The Auk 110(4):736-751, 1993
COMMUNICATIVE
BEHAVIOR
IN
BREEDING OSPREYS (PANDION HALIAETUS):
DESCRIPTION
SIGNALS
AND
RELATIONSHIP
OF
TO LIFE HISTORY
VINCENT BRETAGNOLLE
• AND JEAN-CLAUDETHIBAULT2
•Centred'EtudesBiologiques
de Chiz[,
Beauvoir sur Niort, 79360, France; and
2ParcNaturel R•gionalde la Corse,BP 417,
Ajaccio,Corse,20184, France
AllSTRACT.--The
Osprey(Pandionhaliaetus),
althoughstudiedextensively,is relatively unknown with respectto its behavior,especiallycommunication.We conducteda two-year
study on a residentOspreypopulation in Corsica,and describethe communicativebehavior
of this species.The behavioralrepertoireof Ospreysincluded11 visual displays(resting,
upright, alarm low and high, solicitationlow and high, defense,protection,nestprotecting,
attack,and sky dance)and eight acousticsignals(alarm,solicitationlow, high and very high,
guard, excited,screaming,and copulationcalls).The meaning of eachof the displaysand
callswas inferred from the analysisof behavioralsequences.The communicationsystemof
the Osprey consistedof sexualbehaviors(between partners),such as solicitationand sky
dance,and agonisticbehaviors(betweenbreedersand nonbreeders),suchas nest-protecting
and defensepostures.We alsoanalyzedOspreyrelationshipswith other species(including
man), and found that there was a gradationwithin alarm displaysand alarm callsaccording
to stimulusdistance.In the lastsection,we try to accountfor severalpeculiaritiesof Osprey
behaviors,namely their complexity,the behavioralsexualdimorphism,and the importance
of motivationaldisplays.We suggestthat all thesecharacters
maybe relatedto the life-history
traits shown by this species:semicoloniality,breedingstrategy,and predationrisk (on eggs
and chicks). Received30 March 1992,accepted25 November1992.
THECOMMUNICATIVE
BEHAVIOR
of manybirds
is relatively well known, and the relative com-
[Parabuteo
unicinctus]
and Galapagos
Hawk [Buteogalapagoensis];
Faaborget al. 1980,Faaborg
pletenessof our knowledgehaspermittedde- and Bednarz 1990, Dawson and Mannan 1991)
tailed comparativeanalysis(Tinbergen1959, or colonialraptors.The OspreyexhibitscolonJohnsgard1965,McKinney1965,VanTets1965, iality in somelocal populations(Hagan and
Kear 1970, Jouventin 1982, Kroodsma and MilWalters 1990). For example,on Gardiner'sIsler 1982, Hailman 1989). However, for some land (12 kin2), 300 pairs bred (Palmer 1988),
familiesand ordersour knowledgeis far from with nestsspacedno morethan50 m apart,and
complete (Schleidt et al. 1984, Miller 1989). For someascloseas 10 m (citedin Crampand Simexample,the behavior, especiallycommunica- mons 1980).However, though it is one of the
tion, of raptorshas been virtually ignored most intensely studied raptor species,the Os(Newton 1979, Palmer 1988, Rosenfield and Bie-
prey's communicative behavior has not been
lefeldt 1991),evenin suchwell-studiedspecies fully documented. Illustrations of some disas the PeregrineFalcon(Falcoperegrinus;
Rat- plays can be found in Cramp and Simmons
cliffe 1980),the GoldenEagle(Aquilachrysaetos;(1980), and sonagramsof three vocalizations
Ellis 1979),and the Osprey(Pandionhaliaetus). were publishedby them and by Poole(1989a).
Two possiblereasonsfor this may be that rapWe describethecommunication
systemof the
tors are generally solitary birds, which is usu- Ospreyand, thus,restrictour studyto the disally synonymouswith depauperatebehavioral plays(Moynihan1955),includingthosethatare
repertoires,
andareof largebodysize,meaning signalsand containa message(seeSmith 1977
that their natural population densitiesare usu-
and Beer 1982 for further details), and some
ally low, which reducesopportunitiesfor ob-
elementaryacts(e.g.copulation,fighting).Os-
serving socialbehavior (Brosset1973).
There are,however,social(e.g. Harris' Hawk
prey communicative behavior was found to in-
736
clude 11 visual displays,most of which have
October1993]
Communicative
Behavior
in Breeding
Ospreys
not previously been described,and eight acoustic signals. To understand the meaning of the
displays,we quantified behavioral sequencesin
different contexts:sexualcontextbetweenpartners; agonistic context between breeders and
conspecific intruders; and other contexts involving Ospreys and competitorsor predators.
In the last section, we discussthe significance
of the behavioralrepertoire of the Ospreywith
regard to its life-history strategy.
MATERIALS AND METHODS
Corsica(42øN,9øE)is a largewesternMediterranean
Island (8,722 km2; Fig. 1), where the Osprey population has been monitored since 1977 (Thibault and
Patrimonio 1991). In 1990 and 1991,respectively,16
and 19 pairs nested on the island, all on sea cliffs
(Thibaultand Bouvet1983).Somebirds(mainly males)
are sedentary, while others are at least partial migrants (Thibault and Patrimonio 1989). Males reoccupy nest sitesbefore females.Egg laying occursin
March and April, and fledging in June and July for
the Corsicanpopulation(Fig. 1).
Detailedstudieswere madeduring 20-27 June1990,
12-30 March 1991, and 8-16 June 1991 on 11 nests.
Continuous observations(usually from 0800 to 1900)
were carried out and included the prelaying, egg-
laying, and the end of the chick-rearingperiods(Fig.
1). Observations were made either 300 m from the
nest with a telescope(20-70 x ), or from a blind 40 to
80 m from
nest. Behaviors
were
recorded
continu-
ously on data sheets(continuousfocal-animal sampling; Altmann 1974) and their context noted (e.g.
activity or display given by partner, another Osprey,
or intruder). Sexwasdetermined on the basisof plumage pattern (e.g. Cramp and Simmons 1980). Where
a descriptionexistsin the literature of a display (or
a call), we followed the terminology employed by
previous authors.
Ospreyswere recorded with an Uher 4400 tape recorder
and
a Seinnheiser
MKH
815 unidirectional
microphone at 19.05 cm/s on AGFA PE43 tape. We
recorded 250 calls from nine pairs (1990 and 1991
combined).Calls were analyzed on an Amiga microcomputerusing an analyticpackagethat performsa
fast Fourier transform (sampling rate 6,512 Hz; step
size256 points;Richard 1991).Sonagramswere printed with a Kay 6061BSonagraph.
Both within-
and between-individual
transitions
of
behaviors were studied through the use of contingency tables (matrix of transition; see Standen 1980,
Slater 1983). A first set of matrices was constructed in
which visual and acousticdisplayswere analyzed as
responsesto different contexts(i.e. behavior of partner or presenceof intruder [Osprey,other bird, man,
etc.]). In a secondmatrix, visual displayswere analyzed (in females only) in terms of successiveacts.
737
Behaviorswere tabulatedas stimulus (or preceding)
behaviorsin the columnsand response(or following)
behaviors in the rows. The frequency with which a
stimulus behavior was followed by a responsebehavior was entered in the table (diagonal values, implying a behaviorfollowing itself,were excludedfrom
intraindividual
transition matrix; Standen 1980, Slat-
er 1983). For a behavior to be defined as following a
stimulus, it had to be observed within
15 s of the
latter. Contingencytableswere analyzedfirst with an
overall chi-squaretest (lumping data if frequencies
were too low) for significance (i.e. nonindependence),and secondwith chi-squaretestsperformedon
partitioned 2 x 2 contingencytables to searchfor
more or lessthan expecteddegreesof associationbetween behaviors(for a similar procedure,seeStanden
1980). However, in view of the number of tests that
were performed, P-valueswere consideredsignificant if less than 0.01 when
fewer
than 20 tests were
involved, or if less than 0.001 with 20 or more.
RESULTS
Description
of visualdisplays.--Elementaryacts
included typical bird activities, such as yawning, preening, copulation (described in detail
by Cramp and Simmons 1980), fighting (overt
attack at nest), and resting. This latter activity
constituted the baseline activity of Ospreys, to
which all other displays subsequently were
compared.In adults at least, resting (Figs. 2a, b,
and c) showed slight sexual dimorphism (Figs.
2a and b); malestypically are more upright than
females,with more widely opened wings.
The upright display was distinguished from
resting mainly by the more vertical general body
axis, and the position of the neck (Figs. 2d and
e); wings were held slightly opened. In a highly
motivated expressionof this display, observed
twice, a male showed extensivelyerectedcrest
feathers.
The alarm display (Figs. 2e and f) involved a
marked extension of the neck, which was fur-
ther crooked (unlike in upright display). We
recognized two variants (subsequently analyzed as two different signals) of this display
according to bird motivation (see below).
The solicitation display was given only by
females(Figs. 3a and b) and by chicksnearing
fledging. Two types of this display occurred
(subsequentlyanalyzed as two signals),according to bird motivation (Figs. 3a and b). In both,
the body axis was horizontal, the crestfeathers
were slightly erected,and the wings were held
close to the body.
The protection display (Fig. 3c) and defense
738
BRETAGNOLLE
AND THIBAULT
[Auk, Vol. 110
ARRIVAL
70ø- •
Breeding distribution
of Ospreys
JAN I FEB IMAR
60'-
20 •
1001
LAYING
/-,
I
10'
0*
10'
0 JUN
•JUL
•AU•
•
Fig. •. Studya•eaa•d b•eedi•gphewology
o• Ospreys.
g•eedi•gdistfibutio•o• Ospreys
i• weste•
Pa[ea•ctic
(modi•ed•om C•ampa•d Simmons•980,Poole•989a),showing[ocatio•o• Corsica.
G•aphso•
•ight i•dicatechronology
o• b•eedi•go• •eside•tOspreysi• Corsica.
display(Figs.3e and f; alsoillustratedin Cramp to perform it (Crampand Simmons1980).We
and Simmons 1980) are two rather similar dis- did not seethe "hoveringdisplay"(Crampand
plays,distinguished
by wing positionin rela- Simmons 1980, Poole 1989a) and suspect it is
tiontothebody.In protection
display,
shoulder only a variant of sky-dancedisplay.Thus, the
and carpaljointswere closeto the body,and visual repertoireof the Ospreyincluded nine
the bodyaxiswasusuallymoreor lesshorizon- different signals,and severalelementaryacts
tal; in the defensedisplay, the wings were most-
that shall be included here (i.e. copulation, at-
ly opened,and the carpaljoint was close,or
lyingon theground.In a highlymotivatedversion of this display, the bird could move to a
more horizontalposition,with the tail raised
and contracted(Fig. 3d).
The nest-protecting
display(Crampand Simmons1980)wascharacterizedby wing shaking,
tack and resting).
Description
of calls.--Somepreviouscall descriptionsare to be found in Crampand Simmons (1980) and Poole (1989a:113). The alarm
call (Fig. 4a) hasbeendescribedin both references cited above, and shows a clear sexual di-
morphismas illustrated in Poole (1989a:113).
The solicitationcall (Figs.4b,c, andd) wasonly
We observedonly one type of flight display, given by femalesand has three versionsthat
the sky-dancedisplay (for extensivedescrip- have not previously been noted in the literation, seeCrampand Simmons1980).This be- ture. The three differed in temporal and frehavior was only recordedin malesduring our quencyparameters,but representa continuum,
acstudy,althoughfemalesare apparentlyknown as a female usually gave them successively
a fanned tail, and a horizontal position(Fig. 3d).
October1993]
Communicative
Behavior
in Breeding
Ospreys
RESTING(d")
739
RESTING (JUVENILE)
RESTING(9)
Crest
feethers
Win
position
b
a
c
feathers
Spreed
wings
neck
UPRIGHT
UPRIGHT
EXITED)
(9)
d
o
ALARM LOW
Flattened
Broken
feethers
neck
ALARM
HIGH
Flettened
wings
g
Fig. 2. Visualdisplaysof male,female,and juvenileOsprey.Name of displaygiven in capitalletters.
Arrows indicateimportantfeaturesof body that distinguishdifferentbehaviors(e.g. neck position,wing
position, etc.).
cording to her motivation. The screamingcall
(following Henny in Palmer 1988) was given
by both sexes(Figs.4e and f) and usuallyin
flight (see below). The guard call (following
Poole 1989a:113) and the excited call were also
given by birds of both sexes(Figs.4g and h).
The latter has not been described (although a
sonagramis includedin Poole1989a:113);it alwaysfollowedthe guardcall.Other previously
undescribedcalls include a copulation call (not
illustrated)and different callsof the chicks.Very
youngchicks(under two weeks)gavea version
of the guard call when fed (Fig. 4i). When older,
they begged for food in the same way as the
female (Fig. 4j). At a later stage,when exercising
their wings, young sometimesgave the screaming call.
Associations
betweencallsand visualdisplays.As shown in Table 1, there was no strict concordance
between
vocalizations
and visual
dis-
740
BRETAGNOLLE
A•DTHI•SAULT
/
Head
[Auk,Vol.110
position
b
Tail
•osition
wings
SOLICITATION
LOW
SOLICITATION
HIGH
c
d
Openwing
PROTECTION
POSTURE
NEST-PROTECTING
POSTURE
o
Horizontal
neck
f
Tail
DEFENSE
POSTURE
raised
LOW
DEFENSE
POSTURE
HIGH
Fig. 3. Visualdisplaysof Ospreys.Arrowsindicateimportantfeaturesof bodythat distinguishdifferent
behaviors
(e.g.neckposition,
wingposition,
etc.).Largearrowindicates
wingmovement
in nest-protecting
display.
plays,exceptfor the screamingand solicitation
Behavioral
differences
between
sexes.--Therewas
calls, which were given respectivelyin associ- no obvious sex difference in the rate of emission
ation with flying and solicitationdisplay.Other of visual or acousticsignals(5.28 vs. 6.06 visual
calls, although usually loosely associatedwith displays,and 5.38 vs. 6.42 acousticsignals/h at
one particular display (e.g. defense with the nestfor femalesand males,respectively;Table
guard call; Table 1), were also associatedwith
2). However, we found qualitative and quanothers.Somedisplayswere not associatedwith titative sexual dimorphism of visual displays
vocalizations(alarm display),while otherswere and calls (Table 2). In the case of males, 78% of
systematicallyaccompaniedby calls (solicita- all instances of behavior noted were occurtion, nestprotecting;Table 1). Lastly,there was rencesof upright, defense,and skydance,while
a parallelgradationbetweensomecallsand some alarm,solicitation,and nestprotectingaccountdisplays,namelyfrom guardto excitedthrough ed for 72% of female behaviors (Table 2). With
screamingcalls, and upright, protection, de- regard to calls,screamingand guard callswere
fense, and nest-protectingdisplays(X2 = 28.1, often uttered by males (65%), while females utdf = 6, P < 0.001; Table 1).
tered mainly solicitation calls (55%). Moreover,
October1993]
Communicative
Behavior
in Breeding
Ospreys
Frequency{KHz)
Solicitation
6-
Alarm
741
Call
low
Call
Solicitation
Solicitation
Call high
Screaming
Call
Guard
Call
very high
ScreamingCall
Call
Excited
Call
GuardCall(Chick}
•
Solicitation(Chick•
• Time
(s•
Fig.4. Callsof male,female,andjuvenile(chickstage)Ospreys(timein seconds;
frequencyin kilohertz).
742
BRETAGNOLLE
ANDTHIBAULT
[Auk,Vol. 1I0
TABLE
I. Frequencyof associations
betweenvisualdisplays(columns),and acoustic
signals(rows).
Visual display
Nest
Acoustic
signal
RestUp- Solicita- Feed- Protec- De- protectFlight Alight ing Alarm right
tion
ing
tion
fense
ing
Totals
Alarm call
Solicitation
Low
42
16
0
0
High
Very high
Screamingcall
0
0
34
I
0
0
Guard call
Excited call
18
4
21
2
Totals (with calls)
Totals (without callsa)
Percent (without calls)
98
---
40
38
48
27
3
3
0
7
37
2
27
7
0
0
0
0
2
0
0
I
100
---
6
32
84
0
0
3
7
18
3
0
0
36
17
0
12
0
25
13
34
101
14
0
0
0
78
18
8
0
0
4
7
I
5
0
I
2
14
87
43
55
0
0
0
0
9
5
15
2
11
11
88
25
71
0
0
47
---
25
23
48
23
27
50
42
24
32
477
---
Continuousactivities(e.g. flying) not considered.
on a quantitative basis,significant differences
in frequencyof emissionoccurredin mostdisplays (13 of 17; Table 2).
Influenceof contexton incidences
of displays.We firstanalyzedthe sexualbehaviorof the pair
(i.e. male behavior being taken as a stimulus
possiblyeliciting a responsefrom female). An
overall test of significance(data from Table 3,
regroupinglow and high versionswithin alarm
and solicitation, excluding "take off" due to
sample size; X 2 = 225; df = 32, P < 0.0001)
indicated that male behavior had a strong influence
on female
behavior.
Predominant
fe-
male visual displayswere related to alarm and
solicitation activities (Table 3), which accountTABLE2. Comparisons(chi-square tests) between
sexesof frequenciesand percentagesof displays
and calls.
curred more than would be expected (at P <
Given by•
Display
Upright
Female(%) Male (%)
pb
26 (7.0)
12 (16.7)
<0.01
Low
53 (14.4)
3 (4.1)
ns
High
46 (12.5)
3 (4.1)
ns
Alarm
Solicitation
Low
50 (13.6)
0 (0.0)
<0.001
High
Protection
66 (17.9)
35 (9.5)
0 (0.0)
6 (8.3)
<0.001
ns
Defense
33 (8.9)
17 (23.6)
<0.001
Nest-protecting
Attack
Sky-dance
Alarm call
49 (13.3)
11 (3.0)
0 (0.0)
81 (21.5)
4 (5.6)
0 (0.0)
27 (37.5)
16 (21.1)
ns
ns
<0.001
ns
Solicitation
ed for up to 61.4% of displays.This was also
clear when only those associationsthat oc-
call
Low
65 (17.3)
0 (0.0)
<0.001
High
Very high
Screaming call
92 (24.5)
49 (13.0)
23 (6.1)
0 (0.0)
0 (0.0)
16 (21.1)
<0.001
<0.001
<0.001
Guard call
49 (13.0)
33 (43.4)
<0.001
Excited call
17 (4.5)
11 (14.5)
<0.001
"Totals for femalesand males,respectively,during 1990 and 1991;
acousticsignals, 376 and 76; visual displays, 369 and 72; times of observation, 4,192 and 710 min.
• For theseanalyses,ns usedfor P > 0.01.
0.001)by chancewere considered(Table3). Male
behaviorinducedtwo typesof responses
by females(seeFig. 5). First,the presenceof the male,
whether flying, being at the nest, or close to
the nest,significantlyelicited solicitation(low
or high). Femalebehavior differed whether the
male carried a fish (solicitationhigh), nothing
(solicitation low), or a branch (resting; i.e. no
response).Second,although this was less obvious, males (e.g. when landing at nest) seem
to elicit from females behavior
associated with
being alert, as the latter showedalarm and upright (Table 3 and Fig. 5). Similar resultswere
obtained
for calls, with
solicitation
calls ac-
countingfor 96%of the callsemitted by females
(Table 3) in responseto male behavior.
We alsoanalyzedthe behaviorof the breeders
facingthe intrusionof anotherOsprey(sexundefined) close to the nest (Table 4). In that con-
text, breedersshowed three types of displays
(seeFig. 6): (1) nest protecting,the commonest
visual display; (2) taking off; and (3) guard,
screaming,and excitedcalls(Table 4). Further-
October1993]
FEMALE
Communicative
Behavior
in Breeding
Ospreys
743
BEHAVIOR
BEHAVIOR
•/.'--FLY
MALE
ING
•
INTRUDER
Alarm
low
•
high
Upright
Alarm
Alight / Take off
high
Nest
prote•i•
•
Defense
P <0.05
•P<O.01
Protection
Defense
P<O.001
Fig. 5. Summaryof visualdisplaysrelatedto type of stimulus.Femalebehaviorelicitedby male behavior.
Arrow thicknessindicatesprobability level (data from Tables4 and 6).
more, although samplesize was low for males,
significantsexualdifferenceswere found. Nest
protectingwas almostexclusivelygiven by females, whereas movementswere typical male
responses;
malesalightedif flying overthe nest,
or took off if at the nest(Fig. 6). Other behaviors
were rarely shown. Conversely,no significant
sexual differenceswere found with regard to
calls.
We also analyzed the behavior of male and
female Ospreys when a potential predator/
competitor (i.e. something other than an Osprey) approachedthe nest (Table 5). In each
case,whether the "intruder" was a boat, gull,
raven, or raptor,the display changedasthe dis-
tion in display use was highly significant(X2=
85.7, df = 10, P < 0.001). Similar gradations
were observed for other stimuli (Table 5). The
alarm call on the other hand was mainly associated with human and boat presenceclose to
the Ospreys(Table 5).
Succession
of visualdisplays.--Toevaluate se-
quencesof visualdisplays,we consideredthose
of femalesalone given the small samplesizes
for males, and the calls for both sexes. Overall
testsfor significancerevealed that the following behaviors did not occur at random (Table
6; lumping low and high versionsof alarm and
solicitation, and defense, protection, and nest
protecting in stimulus behavior; X • = 435, df =
32, P < 0.0001).Baselineactivity (resting)was
significantly followed by upright, alarm-low,
ple size was large enough to allow statistical and solicitation-low displays. This indicated
analysis.At 500m or more,this stimuluselicited presumablythat these displaysconveyedthe
no responsein 89% of cases.At less than 250 lowest degree of motivation from the female.
tance
between
the bird
and
the stimulus
de-
creased(Table 5). In the caseof a boat, the sam-
A next step in motivational intensity was reresponses.And at lessthan 100 m femalestook flected by solicitation high and alarm high,
off in 61% of casesand males performed the which significantly followed solicitation low
sky-dancedisplay in 45% of cases.This grada- and alarm low, respectively(Table 6). The three
m, both alarm versions accounted for 57% of
744
BRETAGNOLLE
AND THIBAULT
[Auk, Vol. 110
TABLE3. Behaviorelicited in female as responseto stimulusfrom malea.
Behavior of male (stimulus)
Behaviorof female
(response)
Flying
Alighting
with
Alighting
branch with fish
Alighting
Taking off
At nest
Total
Visual displays
Resting
3
5
0, -***
6
Upright
3
Alarm
7
2
0
1
7
5
7
4
4
2
4
4
0
4
4
0
19
17
25
11
52
33, +***
66
Solicitation low
22,
1
3
0
0
Solicitationhigh
low
Alarm high
2
10
0
Protection
1
Defense
0
Nest protecting
Copulation
1
8
0
0
0
3
Take
0
0
off
Alight
Total
0, -***
41
0, -***
0, -***
1
2
0
0
1
0
0
2
0
0
0
0
3
7
0
6
0
1
0
0
0
0
9, +***
0
0
0
9
29
37
76
257
1
0
0
18
20
5
47
61
30
57
12
6
0
0
0
23, +***
27, +***
46
6
9
1
19
1
Calls
Solicitation
call low
Solicitationcall high
Solicitationcall very high
10
3
Guard call
3
Screamingcall
1
Total
23
6, -***
31, +***
22, +***
16, +***
0, -***
0
0
0
2
0
0
0
0
0
0
0
5
1
0
61
16
1
43
144
• Foreachcell of table,2 x 2 chi-squaretestusedfor comparingobservedand expectedfrequencies.
Forexample,when an association
occurred
significantlymorethan expected,a "+" followsthe frequency(or a .... for a negativeassociation).
Only valueswith P < 0.001(***) judged
significant.
remaining displays--nest protecting, defense,
and protection--showed complex interactions
TABLE
4. Comparison(chi-squareand Fishers'sexact
tests)of frequenciesof responseof femaleand male
Ospreysat their nestto intrusionof anotherOsprey
closeto eyrie (<200 m). Only valueswith P < 0.01
judged significant.
Behavior
Behavior
Female
of
Male
Total
P
Visual displays
Resting
Upright
7
7
4
4
11
11
ns
ns
Alarm
Protection
Defense
12
11
10
0
0
5
12
11
15
ns
ns
ns
Nest protecting
Take off
Alight
48
13
5
3
11
8
51
24
13
0.0004
0.01
0.002
Total
113
35
Total
6
2
27
19
21
0
0
14
6
6
75
26
more or less related
to each other.
Defense and protection displays followed solicitation high, and occurredin sequence;when
the male brought a fish, the female showedsolicitation high until the male gavethe fish,when
femalesshoweddefenseand/or protectiondisplay (Fig. 5). In these types of sequences,nest
protecting was never observed. In a different
context, when another Osprey flew over the
nest,nestprotectingoccurredafter upright display, and followed or preceded (equally) defense and/or protectiondisplays(Table 6 and
Fig. 6).
DISCUSSION
146
Calls
Alarm
Solicitation
Guard
Screaming
Excited
and were
6
2
41
25
27
101
ns
ns
ns
ns
ns
Our interestis in accountingfor the meaning
and function of eachvisual and vocal signal of
the Osprey.Meaningscanbe deducedfrom both
the contextin which the displayoccurred,and
its effectson the receiverbird (for generaldiscussionand definitions of signal, message,and
meaning,seeSmith 1977).After addressingthese
October1993]
Communicative
Behavior
in Breeding
Ospreys
CLOSE
MALE
BEHAVIOR
(stimulus)
TO THE
NEST
745
AT NEST
•Flying
Landed
fish
Restin!
FEMALE
BEHAVIOR
(response)
Solicitation
Defense
low
•
Solicitation
high
P<
O.Ol
===• P < 0.05
•-•p< o.ool
Protection
Fig.6. Summary
ofvisualdisplays
givenbymaleandfemaleOspreys
whenanOspreyintruderapproached
nest(datafromTables5 and 6). Arrowthickness
indicates
probabilitylevel(datafromTables4 and6).
matters,we discussthe biologicalsignificance playscomparedto resting).Also, the white borof behaviorswith regardto the life historyof der on the back outlines the position of the
the Osprey,and emphasizehow behavioraland wings (relevant for defense, protection, and
ecologicallife-history traits are connectedto nest-protectingdisplays).Wing position is an
each other.
agonisticindicator (seebelow). These findings
Ospreycoloration.--Althoughcoloration has are supported by comparison of male, female,
been seldom discussed as a behavioral element
and juvenile coloration. The contrastis reduced
in repertoires,it obviouslycanfunction in com-
in femalescomparedto males(mainly by neck
position in restingand upright, and dark breast
coloration).Moreover, when females beg for
municative behavior (Mock 1980, Jouventin
1982, Zahavi 1988). The coloration of the Os-
prey is interestingas it is simple and of high food(solicitationdisplay),theysubstantially
recontrast.Ospreyflight colorationundoubtedly duce this contrastin both neck (head is kept
is related to its fishing behavior (for a review hunched)and back(wingskept closeto body).
on fish-eating seabirds,see Cairns 1986); com- Conversely,the amountof white shownby the
plex underwing colorationmight enhancefish males on their backs when perched appears
capture efficiencythrough a disruptive effect greater than in females(Fig. 2). Such contrast
(Wilson et al. 1988). We suggestthat the col- is absent from fledgling birds, where white is
orationof Ospreyswhen theyareperchedmay replacedby creamcolor,and blackby rufousor
play a part in communicativebehavior (seealso
Bretagnolle et al. 1994). The black-and-white
contrastmay exaggeratesomeof the visual dis-
plays. It outlines the neck form and shapein
those displaysthat indicate an increasedlevel
of attention(relevantfor alarmanduprightdis-
brown (Fig. 2).
Ospreymating.--Somevisual displays are
mainly found in heterosexualbehavior (i.e. involving partners). For females, these include
solicitationand to a lesserextentalarm and upright, while sky dance was the predominant
746
BRETAGIqOLLE
ANDTHIBAULT
[Auk,Vol. 110
male activity (Table3). Thus,it is expectedthat
the function of thosedisplaysis related to mating and/or pair-bond maintenance.
Male mating behavior included mainly the
sky dance (see also Poole 1989a),which is a
typical raptor mating display found in many
other species(Tubbs 1974, Newton 1979, Wat-
son1977,Gargett1990).It is highly conspicuous
and likely to be directed towards both females
(advertising)and males(exclusion;Poole1989a).
Mating is fairly rapid in the Osprey(Green1976,
Jamiesonet al. 1982, Henny in Palmer 1988,
Poole 1989a).The sky dance,known to be given
frequently by Ospreys (Cramp and Simmons
1980,Poole 1989a),may play a part in this rapid
mating. However, the sky dance was a relatively rare display in Corsica (pers. obs.), and
we suggestthat rapid mating might be a consequencemainly of mate and site fidelity from
year to year in this species(Jamiesonet al. 1982,
Poole1989a,Postupalsky1989,Thibault and Patrimonio 1991).Moreover, CorsicanOspreysare
resident, which may also facilitate pairing.
Though Greene (1987) suggestedthat the sky
dance is used by males to indicate successful
fishing to other males of the colony (following
information-center theory; Ward and Zahavi
1973), we suggestthat his sample sizeswere
limited and do not excludethe possibilitythat
the sky dance is primarily a sexualbehavior.
Female sexual behavior included solicitation,
although it is not strictly related to mating.
Courtshipfeedingis of majorimportancein the
Osprey, especially for female productivity
(Birkhead and Lessel1988, Poole 1989a). Thus,
it is not surprisingthat somedisplaysare devoted to solicitationfor fish. Moreover, feeding
by male Ospreycontinuesthroughoutbreeding
and, therefore, solicitationmay be interpreted
as having a proximate (to obtain food) and an
ultimate (pair-bond reinforcement) function.
Other displays(alarm and upright) are not related to mating, and appearin heterosexualbehavior as a by-productof antagonisticrelationships (see below).
Ospreyagonistic
behavior.--Theagonisticnature of nest-protecting,protection,and defense
displaysis revealed by their occurrencein aggressivecontexts:when an intruder flies over
the nest (especially for nest protecting; Table
4); or when there is a disputebetween the partners for a fish (defenseand protection displays;
Table 6). Nest protecting is a display almost
exclusively given by the female (Tables 2 and
October1993]
Communicative
Behavior
in Breeding
Ospreys
747
4) and directed toward flying birds (Table 4).
Wing shaking in the nest-protectingdisplay,
clearly emphasizedby the white border of the
back (Fig. 4), is especiallyvisible from above.
Nest protectingis highly agonistic,asit is quite
The skydancewasregularlyobservedin males
carrying fish when human observers were at
the nest (i.e. for chick banding). We suggest
often followed by direct attack if the intruder
1989a).
haslanded (Table6). Conversely,when the intruder leaves, nest protecting is followed by
defenseand/or protection(Table 6). This suggeststhat defenseand protectionhave a lower
agonisticcontent,and they are in factlesslikely
believe that callsdo not act as signalsby themselves,but indicate the degreeof motivation of
the emitter bird. First, callsnearly alwaysaccompaniedvisual displaysand, therefore,were
that, in this context,the skydanceis a displacement activity (for similar observations,seePoole
Apart from the alarm call (see below), we
to be directed toward an intruder (Table 4).
rarely uttered alone (Table 1). Second,callswere
Defenseis a very typical raptor display,and
can be regardedas a food-defenseposturethat
generally occursjust after the kill. It appeared
in a slightly differentcontextin the Osprey(i.e.
not associatedwith any specificdisplay (Table
1). Third, there was no significant difference
when
the female obtained
a fish from the male
and wanted to keep it from him). We alsofound
anothercontextin which male Ospreysexhibited defense:at the beginning of the breeding
between
male
and
female
calls when
an in-
truder flies over the nest (Table 4), whereas sex-
biasedresponses
occurredwith visualdisplays.
Only one call (solicitation)appearedin heterosexual context (Table 5), whereas other calls were
season,and typically during the copulationperiod, sightingan Ospreyintruder can inducea
maleto alight and then to showdefensedisplay
(Table 4). In this context,we suggestthat the
male tries to protecthis female from extrapair
mainly agonistic (Table 4). Moreover, these latter calls(guard,screaming,and excited)parallel
the gradually increasingaggressivityof visual
displays(upright, defense,protection,and nest
protecting; Table 1). That calls underline emitter-bird motivation is alsosupportedby the fact
copulation (Mq•ller 1987, Birkhead and Lessel
that somecalls can appear in highly different
1988)as he would protecta prey item.
The distinctionbetweendefenseand protec-
contexts. For example, the screaming call appears in both sexual behavior (sky dance) and
when the female is very frightened (see also
Poole 1989a).The alarm call is the only call that
conveysa signal exclusiveof visual displays;it
is mainly given by the female to alert the chicks
that a potential danger approaches(Table 5).
Thus, in 68% of cases(n = 59) that the female
tion is slight, and the latter might be an atten-
uated version of defense.Protectionis rarely
given by males (Table 3); however, protection
often followsa defensedisplay(Table7) and is
restrictedto the fish-deliverycontext(which is
not the casefor the defensedisplay).Protection,
therefore, might be a version of the defense
display as expressedin a sexualcontext.
Motivationalsignalsin Ospreys.--Two visual
displays,alarm and upright, direct a message
to any bird, whether partner, chick, or conspecific, and occur in all contexts. Both are fre-
quently given by the female (Tables2, 4, 5, and
emitted the call, the chicks flattened themselves
in the nest,increasingthe effectivenessof their
camouflage.
Ospreylife historyand biological
significance
of
behaviors.--Nearlyall raptors are sexually dimorphic (Newton 1979, Mueller and Meyer
1985, Mueller 1990), and the Osprey is no ex-
6), but alarm was seen only rarely in males. ception. Thus, it is not surprising that there is
Alarm displaywas mainly given in responseto also sexual difference in communicative behava potential danger (Table 5); during the brood ior of raptors,although this latter point, poorly
rearing period, it was directed toward chicks documented,hasmainly beendiscussed
in terms
(in order to alert them), but it also occurred of nest defense (Mueller and Meyer 1985, Anfrequently in March when no chickswere pres- dersson and Wiklund 1987). Behavioral different (pers. obs.).Upright also occurredin a sim- ences between male and female Ospreys are
ilar context,and probablysignifiesan increased found in: (1) the number of displays(somevilevel of attention comparedto resting (Tables sualsignalsand callsare given by only one sex);
3 and 4). Both upright and alarm can be fol(2) the form and structureof the display(vocal
lowed by almost any behavior (Table 6). We sexualdimorphism, sexualasymmetryin neck
suggest that they are indicators of bird motiand head position);and (3) the meaningof some
vation.
displays(e.g.screamingcall).Ospreysshowex-
748
BRETAGh/OLLE
ANDTHIBAULT
[Auk,Vol. 110
TABLE6. Transition matrix for intraindividual progression(female only) of visual displays.Cell numbers
represent frequenciesof associationsbetween (preceding) and second(following) behavior; a behavior
cannot follow itself (i.e. diagonalsexcluded)a.
First behavior
Second
behavior
display
Upright
18, +***
Alarm low
20, +***
Alarm high
Solicitation
Alarm
No
9
1
--
22, +***
High
1
0
--
Upright
-1
0
39, + ***
6
0
5
Solicitation high
4, - ***
1
0
7
Defense
0, - ***
0
1
5
Protection
5
0
1
6
Nest protecting
7
1
1
11,
Take off
Attack
Total
low
Low
17
1
0
0
27, +***
0
0
0
119
32
31
35
• For each cell, a 2 x 2 chi-squaretest usedfor comparingobservedand expectedfrequencies.For example,when an association
occurred
significantlymorethanexpected,a "+" followsfrequency(or a .... for a negativeassociation).
Only valueswith P < 0.001(* * * ) judgedsignificant.
treme role partitioning between the sexes.The
male provides all of the food for both female
and young (99% of fish are provided by male;
dimorphismin repertoiresis originatedin this
from the arrival on the breeding site until the
departure of the juveniles (Green 1976, Poole
wide sexual asymmetry of life histories.
Most raptor speciesdefend feeding territories
(Newton 1979), but the Osprey does not, especially in coastalareas(Greene and Freedman
1986;pers. obs.). Moreover, some Osprey pop-
1989a).Conversely,the female Ospreystaysat
ulations (although not at present in Corsica)
Stinson et al. 1988, see also Jamieson et al. 1982),
the nest for more than five months. We suggest breed in loose colonies (references in Cramp
that both female and male repertoires result and Simmons 1980, Palmer 1988, Poole 1989a,
from, and reflect, this difference. For the female,
b, Hagan and Walters 1990). The absenceof
two activitiesare of major importance:food so- feeding territory may be related to diet, as fish
licitation from the male;and nestdefenseagainst are a spatiotemporallyunpredictable resource
Osprey intruders (Green 1976, Poole 1989a,Ha- (Poole 1989b, Edwards 1989). Recently, Greene
gan and Walters 1990) and predators (Stinson (1987) showed that Osprey coloniesmay act as
et al. 1988, Poole 1989a). With respectto food information centers, but this is not a general
provisioning, femalesspendmostof their time rule (Hagan and Walters 1990). Whether colon(frequency of occurrenceof displays)in these iality in the Osprey resultsfrom trophic or soactivities, and the motivational state of the fecial factors (see Hagan and Walters 1990), we
male (an important characteristicof food beg- suggestthat it has led to a complex repertoire
ging) is communicatedby the two versions of with many ritualized displays.This may have
solicitationdisplayand three calls.Femalenest been favored by a high potential rate of contact
defense is achieved through a ritualized dis- between individuals (e.g. Bretagnolle1988,Haplay--nest protecting. Males, however, must gan and Walters 1990).In Corsica,the frequency
provide nourishment for the entire family and of intruder visits could reach 12 per day during
leave the female for long periods of time. Os- the study period (up to 5/h), although landing
preys are also semicolonialbreedersand, thus, of the intruder on another pair's nest is excep-
there is a high rate of potential conflictswith
Osprey intruders. Since males cannot defend
tional, and direct attack is even more rare. This
may be a consequenceof the well-developed
social communicationsystem,which includes
Ospreys have repertoires with very conspicu- several agonisticdisplayswith increasingmoous (e.g. sky dance) and agonistic(e.g. defense) tivation. We suggestthat both a large diversity
displays, in order especially to avoid extrapair and a specialization(ritualization) of displays
copulation (M•ller 1987, Birkhead and Lessel are adaptive responsesto semicoloniality and
1988). Therefore, we conclude that the sexual lack of feeding territories in the Osprey.
the nest and their mate all of the time, the male
October 1993]
TABLE 6.
749
Communicative
Behaviorin Breeding
Ospreys
Extended.
First behavior
Solicitation
Nest
Low
High
2
0
1
0
0
0
--
0
54, +***
0
0
-14, +***
8, +***
Defense
Protection
protecting
Total
1
0
I
25
0
0
0
0
0
1
21
32
0
0
0
0
1
0
51
66
-12, +***
7, +**•
1
-11, +***
2
0
8
0
0
0
0
0
0
0
66
23
20
12
9, +***
13, +***
--
30
45
40
0
53
11, +***
11
36
374
Ospreysbreed on very exposed(Poole 1989a) peoplehelped with field work, but particularthanks
and large nests (up to 3 m in diameter; De- are due to J.-P. Cantera, A. Delestrade, F. Finelli, I.
Naurois 1987). Osprey neststend to be as in- Guyot, O. Patrimonio, and people from the Fonds
accessibleas possible,a responseto terrestrial d'Intervention pour les Rapaces.A. Huggins and S.
J.G. Hall kindly improvedthe English.We acknowledgewith gratitudeJ.C. Bednarz,J.Hagan,C. Hubert,
posedplacementof the nestmightbea response M. Marquiss,and G. D. Schnell for their comments
predation risk (see Poole 1989a), and the ex-
to the Osprey'srelative lack of flying agility
and advice
(Sa'fller 1977). However, nestsare still accessible
Ruchonwho drew the figures.
to birds (e.g. to predatorslike the Common Raven [Corvuscorax],and competitorssuchasHaliaetusspp.), and also are highly vulnerable and
attractive to other Ospreys.Thesepotential dangers may have led to an increaseddegree of
camouflageof chicks(Ospreychicksare brown,
not white, and juvenile plumage is mimetic to
nest color). We suggestthat it has led also to
three major behavioral characteristicsof Os-
preys:(1) the very high intensityof guarding
and attentivenessby female Ospreys;(2) the
large size of the repertoire and the ritualization
(in terms of conspicuousness)
of displays,as
visual signals need to be detected and interpreted at long distancesand, thus, must be unambiguous;and (3) the existenceof numerous
unmistakablemotivational signals(alarm, upright, and virtually all calls),which seemto be
especiallywell developedin the Osprey.These
signals are clearly visible and audible, and
probably clear indicators of motivation to conspecificsand heterospecifics.
ACKNO•EI•MF2q•
Fieldwork was funded by R•serve Naturelie de
Scandola(ParcNaturel R•gionalde la Corse).Many
on an earlier
draft.
Lrm•TUR•
We are indebted
to L.
CITED
ALTMANN,J. 19Y4. Observationalstudy of behaviour: Sampling methods. Behaviour 49:22Y-26Y.
ANDERSSON,S., AND C. G. WIKLUND.
1987. Sex role
partitioning during offspring protection in the
Rough-leggedBuzzardButeolapogus.
Ibis 129:103107.
BEER,C.G. 1982. Conceptualissuesin the study of
communication.Pages279-310 in Acousticcommunication in birds, vol. 2 (D. E. Kroodsma and
E. H. Miller, Eds.). Academic Press,New York.
BIRKHEAD,
T. R., ANDC. M. LESSEL.1988. Copulation
behaviourof the OspreyPandionhaliaetus.
Anim.
Behav. 36:1672-1682.
BRETAGNOLLE,V.
1988.
Social behaviour
of the
SouthernGiant Petrel Macronectes
giganteus.
Ostrich 59:116-125.
BRETAGNOLLE,
V., J.-C. THIBAULT,AND J.-M. DOMINICI.
1994. Head patterns allow field identification of
individual Ospreys.J. Wildl. Manage. In press.
BROSSEr,
A. 1973. Etudecomparativede l'ontog•n•se
descomportementschez les rapacesAccipitrid•s
et Falconid•s.Z. Tierpsychol.32:386-417.
CAIRNS,D.K. 1986. Plumagecolour in pursuit-diving seabirds:Why do penguins wear tuxedos?
Bird Behav.
6:58-65.
CRAMP,S., AND K. E. L. SIMMONS.(EDS.). 1980. The
750
BRETAGNOLLE
ANDTHIBAULT
[Auk, Vol. 110
birds of the western Palearctic, vol. 2. Oxford
Univ. Press, Oxford.
Blue Heronsand Great Egrets.Behaviour72:156-
DAWSON, J. W., AND R. W. MANNAN. 1991. Domi-
MOLLER,A. P. 1987. Copulation behaviour in the
Goshawk, Accipitergentilis.Anim. Behav. 35:755-
nance hierarchies and helper contribution in
Harris'
Hawks.
Auk
763.
108:649-660.
DENAUROIS,R. 1987. Le Balbuzard (Pandionhaliaetus
L.) aux lies du Cap Vert. Annali del Museo di
Storia Naturale
di Genova
170.
MOYNIHAN,M. 1955. Type of hostile display. Auk
72:247-259.
MUELLER,H.C.
86:657-681.
EDWARDS,
T.C. 1989. The ontogenyof diet selection
in fledgling Ospreys.Ecology70:881-896.
ELLIS,D. H. 1979. Development of behavior in the
Golden Eagle.Wildl. Monogr. 70.
FAABORG,J., T. DE VRIES, C. B. PATTERSON,AND C. R.
1990. The evolution of reversed sex-
ual dimorphism in size in monogamousspecies
of birds.
Biol. Rev. 65:553-585.
MUELLER,H. C., AND K. MEYER. 1985. The evolution
of reversed sexual dimorphism in size: A comparative analysis of the Falconiformesof the
western
Palearctic.
Curt.
Ornithol.
2:65-101.
GPdFFtN.1980. Preliminary observationson the
occurrenceand evolution of polyandry in the
GalapagosHawk (Buteogalapagoensis).
Auk 97:581-
NEWTON,I. 1979. Populationecologyof raptors.T.
& A.D. Poyser,Calton, United Kingdom.
590.
PALMER,R. S. (ED.). 1988. Handbook of North Amer-
ican birds, vol. 4. Yale Univ. Press, New Haven,
FAABOR(;,
J.,ANDJ.C. BEDNARZ.1990. Galapagosand
Connecticut.
Harris' hawks: Divergent causesof sociality in
A.F. 1989a. Ospreys.CambridgeUniv. Press,
two raptors.Pages357-383in Cooperativebreed- POOLE,
Cambridge.
ing in birds (P. B. Staceyand W. D. Koenig,Eds.).
POOLE,A. F. 1989b. Regulationin OspreyPandion
CambridgeUniv. Press,Cambridge.
haliaetus
populations:The role of nestsite availGARGETT,
V. 1990. The Black Eagle. Acorn Books,
ability. Pages227-234in Raptorsin the modern
Randburgh,SouthAfrica.
GREEN,
R. 1976. Breedingbehaviourof OspreysPanworld(B.-U.MeyburgandR.D. Chancellor,
Eds.).
dion haliaetus in Scotland. Ibis 118:475-490.
World Working Groupon Birdsof Prey, Berlin.
S. 1989. Osprey.Pages297-313inLifeGREENE,
E.P. 1987. Individuals in an Ospreycolony POSTUPALSKY,
time reproductionin birds.AcademicPress,Londiscriminatebetween high and low quality information.
Nature
don.
329:239-241.
GREENE,E. P., AND B. FREEDMAN. 1986. Status of the
Ospreyin Halifax and Lunenburgcounties,Nova
Scotia. Can. Field-Nat.
100:470-473.
HAGAN,J. M., AND J. R. WALTERS.1990. Foraging
behavior, reproductive success,and colonial
nesting in Ospreys.Auk 107:506-521.
HAILMAN,J.P. 1989. The organizationof major vocalizations
in the Paridac.
Wilson
Bull. 101:305-
RATCLIFFE,
D. 1980. The breedingcycle:Pairingand
courtship.Pages185-204 in The PeregrineFalcon.T. & A.D. Poyser,Calton,United Kingdom.
RICHARD,J.-P. 1991. Sound analysis and synthesis
using an amiga micro-computer. Bioacoustics
3:45-60.
ROSENFIELD,
R. N., AND J. BIELEFELDT.1991. Vocali-
JAMIESON,I., N. SEYMOUR,AND R. P. BANCROFT.1982.
zationsof Cooper'sHawk during the pre-incubation stage.Condor93:659-665.
SAYLLER,
E. 1977. Lesparadeset accouplements
des
Time and activity budgetsof Ospreysnesting in
balbuzards p&cheursen Corse. Nos Oiseaux 34:
343.
northeastern
Nova
JOHNSGARD,
P.A.
Scotia. Condor
65-72.
81:439-441.
1965. Handbook of waterfowl be-
havior. Cornell
Univ.
Press, Ithaca.
JOUVENTIN,
P. 1982. Visual and vocal signalsin pen-
guins,their evolutionand adaptativecharacters.
Advancesin Ethology 24. Porey, Berlin.
KEAR,J. 1970. Theadaptiveradiationofparentalcare
in waterfowl. Pages357-391 in Socialbehaviour
in birdsand mammals:Essayson the socialethology of animalsand man (J. H. Crook, Ed.). Academic Press, London.
KROODSMA, D. E., AND E. H. MILLER. 1982. Acoustic
communication in birds. Academic Press, New
York.
McKINNEY,
Anatidae.
SCHLEIDT,W. M., G. YAKALIS, M. DONNELLY, AND J.
McGARRY.1984. A proposalfor a standardethogram,exemplifiedby an ethogramof the Blue
BreastedQuail (Coturnixchinensis).
Z. Tierpsychol.
64:193-220.
SLATER,
P. J. B. 1983. The study of communication.
Pages9-42 in Animal behaviour, vol. 2. (T. R.
Halliday and P. J. B. Slater,Eds.).BlackwellScientific Publications, Oxford.
SMITtI,W.J. 1977. The behavior of communicating.
Harvard Univ. Press,Cambridge,Massachusetts.
STANDEN,
P.J. 1980. The socialdisplayof the Chilean
Teal Anasfiavirostris
fiavirostris.
J. Zool. (Lond.)
F.
1965.
The comfort
Behaviour
25:120-220.
movements
of
MILLER,E.H. 1989. Descriptionof bird behaviorfor
comparativepurposes.Curt. Ornithol. 5:347-394.
MOCK,D.W. 1980. Communicationstrategies
of Great
191:293-313.
STINSON,C. H., J. LAUTHNER,AND T. R. RUSSELL.1988.
Breedingbehavior of Ospreysin northwestern
Washington.Murrelet 69:24-27.
THIBAULT,
J.-C.,ANDF. BOUVET.1983. Les caract&r-
October1993]
Communicative
Behavior
in Breeding
Ospreys
751
Pandionhaliaetusn•s en Corse (M•diterrann•e).
socialcommunicationpatterns in the Pelecaniformes.Ornithol. Monogr. 2.
WARD,P., AND A. ZAHAVI. 1973. The importance of
certainassemblages
of birdsas'informationcenters' for food finding. Ibis 115:517-534.
Oiseau. Rev. Fr. Ornithol.
WATSON,D. 1977. The Hen Harrier. T. & A.D. Poy-
istiquesdu nid du balbuzardsp•cheurs Pandion
haliaetus en Corse. Nos Oiseaux
37:65-73.
THIBAULT,J.-C., AND O. PATRIMONIO. 1989. Note sur
les mouvementsdesjeunesbalbuzardsp•cheurs
59:171-175.
ser, Calton, United Kingdom.
pectsof breeding successof the Osprey Pandion WILSON, R. P., P. G. RYAN, A. JAMES,AND M.-P. T.
haliaetus in Corsica, west Mediterranean.
Bird
WILSON. 1988. Conspicuouscolorationmay enhance prey capture in some piscivores. Anim.
Study 38:98-102.
Behar. 35:1558-1560.
TINBERGEN,
N. 1959. Comparativestudiesof behaviour of gulls (Laridae):A progressreport.Behav- ZAHAVI,A. 1987. The theory of signal selectionand
iour 15:1-70.
someof its implications.Pages305-327 in ProTUBnS,C. R. 1974. The Buzzard. David and Charles,
ceedingsof the International Symposiumof BiLondon.
ological Evolution (V.P. Delfino, Ed.). Adriatica
Editrica, Bari, Italy.
VANTETS,
G. F. 1965. A comparativestudy of some
THIBAULT,J.-C., AND O. PATRIMONIO. 1991. Some as-