Brenda McCowan et al- Bubble Ring Play of Bottlenose Dolphins (Tursiops truncatus): Implications for Cognition

8/3/2019 Brenda McCowan et al- Bubble Ring Play of Bottlenose Dolphins (Tursiops truncatus): Implications for Cognition

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Journal of Comparative Psychology Copyright 2000 by the American PsychologicalAssociation, Inc.2000,Vol. l14, No. 1,9S-106 0735-7036/00/$5.00 DO I: 10.1037//0735-7036.114.1.98

Bubb le Ring P lay of Bottlenose D olphins (Tu rsiops trunca tus):Im plications for Co gnition

Brenda McCowanU n i v e r s i t y o f C a l if o r n i a , D a v i s a n d S i x F l a g s M a r i n e W o r l d

Lori Marino

E m o r y U n i v e r si t y

Erik Vance and Leah WalkeS i x F l a g s M a r i n e W o r l d

Diana ReissN e w Y o r k A q u a r i u m

Research on the cognitive capacities of dolphins and other cetaceans (w hales and porpoises)has importance for the study of comparative cognition, particularly w ith other large-brainedsocial mammals, such as primates. One o f the areas in which cetaceans can be com pared withprimates is that of object manipulation and physical causality, for which there is an abundantbod y of literature in primates. The authors supplemented qualitative observations withstatistical methods to exam ine playful bouts of underwater bubble ring production andmanipulation in 4 juvenile male captive bottlenose dolphins (Tursiops truncatus). Th e resultsare consistent with the hypothesis that dolphins m onitor the quality of their bubble rings andanticipate their actions during bubble ring play.

O n g o i n g r e s e a r c h i n t o t h e c o g n i t i v e c a p a c i t i e s o f d o l p h in s

a n d o t h e r c e t a c e a n s ( e . g . , w h a l e s a n d p o r p o i s e s ) h a s c a p -

tu red t h e i n t e r es t an d ima g in a t i o n o f b o th t h e sc i en t i f i c

c o m m u n i t y a n d t h e p u b l i c ( H e r m a n , 1 9 8 6 ; R e i s s , M c -

Co wan , & M ar in o , 1 9 9 7 ) . Bo t t l en o se d o lp h in s (Tur s iops

truncatus) are g r e g a r i o u s m a m m a l s th a t s h o w a s tr o n g

p r o p e n s i t y f o r p l a y b e h a v i o r w i t h p h y s i c a l o b j e c t s a n d w i t h

c o n s p e c i f i c s . T h e r e h a v e b e e n p r e v i o u s r e p o r t s t h a t b o t h

c a p t i v e a n d w i l d d o l p h in s p r o d u c e t h e i r o w n o b j e c t s o f p l a y ,

t e r m e d bubb le r ings (M ar t en , S h ar i f f , P sa rak o s , & Wh i t e ,1 9 9 6 ; Re i s s , 1 9 8 8 , 1 9 9 8 ; Tay l e r & S a ay m an , 1 9 7 3 ) . Du r in g

t h e s e e v e n t s , d o l p h i n s e x p e l a i r f r o m t h e i r b l o w h o l e , a n d t h e

ex p e l l ed a i r r i s es t o t h e su r f ace i n a t o ru s o r r i n g l i k e fo rm.

Brenda McCow an, Department o f Population Health and Repro-duction, School o f Veterinary Medicine, U niversity of California,Davis, and Marine Research Center, Six Flags Marine World,Vallejo, California; Lori Marino, Neuroscience and BehavioralBiology Program, Em ory University; Erik Vance and Leah Walke,Marine Research Center, Six Flags M arine Wo rld; Diana R eiss,New Y ork Aquarium, New Y ork.

This research wa s supported in part by Six Flags M arine World

(formally known as Marine W orld Africa USA ).We thank the Dolphin Research Laboratory vo lunteer staf f at the

Marine Research Center who assisted in data collection and entry.We also thank Scott Lilienfeld for discussion of these issues andhelpful comments on this article. Finally, we thank DebbieMarin-Cooney, Terry Samansky, and the Marine Ma mm al Depart-me nt training sta ff at Six Flags M arine W ord who w ere responsiblefor the care and husbandry o f the dolphins.

Correspondence concerning this article should be addressed toBrenda McCowan, Behavioral Biology Laboratory, VeterinaryMedicine Te aching and Research C enter, University of California,Davis, 18830 Road 112, Tulare, California 93274. Electronic m ailma y be sent to bmccowan@ vmtrc.ucdavis.edu.

M a r t en e t a l. d esc r i b ed t h e p h y s i cs i n v o lv ed i n t h e fo rma t io n

o f t h e b u b b l e r i n g as fo l l o ws :

Any spherical bigger than about two centimeters in diameterwill quickly bec om e a ring because o f the difference in w aterpressure above and below the bubble. Water pressure in-creases with depth, so the bottom of the bubble experiences ahigher pressure than the top does. The pressure from belowovercomes the surface tension of the sphere, punching a holein the center to create a doughnut shape. As water rushesthrough the hole, a vortex forms around the bubble. Any

vortex ring travels in the sam e direction as the flow through itscenter; in the case o f these simple a ir rings, the vortex flow, incombination with the air's natural buoyancy, propels thebubbles toward the surface. (p. 84)

A i r - b r e a t h i n g d o l p h i n s a l w a y s p r o d u c e b u b b l e s w h e n

th ey ex p e l a i r u n d erwate r . Bes id es b u b b l e r i n g s , d o lp h in s

a l s o p r o d u c e a w i d e v a r i e t y o f o t h e r b u b b l e t y p e s . T h e y

o c c a s i o n a l l y e m i t b u b b l e s t r e a m s c o n c u r r e n t w i t h v o c a l

ac t i v i ty . W h en su rp r i sed , cu r i o u s , o r ex c i t ed , d o lp h in s o f t en

e m i t a r a p i d e x h a l a t i o n t e r m e d a bubb le bur s t . Brea th in g i n

d o lp h in s , u n l i k e in o th e r mam m al s , i s so l e ly u n d er v o lu n t a ry

co n t ro l (R id g w ay , 1 9 7 2 ) , a c ru c i a l f ea tu re i n t h e i r ad ap t a t i o n

to a fu ll y aq u a t i c ex i s t en ce . Wh er eas t h e p h y s i cs o f r i n g

fo rm at io n is s t r a i g h t fo rwa rd (Lu n d g re n & M an so u r , 1 9 9 1 ),t h e a c t u a l p r o d u c t i o n o f s t a b l e r i n g s m a y r e q u i r e s o m e

p rac t i ce , ex p er t i se , an d fo re th o u g h t b y t h e d o lp h in s .

S e v e r a l r e s e a r c h e r s h a v e e x a m i n e d o b j e c t - r e l a t e d p l a y

(e .g ., s ee F ag en , 1 9 8 1 ; Ha l l , 1 9 9 8 , fo r r ev i ews) an d o b j ec t

ma n ip u l a t i o n i n g en era l ( see An t in u cc i , 1 9 8 9 , 1 9 9 0 ; P ark e r

& Gib so n , 1 9 7 9 ; Ru sso n , Bard , & P ark er , 1 9 9 6 ; To mase l l o

& Cal l , 1 9 9 7 ; Vi sa lb e rg h i & To mas e l l o , 1 9 9 8 , fo r em p i r i ca l

an d t h eo re t i ca l r ev i ews o f t h i s i s su e) t o g a in i n s ig h t i n to

n o n h u m a n l e v e l s o f p h y s i c a l c a u s a l u n d er s t a n d in g ( K u m -

mer , 1 9 9 5 ; Vi sa lb e rg h i & To mase l l o , 1 9 9 8 ) . We ex amin ed

b o u t s o f u n d e r w a t e r b u b b l e r i n g p r o d u c t i o n a n d m a n i p u l a -

98



BUBBLE RING PLAY OF BOTII,ENOSE DOLPHINS 99

t i o n i n 4 j u v e n i l e m a l e c a p t i v e b o t t l e n o s e d o l p h i n s (Tursiops

truncatus) t o d e t e r m i n e w h a t t h is b e h a v i o r m a y t e ll u s a b o u t

t h e d o l p h i n s ' l e v e l o f u n d e r s ta n d i n g i n t e r m s o f t h e c a u s a l

r e l a t io n s b e t w e e n o b j e c ts .

D o l p h i n s i n d i ff e r e n t o c e a n a r i u m s h a v e b e e n r e p o r t e d t o

p r o d u c e b u b b l e r i n g s . F o r e x a m p l e , R e i s s ( 1 9 8 8 , 1 9 9 8 )

r e p o r t e d t h a t t h e d o l p h i n s w o u l d s w i m t o t h e b o t t o m o f t h ep o o l , s t o p , a s s u m e a h o r i z o n t a l p o s i t i o n , a n d t h e n w i t h a

s h a r p u p w a r d j e r k o f t h e h e a d , e x p e l a r i n g o f a i r t h r o u g h

t h e i r b l o w h o l e . M a r t e n e t a l . ( 1 99 6 ) d e s c r i b e d a m o r e v a r i e d

r e p e r t o i re o f b u b b l e r i n g p r o d u c t i o n , i n c l u d i n g t h e p r o d u c -

t i o n o f b o th v e r t i ca l an d h o r i zo n t a l t r a j ec to r i es o f t h e r i n g s .

In a l l t h r ee r ep o r t s , t h e d o lp h in s w ere d esc r i b ed as ex h ib i t i n g

ch arac t e r i s t i c p o s tu res i n sp ec i f i c l o ca t i o n s i n t h e wa t e r

c o l u m n j u s t p r i o r to t h e p r o d u c t i o n o f b u b b l e r i n g s . R e i s s

( 1 9 9 8 ) s u g g e s t e d t h a t a l t h o u g h d o l p h i n s r e l e a s e a i r i n m a n y

f o r m s , d o l p h i n s a p p e a r t o c o n t r o l b o t h t h e f o r m a n d t h e

t i m i n g o f t h e r e l e a s e o f a i r d u ri n g t h e p r o d u c t i o n o f b u b b l e

r i n g s . He fu r t h e r su g g es t ed t h a t t h e d o lp h in s ' ch arac t e r i s t i c

s p a t ia l p o s i t i o n in g p r i o r t o b u b b l e r i n g p r o d u c t i o n p r o v i d e ss u g g e s t i v e e v i d e n c e o f " a n t i c i p a t o r y b e h a v i o r , a n a w a r e n e s s

o f t h e c o n t i n g e n c i e s o f t h e i r p a s t a c ti o n s , a n d a n a w a r e n e s s

o f t h e co n t i n g en c i es o f fu tu re ac t s " (R e i s s , 1 9 9 8 , p . 5 5 7 ).

D o l p h i n s f r e q u e n t l y m a n i p u l a t e t h e i r b u b b l e r i n g s b y

g en era t i n g v o r t i ces a ro u n d t h e o b j ec t s , wh ich cau se t h e

b u b b l e r i n g s t o t u rn v e r t i ca l l y b y 9 0 ° o r f l i p in o r i en t a t i o n

1 8 0 ° ( M a r t e n e t a l ., 1 9 9 6; B . M c C o w a n , p e r s o n a l o b s e r v a -

t io n ) . B u b b l e r i n g p l a y c a n r e s u l t i n a s e q u e n c e o f t w o

b u b b le r i n g s , su ch t h a t t h e seco n d b u b b l e r i n g j o in s t h e f i r s t

b u b b l e r i n g t o f o r m a l a r g e b u b b l e r i n g , w h i c h i s o f t e n t h e n

f u r t h e r m a n i p u l a te d . S o m e t i m e s a t h i r d s m a l l e r b u b b l e r i n g

ex t ru d es f ro m th e l a rg e r r i n g as a r esu l t o f t h e fo rce o f

i m p a c t b e t w e e n t h e f i r s t a n d s e c o n d b u b b l e r i n g s ( B .

M c C o w a n , p e r s o n a l o b s e r v a t i o n ) . T h i s t h i r d b u b b l e r i n g i s

f r e q u e n t l y m a n i p u l a t e d b y t h e d o l p h i n s i n a s i m i l a r m a n n e r

a s d e s c r i b e d a b o v e f o r s i n g l e r i n g s w h e r e t h e d o l p h i n s

v er t i ca l l y t u rn t h e b u b b l e r i n g o r co mp le t e ly f l i p t h e r i n g .

H o w e v e r , n o t a l l s e c o n d b u b b l e r i n g s c a t c h a n d j o i n f ir s t

b u b b l e r i n g s , n o r d o d o l p h i n s a l w a y s p r o d u c e s e c o n d b u b b l e

r i n g s . I n ad d i t i o n , b u b b l e r i n g s o f v a r i ab l e q u a l i t y can

em erg e d e p en d in g o n t h e i n t eg r i t y o f t h e r i n g s t ru c tu re .

Th e p resen t s t u d y r ep resen t s t h e f i r s t sy s t emat i c an a ly s i s

o f d o l p h i n s ' b u b b l e p l a y b e h a v i o r t h a t g o e s b e y o n d t h e

a n e c d o t a l n a t u r e o f p r i o r o b s e r v a t i o n a l s t u d i e s . W e e x a m -

i n e d s e v e r a l a s p e c t s o f d o l p h i n s ' b u b b l e r i n g p r o d u c t i o n b y

s u p p l e m e n t i n g q u a l i t a t i v e o b s e r v a t i o n s w i t h q u a n t i t a t i v e

o n e s , w h i c h a l l o w e d u s t o q u a n t i f y t h e c o v a r i a t e r e l a t i o n -s h i ps a m o n g t h e p h y s i c a l c o m p o n e n t s o f b u b b l e r in g b e h a v -

i o r . T h e r e f o r e , i n t h i s s t u d y , w e m o v e b e y o n d s o l e l y

d e s c r i p t i v e o b s e r v a t io n s t o i n c l u d e a q u a n t i t a t iv e f r a m e w o r k

f o r t e s t i n g h y p o t h e s e s a b o u t t h e c o g n i t i v e b a s i s o f t h e s e

b e h a v i o r s .

W e p ro v id e q u a l i t a t i v e o b se rv a t i o n a l d esc r i p t i o n s o f d o u b l e

b u b b l e r i n g p l a y b e h a v i o r i n 4 j u v e n i l e c a p t i v e b o t t l e n o s e

d o l p h in s . F u r t h e r m o r e , w e u s e d s y s t e m a t i c q u a n t i ta t i v e

a n a l y s e s t o u n c o v e r p a t t e r n s i n t h e d o l p h i n s ' b u b b l e r i n g

b e h a v i o r t h a t m a y s h e d l i g h t o n t h e l e v e l o f c o g n i t i o n

in v o lv ed i n t h i s b eh av io r . F i r s t , t o es t ab l i sh t h e p l au s ib i l i t y

o f a n i n c e n t i v e f o r t h e d o l p h i n s t o m o n i t o r t h e q u a l i t y o f

t h e i r b u b b l e s , w e d e t e r m i n e d w h e t h e r t h e q u a l i t y o f t h e f i rs t

b u b b l e r i n g i s r e l a t e d t o w h e t h e r t h e s e c o n d b u b b l e r i n g ,

wh en i t i s p ro d u ced , ca t ch es an d j o in s t h e f i r s t . S eco n d , t o

d e t e r m i n e w h e t h e r t h e d o l p h i n s m o n i t o r th e q u a l i t y o f t h e i r

b u b b l e r i n g s , w e e x a m i n e d t h e a s s o c i a t i o n b e t w e e n t h e

q u a l i t y o f t h e f i r s t b u b b l e r i n g an d t h e p ro b ab i l i t y o f

p r o d u c i n g a s e c o n d b u b b l e r i n g. T h i r d, t o d e t e r m i n e w h e t h e rt h e d o l p h i n s s h o w e d e v i d e n c e o f a n t i c i p a t o r y p l a n n i n g ,

e v i d e n c e d b y p o s i t i o n i n g t h e i r b o d i e s a t l o w e r d e p t h s

i m m e d i a t e l y p r i o r to t h e a c t o f b u b b l e r i n g p r o d u c t io n , w e

e x a m i n e d t h e a s s o c i a t i o n b e t w e e n l o c a t i o n i n t h e w a t e r

c o l u m n a n d p l a y b u b b l e p r o d u c t io n .

M e t h o d

S u b j e c ts a n d H o u s i n g

The subjects were 4 captive-born juvenile male bottlenosedolphins (Tursiops truncatus), ranging from 3 to 8 years of age,

from Six Ha gs Marine W orld in Vallejo, California. The subjectswere housed in an oval pool (dimensions: 18.0 m long x 12.0 mwide × 4.5 m deep; volume: 795,109 L) with an underwaterviewing window at which observers collected data on the su bjects 'bubble behavior. Observers neither fed nor interacted with thedolphins immediately prior to, during, or immediately after anobservational session. Six Hags Marine World trainers fed thedolphins during training and feeding sessions three to four times

per day.

D a t a C o l l e c t i o n

Data on bubble production and play were systematically col-lected using a foc al animal event sampling design (Altmann, 1974).

Each juvenile was observed for fifteen 30-min sessions over a6-month period. The juveniles were betwe en 3 and 8 years old a t

the t ime of the stud y. The order for sampling the subjects w aspseudorandomly selected, and a total of two or three sessions w ereconducted each w eek between the hours o f 8 a.m. and 5 p.m. A totalof 718 bubble be havior events were collected ove r the 6-monthperiod from the 4 m ale juveniles. O f the 718 events, 181 eventswere bu bble ring play beha vior and consisted of single and doublebubble ring play. Social bubble behaviors, which included bubblebursts, bubble streams, and bubble clouds, were defined as t inyspherical bubbles in varying amounts and tem pora l sequenceproduced b y individually identified dolphins during social surprise,whistle production, and chases b etween socially interactive individu-als. Solitary play bub ble behaviors were defined as b u b b l e s

produced by individually identified dolphins in nonsocial contexts

that were frequently manipulated with their bodies, mouths, andtoy objects or were occasionally simply observed or infrequentlyignored afte r their production. These solitary play bubb le behaviorsincluded structurally discrete categories of bubbl e production:single conical bubbles, conical bubbles in sequence trails, and bothsingle and double large torus-shaped bubbles, known as bubblerings (Marten et al., 1996; Reiss, 1988, 1998; see Table 1). Singlebubble ring play behavior wa s defined as the production of a singlering (see Figure 1A for an example of dolphins' single ringproduction). Double bubble rin g play behavior was defined as aclose sequence o f two bubble rings such that the second bubble ringwas produced within 5 s of the first ring production (regardless ofquality; see below). The 5-s interval allowed the second ring theopportunity to join any first bubble ring to for m a larger third ring.



10 0 McCOWAN, MARINO, VANCE, WALKE, AND REISS

T a b l e 1

Descriptive List of Bubble Play and Nonplay Behav iors Produced by 4 Juvenile Dolphins

Behavior Type Descr iption

Bubble stream Social

Bubble burs t Social

Bubble c loud Social

Single bubble Solitary playBubble trail Soli tary play

Single bubble ring Solitary play

Double bubble r ing Sol i tary play

Line of single small bubbles usually released during vocalization

Large number of smal l bubbles s imul taneously released dur ing contextsof surprise or fright

Large num ber of sma ll bubbles released during aggress ive interactionwith conspecifics, especially during chases

Single large bubble released and either manipu lated by rostrum or bit ten

Line of single large bubbles released approxima tely 1 ft (0.3048 m )apart , frequently each of which is bit ten in turn

Air bubb le with a ring formation that is frequently manipulated in manyand complex ways

Two rings em itted sequentially (second ring produced within 5 s o f firstring) that sometimes join to produce one large ring

Figure 1. A: Photograph of a juveni le male dolphin producing a

single bubble ring. B: Drawing of the categories of bubble ring

quality.

Several categories of behavior associated with bubble ring and

other bubble play production were collected. Table 2 presents a

descriptive l ist of these variab le behaviors. The observer collected

the event data by narrating events into an audiocassette recorder.The type of bubble play event , the qual i ty of bubble r ing product ion

(see below), the location in the water column where the dolphins

engaged in bubble pla y production (interobserve r reliabil i ty scores

were unnecessary for the location where the dolphins engaged in

bubble play because structural features in the dolphins' pool were

used as markers to indicate depth [surface, middle, bottom]), and

the presence o f dolphin-init iated behaviors toward bu bbles, such as

second bub ble ring production and bit ing of bubbles, were noted.

A 4-point scale was used to assess the quali ty of the first bubble

ring production (Figure 1B) immediately after production, both

prior to second bubb le ring production when i t occurred and when

second ring production did not occur. Figure 1B shows representa-

t ive examples o f each category o f bubble ring quali ty. The q uali ty

of a first bubble ring was assessed prior to the production of a

second bubble ring by the subject to avoid any potential bias inbubble ring quali ty assessment. Although dev eloping a quantitative

test was an important objec tive for our study group and given the

current l imitations in quantitative video an alysis, the qu ali ty of the

bubble rings was determ ined by visual inspection of the bubble ring

during each event. The quali ty of the bubble rings was determ ined

by assessing the ring structure for both integrity (t ightness) and

completeness o f the ring formation (see Figure 1B). Poor and fair

rings exhibited partial and wide ring formations that differed in

thei r degree of completeness . Good r ings exhibi ted a complete but

wide ring formation. Excellen t rings exhibited both a com plete and

a very t ight ring formation. One observer collected all of the

event-ba sed data and thus assessed the quali ty of each bubble ring

event included in the data. However, to ensure that bubble ring

quali ty was system atically analyzed, we condu cted a post hoc

interobserver re liabi l i ty tes t between Brenda M cCowan and thesole observer on the quali ty of the bubble rings by using videotap escollected during the study period on the bubble ring play of the

subjects. Using 50 bu bble ring events playe d back in real t ime on a

VCR, we fou nd that the interobserver reliabil i ty scores ranged from

90% to 97% by calculating a raw percentage of the correspondence

between the two o bserve rs ' rat ings for each category of bubble ring

quality.

Data Analysis

The data were entered into an Excel spreadsheet and coded for

statist ical analysis. First , we determined the relative amounts of



BUBBLE RING PLAY OF BOTILENOSE D OLPHINS

Table 2

Descriptive List o f Behaviors and Measures Collected on Bubble Play Events

Behav ior or measure Description

Quality of bubble r ingLocation in water column

Watch float

Ignore

BitePectoral, rostral, or fluke swipe

Swim throughRostra] vertical turn play

Catch and join

Ring extrusion

Excellent, goo d, fair, or po or (see Figure 1B and text)The depth (in meters) in the water colum n at which produc-

tion of each bubble play event occurredDolph in explicitly observed bubble(s) float toward the sur-

faceDolphin departed from bubble(s) and engaged in another

activityDolphin bit bubble(s)Dolphin used pectoral fin, rostrum, or fluke to destroy

bubble(s)Dolphin swam thro ugh bubble(s)Dolphin manipulated without destroying single or double

ring using the rostru m and turned ring in a verticalfashion

A second ring in a double r ing event caught and joined thefirst ring to form on e large double ring

A third smaller ring extruded from the impa ct of the secondring catching and joining the first ring

101

bubble prod uction for solitary p lay and social behaviors. Second,we assessed the relative a mounts o f different ty pes of bubble play.Finally, we analyzed single and double bubble ring play withrespect to a number of covariates, such as quality of bubble ring

production, play behavior type, and the location where the dolphinwas in the water column prior to the production of bubble r ingsversus other bubble p lay types. The variables tested w ere categori-

cal in structure and included quality o f bubble ring production(excellent vs. other) and location in water colu mn (surface vs.middle vs. bottom). The outco mes, for example, catch and join (did

vs. did not), produ ction of secon d ring (yes vs. no), and bubble p layevent (ring vs. other), in eac h of the analyses were categ orical and,

more specifically, binary in structure. Thus, we used logisticregression as the statistical method (EGRET Reference Manual,1997). Logistic regression is the statistical metho d of choice forbina ry data, bec ause unlik e other tests, such as chi-square, logistic

regression indicates the significance as well as the magnitude of theassociation. Furthermore, logistic regression is free of a num ber of

problematic distribution assumptions that affect other types ofanalyses.

Using mixed-effects logistic regression in EGRET statistical

software for the PC (EGRE T Reference Man ual, 1997), weassessed the hypothesis that dolphins have an incentive to monitorthe quality of their bubble rings during double ring events byanalyzing the association between the quality of the first bubblering and the probability that the two bubble rings in that eventjoined. We assessed the hypothesis that dolphins actually monitor

the quality of their bubble rings by analyzing the relationshipbetween the probability that subjects would blow a second bubblering and the quality of their first bubble ring (excellent vs. other).Finally, we tested evide nce for anticipatory planning of bubble ringproduction by the dolphins by analyzing the association betweentheir location in the water column (as defined by pool depth:bottom vs. middle vs. surface) and the probability of theirproduction of a bubble ring event versus other bubble play events.Because w e studied 4 juvenile m ales by using a repeated measuresdesign, we designated "indiv idual" (the identity of each dolphin)as the rand om effect (or repeated measure) in each analysis (Searle,Casella, & McC ulloch 1992).

Fo r all statistical tests, significance was eval uated at the .05level. W e conduc ted goodn ess-of-fit statistics for each mod el

by using a likelihood-ratio chi-sq uare statistic (Agresti, 1 990).All models presented below exhibited appropriate goodn ess of

fit.

R e s u l t s

Types o f Bubble Product ion an d Bubble Play E vents

The dolphins pr oduced s ix d i f f e r en t ca tegor ies o f bubble

events in so l i t a ry p lay and soc ia l contex ts . The pr opor t ion of

events f or each ca tegor y of bubble pr oduc t ion i s shown in

F igur e 2 , which shows tha t bubble p lay events accou nted f or

appr oximate ly 94 % o f a l l bubble events . W hen b ubble p laywas cons ide r ed a lone , bubble r ing p lay events accoun ted f or

appr oximate ly 25% of bubble p lay events tha t occur r ed .

Bubble t ra i ls accou nted f or 40% of a ll bubble p lay behavior .

S ing le bubbles accou nted f or 29% o f to ta l bubble p lay

behavior . W hen bubble r ing p lay was cons ide r ed a lone ,

s ing le bubble r ings ( N = 151) accounted f or 83% and double

bubble r ings ( N = 30) accounted f or 17% of bubble r ing

events by the 4 subjects .

Figure 2. Proportion of events for bubble prod uction types.



1 0 2 M c C O W A N , M A R I N O , V A N C E , W A L K E , A N D R E I S S

T a b l e 3

Raw Data on Bubble Ring Play Behavior Events and Measures for Each Juvenile Subject

B u b b l e r i n g p r o d u c t i o n S u b j e c t

a n d o u t c o m e A v a l o n B r i s b e e L i b e r t y N o r m a n

Sing le r ing p rodu c t ion 88 13 20 30

Exce l len t qua l i ty 28 4 7 2Oth er qua l i ty 58 9 12 23Q u a l i t y d a t a m i s s i n g a 2 0 1 5W a t e r c o l u m n : T o p 1 0 0 2W a t e r c o l u m n : M i d d l e 2 0 3 3 5W a t e r c o l u m n : B o t t o m 6 3 1 0 1 7 1 5W a t e r c o lu m n : D a t a m i s s i n g~ 4 0 0 8

D o u b l e r i n g p r o d u c t i o n 1 3 9 1 7Exce l len t qua l i ty b 9 8 1 6Oth er qua l i ty b 4 1 0 0Q u a l i t y d a t a m i s s i n g a 0 0 0 1W a t e r c o l u m n : T o p 0 0 0 0W a t e r c o l u m n : M i d d l e 1 0 0 1W a t e r c o l u m n : B o t t o m 1 2 9 1 5W a t e r c o l u m n : D a t a m i s s i n g a 0 0 0 1

C a t c h a n d j o i n 5 4 0 3R i n g e x t r u s i o n 2 1 0 1R e s p o n s e t o o r m a n i p u l a t i o n o f b u b b l e r i n g

W a t c h f l o a t 2 2 0 0 0Ros t ra l ve r t ica l tu rn 13 2 0 0S w i m t h r o u g h 1 0 0 3R o s t r a l s w i p e 1 2 0 0P e c t o r a l s w i p e 1 0 0 0I g n o r e 1 0 2 0 4B i te 88 18 21 30

~ O b s er v at io n o f th i s m e a s u r e w a s m i s s i n g f o r th e n u m b e r o f e v e n t s i n d ic a t e d f o r e a c h s u b j e c t, b R e p-resen ts the qua l i ty o f the f i r st r ing in the doub le bub b le r ing even t . ¢Th is ca tego ry rep resen tse x p l i c i t o b s e r v a t i o n o f b u b b l e r i n g s ; a ll b u b b l e r i n g s h a d t o b e i m p l i c i t l y o b s e r v e d w h e n s u b s e q u e n tm a n i p u l a t i o n o c c u r r e d .

T a b l e 3 p r e s e n t s t h e r a w d a t a o n t h e t y p e s o f b u b b l e r i n g

e v e n t s , t h e q u a l i t y a n d l o c a t i o n o f s u c h e v e n t s , a n d t h e

p o s t p r o d u c t io n o b s e r v a t io n a n d m a n i p u l a t io n o f b u b b l e

r i n g s f o r e a c h s u b j e c t . A s i n d i c a t e d i n T a b l e 3 , b u b b l e r i n g

p r o d u c t i o n a n d m a n i p u l a t io n w e r e v a r i a b l e b o t h w i t h in a n d

b e t w e e n t h e ju v e n i l e s u b j e c t s . A l l o f t h e d o l p h i n s m u s t h a v e

i m p l i c i t l y o b s e r v e d t h e i r b u b b l e r i n g s v i s u a l l y o r b y e c h o l o -

c a t i o n p r io r t o a n y p o s t p r o d u c ti o n m a n i p u l a t i o n o f b u b b l e

r i n g e v e n t s ( n o t e t h a t t h e c a t e g o r y ignore d i d n o t i n v o l v e

p o s t p r o d u c t io n o b s e r v a t i o n b u t c o n s i s te d o f o n l y 1 1 % - 1 3 %

o f th e b u b b l e r i n g e v e n ts a c r o s s s u b j ec t s; 8 7 % - 8 9 % o f a ll

b u b b l e r i n g s w e r e m a n i p u l a t e d b y t h e s u b j e c t s ) . H o w e v e r ,

e x p l i c i t v i s u a l o b s e r v a t i o n w a s i d e n t i f i e d w h e n t h e d o l p h i n s

f a c e d a n d c l o s e l y f o l l o w e d t h e t r a j e c t o r y o f t h e b u b b l e

p r o d u c t i o n , a s o b s e r v e d f o r A v a l o n i n T a b l e 3 . T h e m o s t

f r e q u e n t f i n a l r e s p o n s e f o r a l l s u b j e c t s w a s t o b i t e a n d t h u s

d e s t r o y t h e b u b b l e r i n g s ( T a b l e 3 ) . O t h e r d e s t r u c t i v e b e h a v -

i o r s in c l u d e d p e c t o r a l , f l u k e, a n d r o s t r a l s w i p i n g o f t h e r i n g s

( T a b l e 3) . I n a d d it i o n , s o m e m a n i p u l a t i o n s w e r e m o r e

c o m p l e x t h a n o t h e r s . T w o o f t he d o l p h i n s g e n e r a t e d v o r t ic e s

a r o u n d t h e b u b b l e r i n g s , t h u s c a u s i n g t h e r i n g s t o t u r n

v e r t i c a l l y b y 9 0 ° o r t o c o m p l e t e l y f l ip i n o r i e n t a t i o n b y 1 8 0 ° .

W e t e r m e d t h i s b e h a v i o r rostral vertical turn ( T a b l e 3 ;

M a r t e n e t a l ., 1 9 9 6 ; B . M c C o w a n , p e r s o n a l o b s e r v a t i o n ) .

S o m e t i m e s d u r i n g d o u b l e r i n g p l a y , t h e s e c o n d r i n g c a u g h t

u p a n d j o i n e d t h e f i rs t r i n g a n d g e n e r a t e d a th i r d s m a l l e r

b u b b l e r i ng r e s u lt i ng f r o m t h e f o r c e o f im p a c t b e t w e e n t h e

f i rs t a n d s e c o n d b u b b l e r i n g s , w h i c h w e t e r m e d ringextrusion ( T a b l e 3 ) . T h i s t h i r d b u b b l e r i n g w a s s o m e t i m e s

m a n i p u l a t e d b y t h e d o l p h i n s i n a s i m i l a r m a n n e r a s d e -

s c r i b e d a b o v e f o r s i n g l e r i n g s w h e n t h e d o l p h i n s v e r t i c a l l y

t u r n e d t h e b u b b l e r i n g o r c o m p l e t e l y f l i p p e d t h e r i n g ( B .

M c C o w a n , p e r s o n a l o b s e r v a t i o n ) . H o w e v e r , n o t a l l s e c o n d

b u b b l e r i n g s c a t c h a n d j o i n f i r st b u b b l e r i n g s ( 5 0 % o f a ll

d o u b l e b u b b l e r i n g e v e n t s ) , n o r d o d o l p h i n s a l w a y s p r o d u c e

s e c o n d b u b b l e r i n g s ( 1 7 % o f a l l b u b b l e r i n g e v e n t s w e r e

d o u b l e b u b b l e r i n g e v e n t s ) .

Quality of First Bubble Ring and Probability of

Second Bubble Ring Production

T o d e t e r m i n e w h e t h e r t h e r e w o u l d b e a n y i n c e n ti v e b y t h e

d o l p h i n s t o m o n i t o r t h e q u a l i t y o f f ir s t b u b b l e r i n g p r o d u c -

t i o n , w e n e e d e d t o e s t a b l i sh t h a t t h e q u a l i t y o f t h e f ir s t

b u b b l e r i n g w a s a s s o c i a t e d w i t h w h e t h e r a s e c o n d b u b b l e

r i n g w o u l d s u c c e s s f u l l y c a t c h a n d j o i n t h e f i rs t r i n g . I n d e e d ,

s u c h a n a s s o c i a t i o n w a s f o u n d ( F i g u r e 3 A ; 1 3 = 3 . 1 , p <

. 0 0 5 , o d d s r a t i o [ O R ] = 2 1 . 8 , df = 1 6 9 ). S e c o n d b u b b l e

r i n g s p r o d u c e d a f t e r " e x c e l l e n t " f i r s t b u b b l e r i n g s s h o w e d

a n O R o f a p p r o x i m a t e l y 2 2 : 1 i n c a t c h i n g a n d j o i n i n g f i rs t



BUBBLE RING PLAY OF BOTTLENOSEDOLPHINS 103

Figure 3. Logistic regression model f or the association between the q uality of the first ring and thejoining o f the second ring (A) and the quality o f the first ring and the production of a second ring bythe dolphins (B).

r ings over second bubble r ings produced af ter "other" f irst

bubb le rings. This exU'emely high O R indicates that excellent-

quali ty f irst r ings are highly associa ted with the successful

fusion o f second and f irst rings.

As indicated above, bubble r ing play behavior can be

highly var iable and thus may be useful in revealing what

dolphins understand about physical causation. We tested

whether the double bu bble r ing behavio r of the subjects was



10 4 McCOWAN, MARINO, VANCE,WALKE,AND REISS

Figure 4. Logistic regression model for the association between bubble ring production by thedolphins and their location in the water column .

consistent with the notion that dolphins make decisions

about whether to produce a second bubble ring that arecontingent on the probabi l ity of the second ring catching up

and joining the first ring. Therefore, given that the qu ality ofthe first ring is related to whether a second ring will

successful ly catch and join i t , we examined whether thedolphin 's ow n behavior reflected this cont ingency by analyz-

ing the association between the quality of the first bubble

ring and the probability of production of a second bubblering by the same dolphin. The associat ion between qual i ty of

the fi rs t bubble ring and whether each dolphin produced a

second bubble ring w as hig hly significant (Figure 3B ; 13 =

7.8,p < .002, OR = 8,1, d f = 169). It is v ery impo rtant tonote that this result was no t a function of all rings being of

excellent quality (single rings: N = 151, 27% e xcellent, 73%other; first ring of double rings: N = 30, 80% excellent, 20%

other). The proportions o f single bubble rings versus the firstr ing of double rings that were of excel lent versus other

quality also differed substantially for each of the subjects

(Table 3). Therefore, these results established a plausibleincentive for dolphins to mon itor the quality of bubble ringsbecause the quality of the first ring is strongly correlated

with whether a second bubble ring wil l catch and join the

first. In addition, these results provide ev idence that d olphinsactually do monitor the quality of their first bubble ringsbefore deciding whether to produce a second bubble ringduring this play behavior.

Spatial Locat ion o f Bubble Ring Product ion

We further tested whether the dolphins moved to aspecific location in the water colum n to produce both single

and double bubble rings versus other types of bubble playbehavior. A significant outcome for this test would beconsistent with the notion that dolphins show anticipatoryplanning if dolphins physically position themselves at a

specified location in the water column before producingbubble tings b ut not other types of bubble pla y behaviors. As

we predicted, the dolphins did produce bubble tings in aspecified location in the water column, which was usually

near the bottom of the pool (Figure 4; bottom: 13 = 3.3, p <

.001, OR = 37.5, d f = 424; mi ddl e: 13 = 2.2, p < .001,OR = 9.5, d f = 424). Importantly, this result was indepen-

dent of the qua lity of rings produced (13 = 21.7, d f = 159,p = 1.0), indicating that all types of bubble rings, whether

single or double or whether of low or high quality, were

produced at a specific location by the dolphins (also seeTable 3). Therefore, the location of the water colu mn did notaffect the quality of the ring prod uced by the dolphins, only

whethe r the dolphins produced a bubble ring versus anothertype of bubble play event .

D i s cu s s i o n

The prese nt results are consistent with the hypothesis thatdolphins monitor the quality of their bubble rings and

engage in low-level planning prior to actual bubble ringproduction. The qualitative observations demonstrated that

there is flexibility in single and double bubble ring behavior,

particularly with regard to the manipulations of doublebubble rings after the two have joined.

Although the cognitive abilities of bottlenose dolphinshave not been exh austively explored, the existing literaturesuggests that bottlenose dolphins are capable o f a number ofpossibly related cognitive capacities, such as self-monitor-ing, that may be consistent with the present findings. Smith

et al. (1995) re ported that bottlenose dolphins were capableof monitoring their own level o f uncertainty in a psychophysi-cal experiment. There is also suggestive evidence thatdolphins recognize themselves in mirrors, although moresystematic examination of this possibility is necessary(Marino, Reiss, & Gallup, 1994; Marten & Psarakos, 1994).



BUBBLE RING PLAY OF BOTrLENOSEDOLPHINS 105

I n addi t ion , the ab i l i ty to r epor t on the pr esence or absence

o f o b j e c t s , w h i c h h a s b e e n d e m o n s t r a t e d i n b o t t l e n o s e

dolphins ( H er man, Richar ds , & Wolz , 1984) , a r guably

r e q u i r e s m o r e t h a n a r u d i m e n t a r y c a p a c i t y f o r m e n t a l

r e p r es e n t a ti o n . E v i d e n c e f o r s y n c h r o n i z e d n o v e l b e h a v i o r s

b e t w e e n t w o b o t t l e n o s e d o l p h i n s s u g g e s ts t h e p o s s i b i l it y o f

f or ep lanning ( Br as lau- Schneck , 1994) . F ina l ly , a r ecentr epor t p r esen ted the f i rs t sys temat ic obse r va t ions o f too l use

in w i ld bo t t l enose do lphins ( Smolker , Richar ds , Connor ,

Mann, & Ber ggr en , 1997) .

W i t h i n a b r o a d e r c o m p a r a t i v e c o n t e x t , t h e c o g n i t i v e

l i te r a tu r e o n n o n h u m a n p r i m a t e s o f f e rs t h e m o s t e x t e n s i v e

e m p i r i c a l b a si s f o r c o m p a r i s o n . W i t h in n o n h u m a n p r i m a te s ,

t h e p o n g i d s ( g r e a t a p e s) r e p r e s e n t a r e a s o n a b l e c o m p a r i s o n

gr oup f o r do lphins , pa r t i cu la r ly on the bas i s o f encepha l iza -

t ion leve l ( Mar ino , 1998) . Cur r en t ly , r e su l t s conver ge on

e v i d e n c e f o r a l l o f t h e a f o r e m e n t i o n e d c a p a c it i e s i n g r e a t

a p e s , f o r e x a m p l e , t o o l u s e o f v a r i o u s l e v e l s o f c o m p l e x i t y

( e .g . , Matsuzaw a & Y amakoshi , 1996; McG r ew , 1992;

Par ker & G ibson , 1977 , 1979; Sugiyama, 1997) , s e l f -

r ecogni t ion ( see Par ker , Mi tche l l , & Bocc ia , 1994 , f or a

r e v i e w ) , p l a n n i n g o f t o o l - u s e a c t i v i t y ( e .g . , B o e s c h -

A c h e r m a n n & B o e s c h , 1 9 9 4 ; L i m o n g e l l i , B o y s e n , & V i s al -

be r ghi , 1995) , and phys ica l causa l under s tanding ( L imon-

ge l l i e t a l. , 1995; V isa lbe r ghi & To mase l lo , 1998) .

A t th i s po in t , the pr esen t f ind ings cannot r evea l w he ther

t h e o b s e r v e d b e h a v i o r s a r e b a s e d o n a s s o c i a ti v e l e a rn i n g o r a

d e e p e r c o g n i t i v e u n d e r s t a n d i n g o f p h y s i c a l e v e n t s . T h i s

i s s u e h a s b e e n e l e g a n t l y l a i d o u t b y K u m m e r ( 1 9 9 5 ) a s a

c o n t i n u u m f r o m w e a k t o s t r o n g c a u s a l k n o w l e d g e . S o m e

e v i d e n c e f o r l e a r n i n g i n b u b b l e r i n g p r o d u c t i o n d o e s e x i s t .

A n e c d o t a l o b s e r v a t io n s s u g g e s t t h a t i n fa n t d o l p h i n s w a t c h

a n d l e a r n t o p r o d u c e b u b b l e r i n g s f r o m t h e i r m o t h e r s ( B .M c C o w a n , p e r s o n a l o b s e r v a ti o n ) . D u r i n g r in g p l a y , m o t h e r s

f r equent ly w a tch and echoloca te on the i r in f an ts ' f i r s t

a t t em p t s a t b u b b l e r i n g p r o d u c t i o n a n d p r o d u c e b u b b l e r i n g s

in r esponse to the i r in f an ts ' a t t empts , w hich inf an ts in tu r n

echoloca te on and w atch f loa t to the sur f ace . A s such , bo th

t h e q u a l i t y a n d t h e c o m p l e x i t y o f ri n g p r o d u c t i o n a p p e a r t o

inc r ease dur ing dev e lopm ent , pe r haps as a r esu l t o f th i s

pr ac t ice as w e l l a s the input f r om m other s . Y e t, mother s a r e

n o t t h e o n l y i n d i v id u a l s t h a t s e r v e a s e x a m p l e s o f h i g h -

q u a l i t y r i n g p r o d u c t i o n . F o r e x a m p l e , a n i n f a n t h o u s e d

s e p a r a te l y f r o m t h e j u v e n i l e m a l e s i n t h i s s t u d y w a s

f r e q u e n t l y o b s e r v e d t o b e w a t c h i n g t h e j u v e n i l e s e n g a g e d i n

b u b b l e r i n g p l a y a n d s u b s e q u e n t l y p ra c t i c in g h i s o w n r i n gpr odu c t ion a t the ga te tha t s epar a ted them.

I n conc lus ion , the pr esen t f ind ings sugges t tha t do lphins

a n t i c i p a t e t h e i r a c t i o n s a n d m o n i t o r t h e o u t c o m e o f t h e i r

b e h a v i o r d u r i n g b u b b l e r i n g p r o d u c t i o n . F u t u r e s t u d i e s o f

b u b b l e p l a y b e h a v i o r i n d o l p h i n s s h o u l d f o c u s o n t h e

o n t o g e n e t i c d e v e l o p m e n t o f t h i s b e h a v i o r s o a s t o m o r e

c o n c l u s i v e l y a d d r e s s q u e s t i o n s a b o u t t h e u n d e r l y i n g

cogni t ive bas i s f or th i s behavior . O n a mor e gener a l

leve l , the r e la t ionsh ip be tw een bubble p lay and manipula -

t ion and r e la ted cogni t ive capac i t i e s should be f ur the r

e x p l o r e d .

R e f e r e n c e s

Agresti, A. (199 0). Categorical data analysis. New Y ork: Wiley.Altmann, J. (1 974 ). Observational study o f behavior: Sampling

methods. Behaviour, 49, 227-265.Antinucci, E (E d.). (1989). Cognitive structure and developme nt in

nonhuman primates. Hillsdale, NJ: Erlbaum .Antinucci, E (1990). Cognitive ontogeny in four primate species.

In S. T. Parker & K . R. Gibson (Eds.), Language and intelligencein monkeys and apes: Comparative developmental perspectives(pp. 157 -171). New Yo rk: Cam bridge University Press.

Boesch-Achermann, H., & B oesch, C. (1994). Hominization in th erainforest: The chimpanzee's piece o f the puzzle. EvolutionaryAnthropology, 3, 9-16.

Braslau-Schne ck, S. (1994). Innovative behaviors and synchroniza-tion in bottlenosed dolphins. Unpublished master's thesis, Uni-versity o f Hawaii, Honolulu.

EGRET reference manual (Revision 4). (1997). Camb ridge, MA:Cytel Software Corporation.

Fagen, R. (1981). Animal play behavior. New York: OxfordUniversity Press.

Hall, S. L. (1998). Object play by adult animals. In M. B eko ff & J.Byers (Eds.) , Animal play: Evolutionary, comparative, andecological perspectives (pp . 45-60). New Y ork: CambridgeUniversity Press.

Herman, L. M. (1986). Cognition and language competencies ofbottlenosed dolphins. In R. J. Schusterman, J. A. Thomas, &E G. Wood (Eds.), Dolphin cognition and behavior: A compara-tive approach (pp. 221-25 2). I-Iillsdale, NJ: Erlbaum .

Herma n, L. M., Richards, D. G., & Wo lz, J. P. (1984). Comp rehen-sion of sentences by bottlenosed dolphins. Cognition, 16,129-219.

Kumm er, H. (1995). Causal knowledge in animals. In D. Sperber,D. Premack, & A. J. Premack (Eds.), Causal cognition: Amultidisciplinary debate (pp. 26-39). Oxford, England: Claren-don Press.

Limo ngelli, L., Boysen, S. T., & Visalberghi, E. (1995 ). Com prehen-sion of cau se-effect relations in a tool-using task by chimpan-zees (Pan troglodytes). Journal of Comparative Psychology,109, 18-26.

Lundgren, T. S. , & Mansour, N. N . (1 991). Vortex ring bubbles.Journal o f Fluid Mechanics, 225, 177-196.

Marino, L. (199 8). A com parison of encephalization betweenodontocete cetaceans and anthropoid primates. Brain, Behavior

and Evolution, 51,23 0-238 .Marino , L., Reiss, D., & Gallup, G. G., Jr. (199 4). Mirror

self-recognition in bottlenose do lphins: Implications for compara-tive investigations of highly dissimilar species. In S. T. Parker,R. W. Mitchell, & M. L. Boccia (Eds.), Self-awareness inanimals and humans: Developmental perspectives ( pp . 380-

391). New York: Cambridge University Press.Marten, K., & Psarakos, S. (1994). Evidence of self-awareness in

the bottlenose dolphin (Tursiops truncatus). In S. T. Parker,R. W. Mitchell, & M. L. Boccia (Eds.), Self-awareness inanimals and humans: Developmental perspectives ( pp . 361-379). New York: Cambridge University Press.

Marten, K., Shariff, K., Psarakos, S., & White, D. J. (1996,August) . Ring bubbles of dolphins. Scientific American, 275,83-87.

Matsuzawa, T., & Yamakoshi, G. (1996). Comparison o f chimpan-zee material culture between Boussou and Nimba, W est Africa.In A. E. Russon, K . A. Bard, & S. T. Parker (Eds.), Reaching intothought: The minds of the great apes (pp. 211-232). New York:

Cambridge University Press.



106 McCOWAN, MARINO , VANCE, WALKE, AND REISS

McG rew, W. C. (1992). Chimpanzee m aterial culture: Implicationsfor human evolution. Cambridge, England: Cambridge Univer-sity Press.

Parker, S. T., & Gibson , K. R. (1977). Obj ect manipul ation, too luse, and sensorimo tor intelligence as feeding adaptation in cebus

monkeys and great apes. Journal o f Human Evolution, 6,623--641.

Parker, S. T., & Gibson, K. R. (1979). A dev elopmental m odel forthe evolution of language and intelligence in early hominids.Behavioral an d Brain Sciences, 2, 367-408.

Parker, S. T., Mitchell, R. W., & Boccia, M. L. (Eds.). (1994).

Self-awareness in animals and hum ans: Developmental perspec-tives. New York: Cambridg e University Press.

Reiss, D. (1988). Can we com municate with o ther species on thisplanet? In G. Marx (Ea:l.), Bioastronomy--The next steps (pp.253-264). Norwell, MA: Kluwer Academic.

Reiss, D. (1998). Cognition and communication in dolphins: A

question o f consciousness. In S. R. Hameroff, A. W. Kaszniak, &A. C. Scott (Eds.), Towa rd a science o f consciousness II: Thesecond T ucson discussions a nd debates (pp. 551-560). Cam-bridge, MA: M IT Press.

Reiss, D., McCowan, B., & Marino, L. (1997). Commu nicative and

other cognitive characteristics of bottlenose dolphins. Trends inCognitive Sciences, 1, 140-145.

Ridgway, S. H. (1972). Homeost asis in the aquatic environment. InS. H. Ridgway (Ed.), Mammals of the sea: Biology and medicine(pp. 590--747). Sp ringfield, IL: Charles C Thom as.

Rnsson , A. E., Bard, K. A., & Parker, S. T. (Eds.). (1996). Reaching

into thought: The minds o f the great apes. New York: Cambridg eUniversity Press.

Searle, S. R., Casella, G., & McCulloch, C. E. (1992). Variancecomponents. New York: Wiley.

Smith, J. D., Schull, J., Strote, J., McGee, K., Egnor, R., & Erb, L.(1995). The uncertain response in the bottlenosed dolphin(Tursiops truncatus). Journal of Experimental Psychology:

General, 124, 391-408.Smolker, R., Richards, A., Connor, R., Mann, J., & Berggren, P.

(1997). Sponge carrying by dolph ins (Delphinidae, Tursiopssp)---A foraging specialization involving tool use. Ethology,103, 45 A. A.55.

Sugiyama , Y. (1997). Social tradition and the use o f tool-composites by wild chimpanzees. Evolutionary Anthropology, 6,23-27.

Tayler, C. K., & Saaym an, G. (1973). Imitative behavior by IndianOcean bottlenose dolphins (Tursiops aduncus) in captivity.Behaviour, 44, 286-298.

Tomasello, M., & Call, J. (1997). Primate cognition. New York:Oxford Un iversity Press.

Visalberghi, E., & Tomasello, M. (1998). P rimate causal understan d-ing in the physical and psychological domains. BehaviouralProcesses, 42, 189-203.

Rece ived O c tober 2 , 1998

Revis ion r ece ived Augus t 24 , 1999

Accepted Augus t 31 , 1999 •

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