o r m a t i o n i s used? Animal Behaviour 45: 721 - 728. Vander W a l l , Stephen B. 1982. An experimental a n a l y s i s o f cache recovery i n C l a r k ' s n u t c r a c k e r . Animal Behaviour 30: 84 - 94. 179  Vander W a l l , Stephen B. 1991. by y e l l o w p i n e chipmunks. 863 . van  Mechanisms of cache r e c o v e r y Animal Behaviour 41: 851 -  L u i j t e l a a r , E. L. J . M., F. J . van der Staay and J . M. L. Kerbusch. 1989. S p a t i a l Memory i n Rats: A c r o s s v a l i d a t i o n study. The Q u a r t e r l y J o u r n a l of Experimental Psychology B 41(3): 287 - 306.  Warburton, Kevin. 1990. The use of l o c a l landmarks by f o r a g i n g g o l d f i s h . Animal Behaviour 40: 500 - 505. Warren, J . M. and Helen M. Warren. 1973. P r e t r a i n i n g and d i s c r i m i n a t i o n r e v e r s a l l e a r n i n g by rhesus monkeys. Animal Learning and Behavior 1(1): 52 - 56. Weis,  A r t h u r E. 1983. Patterns of P a r a s i t i s m by capite on hosts d i s t r i b u t e d i n small p a t c h e s . of Animal Ecology 52: 867 - 877.  Weiss, George H. 1983. Random walks and a p p l i c a t i o n s . American S c i e n t i s t 71: 65-71.  Torymus Journal their  W e l l i n g t o n , W. G. and D. Cmiralova. 1979. Communication of h e i g h t by f o r a g i n g honey bees, Apis mellifera ligustica (Hymenoptera, Apidae). Annals of the E n t o m o l o g i c a l S o c i e t y of America 72(1): 167 - 170. Wertheimer, M. 1950. Laws of o r g a n i z a t i o n i n p e r c e p t u a l forms. In A Source Book of G e s t a l t Psychology. W. D. E l l i s , e d i t o r . Humanities Press, New York. Wheeler, Thomas G. 1980. Experiments i n f e e d i n g b e h a v i o r of the Anna hummingbird. Wilson B u l l e t i n 92(1): 53 Wickelgren, Wayne A. 1979. Chunking and c o n s o l i d a t i o n : A t h e o r e t i c a l s y n t h e s i s of semantic networks, c o n f i g u r i n g i n c o n d i t i o n i n g , S-R versus c o g n i t i v e l e a r n i n g , normal f o r g e t t i n g , the amnesic syndrome, and the hippocampal a r o u s a l system. P s y c h o l o g i c a l Review 86(1): 44 - 60. W i l k i e , Donald M. 1986a. F a c t o r s a f f e c t i n g pigeon v i s u a l t r a c k i n g behaviour. B e h a v i o u r a l Processes 12(3): 287 W i l k i e , Donald M. 1986b. Pigeon s p a t i a l memory: P r o a c t i v e i n t e r f e r e n c e i n delayed matching. Animal L e a r n i n g and Behaviour 14(3): 257 - 266. W i l k i e , Donald M. and Duncan J . Kennedy. 1987. Computer s i m u l a t i o n of pigeon's performance on a s p a t i a l memory t a s k . B e h a v i o u r a l Processes 14(1): 105 - 122. 180  W i l k i e , Donald M. and Marcia L. Spetch. 1980. Pigeons' d e l a y e d matching t o sample e r r o r s a r e not always due to forgetting. Behaviour A n a l y s i s L e t t e r s 1: 317 - 323. W i l k i e , Donald M., Marcia L. Spetch and L i n c o l n Chew. 1981. The r i n g dove's short-term memory c a p a c i t y f o r s p a t i a l i n f o r m a t i o n . Animal Behaviour 29(2): 639 - 641. W i l k i e , Donald M., Robert J . W i l l s o n and Kevin Lee. 1990. F u r t h e r support f o r the " d r i f t " model o f pigeons' s h o r t - t e r m memory f o r s p a t i a l l o c a t i o n . Behavioural Processes 22: 113 - 119. Wolf, L a r r y L. and F. Reed Hainsworth. 1983. Economics of > f o r a g i n g s t r a t e g i e s i n Sunbirds and Hummingbirds. In Behavioural energetics : Tiie cost of s u r v i v a l i n vertebrates. E. P. Aspey and S. I . L u s t i c , e d i t o r s . Ohio S t a t e U n i v e r s i t y Press, Columbus. Wolf,  L a r r y L. and F. Reed Hainsworth. 1991. Hummingbird foraging patterns: Visits t o clumps o f Ipomopsis aggregata i n f l o r e s c e n c e s . Animal Behaviour 41(5): 803 - 812.  Wolf,  L a r r y L., F. Reed Hainsworth and F. Gary Stiles. 1972. E n e r g e t i c s of f o r a g i n g : Rate and e f f i c i e n c y of n e c t a r e x t r a c t i o n by hummingbirds. S c i e n c e 176: 1351 - 1352.  Woodard, W i l l i a m T. and M. E. Bitterman. 1973. F u r t h e r experiments on p r o b a b i l i t y learning i n goldfish. Animal L e a r n i n g and Behavior 1 ( 1 ) : 25 - 28. Wright, Anthony A. 1994. Primacy e f f e c t s i n animal memory and human non-verbal memory. Animal L e a r n i n g and Behavior 22(2): 219 - 223. Wunderle, Joseph M., J r . and J u l i o S. M a r t i n e z . 1987. Spatial learning i n the n e c t a r i v o r o u s bananaquit: J u v e n i l e s versus a d u l t s . Animal Behaviour 35: 652 658. Z e n t a l l , Thomas R., J a n i c e N. S t e i r n and Pamela JacksonSmith. 1990. Memory strategies i n pigeons' performance of a r a d i a l - a r m maze analog t a s k . Journal of Experimental Psychology A 16: 358 - 371.  181  

Cite

Citation Scheme:

        

Citations by CSL (citeproc-js)

Usage Statistics

Share

Embed

Customize your widget with the following options, then copy and paste the code below into the HTML of your page to embed this item in your website.
                        
                            <div id="ubcOpenCollectionsWidgetDisplay">
                            <script id="ubcOpenCollectionsWidget"
                            src="{[{embed.src}]}"
                            data-item="{[{embed.item}]}"
                            data-collection="{[{embed.collection}]}"
                            data-metadata="{[{embed.showMetadata}]}"
                            data-width="{[{embed.width}]}"
                            async >
                            </script>
                            </div>
                        
                    
IIIF logo Our image viewer uses the IIIF 2.0 standard. To load this item in other compatible viewers, use this url:
http://iiif.library.ubc.ca/presentation/dsp.831.1-0086804/manifest

Comment

Related Items