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Anim. Behav., 1988, 36, 44-54
T h e e f f e c t o f a g e a n d v i s u a l c u e s o n f l o r a l
p a t c h u s e b y b a n a n a q u i t s ( A v e s: E m b e r i z i d a e )
J O S E P H M . W U N D E R L E , J R * & D . J E A N L O D G E r
* Department o f Biology, U niversity o f Puerto Rico, Cayey, P R 00 633 , U.S.A .t Terrestrial Ecology D ivision, Center fo r E nergy an d Environment Research, G.P.O. 3682, San Juan,
PR 00936 , U .S .A .
A b s t r a c t . T h e f o r a g i n g a b i l i ti e s o f n a i v e , h a n d - r e a r e d j u v e n i l e b a n a n a q u i t s , Coereba flaveola, w e r e
c o m p a r e d t o t h o s e o f c a p t i v e w i ld a d u l t s f o r a g i n g i n a n a r ti f ic i a l f l o w e r p a t c h c o n t a i n i n g e i th e r o p e n o r
c l o s e d f l o w e r s . F o r a g e r s r e m o v e d t h e t o p s f r o m c o v e r e d f l o w e r s i n o r d e r t o f e e d , t h e r e b y m a r k i n g a l l
v i s i te d f l o w e rs . O p e n f l o w e r s p r o v i d e d n o c l u e s a s t o p r e v i o u s v i s i t a t i o n . A d u l t s s e a r c h e d t h e p a t c h m o r e
t h o r o u g h l y a n d m a d e f e w e r f lo w e r re v i si t s d u r i n g e a c h f o r a g i n g b o u t t h a n d i d j u v e n il e s. F l o w e r
r e v i s it a t io n s b y j u v e n i l es w e re m o r e t h a n e x p e c t ed b y c h a n c e w h i l e t h o s e m a d e b y a d u l t s w e r e f e w e r t h a n
e x p e c t e d b y c h a n c e . T h i s w a s t r u e f o r b o t h o p e n a n d c o v e r e d f l o w e r t y p e s . T h e i n c r e a s e i n f o r a g i n ge f fi c ie n c y w i t h a g e i n v o l v e s s e v e r a l d i ff e r e n t c h a r a c te r i s t i c s. O n o p e n f l o w e r s , a d u l t s a n d j u v e n i l e s d i ff e r e d
i n t h e f re q u e n c y o f t h e i r p a t c h d e p a r t u r e s a n d r e t u rn s , a n d i n t h e i r p a t t e r n o f t u r n i n g i n t h e p a tc h , t h u s
r e s u ! t in g i n a m o r e c o m p l e t e s e a r c h o f th e p a t c h b y a d u l t s . O n c o v e r e d f l o w e r s , h o w e v e r , t h e t w o a g e
c l a ss e s d i f f e re d p r i m a r i l y i n t h e i r p a t t e r n s o f t u r n i n g , a n d a d u l t s m a d e a m o r e c o m p l e t e s e a r c h o f t h e
p a t c h . B o t h a g e c l a s se s u s e d t h e p r e s e n c e o r a b s e n c e o f f l o w e r c o v e r s a s a c l u e t o p r e v i o u s v i s i t a t i o n .
F o r a g e r s f r e q u e n t l y e n c o u n t e r f o o d i t e m s i n
c l u m p s o r p a t c h e s ( G i b b 1 95 8; T a y l o r 1 9 61 ; W i e n s
1 97 6). T h e f r e q u e n t o c c u r r e n c e o f t h i s r e s o u r c e
d i s p e r s i o n p a t t e r n a n d t h e p r o b l e m s f a c e d b y
c o n s u m e r s a s t h e y f o r a g e i n p a t c h e s h a s f o s t e r e d
n u m e r o u s t h e o r e ti c a l a n d e m p i r i c a l i n v e s t ig a t i o n s
( f o r r e c e n t r e v i e w s see : K r e bs e t a l . 1983 ; K r e b s &
M c C l e e r y 1 9 8 4 ; P y k e 1 9 8 4 ; G a s s & S u t h e r l a n d
1 98 5). M a n y o f t h e s e s t u d i e s h a v e f o c u s e d o n
n e c t a r i v o r e s w h i c h t y p i c a l l y f o r a g e i n f lo w e r
p a t c h es . N e c t a r i v o r e s m a y o b t a i n i n f o r m a t i o n
a b o u t t h e q u a l i t y a n d v a r i a b i l i ty o f r e w a r d s i n a
p a t c h a s t h e y f o r a g e ( P y k e 1 9 7 8 a , 1 9 8 1 ; H o d g e s
1 98 1). A s a n e c t a r i v o r e c o n t i n u e s t o f o r a g e , h o w -
e v e r, t h e p r o b a b i l i t y o f r e v i s i t in g a f l o w e r in c r e a s e s
( e .g . P y ke 1978b , 1981, 1982 ), t h e r e b y de c r e a s in g
p a t c h q u a l i t y . W h i l e v a r i o u s m o d e l s o f p a t c hc h o i c e a n d p a t c h d e p a r t u r e h a v e b e e n t e s t e d ( e . g .
K r e b s e t a l . 1 9 7 4 ) , t h e r e h a v e b e e n n o p r e v i o u s
s t u d ie s o n t h e o n t o g e n y o f p a t c h - u s e b e h a v i o u r .
F o r n e c t a r i v o r o u s b i r d s , n e c t a r i n fl o w e r s r e p r e -
s e n t s a f o o d r e s o u r c e t h a t i s e x h a u s t e d o n a s i n g l e
v i s i t a n d r e q u i r e s t i m e t o b e r e p l e n i s h e d . A n e c t a r i -
v o r e r e t u r n i n g t o a r e c e n t l y e m p t i e d f l o w e r w o u l d
h a v e a l o w e r r a t e o f n e t e n e r g y g a i n t h a n a n
i n d i v i d u a l m o v i n g t o a n o t h e r , a s y e t u n v is i te d
f l o w e r . B i r d s s h o u l d t h e r e f o r e a v o i d r e v i s i t s t o
f l o w e rs d u r i n g a f o r a g i n g b o u t . F i e l d s tu d i e s h a v e
c o n f i r m e d t h a t s u n b i r d s ( G i l l & W o l f 1 97 7) a n d
s o m e H a w a i i a n h o n e y c r e e p e r s (K a m i l 1 97 8) a v o i d
f l o w e r r e v i si t s. L e a r n i n g e x p e r i m e n t s h a v e f u r t h e r
d e m o n s t r a t e d t h a t w i l d a d u l t h u m m i n g b i r d s ( C o l e
e t a l . 1 98 2) a n d b a n a n a q u i t s (Coereba flaveola;
W u n d e r l e & S o t o 1 98 7) c a n b e m o r e e a s i ly t r a i n e d
t o v i s i t a f l o w e r in a n e w l o c a t i o n t h a n i n a l o c a t i o n
j u s t v i s i t e d e v e n w h e n t h e b i r d s a r e r e w a r d e d f o r
r e v i s i t s . I n t h e s e e x a m p l e s , a d u l t b i r d s m a y h a v e
l e a r n e d t o a v o i d r e v is i ts t h r o u g h p r e v i o u s e x p e r-
i e n ce , b e c a u s e r e v i s it s t o e m p t y f l o w e rs i n t h e w i l d
w o u l d r e s u l t i n r e d u c e d f o r a g i n g e f fi c ie n c y .
I m p r o v e d f o r a g i n g e f fi c ie n c y h a s b e e n c o r r e l a t e d
w i t h e x p e r i e n c e f o r a v a r i e t y o f b i r d s p e c ie s , e . g.
b r o w n p e l i c a n s (Pelicanus occidentalis, O r i a n s
1969 ; B r a nd t 1984 ; C ob le n t z 1986 ) , o l i va c e ous
c o r m o r a n t s (Phalacrocorax olivaceus, M o r r i s o n e t
a l . 1978 ), l i t t l e b lue he r ons (Florida caerulea,R e c he r & R e c he r 1969 ), c a t t l e e g r e t s (Ardeola ibis,
S ie g f r i e d 1972 ) , m oor he ns (Gall inula choropus ,
S u the r l a nd e t a l . 1986 ) , oys t e r c a t c he r s (Haemato-
pus os t ra legus , N o r t o n - G r i f f i t h s 1 9 6 8 ) , B o n a -
p a r t e ' s g u l l (Larus philadelphia, M a c L e a n 1 9 8 6 ) ,
r i n g - b i l l e d g u l l (L. delawarensis, M a c L e a n 1 9 8 6 ) ,
h e r r i n g g u l l s (L. argentatus V e r b e e k 1 9 7 7 ; M a c -
L e a n 1 98 6), g l a u c o u s - w i n g e d g u ll s (L. glaucescens,
S e a r c y 1978 ), r oy a l t e r n s (Sterna max ima, B u c k l e y
& B uc k le y 1974 ) , s a ndw ic h t e r n s (S. sandvicensis,D u n n 1 97 2), A m e r i c a n r o b i n (Turdus migratorius,
G o c h f e l d & B u r g e r 1 9 8 4), n o r t h e r n m o c k i n g b i r d s
44
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Wunderle & Lodge." Floral patch use by bananaquits 45
(Mimus polyglottos, Breitwisch et al. 1987), and
starlings (Sturnus vulgaris, Stevens 1985). In these
species, the improved foraging efficiency of adult s
results from more successful searches or more prey
captures.Whereas previous work suggests that adult
bananaquits should be more efficient foragers than
juveniles, it has not yet been shown in what manner
the foraging behaviour of bananaquits differs
between adults and juveniles. Impro ved patch use
due to experience could involve more efficient
movement patterns, the ability to recognize pre-
viously visited flowers, and decisions regarding
when to leave a patch, all of which may be partial ly
dependent on learning. In this study we investi-
gated these possibilities by comparing the foraging
patterns of captive, wild adult bananaqui ts (experi-
enced) with those of hand-reared juveniles (naive)
as they foraged in a patch containing a random
distribution of artificial flowers. We compared
juvenile and adult foraging abilities on open
flowers, which provided no external clues as to
previous visitation, versus covered flowers, which,
because they must have their tops removed by the
forager, provided potential visual clues as to
previous visitation.
We deliberately chose to compare revisitation
rates to open flowers versus closed flowers in aneffort to mimic field conditions. Bananaquits leave
no evidence of visitation on flowers with short
corollas, since they enter the front of the flower to
extract nectar. In contrast, bananaquits pierce the
base of the calyx or corolla of long flowers, thereby
providing a potential clue for subsequent bouts or
visitors. Such clues might be used by bananaquits
in selecting flowers or patches, just as sunbirds can
discriminate between open and closed mistletoe
flowers (Phragmanthera dshallensis, Gill & Wolf
1975).
M E T H O D S
Nestling bananaquits were collected and hand-
reared in Cayey, Puerto Rico during June and July
1984. Once fledglings were capable of feeding
themselves, their solid food mixture (Wunderle &
O'Brien 1985) was placed in a shallow dish at the
bottom of their cage. Twenty bananaquits were
housed in two cages (1 x 0-5 x 0.5 m) that received
indirect sunlight and a natural photoperiod(approximately 12 h of light and 12 h of darkness).
All juveniles were at least 45 days of age at the time
of the experiments and were capable of sustained
flight. Prior to the experiments, the hand-reared
juveniles had neve r fed from flowers. Ten juveniles
were used for these experiments, five for the openflowers and five for the cove red flowers.
Wild bananaquits were captured in mist nets in
Cayey, Puerto Rico in January and February 1985.
All wild birds were in adult plumage, indicating
that they were at least 1 year of age. They were
placed together in a cage and kept under the same
conditions as the hand-reared juveniles. Ten adults
were used for the experiments, five for the open
flowers and five for the covered flowers. At the end
of the study, all adults were released.
The experiments were conduc ted in a flight cage
measuring 1 × 1 × 3 m with a floral board, measur-
ing 1 × 1 m, til ted 20 ° from the vertical at the back
of the cage. The flight cage was covered with a
black plastic sheet, except for the front, where a
one-way mirror measuring 35 x 60 cm was located
for observation. A fluorescent light was affixed to
the interior cage-top for illumination of the floral
board. The floral board contained a random array
of 85 red and 85 yellow artificial flowers inter-
spersed within a grid of 19 vertical and 19 horizon-
tal perches. Two flower colours were used in our
experiments because the results are intended toserve as the basis for future wo rk on the response of
bananaquits to differences in food rewards between
the two flower colours. As in previous work
(Wunderle & O'Brien 1985), we found that the
bananaquits showed no colour preferences when
both flower colours provided the same rewards.
Each flower consisted o f a straw floral tube l cm
long x 0"6 cm in diamet er at tached with a plastic
sealant to the centre of a numbered coloured tape
background (3-5 x 3"5 cm). The distance between
the closest flowers was 4-5 cm. For some experi-
ments, the floral tubes were left uncovered (desig-
nated open flowers) while in other experiments all
floral tube openings were covered with a coloured
tape disk (designated covered flowers), which the
bird had to pry off prior to feeding. To train the
birds to feed on the board, all flowers were filled
with a 15% sucrose solution (the same solution,
henceforth called nectar, was used in all experi-
ments). A group of birds was placed in the flight
cage, and within 45 min all individuals had learned
to feed from the open flowers. Once an individual
had learned to feed on open flowers, it was trainedto feed on covered flowers by presenting it with
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46 Anim al Behaviour, 36, 1
partially covered flowers on the edge of the floral
board and covered flowers in the centre. Each
flower was filled with 10 #1 of nectar for the
experiments. We measured the quantity of nectar
remaining in flowers following a single feeding visitby probing the flower with a micropipette. Five
visited flowers were sampled for each individual
(five juveniles and five adults; N= 50) and no
remain ing nectar was detected. Thus , we assume
that all nectar was removed dur ing a forager's first
visit to a flower.
Once it became accustomed to feeding on the
board, an individual was released into a flight cage
containin g no food or water. After an adjustment
period of 1 h, the bird was presented with the floral
board. All behaviour was recorded by an observer
watching through the one-way mirror. The bird
usually flew immediately to the floral board, and
the sequence of numbered flower visits was entered
on a computer. The board was removed after the
bird ceased to forage for 1 min; most foraging
periods were 10-15 min. Foraging periods were
separated by a 1-h interval in which the bird
received no food. Each ind ividual was given three
consecutive presentations (designated as runs) in
the morn ing (0600-1130 hours). Exper iments with
juven iles with open flowers were ru n in the first
week of October followed by experiments withjuveniles with covered flowers in the second week.
Experiments with adults with open flowers were
run in the first week of June followed by experi-
ments with adults with covered flowers in the
second week.
In these experiments a probab ility of type I error
of 0-05 or less was accepted as significant, but we
show greater values for descriptive purposes.
RESULTS
F l o w e r R e v i s i t a t io n s
To compare flower revisitation rates for adult
and juvenile bananaquits foraging on open and
covered flowers, we calculated the total number of
flower visits and revisits during each foraging
sequence. The numbers of visits and revisits were
greater in juveniles (open flowers: )(-+_so = 172.0 +
61.2 visits, with )?+SD=77.7_+56-7 revisits;
covered flowers: .(±SD = 112-4_+ 30'0 visits, with
)? + SD = 49-2 + 22'8 revisits) than in adul ts (open
flowers: .('+SD = 138"4+40.9 visits, with ) ?+so =30'5+22"2 revisits; covered flowers: )?+so=
102.1+26.1 visits, with )~-I-SD=17.7+ 15-8 re-
visits). A two-way analysis of covariance
(ANCOVA) with repeated measures was used to
analyse the relationship of revisits with two treat-
ments, bi rd age (juvenile or adult), and flower type(open or covered), while removing variation due to
the total number of flower visits (the covariate).
The total num ber of flower visits was foun d to co-
vary significantly with revisits ( F= 146.99, df= 1 ,P < 0.0001). The ANCOVA indicates that age had
a s ignificant effect on revisitation, after vari ation
due to the total number of flower visits was
removed by the covariate (F=22-27, d f = l ,P=0-0003). Juveniles made far more revisits per
total n umber o f visits than adults. Flower type also
signif icantly affected revis itation (F= 10.54, d f= 1,
P = 0'005), and the birds were more likely to revisit
in the open-flower than in the closed-flower treat-
ment. Although the data suggest that juveniles
behaved similarly regardless o f flower type, adults
revisited covered flowers less fr equently than open
flowers. No significant interaction was found,
however, between age and flower type in the
ANCOVA (F= 0.10, d f= 1, P = 0.76). Differences
in revisitation behaviour between runs were only
suggestive (F=3'00, d f = 2 , P=0-06), but there
were no significant interactions with either age
(run x age: F= 0.84, dr= 2, P= 0.44) or flower type(ru n x flower: F= 1-90, d f = 2 , P=0.17). This indi-
cates that overall revisitation behaviour differed
only slightly between runs, and that behaviour over
runs was no t related to age or flower type.
To examine the patterns of flower revisitations
further, a frequency distribution (tabulating the
number of flowers receiving zero visits, one visit,
etc.) was calculated for each bird during the third
run (run C). If each visit to a flower was indepen-
dent of all other visits by the same ind ividual, the
observed distribu tions should approximate a Pois-
son distribution. The frequency distributions for
each individua l differed significantly from a Pois-
son distribution (goodness-of-fit test with a G-
statistic), regardless of the flower type or age. Data
were then pooled within age classes when no
significant heterogeneity among individuals was
indicated by a replicated goodness-of-fit test with a
G-statistic (Sokal & R ohl f 1981). The pooled
frequency distribution for juvenile visits to open
flowers was signif icantly different from the
expected Poisson distribution (P<0.005), with
juveniles revisiting more flowers than expected bychance (Table I). Similarly, the distribution of
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Wunderle & Lodge: Floralpatch use by bananaquits
Table I . Observed dist r ibut ions of visi t s and revisit s by fo raging juveni le and ad ul tbananaqu i t s com pared w i th the Po i sson d i s t r i bu t ion
47
Age* F lower t ype Di s t r i bu t i on
N u m b e r o f v i s it s t
0 1 2 3 > 4 G-value
Juveni le Op en Obs erved 609 150 66 22 3Pois son 557 236 50 7 1 68.255
Ad ul t O pen Obs erved 517 293 38 2 - -Pois son 547 241 53 9 23-255
Juveni le Cov ered Obs erved 600 154 74 20 2Pois son 550 239 52 8 1 188.17,
Ad ul t Cov ered Obs erved 510 305 35 0 0Poisson 547 241 62 - - 40.82*
* Each grouping i s poo led for f ive individuals dur ing runt No te tha t two or m ore visi ts i s equivalent to a revisi t.
* P < 0.005.
C .
j u v e n i l e v i s it s to c o v e r e d f l o w e r s w a s s i g n i f i c a n tl y
d i ff e re n t f r o m e x p e c t e d ( P < 0 . 0 0 5 ) , a g a i n w i t h
r e v is i ts h i g h e r t h a n e x p e c t e d . A l t h o u g h a d u l t s a l s o
s h o w e d s i g n i f i c a n t d i f f e r e n c e s f r o m t h e e x p e c t e d
P o i s s o n d i s t r ib u t i o n ( o p e n , P < 0 - 0 0 5 ; c o v e r e d ,
P < 0. 0 0 5) , t h e y m a d e f e w e r r e v i si t s t h a n e x p e c t e d .
Overal l Coverage of the Patch
T o q u a n t i f y t h e p r o p o r t i o n o f p a t c h a r e a v i s i t ed
b y a f o r a g e r d u r i n g e a c h r u n , w e d i v i d e d t h e p a t c h
i n t o 3 6 s e c t o r s a n d c a l c u l a t e d t h e t o t a l n u m b e r o f
s e c t o r s v i s i t e d b y t h e f o r a g e r . E a c h s e c t o r w a s
1 5 x 1 5 c m , s i nc e (1 ) a f o r a g i n g b a n a n a q u i t c o u l d
r e a c h f l o w e r s f r o m a c e n t r a l l o c a t i o n w i t h o n l y
m i n i m a l m o v e m e n t , a n d ( 2) t he 1 5 -c m d i m e n s i o n s
a l l o w e d e q u a l d i v i s i o n o f t h e f l o r a l b o a r d a l o n g
h o r i z o n t a l a n d v e r t i c a l p e r c h e s . S t a n d a r d
A N C O V A p r o c e d u r e s w e r e u s e d t o a n a l y s e t h e
r e l a t i o n s h i p o f t o t a l s e c t o r v i s it s w i t h a g e a n d
f l o w e r t y p e u s i n g t h e t o t a l n u m b e r o f f lo w e r v i s i ts
a s th e c o v a r i a t e . T h e n u m b e r o f s ~J cto r v i s it s d i d n o t
c o - v a r y s i g n i f i c a n t l y w i t h t o t a l f l o w e r v i s i t s i n a
f o r a g i n g s e q u e n c e ( F = 0 . 7 9 , df= 1, P = 0 . 3 9 ) . A g e
s i g n if i c a n tl y a ff e c t e d th e n u m b e r o f s e c t o r s v i s i t e d
( F = 4 . 4 1 , df= l , P = 0 . 0 5 ) . J u v e n i le s v is i te d fe w e r
s e c to r s e v e n t h o u g h t h e y m a d e m o r e f l o w e r vi s it s
t h a n a d u l t s . F l o w e r t y p e a l s o s i g n i f i c a n t l y
i n f l u e n c e d t h e n u m b e r o f s e c t o r s v i s i t e d ( F = 6 . 1 7 ,
df=l, P = 0 - 0 2 ) , w i t h c o v e r e d f l o w e r s e l ic i ti n g
m o r e s e c t o r v i si t s t h a n o p e n f l o w e r s . N o s i g n i f i c a n t
i n t e ra c t io n w a s f o u n d b e t w e e n a g e a n d f l o w e r ty p e( F - - 0 . 0 1 , df= 1 , P = 0 . 9 3 ) . I n a d d i t i o n , t h e r e w e r e
n o d i f fe r e n c e s i n b e h a v i o u r b e t w e e n r u n s ( F = 0 . 3 1 ,
df=2, P = 0 . 7 3 ) , n o r w e r e t h e r e a n y s i g n i f i c a n t
i n t e r a c t i o n s w i t h r u n s ( r u n x a g e : F = 0 . 4 2 , df= 2,P = 0 . 6 6 ; r u n x f lo w e r: F = 0 . 1 3 , df=2, P = 0 . 8 8 ;
r u n x a g e x fl o w e r : F = 1 .2 8 , df= 2, P = 0-29) .
S t r o n g e v i d e n c e f o r s y s te m a t i c p a t t e rn s o f m o v e -
m e n t b y a d u l t s i s i l l u s tr a t e d b y s i g n i f i c a n t p o s i ti v e
c o r r e l a t i o n s b e t w e e n t h e n u m b e r o f s ec t o r s v is i te d
a n d t o t a l f lo w e r v i s it s f o r b o t h o p e n a n d c l o s e df lo w e rs ( r = 0 . 8 1 2 , P < 0 . 0 1 ; r = 0 - 8 9 3 , P < 0 . 0 1 ,
r e s p e c t i v e l y ) . I n c o n t r a s t , j u v e n i l e s s h o w e d n o
s i g n i f ic a n t c o r r e l a t i o n s b e t w e e n t h e n u m b e r o f
s e c t o r s v i s i te d a n d t o t a l f l o w e r v i s it s f o r e it h e r o p e n
( r = 0 . 1 2 7 ) o r c o v e r e d fl o w e rs ( r = 0 . 4 6 7 ) . T h e s e
d i f f e r e n c e s b e t w e e n a d u l t s a n d j u v e n i l e s e x p l a i n
w h y s e c t o r v i s i ts d i d n o t s i g n i f ic a n t l y c o - v a r y w i t h
f lo w e r vi si ts in t h e A N C O V A a b o v e .
P o s i t i o n e f f e c t s w e r e p r e v i o u s l y o b s e r v e d i n
b a n a n a q u i t s f o r a g i n g i n a f lo r a l p a t c h ( W u n d e r l e ,
u n p u b l i s h e d d a t a ) a n d g i v e n a c h o i c e o f fl o w e r s in
t w o d i f f e r e n t p o s i t i o n s ( W u n d e r l e & S o t o 1 98 7). T o
q u a n t i f y s u c h a p o s i t i o n e f f e c t , w e c a l c u l a t e d a l l
s e c t o r v is i ts a b o v e a n d b e l o w t h e h o r i z o n t a l m i d -
l i n e o f t h e f lo r a l b o a r d ( T a b l e I I ) , a n d a l l s e c t o r
v i s it s o n t h e l e f t a n d r i g h t o f t h e v e r t i c a l m i d - l i n e .
S i g n i f i c a n t p r e f e r e n c e s f o r t h e u p p e r p a r t o f t h e
b o a r d o c c u r r e d w h e n ju v e n i l e s f e d o n o p e n f l ow e r s
( t w o - t a i l e d , W i l c o x o n s i g n e d - r a n k s t e s t , T = 1 18 .5 ,
P < 0 . 0 0 1 ) a n d o n c o v e r e d f lo w e rs ( T = l I 4 . 0 ,
P < 0 - 0 0 2 ) . A d u l t s s h o w e d a s i m i l a r p r e f e r e n c e f o r
t h e u p p e r p a r t o f th e p a t c h w h e n p r e s e n t e d w i th
o p e n f l o w e r s ( T = 1 0 2. 5, P < 0 . 0 01 ) , b u t s h o w e d n os i g n i f i c a n t p r e f e r e n c e w h e n f e e d i n g o n c o v e r e d
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4 8 Animal Behaviour, 36, 1
Table I I . Pos i t ion preferences of juveni le and adul t banan aqui ts foraging in an ar t i f ic ia l f lower pa tchwi th op en and covered f lowers for a ll individuals and a l l runs
Nu mb er of sec tors visi ted (Mean_+ SE)*F l o w e r
Age type Up pe r ha l f L ower ha l f P :~ R igh t ha l f L e f t ha l f P
Juveni le Op en 17.0- t-0 .3 11.2_+ 1.2 < 0 . 00 1 1 4. 6 _+ 0. 7 13.7+0.9 NSAd ul t 16 .9+0 .3 13"8_+0"7 < 0"0 01 15" 0_+ 0"6 15"7+0"5 NSJ u ve n il e C o v e re d 1 4 . 3 _ + 0 . 6 8 . 5 _ _ _ 0 . 9 < 0 .0 0 2 1 1 - 3 - t - 0 . 9 1 1 .3 _ + 0. 9 NSAd ul t 13.5+0 .8 11.9 _+0 .8 NS 13"0+0"8 12"4+0"9 NS
* The n um ber of 15 x 15-cm sec tors visi ted by foragers on each ha l f of the f lora l boa rd was used to testfor posi t ion preferences ( tota l numb er of sec tors = 36) .
:~ W ilcox on signe d-rank s tests, two-ta iled.
r " - "3 ADULT/
0 . 28 "~ m J U VEN ILE
IO. r 6 ~
0.12
0.08
0 .04
0.12
0.08
0.04
-135" -900 -45 " (7 45* 90* 135" 180"
A N G L E
Figure I . Dist r ibut ion of turning angles for adul t andjuven i le bananaqu i t s f e ed ing on op en (A) and cove red (B)flowers in an art ificial floral patch. See text for anexplanat ion of turning angles.
f l ow e r s ( T = 4 6 - 5 , P > 0 . 6 0 ) . N o e v i d e n c e f o r a
r i g h t / l e f t p o s i t i o n b i a s w a s f o u n d f o r e i t h e r a d u l t s
o r j u v e n i l e s f e e d i n g o n e i t h e r f l o w e r t y p e .
M o v e m e n t P a t t e r n s i n t h e P a t c h
A n i m p o r t a n t f a c t o r r e s p o n s i b le f o r d i ff e re n c es
i n a f o r a g e r ' s c o v e r a g e o f th e p a t c h a n d a s s o c i a t e d
f l o w e r r e v i s i ta t i o n s m a y b e t h e p a t t e r n o f t u r n i n g .
T o q u a n t i f y t u r n in g , w e m e a s u r e d a f o r a g e r ' s t u r n
a n g l e t o a th i r d f l o w e r f r o m a l i n e o f m o v e m e n tf o r m e d b y t h e t w o p r e v i o u s f l o w e r v i s it s . F o r
e x a m p l e , w e m e a s u r e d t h e a n g l e f r o m f l o w e r o n e
a n d t w o t o f l o w e r t h r e e , t h e n t h e a n g l e f r o m f l o w e r s
t w o a n d t h r e e t o f l o w e r f o u r a n d s o o n . O n t h e
f l o r a l - b o a r d g r i d , t h e s e a n g l e s c o u l d r a n g e f r o m
f o r w a r d m o v e m e n t w i t h n o c h a n g e ( 0° ), f o r w a r d t o
t h e r i g h t b y 4 5 ° , p e r p e n d i c u l a r t o t h e r i g h t ( 9 0 ° ),
b a c k t o t h e r i g h t ( 1 3 5 ° ) , o r a c o m p l e t e r e v e r s a l o f
1 80 ° C o r r e s p o n d i n g t u r n s t o t h e l e ft o f t h e d i re c -
t i o n o f m o v e m e n t w e r e - 4 5 ° , - 9 0 ° , o r - 1 35 °. W e
r e c o r d e d a l l t u r n i n g a n g l e s i n e a c h f o r a g i n g b o u t ,
e x c l u d i n g t h o s e e n d i n g i n a fl i g h t d e p a r t u r e , b e g i n -
n i n g w i t h a f li g h t r e t u r n , a n d t h o s e w i t h f l o w e r s
a l o n g t h e f l o r a l - b o a r d p e r i m e t e r . T h e f r e q u e n c yd i s t r ib u t i o n s o f t u rn s a m o n g t h e ei g h t tu r n i n g -
a n g l e c a t e g o r i e s w e r e a n a l y s e d f o r h e t e r o g e n e i t y
a m o n g r u n s w i t h i n i n d i v i d u a l s , h e t e r o g e n e i t y
a m o n g i n d i v i d u a l s w i t h i n a g e c l a s s e s , d i f f e r e n c e s
b e t w e e n a g e c l as s e s , a n d g o o d n e s s - o f - f i t t o a n
e q u a l d i s t r i b u t i o n u s i n g r e p l i c a t e d g o o d n e s s - o f - f i t
t e s t s a n d G - s t a t i s t i c s ( S o k a l & R o h l f 1 9 8 1 ) .
T h e d i s t r i b u t i o n o f t u r n i n g a n g l e s in t h e o v e r a l l
g o o d n e s s - o f - f i t t e s t i n d i c a t e s t h a t t h e f o r a g e r s d i d
n o t t u r n e q u a l l y i n a l l o f t h e e i g h t p o s s ib l e d i r e c -
t i o n s ( G - s t a t i s ti c s , P < 0 ' 0 5 ). A g e a n d f l o w e r t y p e
w e r e b o t h a s s o c i a t e d w i t h d i f f e re n t p a t t e r n s o f
t u r n i n g ( F i g . 1 ). B o t h j u v e n i l e s a n d a d u l t s d i s -
p l a y e d s i g n i f i c a n t h e t e r o g e n e i t y a m o n g i n d i v i d u a l s
w i t h i n a g e c l a s s e s w h e n f e e d i n g o n o p e n f l o w e r s
( juven i l e s : G = 71 .05 , P < 0 -005 ; a du l t s : G = 46 .38 ,
P < 0 . 0 2 5 ) . F u r t h e r m o r e , s i g n i fi c an t h e t e r o g e n e i t y
a m o n g r u n s w a s f o u n d f o r t w o j u v e n i le s w h e n
f o r a gi n g o n o p e n f lo w e rs (G = 2 5 . 7 2 , P < 0 . 0 5 ;
G = 3 2 . 8 3 , P < 0 .0 0 5 ) , b u t n o a d u l t s s h o w e d h e t e r o -
g e n e i t y a m o n g r u n s . T h e s e r e s u l t s s u g g e s t t h a t
a l t h o u g h a d u l ts v a r y i n th e i r m o v e m e n t p a t t e rn s ,
i n d i v id u a l s h a v e c o n s i s t e n t p a t t e r n s o f t u r n i n gw h i c h m a y h a v e d e v e l o p e d t h r o u g h p r e v i o u s e x -
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Wu nderle & Lodg e: F loral patch use by bananaquits 4 9
p e r i e n c e w i t h o p e n f l o w e r s . O v e r a l l , t h e t u r n i n g
m o v e m e n t s o f a d u l t s ( a l l r u n s p o o l e d ) w e r e s ig n i fi -
c a n t l y d i f f e r e n t ( G = 1 6 4 . 7 6 , P < 0 - 0 0 5 ) f r o m t h o s e
o f t h e j u v e n i l e s ( a ll r u n s p o o l e d ) w h e n f e e d i n g o n
o p e n f l o w e r s (F i g . 1 A ) . J u v e n i l e s a s a g r o u p t e n d e dt o m a k e a l i n ea r p r o g r e s s i o n a n d r a r e ly t u r n e d
w h e n f e e d i n g , w h e r e a s a d u l t s t u r n e d e q u a l l y i n a l l
d i r e c t i o n s e x c e p t 1 80 ° ( F i g . 1 A ) .
W h e n f e e d i n g o n c o v e r e d f l o w e r s, j u v e n i l e s a n d
a d u l t s s h o w e d n e i t h e r h e t e r o g e n e i t y w i t h i n i n d i -
v i d u a ls ( a ll i n d iv i d u a ls , P > 0 . 0 5 ) , n o r h e t e r o g e -
n e i t y a m o n g i n d i v i d u a l s w i t h i n e a c h a g e c l a s s
( j u v en i le s : G = 2 7 . 0 8 , N S; a d u l t s : G = 3 9 . 5 5 , M S ).
T h u s , a l l j u v e n i l e s c o n s i s t e n t l y t u r n e d i n t h e s a m e
m a n n e r a n d a l l a d u l ts c o n s i s t e n t l y tu r n e d i n t h e
s a m e m a n n e r w h e n f e e d i n g o n c o v e r e d fl o w e rs . W e
t h e r e f o r e p o o l e d a l l th e i n d i v i d u a l j u v e n i l e t u r n i n g
r e su l ts f o r c o v e r e d f lo w e r s a n d c o m p a r e d t h e m
w i t h t h e p o o l e d a d u l t r e s u l t s ( F i g . 1 B). T h e a n a l y s i s
i n d i c a t e s a s i g n i f i c a n t d i f f e r e n c e ( G = 6 0 . 6 6 ,
P < 0 . 0 0 5 ) b e t w e e n a d u l t a n d j u v e n i l e t u r n i n g
a n g le s w h e n f e e d in g o n c o v e r e d f lo w e rs . T h e m a j o r
d i f f e r e n c e b e t w e e n t h e t w o a g e c l a s s e s i s i n t h e
d i s p r o p o r t i o n a t e l y h i g h f r e q u e n c y o f 1 80 ° t u r n s
m a d e b y j u v e n i l e s , s in c e e l i m i n a t i o n o f t h is c a t e -
g o r y a n d a n a l y s i s o f t h e s e v e n r e m a i n i n g c a t e g o r i e s
i n d i c a te s n o s i g n i fi c a n t d i f f e re n c e ( G = 6 . 4 2 , M S)
b e t w e e n t h e t w o a g e c l a s s e s . T h u s , j u v e n i l e sr e v e r s e d t h e i r m o v e m e n t p a t h m o r e o f t e n t h a n
a d u lt s w h e n f e e d in g o n c o v e r e d f l o w e rs .
T h e p r e s e n ce o r a b s e n c e o f c o v e r s o n t h e f l o w e r s
w a s a s s o c i a t e d w i t h d i f f e r e n c e s i n t h e p a t t e r n o f
t u r n i n g w i t h e a c h a g e c l as s . S i g n i f i c a n t d if f e r e n c e s
i n t u r n i n g p a t t e r n s w e r e f o u n d b e t w e e n o p e n a n d
c l o s e d f l o w e r s f o r j u v e n i l e s ( G = 2 1 3 . 5 4 , P < 0 . 0 0 5 ) ,
a n d a l s o f o r a d u l t s ( G = 2 1 . 44 , P < 0 - 00 5 ). T h e r e -
f o re , t h e p a tt e r n o f t u r n i n g a n d m o v e m e n t t h r o u g h
t h e p a t c h d i f f er e d , d e p e n d i n g u p o n b o t h a g e a n d
f l o w e r t y p e .
Pa tc h D e p a r tu r e s an d R e W r n s
F l i g h t s o f f t h e f lo r a l b o a r d t o a n e a r b y p e r c h
f o l l o w e d b y re t u r n f l ig h ts w e r e i m p o r t a n t c o m p o -
n e n t s o f th e f o r a g i n g m o v e m e n t s o f al l b a n a n a -
q u i ts . D u r i n g e a c h f o r a g i n g s e q u e n c e , w e r e c o r d e d
t h e n u m b e r o f t i m e s a b i rd d e p a r t e d f r o m a n d
r e t u r n e d t o t h e f l or a l b o a r d . U s i n g t h e n u m b e r o f
f l o w e r v i si ts as a c o v a r i a te , w e u s e d a n A N C O V A
a n a l y s is o n a l l b i r d s a n d a l l r u n s t o e x a m i n e t h e
e ff ec t o f a g e a n d f l o w e r t y p e o n t h e n u m b e r o f t i m e sa fo r a g e r d e p a r t e d f r o m t h e f l o ra l b o a r d d u r i n g a
Table I I1 . Average number ( )?+SE) of ful l and emptyflowers within a 10 cm radius of a flower at t ime ofdepar ture are compared w i th those wi thin a 10 cm radiusat si te of return
F l o w e rFlower
Age type Behav iour Fu l l E m pty Ar t
Juveni le Open Depar ture 2.7__+0.3 4 .9+ 0.3
Re tu rn 2 -5+0 .4 4 -3+0 .3 25P* NS NS
Adul t Open Depa r tu re 3 .3+0 .4 5 .2+0 .5Re tu rn 5 .4+_ 0-5 3 .8+0 .6 29
P <0 .01 <0 .05Juven i le Cove red Depa r tu re 6 .0+0 .8 3 .7+0 .5
Re tu rn 7 .2+0-5 1 .4+0 .3 27P <0 .02 <0 .001
Adul t Cove red Depa r tu re 2 .9+0 .8 6 .1+1 .1Re tu rn 6 .4+0 .7 2 .9+ 0 .6 23
P <0-001 <0-02
* P-values are given for paired t-tests as explained in thetext.
t N represents the numb er of pa i red depar tures andreturns.
f o r a g i n g r u n ( T a b l e I II ). T h e n u m b e r o f d e p a r t u r es
d i d n o t s i g n if i ca n t ly c o - v a r y ( F = 0 . 0 2 , df= 1,
P = 0 .9 0 ) w i t h t h e n u m b e r o f f l o w e r v i si t s d u r i n g a
f o r a g i n g r u n . A g e w a s s ig n i f i c a n t ly a s s o c i a t e d w i t hd i f fe r e n c e s i n t h e n u m b e r o f d e p a r t u r e s d u r i n g a
f o r a g i n g s e q u e n c e ( F = 8 . 0 2 , d f = l , P = 0 . 0 1 ) .
F u r t h e r a n a l y s i s d e m o n s t r a t e d s i g n i f i ca n t c o r r e l a -
t i o n s b e t w e e n f l o w e r v i s it s a n d f l ig h t d e p a r t u r e s f o r
adu l t s (open : r = 0 -814, P < 0"01 ; co ve red : r = 0 ' 736 ,
P < 0 "0 1), b u t n o t f o r j u v e n i l e s (o p e n : r = 0 . 1 9 0 , y s ;
cov e red : r = - 0" 139, NS). F l ow er t yp e a l s o s i gn i f i -
c a n t l y in f l u e n c e d t h e n u m b e r o f d e p a r t u r e s
( F = 9 -9 9, df= 1 , P = 0"007), an d b i rd s l e f t t he pa t ch
w i t h o p e n f l o w e r s m o r e f r e q u e n t l y t h a n w i t h c l o s e d
f l o w e r s . N o s i g n i f i c a n t i n t e r a c t i o n o c c u r r e d
b e t w e e n a g e a n d f l o w e r t y p e ( F = 3 . 3 5 , df= 1,P = 0 . 0 9 ) .
E x p e r i e n c e o b t a i n e d d u r i n g t h e t h r e e p r e s e n -
t a t i o n s ( r u n s) s i g n i f ic a n t ly a ff e c t e d t h e n u m b e r o f
f o r ag e r d e p a rt u re s ( A N C O V A , F = 5 . 3 8 , d f = 2 ,
P = 0 . 0 0 9 ) , b u t t h e e f fe c t o f e x p e r i e n c e w a s c o m -
p l e x . T h e r e w a s a s i g n i f i c a n t i n t e r a c t i o n b e t w e e n
a g e a n d r u n ( F = 3 " 2 8 , d f= 2 , P = 0"05) , and adu l t s
t e n d e d t o d e c r e as e t he n u m b e r o f d e p a r t u r e s w h i l e
j u v e n i l e s te n d e d t o i n c r ea s e t h e n u m b e r o f d e p a r -
t u r e s o v e r r u n s . A s i g n if i ca n t in t e r a c t i o n b e t w e e n
f l o w e r t y p e an d r u n w a s a l s o o b s e r v e d ( F = 5 - 1 1 ,d f= 2 , P = 0 . 0 1 ); f o r ag e r s d e p a r t e d m o r e f r e q u e n t l y
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50 Animal Behaviour, 36, 1
from the open-flower patch than the closed-flower
patch with each run. The suggestive (F=3-09,
df= 2, P = 0-06) interaction of run, age and flower
type indicates that these factors together may
influence patch departures by the foragers.To determine whether the foragers consistently
left depleted areas and flew to unvisited sites, we
calculated the number of full and empty flowers
within a 10 cm radius of both the last flower visited
prior to departure and the first flower visited on
returning. We selected 10 cm as a distance over
which a forager could reach other flowers without
flying, and with a minim um o f hopping movement.
A paired t-test was used to compare the full flowers
near the sites of depar ture and return; the analysis
was repeated for empty flowers. Lower local
resource availability near patch borders would be
reflected in fewer full flowers within the 10 cm
radius. The distribution of empty flowers was not
simply the inverse of full flowers since much of the
floral board contai ned no flowers. If the birds were
flying from the patch edge or depleted areas to
unvisited areas in the patch, we would expect
differences in the numbers of full and empty flowers
near the site of departure and return.
For juveniles feeding on open flowers, the patch
departures and returns were unrelated to local
resource availability. This was evident from thealmost identical numbers of full flowers within 10
cm of the points of departure and return (Table
III); similar results were found for empty flowers.
These data indicate that juveniles did not
remember where they had previously fed. Covered
flowers, however, may provi de clues enabling juve-
niles to leave depleted areas for richer sites in the
floral patch. For instance, there were significantly
more full flowers at the return site than on
departure (t=2.59, P<0-02), and significantly
fewer empty flowers on the return (t=3"86,
P<0.001) when juveniles foraged on covered
flowers. Thus the juveniles were able to use the
covered flowers for locating richer areas of the
floral patch, but were unable to do so when the
flowers were open. Yet, despite the finding that
juveniles were able to use covered flowers for
locating richer areas of the floral patch when
departing and returning, they still displayed similar
revisitation rates fo r open and covered flowers. We
attribute this to the previously mentioned tendency
of juveniles to reverse their path of movement to
revisit flowers while moving across the patch withcovered flowers.
Adults departed from areas with low resources
and moved to richer areas, whether foraging on
open or closed flowers. For instance, with covered
flowers, more full flowers were at the site of return
than at the site of departure (t= 3-93, P< 0.001),and more empty flowers were at the site of
departure t han at the site of return (t =2-76,
P < 0.02). This same trend was found with open
flowers in which more full flowers were at the site of
return than that of departure (t=3-12, P< 0.01)
and correspondingly fewer empty flowers were in
the area of return than near the site of departure
(t=2. 38, P<0. 05) . Thus, adults were capable of
remembering the areas of the patch in which they
had fed even without clues, while juveniles did no t
do so unless provided with visual clues.
D I S C U S S I O N
As expected, adults searched the patch more
thoroughly (i.e. visited more sectors) and made
fewer flower revisitations during each foraging
bout than did the juveniles. Flower revisitations by
juveniles were more than expected by chance while
those made by adults were fewer than expected by
chance. This was true for both the open and
covered flower types. The adults were apparentlyable to re member the locations of previously visited
flowers, even though the open flowers may have
provided no information about previous visi-
tations. Hence, it appears that an increase in
foraging efficiency with age involves several differ-
ent characteristics.
A major difference between adults and juveniles
foraging on open flowers was in patch departures
and returns. The frequency of adult departures was
correlated with the number of flower visits, and
adults tended to fly from dep leted areas and the less
productive patch edge to unvisited areas of thepatch. This was not characteristic of the juveniles,
which departed and returned to the patch in a
ran dom manner. A second age difference, seen with
open flowers, was in the pattern of turning: juve-
niles tended to probe the flowers directly in front of
them, while adults turned widely to feed on nearby
flowers. The overall forward mov ement pattern of
juveniles frequently resulted in open flower revisits
when juveniles reached the patch edge, reversed
direction, and revisited all the flowers along the
same horizontal perch.Covered flowers have the potential to provide
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Wunderle & Lodge: Floral patch use by bananaquits 51
foragers with clues regarding previous visitat ions,
and it was evident that these clues were used by
adults and sometimes by juveniles. Under these
circumstances, the patterns of turning differed
between individuals within each age class but wereconsistent for each adult and most o f the juveniles.
When vis iting covered flowers, adul ts differed from
juveniles primarily in the patter n of turning, espe-
cially in the frequency of 180 ° turns. Adults rarely
reversed their direction of movement, while juve-
niles frequently did so. Yet, juveniles, as well as
adults, departed from nectar-poor areas of the
board for nectar-rich areas, suggesting that both
used flower covers as a clue.
Whereas the flower covers used in our experi-
ments are certainly more obvious visual clues than
flower-punctures in nature, the speed with which
both captive adults and naive juveniles responded
to them suggests that wild banana quits probably
also use available visual clues which indicate
previous visitation. This is supported by observa-
tions that bananaquits (Wunderle, unpublished
observations) and other nectarivorous species may
use flower-punctures in assessing resources in the
wild. For example, orchard orioles, leterus spurius,
feeding on Malvaviseus sp. flowers puncture the
corolla near its base and remove nectar. Flowers
punctured by orioles produce no more nectar, andhummingbi rds avoid visiting such flowers possibly
by using the oriole punctures as clues (Montgo-
merie 1979).
Previous experimental work by Hainsworth et al.
(1983) indicated that three-dimensional inflores-
cences resulted in fewer revisits by hummingbirds
relative to total flower visits than did two-dimen-
sional infloreseences. In our study the two-dimen-
sional patch may have cont ributed significantly to
flower revisitations, even by experienced adults.
While foraging on the board, adults occasionally
revisited a flower as they moved towards an
unvisited area. A three-dimensional patch might
reduce this tendency. Thus, by perching off the
floral board they may have obtained a better
perspective of the patch that was useful both for
remembering areas of previous visits and for
locating new areas.
Memory plays a valuable role in the foraging
behaviour of a variety of animals (Shettleworth
1984). For example, memory is particular ly impor-
tant in many parid and corvid species that store
food and recover it at a later date (Balda 1980;Shettleworth & Krebs 1982; Vander Wall 1982;
Sherry 1984a, b; Kamil & Balda 1985; Bunch &
Tomback 1986). In avian nectarivores, memory
undoubtedly is also important in reducing flower
revisits by foragers (Gill & Wol f 1977; Kamil 1978).
In our study, the importance of memory is sug-gested by the departure of adults from depleted
areas of the patch and their movement to unvisited
areas when they foraged on open flowers (i.e.
flowers with no clues indicating previous visi-
tation). It seems likely that a particular pattern of
the random array of red and yellow flowers in one
section of the patch is remembered by the depar ting
bananaquit and thus avoided on its return. Simi-
larly, wild hummingbirds remember the location of
resource patches relative to one another (Miller &
Miller 1971). On a finer scale, however, it may be
impossible to remember numerous individual
flowers within a patch during a foraging bout, and
thus revisits are inevitable. Even wild humm-
ingbirds revisit some flowers during the same
foraging bout at frequencies of 5-10% (Pitelka
1942). In this instance, natural selection may be
unab le to 'fine tune' memory for recall of individual
flowers within a dense patch, because the time and
energy costs of occasional revisitation are probably
quite low.
The movement patterns of foragers in response
to variation in resource density can affect netenergy intake (e.g. Tinbergen et al. 1967; Croze
1970; Cody 1971; Smith 1974a, b; Char nov et al.
1976). For example, bees show greater turning
angles upon visiting flowers or inflorescences with
higher rewards than after visits to flowers contain-
ing lower rewards (Pyke 1978b; Heinrich 1979).
This area-restricted searching has the net effect of
keeping bees in food-rich areas, but allows them to
pass through areas with less food. The turning
angles of adult bananaquits in our floral patch fit
the pattern of area-restricted searching, as evi-
denced by the lack of a strong modal turn ing angle
for the frequency dist ribut ion of turning angles for
both open and closed flowers. Furthermore, the
juveniles resembled adults when foraging on
covered flowers since they also showed no strong
directional preference, with the exception of rever-
sals. In the open-flower patch, however, the juve-
niles showed little evidence of area-restricted
searching (less consistent than adults) and they
mostly probed the flowers directly in front of their
path of movement, as indicated by the modal
tur nin g angle of 0 ~. Thus it is possible that the cluesprovided by unopened flowers help inexperienced
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52 Animal Behaviour, 36, 1
b a n a n a q u i t s l e a r n t o p r o b e a l l f lo w e r s w i t h i n
i m m e d i a t e r e a c h , r e g a r d l e s s o f d i r e c t i o n ( a n g l e ) ,
b e f o r e m o v i n g o n t h r o u g h t h e p a t c h .
F o r a g e r s m a y l e a v e a p a t c h b e c a u s e th e y h a v e
d e p l e t e d t h e r e s o u r c e , o r b e c a u s e t h e y h a v ea s s e s s e d t h a t r e s o u r c e s a r e l o w . T h e c u e s o r
i n f o r m a t i o n u s e d b y f o r a g e r s h a v e b e e n s u m m a r -
i z e d i n a d i v e r s i t y o f p a t c h d e p a r t u r e r u l e s
( r e v i ew e d b y P y k e 1 98 4). T h e s e d e p a r t u r e r u l e s c a n
i n v o l v e t i m e p e r p a t c h , f o o d p e r p a t c h , o r g i v i n g -u p
t im e . A l t h o u g h o u r e x p e r i m e n t s w e r e n o t d e s i g n e d
t o d i s c r i m i n a t e b e t w e e n t h e v a r i o u s p a t c h d e p a r -
t u r e m o d e l s , w e s u g g e s t t h a t f l o w e r r e v i s i t a t i o n s
c o u l d a f f e c t a n e c t a r i v o r e ' s p a t c h d e p a r t u r e d e c i -
s i o n s u n d e r s o m e c i r c u m s t a n ce s . F o r e x a m p l e , t h e
h i g h f l o w e r - r e v i s i t a t i o n r a t e s o f j u v e n i l e s c o u l d
a d v e r s e l y i n f l u e n c e t h e i r a b i l i t y t o a s s e s s t h e d e g r e e
o f r e s o u r c e d e p l e t i o n w i t h i n a p a t c h a c c u r a t e l y ,
c a u s i n g t h e m t o d e p a r t p r e m a t u r e l y . T h e r e f o r e ,
j u v e n i le s m a y b e l e a v i n g p a t c h e s b e f o r e t h o r o u g h l y
s a m p l i n g o r c o n s u m i n g t h e a v a i l a b l e n e c t ar . C o n -
s i s t e n t w i t h t h i s a r e o u r o b s e r v a t i o n s t h a t j u v e n i l e s
g e n e r a ll y s t o p p e d f o r a g i n g w i t h o u t s a m p l i n g
f lo w e rs in t h e l o w e r p o r t i o n o f th e p a t c h , a n d t h a t
t h e l e n g t h o f t h e i r f o r a g i n g b o u t ( i n t e r m s o f t h e
n u m b e r o f f lo w e r s v i s it e d ) w a s n o t c o r r e l a t e d w i t h
t h e n u m b e r o f s e c to r s v i si te d . F u r t h e r m o r e , j u v e -
n i l es d i d n o t s y s t e m a t i c a l l y l e a v e a r e a s w i t h l o wr e s o u r c e s a n d m o v e t o a r e a s w i t h h i g h e r r e s o u r c e s
w h e n f o r a g i n g o n o p e n f l o w e r s . T h u s t h e h i g h
f l o w e r - r e v i s i t a t i o n r a t e s o f j u v e n i l e s n o t o n l y
r e d u c e f o r a g i n g e f fi c ie n c y b y r e d u c i n g t h e r a t e o f
e n e r g y i n t a k e , b u t m a y a l s o i n t e r f e r e w i t h t h e i r
a b i l i t y t o a s s e s s r e s o u r c e d i s t r i b u t i o n s w i t h i n a n d
a m o n g p a t c h e s .
A s n o t e d p r e v i o u s l y ( W u n d e r l e & O ' B r i e n 1 98 5),
n a i v e j u v e n i l e b a n a n a q u i t s t e n d t o r e v i s i t f l o w e rs
i m m e d i a t e l y f o l l o w i n g t h e i r f i r s t v is i t. I n o p e n
f l o w e r s , t h i s o f t e n i n v o l v e d t u r n i n g a t t h e p a t c h
e d g e a n d t h e n m o v i n g f o r w a r d t h r o u g h t h e v is i te d
a r e a a g a i n , w h i l e i n c o v e r e d f l o w e r s i t i n v o l v e d
f r e q u e n t t u r n i n g r e v e r s a l s t o r e s a m p l e a p r e v i o u s l y
o p e n e d f l o w e r. A d u l t s t e n d e d t o m o v e a w a y f r o m
p r e v i o u s l y v i s i t e d f l o w e rs . T h i s a d u l t p a t t e r n o f
f l o w e r v i s i t a t i o n w a s c o n s i s t e n t w i t h p r e v i o u s
s t u d ie s o f a d u l t b a n a n a q u i t s ( W u n d e r l e & S o t o
1 98 7) a n d a d u l t h u m m i n g b i r d s ( C o l e e t a l. 1 9 82 )
w h i c h i n d i c a te t h a t t h e y s w i t ch m o r e r e a d i l y f ro m a
l o c a t i o n w h e r e i n i t i a ll y r e w a r d e d t o a n e w l o c a t i o n
( w i n - s h i f t ) , r a t h e r t h a n r e t u r n t o t h e e x a c t l o c a t i o n
w h e r e o r i g i n a l l y r e w a r d e d ( w i n - s t a y ) . H o w e v e r ,h a n d - r e a r e d j u v e n il e b a n a n a q u i t s l e a r n e d w i n -
s h i f t a n d w i n - s t a y p r o b l e m s w i t h e q u a l f a c i l i t y
( W u n d e r l e & S o t o 1 98 7) . T h e s e r e s u l ts s u g g e s t t h a t
j u v e n i l e s a r e f l e x ib l e i n t h e i r s p a t i a l l e a r n i n g a b i l i -
t i e s a n d t h a t t h e a d u l t w i n - s h i f t b i a s r e s u l t s f r o m
p r e v i o u s e x p e r i e n c e w i t h e x h a u s t a b l e r e s o u r c e s .T h i s j u v e n i l e l e a r n i n g f l e x i b i li t y ( i. e. n o p r e d e t e r -
m i n e d w i n - s h i f t r e s p o n s e ) m a y a c c o u n t f o r t h e i r
h i g h l e v e l o f f l o w e r r e v i s i t a t io n s . I n t h e e a r l y s t a g e
o f l e a r n i n g t o f o r a g e i n p a t c h e s , a j u v e n i le b a n a n a -
q u i t m a y r e t u r n t o t h e l o c a t i o n o f sp e c if ic f l o w e r s o r
p a t c h e s w h e r e i t w a s i n i t i a l l y r e w a r d e d ( e ve n
t h o u g h i t is n o t r e w a r d e d f o r s u b s e q u e n t v i s it s ). A
l a g p e r i o d m a y b e i n v o l v e d in l e a r n i n g t o g e n e r a l i ze
t h e r e c e i p t o f r e w a r d s f r o m a l l s i m i l a r f l o w e r s
r a t h e r t h a n f r o m s p e c if i c f l o w e r s. W i t h e x p e r i e n c e ,
j u v e n i le s m a y a s s o c i a te m e m o r y a n d a v o i d a n c e o f
p r e v i o u s l y v i s i t e d f l o w e r s w i t h i n c r e a s e d e n e r g y
i n t a k e p e r f o r a g i n g e ff o rt . T h u s b a n a n a q u i t s m a y
i m p r o v e t h e i r f o ra g i n g a b i l i t y b y l e a r n i n g t o u s e
t h e i r m e m o r y a n d b y g e n e r a li z i n g t o f l o w e rs w i th
c h a r a c t e r i s t i c s s i m i l a r to t h o s e f r o m w h i c h t h e y
r e c e i v e d e a r l i e r r e w a r d s .
W h i l e t h e a g e d i f fe r e n c e s i n f o r a g i n g b y b a n a n a -
q u i t s m a y b e a t t r i b u t e d p r i m a r i l y to e x p e r i en c e
( p r a c t i c e ), w e a r e u n a b l e t o e x c l u d e c o m p l e t e l y t h e
p o s s i b i l i ty o f a g e n e r a l i m p r o v e m e n t i n s p a t i a l
p e r c e p t i o n o r n e u r o m u s c u l a r c o o r d i n a t i o n a s s o -
c i a t e d w i th m a t u r a t i o n . F o r i n s t an c e , th e p e c k i n gb y y o u n g c h i c k s a t g r a i n i n v o l v e s p e c k i n g , s e i zi n g
a n d s w a l l o w i n g , a l l o f w h i c h i m p r o v e w i t h a g e
( B r e e d 1 91 1). H o w e v e r , e x p e r i m e n t a l s t u d i e s i n d i -
c a t e t h a t t h e i m p r o v e m e n t t h a t a c c o m p a n i e s p ra c -
t i c e i n t h e d e v e l o p i n g c h i c k m a y r e s u l t f r o m
i n c r e a s e d p o s t u r a l s t a b i l i t y a s w e ll as l e a r n i n g
( C r u z e 1 93 5) . H e n c e t h e d e v e l o p m e n t o f m o t o r o r
p e r c e p t u a l a b i l i t i e s c o u l d i n f lu e n c e t h e f o r a g i n g
a b i l i t i e s o f j u v e n i l e b i r d s , b u t u n f o r t u n a t e l y t h i s
a s p e c t o f o n t o g e n y r e m a i n s u n k n o w n .
T h e h i g h f r e q u e n c y o f f l o w e r r e v i s i t a t i o n b y
j u v e n i l e b a n a n a q u i t s c o u l d b e a n i m p o r t a n t f a c t o r
i n t h e i r s e l e c ti o n o f f o o d i t e m s . F o r e x a m p l e , t h e i r
f o r a g i n g i n e f f ic i e n cy m i g h t c a u s e t h e m t o a v o i d
d e n s e f l o w e r p a t c h e s a n d s e l ec t m o r e w i d e l y d i s -
p e r s e d f l o w e rs . O r , a s f o u n d i n E u r o p e a n s t a r l i n g s
( S te ve ns 1985 ) , j uve n i l e s m a y se l e c t f ood i t e m s
r e qu i r ing l e s s f o r a g in g sk i l l , suc h a s f r u i t . I n f a c t , a t
t h e e n d o f t h e b r e e d i n g s e a so n , ju v e n i l e b a n a n a -
q u i t s t e n d t o c o n g r e g a t e a r o u n d f r u it i n g tr e es ,
w h e r e a s a d u l t s f e e d o n n e c t a r a n d i n s e c t s w h i c h
p o s s i b l y r e q u ir e m o r e f o r a g i n g s k i l l ( W u n d e r l e ,
u n p u b l i s h e d d a t a ) . F u r t h e r m o r e , p e r i o d i cd r o u g h t s a r e k n o w n t o r e d u c e s o m e b a n a n a q u i t
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W u n d e r l e & L od ge ." F l o r a l p a t c h u s e b y b a n a n a q u i t s 53
p o p u l a t i o n s ( F a a b o r g e t a l . 19 84 ) a n d m a y d i s p r o -
p o r t i o n a t e l y a f f e ct j u v e n i l e s w h i c h h a v e i n e f f i ci e n t
f o r a g i n g s k i l l s .
A C K N O W L E D G M E N T S
W e w i s h t o a c k n o w l e d g e t h e f i n e a s s i s t a n c e p r o -
v i d e d b y t h e f o l l o w i n g s t u d e n t s : A n n e t t e B o n i l l a ,
F e r n a n d o C a l i m a n o , Z o r a i d a C o t t o , C a r l o s C r u z,
J os 6 F e r n a n d e z , E d g a r R o d r i g u e z a n d M a r i a
S a n t a . A s s i s t a n c e i n c a r i n g f o r t h e b i r d s w a s
p r o v id e d b y M i c h a el M e l a m p y , C h a r l o t te T a y l o r ,
R o b e r t R o s s a n d J o s 6 V e l a z q u e z . T h e b i o l o g y
d e p a r t m e n t d i r e c t o r a t U . P . R . , C a y e y , D r J o s 6
V e l a z q u e z , p r o v i d e d v a l u a b l e a s s i s t a n c e a n d e n -
c o u r a g e m e n t d u r i n g t h e r e s ea r c h . V a l u a b l e a s s is t -
a n c e w i t h t h e s t a t i s t i c a l a n a l y s i s w a s p r o v i d e d b y
S a r a h N u s s e r , J o r g 6 P r r e z -C o f f i e a n d M i c h a e l
W i l l ig . T h e m a n u s c r i p t b e n e f i t e d f r o m t h e c r i t i c a l
c o m m e n t s o f R a n d a l l B r e it w i s ch , M i l b r e y L e i g h -
t o n , T i m o t h y C . M o e r m o n d a n d M i c h a e l W i l l i g .
F i n a n c i a l s u p p o r t w a s p r o v i d e d b y N a t i o n a l
S c ie n c e F o u n d a t i o n g r a n t B N S 8 4 -0 5 65 5 .
R E F E R E N C E S
Balda , R . P. 1980. Reco very of cached seeds by a cap t ive
Nucifraga caryocatactes. Z. Tierpsychol., 52, 331-346.Brandt , C. A. 1984. Ag e and h unt ing success in the brow n
pelican: influences o f skill and patc h choice on for agin gefficiency. Oecologia (Berl.), 62, 132-137.
Breed, F. S. 1911. The de velop men t of cer ta in inst inc tsand habits in chicks. Behav. Monogr., 1, 1-78.
Bre itwisch, R. , D iaz , M. & Lee , R. 1987. Fo ragin geffic iencies and techniques o f juven i le and adul t nor th-e rn m ock ingb i rds (M imu s polyglottos). Behaviour, 101,225-235.
Buckley, F. G. & Buckley, P. A. 1974. Co mp ara t iv efeed ing eco logy o f win t e r ing adu l t and j uven i l e roya lterns (Aves: Laridae, Sterninae). Ecology, 55, 1053-1063.
Bunch, K. G. & Tom back, D. F. 1986. Bolus recovery bygrey jays: an exper imenta l analysis . Anim. Behav., 34,754-762.
Cha rnov , E . L . , Or i ans , G . H. & Hya t t , K . 1976 .Ecologica l impl ica t ions of resource depression. A m .Nat . , 110 , 247 259.
Coblentz , B. E . 1986. A possible reason for age-di f feren-tial success in bro wn pelicans. J. FieM Ornithol., 57, 63 -64 .
Cody, M . L . 1971. Finch f locks in the M ojav e Deser t .Theor. Pop. Biol., 2, 142-158.
Cole, S. , Hain swo rth , F . R. , Kam il , A. C. , Me rc ier , T . &Wolf , L . L . 1982. Spat ia l learning as an adapta t ion inhum m ingb i rds . Science, N.Y., 217, 655~557.
Croze , H. 1970. Searching image in carr ion crow s. Z .Tierpsychol., 5, 1-85.
Cruze , W . W. 1935. M atura t ion and learning in chicks. J .comp. Psychol., 19, 371~,09.
Du nn, E . K. 1972. Effec ts o f age on the f i shing ab i l i ty ofsandwich te rns, Sterna sandvicensis. Ibis, 1 1 4 , 3 6 ~ 3 6 6 .
Faab org, J . , Aren dt , W. J . & Kaiser , M. S. 1984. Rainfa l l
corre la tes of bi rd popula t ion f luc tua t ions in a Puer toRican dry forest : a nine year s tudy. Wilson Bull., 96 ,575-593.
Gass, L . G. & Su ther land, G . D. 1985. Specia l iza t ion byt e r r it o r i a l hum m ingb i rds on expe r im en ta ll y en r ichedpatches of flowers: energetic profitabil i ty and learning.Can. J. Zool. , 63, 2125-2133.
Gib b, J . 1958. Pred at ion by t it s and squi rre ls on eucosm idEnarmonia conicolama (Heyl.). J. Anim. Ecol. , 27, 375-396.
Gi l l , F. B. & Wolf , L . L . 1975. Fora ging st ra tegies andenergetics of East Afr ican sun birds a t m ist le toeflowers. Am. Na t . , 109, 491-510.
Gi l l , F. B. & Wolf , L . L . 1977. Nonrandom foraging by
sunbirds in a pa tchy envi ronment . Ecology, 58, 1284-1296.Goc hfe ld , M . & Burger , J . 1984. Ag e dif ferences in
fo rag ing behav iour o f t he Am er i can rob in (Turdusmigratorius). Behaviour, 88, 227 239.
Hain swo rth , F. R . , Me rc ier , T . & Wolf , L . L . 1983. Flora la r r angem ent s and hum m ingb i rd f eed ing . Oecologia(Berl.), 58 , 225-229.
Heinr ich, B. 1979. Resource he terogenei ty and pa t te rnso f m ovem ent i n fo rag ing bum blebees . Oecologia(Berl.), 40, 235-246.
Hodges , C . M. 1981 . Op t im a l fo rag ing i n bum blebees :hunt ing by expecta t ion. Anim. Behav., 29, 1166-1171.
Kam il , A. C. 1 978. Systemat ic foraging by a nec tar-feeding bi rd , the amakihi (Loxops virens). J. comp.physiol. Psychol., 92, 388 396.
Kamil , A. C. & Balda , R. P. 1985. Cache recovery andspa t i a l m em ory i n C la rk ' s nu t c racke r s (Nuc(fragacolumbiana). J. exp. Psychol.: Anita. Behav. Proc., l l ,95-111.
Krebs, J . R. & McCleery, R. H. 1984. Opt imiza t ion inbehaviora l ecology. In: Behavioral Ecology (Ed. by J .R. K rebs & N. B. Davies) , pp. 91 121. Sund er land,Massachusetts: Sinauer.
Krebs, J . R. , Ryan, J . C. & Charn ov, E . L . 1974. Hu nt ingby expec t a t ion o r op t im a l fo rag ing? A s tudy o f pa t chuse by chickadees. Anim. Behav., 22, 953-964.
Krebs, J . R, Stephens, D. W. & Suther land, W. J . 1983.Perspect ives in opt imal foraging. In: Perspectives in
Ornithology (Ed. by A. H. Brush & G . A. Clark, Jr ) , pp.165-216. Cam bridge: Cam bridge U niversi ty Press.
M acLean, A. A . E . 1986. Age-specif ic foraging abi l i ty andthe evolut ion of deferred breeding in three species ofgulls. Wilson Bull., 98, 267 279.
Mil le r , R. S. & Mil le r , R. E . 1971. Feedin g ac t ivi ty andco lo r p re ference o f ruby- th roa ted hum m ingb i rds . Con-dor, 73 , 30~313 .
Montgom er i e , R . D. 1979 . E ne rge t i c s o f fo rag ing andcom pe t i t i on i n som e Mexican hum m ingb i rds . Ph .D.thesis, M cGil l Universi ty .
Morr ison, M. L . , Slack, R. D. & Shanley, E . , Jr . 1978.Age and foraging abi l i ty re la t ionships of ol ivaceouscorm oran t s . Wilson Bull., 90, 414-422.
Nor ton-Gr i f f it h s , M. 1968 . T he f eed ing behav iour o f t he
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http://slidepdf.com/reader/full/8802483-mainyhj 11/11
54 A n i m a l B e h a v i o u r, 3 6 , 1
oystercatcher (Haematopus os tralegus) . Ph.D. thesis,Oxford University.
Orians, G. H. 1969. Age and hunting success in the brownpelican (Pelic anu s occidentalis). A nim. B ehav., 17, 316-
319.
Pitelka, F. A. 1942. Territoriality and related problems inNorth American hummingbirds. Condor, 44, 189-204.Pyke, G. H. 1978a. Optimal foraging in hummingbirds:
testing the marginal value theorem. A m . Z o o l ., 18, 739-752.
Pyke, G. H. 1978b. Optimal foraging: movement patternsof bumblebees between inflorescences. Theor. Pop.Biol . , 13, 72-98.
Pyke, G. H. 1981. Honeyeater foraging: a test of optimalforaging theory. Anim. Behav. , 29, 878 888.
Pyke, G. H. 1982. Foraging in bumblebees: rule ofdeparture from an inflorescence. C an . J . Zoo l . , 60 , 417-428.
Pyke, G. H. 1984. Optimal foraging theory: a critical
review. A. Rev . Ecol . Sys t . , 15, 523 575.Recher, H. F. & Recher, J. A. 1969. Comparativeforaging efficiency of adult and immature little blue
herons, Flor ida caerulea. Ani ta . Behav . , 17, 320-322.Searcy, W. A. 1978. Foraging success in three age classes
of glaucous-winged gulls. A u k , 95, 586-588.Sherry, D. F. 1984a. Food storage by black-capped
chickadees: memory for the location and content s ofcaches. Anim. Behav . , 32, 451-464.
Sherry, D. F. 1984b. What food-storing birds remember.Can. J . Psychol . , 38, 304-321.
Shettleworth, S. J. 1984. Learning and behavioral eco-logy. In: Behav ior a l Eco logy (Ed. by J. R. Krebs & N. B.
Davies), pp. 170-184. Sunderland, Massachusetts:Sinauer.
Shettleworth, S. J. & Krebs, J. R. 1982. How marsh titsfind their hoards: the roles o f site preference and spatialmemory. J . exp. Psychol .: Anim. Behav. Proc . , 8, 354-375.
Siegfried, W. R. 1972. Aspects of the feeding ecology of
cattle egrets, Ardeola ib is , in South Africa. J . AnOn.
Ecol., 41, 71 78.Smith, J. N. M. 1974a. The food searching behaviours of
two European thrushes. I: description and analysis o f
search paths. Behaviour, 48, 276-302.
Smith, J. N. M. 1974b. The food searching behaviours oftwo European thrushes. II: the adaptiveness of thesearch patterns. Behaviour, 49, 1~51.
Sokal, R. R. & Rohlf, F. J. 1981. Biome t r y . SanFrancisco, California: W. H. Freeman.
Stevens, J. 1985. Foraging success of adult and juvenilestarlings Sturnus vulgaris ." tentative explanation for thepreference of juveniles for cherries. Ibis , 127, 341-347.
Suther land, W. J., Jones, D. W. F. & Hadfield, R. W.1986. Age differences in the feeding ability of moorhens
Gallinula choropus. Ibis , 128, 414-418.Taylor, L. R. 1961. Aggregation, variance and the mean.
N atur e , Lond . , 189, 73~735.Tinbergen, N., Impekoven, M. & Franck, D. 1967. An
experiment on spacing out as a defence against preda-tion. Behaviour, 28 , 307-320.Vander Wall, S. B. 1982. An experimental analysis of
cache recovery in Clark's nutcracker. Anim . Behav. , 30,84-94.
Verbeek, N. A. M. 1977. Comparat ive feeding behaviorof immature and adult herring gulls. Wilson Bul l . , 89,415-421.
Wiens, J. A. 1976. Populat ion responses to patchyenvironments. A. Rev . Ecol . Sys t . , 7, 81-120.
Wunderle, J. M. & O'Brien, T. G. 1985. Risk aversion inhand-reared bananaquits. Behav. Ecol. Sociobiol., 17,371 380.
Wunderle, J. M. & Soto, M. J. 1987. Spatial learning inthe nectarivorous bananaquit: juveniles versus adults.
Anim. Behav . , 35, 652~58.
(Rece ived 10 N ovember 1986; r ev i s ed 2 M ar ch 1987;M S . n u m b e r : A 4 8 9 4 )
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