TheAuk 112(3):603-612, 1995
VOCALIZATIONS
AND
IN NESTLING
OTHER
STIMULI
BLACK-CAPPED
THAT
ELICIT
GAPING
CHICKADEES
(PARUS ATRICAPILLUS)
JANINE R. CLEMMONS
Departmentof Zoology,Universityof Wisconsin,
Madison,Wisconsin
53706,USA
ABs?Po,
cr.--Parental vocalizationsthat influencethe feedingprocessof nestlingpassetines
havenot beenwell studied.Vocalizationsof Black-capped
Chickadees(Parusatricapillus)
were
analyzed by audio and video recordingswithin the nesting cavity. One vocalization,the
"squawk,"stimulatedgapingin nestlingsduring the feedingprocess.Parentsgavesquawks
most during the first 48 h posthatchingwhen nestlingswere frequently unresponsiveto
vocalizationsand equally or more responsiveto vibratory and other stimuli. Contrary to
reportsaboutother species,spontaneous
gapingdid not occurfrequentlyat any age.Within
the first 48 h posthatching,however, gapesfrequentlyoccurredto "irrelevant" stimuli. As
nestlingsaged,they gapedmorefrequentlyto stimulidirectlyassociated
with feeding,such
as to squawksat three to sevendays of age and to the parents'arrival at older ages.The
parents'vocalizationplaysan importantrole in couplingthe nestlings'gapingresponse
with
the appropriatesituation,especiallyduring the first daysposthatchingwhen nestlingresponsesare coarselytuned to appropriatestimuli. Received
13 January1994,accepted
18 June
1994.
opment of sensoryorganization and reaction to
stimuli directly associated with feeding.
Bengtssonand Ryd•n (1981) investigatedthe
1909, Messmet and Messmer 1956, Collias 1960,
use of the parent's vocalization among other
Bengtssonand Ryd•n 1981,Schuchmann1983, factorsregulating feeding of asynchronously
Khayutin 1985,Welty and Baptista1988).These hatched nestlings. Little is understood, howstudiesalso indicate that nestlingsgape to a ever, about the range of stimuli that elicit gapvariety of stimuli other than the parents' vo- ing in the wild, or how the vocalization is used
calization and that patterns of gaping change in a broader context of adult vocal behavior at
during development.The timing and frequen- the nest site.
Despitethe number of descriptionsand studcy of nestling gaping may have important implicationsfor feeding efficiencyin termsof the ies of vocalizationsof the Black-cappedChickparents' investment of time, as well asthe nest- adee (Ficken et al. 1978, Smith 1991), an adult
lings' rate of feeding and subsequentsurvival vocalizationused to stimulate gaping in nest(Perrins1965,Bengtsson
and Ryd•n 1981).I ex- lings was only briefly mentioned in Clemmons
amine how the parent's vocal behavior is in- and Howitz (1990). The vocalization, named the
volved in coupling the gaping of nestlingswith "squawk,"consistsof usuallya singlenote with
the presentationof food in the Black-capped a broadfrequencyrangeand brief duration(Fig.
la; Clemmons 1993). Experimental analysesof
Chickadee(Parusatricapillus).
Few investigatorshave studied how parents the squawkas a stimulusfor eliciting gaping
influence the feeding processwith vocaliza- and the possiblerole of learning are reported
tions, despite the apparently wide occurrence elsewhere (Clemmons 1993, 1995). Here, I charamong passetinesof a vocalization that elicits acterize: (1) the acoustic environment of the
nestling gaping (Welty and Baptista 1988). nestling with regard to conspecificvocalizaKuhlmann (1909) examined artificial stimuli and tions;(2) the rangeof stimuli to which nestlings
a parental vocalization that elicited gaping in gape;(3) the relationship of the parents'vocalfive speciesof passerines,but the resultswere ization to the nestlings' gaping response;and
not quantified. Khayutin and colleagues(sum- (4) the changesin all thesewith ageof the nestmarized in Khayutin 1985) studied the devel- lings.
AVIANSPECIES
are reported to usea variety of
stimuli including specialvocalizationsto evoke
gaping during feeding of nestlings(Kuhlmann
603
604
J^NINER. CLEMMONS
METHODS
In May and Juneof 1991,nestlinggapingand other
details of the feeding processwere videotapedat the
nestsof seven families (35 nestlings total) at l-.cnic
Point, University Arboretum, and ShorewoodHills
of the Madisonarea,Dane County,Wisconsin.Adults
were individually identifiedby coloredleg bandswith
the exceptionof one pair that was unbanded. Four of
the familieshad excavatedtheir own cavitiesin snags
of rotting wood, and three familiesnestedin wooden
nest boxes.Approximately 55 h of video recordings
of chickadeesat the nest siteswere analyzed.
Video recordings were made with an RCA CC520
Proedit
Video
Camcorder
with
a 15-mm
electret
con-
denser microphone (Sony ECM-150T) placed inside
the nesting cavity or box and connectedto the camcorder. In order to videotape families inside nest boxes,the box was openedat the top and the camcorder
[Auk, Vol. 112
only oncefor this visit. The proportionof responses
for eachstimuluscategorywas determinedfor each
familyat eachage.The plottedmeansof eachstimulus
categoryand table valuesrepresentthe averageresponsesof families.
i recorded620 visits to the nestsby parents;547 of
these were feeding trips. Squawksand feeding attempts were counted during each feeding visit of a
parent to the nest.A feeding attempt was defined as
when a parent placed food in the nestling'smouth
or touchedthe nestling'sbill with food.The number
of visitsto the nestper recordingsessionvaried from
0 to 39.
Mean numbersof visitswith squawks,squawksper
visit, and feedingattemptsper visit were determined
for eachfamily at eachsamplednestlingage. The
successrate at which squawks elicited gaping was
calculatedby dividing the proportionof squawksassociatedwith gapingby the numberof squawksgiven
attached to the tree. With families in natural cavities,
during that visit to the nest. Means were calculated
holes were cut through the snagsabove nest level
and the camcorderwas supportedby a tripod. A pen
light was used to increaseillumination when necessary. The camcorderwas turned on, and then the
observerwalked about 10 m away from the cavityand
observedthe activities of the parentsfrom a distance.
When the camcorderwas not in use, a piece of bark
for eachfamily at eachnestlingage.In thisanalysis,
there were 25 visits to the nest in which squawks
occurred,and both parents were inside the cavity
while the femalewasbrooding.Thesevisitswere not
was wired
over the hole.
included in the analysisbecausethe female was sit-
ting on the young;asa result,whetherthe nestlings
gaped in responseto the squawk could not be determined.
Statisticalanalysesvaried accordingto the type of
Observationsof behavior inside the nesting cavity
were madein conjunctionwith playbackexperiments data and questionsbeing addressed.I employedperthat testedthe nestlings'responses
to variousacoustic mutation testsusing P-statwritten by Bill Engels(Destimuli (Clemmons1993, 1995). Recordingsof feed- partment of Genetics,University of Wisconsin-Madings were madebefore and betweenthree playback ison),Spearmanrank correlations,Friedmantwo-way
analysisof variance(Systat1992),multiple-compariexperimentsspacedat least 15 min apart on day 0
(day of hatching), 2, 4, 6, and 12 (or within 24 h of son tests (Daniel 1990), and a variance test for homogeneityof the binomial distribution(Snedecorand
these ages).Observationsand experimentswere reCochran
1967).
peated on the same day after at least 2 h following
the first session,exceptin casesof inclement weather
or equipment failure. One family was lost to predaRESULTS
tion before day 6. Observationsin one family of four
nestlingswasinitiated on day 2 and in anotherfamily
The motorresponse
of gaping.--Gaping is the
of seven nestlingson day 6.
wide opening of the bill with the headand neck
The microphoneinside the nestingcavity recorded
soundsoriginating from both inside and outside of extendedupwards in a postureto receivefood.
the cavity,allowing comparisonof adult vocalizations More specifically,gapingtypicallyinvolvedthe
in these
two
contexts
and determination
of events
that were associatedwith nestling gaping. An event
was recordedas being associatedwith gaping if the
event preceded gaping within 1 s. Caseswhere two
or moreeventsoccurredwithin 1 s precedingthe gape
were classifiedas "ambiguous"events;caseshaving
unidentified or no apparent events associatedwith
gapeswere classifiedas "unknown."
The eventsassociatedwith gaping were tallied for
each recording sessionaccordingto frequenciesof
occurrence.Each event was counted only once per
visit to the nestby a parent.For example,if a parent
producedsquawksthat were followed by gaping 10
times during a single visit, the squawk was counted
followingmovementsandpostures:
(1) The head
was lifted and the neck extendedupward, usually with a sudden movement.Lifting of the
headoccurredin about57 ms(range7-133 ms),
asmeasuredby freeze-framecountsfrom video
recordingsof 28 gapingobservationsfrom three
familiesof nestlingsat day 0. (2) The headwas
held up, usuallyfree from contactwith surfaces.
(3) The mouth wasopenedwidely with the outer membranesforming a nearly completecircle
or slight oval. (4) During the upward thrust of
the head,the bodywaskept in balanceby bracing the forelimbson a substrate(e.g.bottomof
July1995]
Vocalizations
andNestling
Gaping
605
TABLE1. Mean proportion (+SE) of gapesfollowing four categoriesof events(vocalization,parent'sarrival,
unknown, and other). Proportion of gapesto each categoryfirst determined by family, and then mean
proportions calculatedacrossfamilies. Friedman analysesof differencesamong categoriesby age and
pairwise comparisonsreported at bottom. Family differencesindicated by asterisks(variancetest for homogeneity of binomial test): *, P < 0.05; **, P < 0.01.
Agea (days)
0
Vocalization
Parent arrives
Other
Unknown
Total no. gapes
0.207
0.069
0.602
0.122
+
+
+
+
2
0.084**
0.034*
0.074*
0.089**
0.678
0.103
0.194
0.025
138
Friedman test (P)
+
+
+
+
0.137'*
0.049**
0.097**
0.025**
152
0.030
Multiple comparisons
b
4
0.561
0.208
0.193
0.038
+
+
+
+
b
0.083**
0.055**
0.063*
0.020
0.518
0.342
0.119
0.021
159
0.051
a
6
+
+
+
+
12
0.061
0.051
0.037
0.021'
136
0.003
0.002
b, c, d
b, c, e
0.243 + 0.039
0.679 + 0.031
0.109 + 0.043
0
178
0.001
b
ßAt age0, n; 5 families;at all otherages,n = 6.
bLetters refer to; (a) other x unknown; (b) vocalization x unknown; (c) arrival x unknown; (d) vocalization x other; (e) arrival x other.
nest, sidesof nest, cavity wall, or on siblings).
(5) The gape was held for severalseconds(œ=
7.52 s, n = 28, range 2.3-22.0 s). At the end of
the gape, the mouth was closedslowly while
and near the nesting cavity; (2) parent'sarrival
at the nest or cavity entrance; (3) unknown
events; and (4) other events ("other") of which
most were tactile or vibratory (Tables1 and 2).
the head was lowered and the neck withdrawn.
Often an event was followed by more than one
Although the above description was the typ- nestling gaping. Becauseonly the first nestling
ical pattern of gaping, sometimesone or more to gapewas considered,thesecategoriesdo not
of the above components were not involved. take into accountthe possibilitythat the actions
For example, the head and neck already may or vocalizationsassociatedwith gaping of the
have been extended when a nestling gaped first nestlingmay have servedasa stimulusfor
(usually from previous stimulation), or the gaping of other nestlings.
On day 0 the mostcommoneventspreceding
mouth may have been openedto a lesserdegree
and for shorter periods of time. Sometimes a gaping were representedby parental vocalizanestling displayedall of the abovecomponents tions, as well as various vibratory and tactile
except opening of the mouth. An action was stimuli associated with movement of the nest
consideredto be a gape only if the mouth was or of birds within the nest ("other" category;
Table 2). Multiple comparisons(c•= 0.15) with
open for more than 1 s.
Eventsprecedinggaping.--Four general cate- the Friedman test indicated no significant difgoriesof eventsimmediately precededthe gap- ferencesbetween the frequency of gapes foling of nestlings:(1) parental vocalizationsin lowing the "vocalization" and "other" catego-
TABLE2. Detailed information on "other" category(Table 1) showing gapesthat followed eventsother than
vocalizations,unknown events,or parent landing at the nest or cavity entrance.Valuesare œ+ SD by
family (range in parentheses).
Age' (days)
Stimulus
Parent leaves nest
0
2
4
6
3 + 4 (0-11)
2 + 2 (0-6)
1 + 1 (0-4)
1 + 1 (0-3)
12
0.8 + 1 (0-2)
Parent or sibling
movement in nest
5 + 3 (1-9)
Outdoor soundsb
0.4 + 0.5 (0-1)
Movement of nest
5 + 4 (1-10)
Ambiguous
Total no. gapes
3 + 2 (1-6)
84
ßAt age0, n = 5 families;at all otherages,n = 6.
b Noise from truck, human voice, etc.
0.7
0.8
0.8
0.3
+
+
+
+
1 (0-3)
1 (0-3)
1 (0-3)
0.8 (0-2)
27
1 + 2 (0-5)
0.8 + 1 (0-3)
0.2 + 0.4 (0-1)
0.5 + 0.8 (0-2)
26
0.5 +
0.7 +
0.2 +
0.7 +
0.8 (0-2)
0.8 (0-2)
0.4 (0-1)
1 (0-3)
17
0
0.3 + 0.5 (0-1)
0.2 + 0.4 (0-1)
0.7 + 1 (0-3)
12
606
JANINE
R. CLEMMONS
ries (P > 0.05), but in four of the five families,
the "other" category ranked higher. The frequency of gapes following events from the
"other" categorywassignificantlydifferent from
gapesfollowing unknown events(P < 0.05)and
approachedsignificancefrom gapes following
the parent's arrival.
As the nestlings aged, dramatic changesoccurred in the relative frequencies of the four
categoriesof events that preceded gaping, except for the unknown category,which was low
for all ages. The frequency of gapes that followed events from the "other" category decreasedsuddenly after day 0, whereas the frequency of gapes that followed vocalizations
peaked at day 2 (Table 1). After day 2, the frequency of gapes following vocalizations decreasedsteadilywhile an increasingproportion
of gapesfollowed the parent's arrival. The parent's arrival was the most common event preceding gaping by day 12.
Contexts
of adultvocalizations
insideandnearthe
nesting cavity.--Despite numerous studies on
Black-cappedChickadee vocalizations (Ficken
et al. 1978, Smith 1991), there is very little published
on adult
vocalizations
of birds
around
the nest. I recorded six types of vocalizations
produced inside the nesting cavity (Table 3). A
seventh type, the "hiss," which is typically given to predators near (Clemmons and Lambrechts 1992) or inside the cavity (Odum 1942,
Sibley 1955, Ficken et al. 1978), also occurred
sometimeswhile I was setting up the camera
and before the recording started.
The squawk (Fig. la) was the most frequent
adult vocalization inside the cavity at mostages,
approaching statistically significant levels on
days0 to 2 and significantly higher than other
vocalizations at all other ages (Fig. 2). Other
vocalizations inside the cavity included "twitters," "broken dees,"notesof the "A-complex,"
"faint feebees,"and "composite" vocalizations
(described below). The twitter (Fig. lb) commonly occurredwhen the male approachedthe
brooding femaleand while he gaveher the food,
a contextual use not previously described for
this vocalization. Broken dees (Fig. lc), analogous to "courtship begging" vocalizationsin
other species,alsowere associatedwith the male
feeding the femaleand sometimeswere elicited
from the brooding female by the male's nestapproachvocalizations.Faint feebees(soft renditionsof the territorial song;Fig. lh) and A-like
notes (A-complex;Fig. 1d-f) have been associ-
[Auk, Vol. 112
ated with approach to the nest hole (Smith 1972,
Ficken et al. 1978), but I sometimes recorded
them inside the cavity. The "chatter" (Fig. lf)
consistsof a series of short duration, rapidly
repeatedA-like notes that may or may not be
preceded with a longer-duration, higher-frequency note, suchas pictured in the figure, and
is sometimesfollowed by one or more faint feebee notes.
The
name
"chatter"
was borrowed
from a similar appearing sonagram recorded
from captivechickadeespublished in Dixon and
Stefanski(1970).One type of note in the A-complex, the "peek" note, is previously undescribed; it differs from other A-like notes by
having a broad frequency range and strong emphasis in the initial upward frequency sweep
(compareFig. lg with Fig. 1d-f). The contextual
useof this note was not clear; it was given when
the caller appeared to be hesitating or indecisive. Compositevocalizationsconsistedof combinations
of notes from
the traditional
vocal-
ization types describedin Ficken et al. (1978)
and occurred in a variety of contexts (Clemmons 1993). Although the variable see (Ficken
et al. 1978) did not occur inside the nesting
cavity in this study, I have previously observed
the vocalization
in the same context
or in com-
bination with the twitter (unpubl. data).
There were nine vocalization types recorded
outside but near the nesting cavity (Table 3),
including the six types recorded inside the cavity plus three others--the chick-a-deecall (Fig.
li) given in situations of potential danger, the
variable see given during various intrapair interactions,and the gargle, which precededcopulation and occurred in agonistic encounters
with nonmates (Ficken et al. 1978, Ficken and
Weise 1984, Ficken et al. 1987). There were no
adequaterecordingsof the variable seeand gargle.
In contrastto the context within the nesting
cavity,squawkswere significantlylessfrequent
outside of the cavity than other vocalizations
combined at each age sampled (Fig. 2). There
was no single dominant type of vocalization,
but the faint feebee was the most common, con-
stituting 43.0% of the vocalizationsgiven on
day 0 and 38.4%on day 12 (Table 3). Faint feebees were significantly more frequent than
squawksoutside of the nest at all ages except
day 0 (multiple comparisonswith Friedman test,
P > 0.05, n = 6). Faint feebeesusually were
more frequent than other vocalizations except
for chick-a-deecallsand the A-complex.
July1995]
Vocalizations
andNestling
Gaping
607
II
608
10-
JAIqlNE
R. CLEMMONS
a)Squawk
b)Twitter
ß SquawksInside [] SquawksOutside
c)Broken
Dee
d)A-note
e)A-coupletf)Chatter
•)•
[Auk,Vol. 112
0.6,
0-•' ''•"
8
............
h)Faint
Feebee
j
0.2
--
o.o,
i)Chick-a-dee
0
2
4
6
12
Age (days)
that were
Proportion of vocalizations
squawksoccurring inside (solid) and outside nesting
cavity (hatched).Whiskersindicate SE. Asterisksindicatesignificancelevels testingwhether there were
differences in frequencies of occurrencebetween
• • •[•.•••,Fig.
2.
i.......i..... i-•--T
0
sec
-
.8
squawks
andothervocalizations
withineachcontext
(Wilcoxon matched-pairs signed-ranks test: *, P <
Fig.1. Sonagrams
of parents'
vocalizations
occur- 0.10;**, P < 0.05).Samplesizefourfamilies(inside)
ringinsideandnearnestingcavity.Gargles
andvari- and five (outside)for age0, and six for otherages.
able seesnot shown.
Comparing the two contextsinside and outside the nesting cavity, there were significant
family differencesin frequenciesof occurrence
for most vocalization types with large sample
sizes(> 15), exceptfor squawkson day 6 inside
the cavity (P < 0.05, variance test for homogeneity of the binomial distribution). Differencesin the proportionalfrequenciesof squawks
occurring inside the nesting cavity compared
with outside approachedsignificanceat day 0
and were significant at all other ages (day 0, P
= 0.068; all other ages, P < 0.05, Wilcoxon
matched-pairssigned-rankstest) and for faint
feebeesat each sampledage except day 0 (day
0, P = 0.068; all other ages,P < 0.05). The frequenciesof occurrences
of twitters,A-complexes,broken dees,or compositevocalizationsdid
not differsignificantlybetweenthe "inside"and
"outside" contextsat any age (P > 0.075).
Association
of squawks
with nestlinggapingand
feeding.--Thesquawkwasthemostcommonvocalizationassociatedwith nestling gaping. The
differencebetween the proportion of gapesfollowing squawkscompared with other vocalizations approachedsignificanceat day 0 and
Total number of eachvocalizationtype for eachcontext provided in Table 3.
wassignificant(P < 0.05) at all other ages(Fig.
3). In three families, gapes followed only
squawks.The Spearmancorrelation coefficient
betweenthe total frequencyof squawksand the
frequencyof squawksthat precededgapingwas
positivein two of the other familiesand negative in two. Although nestlingsgapedmostly
at squawksand squawkswere the most frequentlyoccurringvocalizationin the cavity(Fig.
2), there was no clear associationbetween the
proportionof gapesto squawksand the frequencyof occurrenceof squawks.
Productionof squawkswas greatestat day 0
(Fig. 4). As nestlingsaged,the parentsproduced
fewer squawksper visit (rs= -1.0, n = 5, P =
0.05; two-tailed Spearmanrank correlationtest
of means at each age). By day 4, squawksoccurredin 68.0%of the visitsat the rate of only
one or two per visit; by day 12, they occurred
in 20.0%of the visits, but usually only once.
If the parentsusethe squawkto activatenestling gapingduring feeding,parentsshouldcarry food when they squawk,and they should
squawk if no nestlingsare gaping. A family
July1995]
Vocalizations
andNestling
Gaping
ß
Squawk
[] Other
Vocalizations 10
.337/93
Squawks
100/2
o.81
609
Feeding
Attempts
94/3
69/1
0.6
'•.__
_t3•83
49/210
4O/4
Age(days)
0.0.
0
2
4
Age (days)
6
12
Fig. 4. Family mean rates + SE of squawksand
feeding attemptsby parentswith age of nestlings.
Feedingattemptdefinedas touchingnestling'sbill
with foodor placingfoodin nestling'smouth.Sample
size four families for age 0 and six for other ages.
Total number of squawks (above) and feeding attempts(below) given abovedatapoints.
Fig. 3. Proportionof nestlinggapesthat followed
squawks compared with other adult vocalizations
(Wilcoxon matched-pairssigned-rankstest: *, P <
0.10; **, P < 0.05). Whiskersindicate SE.Samplesize the parent was positionedso that it could not
four families for age 0 and six for other ages.Total see the gaper; or (4) a parent could not reach
numberof gapesfollowing squawks(above)and oth- the gaper. In at least one casethe squawk reer vocalizations(below) given abovebars.
suited in already gaping nestlings extending
their headshigher sothat the parentcouldreach.
Most squawkswere given upon entry into
averageof 84.8 _+SD of 16.8%of the squawks the nestingcavity or as a parent landed at the
were given inside the nesting cavity (P < 0.01, entrance. Sometimesthe male perched at the
n = 7 families; two-tailed permutation test). entranceand passedfood to the brooding feCallers carried food in an average of 93.2 + male who then sometimes emitted one or more
10.8% of the cases where it could be observed
squawkseither beforeor after the male flew off.
whether or not a caller carried food (P < 0.002, Older nestlingstypically vocalizedand gaped
n = 7 families;two-tailedpermutationtest).That vigorously as soon as a parent landed at the
the caller sometimeshas an empty bill suggests cavity entrance.This obviatedthe need for adan alternative use or uses of the vocalization, a
ditional stimuli and may explain why squawks
possibility analyzed in another study (Clem- were less common after the first week postmons1993).Although adultspossiblycouldcar- hatching (Table 1). With older nestlings,
ry hidden food for themselves,whether or not squawkssometimeswere given during the first
they carry food for the young is reliably ob- visits after the camcorder had been set up.
served.Parentswith "apparently"empty bills, Hence, the nestlings may have been in a defor example,never fed nestlingsduring any of fenseposturewhen the parentfirst arrived and
the observations.
the parentusedthe signalto releasethem from
Usually, a parent with food squawkedinside this posture.
the nesting cavity if there were no nestlings
Squawks,gaping, and feeding efficiency.--If
gaping (P < 0.001, n = 7 families; two-tailed squawksare usedto sustainthe feeding process
permutation test). Of 1,150 squawkswhere all until successfulfeeding has occurred,the rate
of the nestlings'responseswere visible in the of squawksshould decreaseas fewer feeding
video recording, only 5.9% were given when attemptsare required.This prediction was supone or more nestlingswere alreadygaping. In ported by observations(Fig. 4; rs= 0.90, n = 5,
these cases:(1) the parent was unsuccessfulat P = 0.05;one-tailed Spearmanrank correlation
feeding the gaper and then squawked appar- test of meansat each age). Note that in Figure
ently to stimulate a different nestling to gape; 4 on day 0, the numberof feedingattemptswas
(2) the gape was closingor not fully open; (3) low relative to the number of squawks.Fre-
610
JANINER. CL•MO•S
[Auk, Vol. 112
quently,
atthisage,a parent
brought
foodto
thenestandsquawked
numerous
times,
butthe ._.9.1.0.
nestlingswere slowto gapeor noneof the nest-
184
139
4
6
49
lingsgaped;
therefore,
the parentcouldnot
makeafeeding
attempt
(asdefined
in thisstudy).
Inthese
cases
theparent
either
atethefood
or
leftthenestwhilestillcarrying
food.At this • • 0.6.
ageofthenestlings,
therateofsquawks
(which o"•.
reflects
the parent'sattemptto stimulate
gap- • O 0.4
ing)wasa betterindicatorof theparents'
active ._
rolein regulatingfeedingthanrateof feeding cr
alone,assometimes
usedin otherstudies.
p
0.2
As the nestlings aged, they not only were
morelikelyto swallowthefoodpresented,
but
also became more responsiveto the squawk,
although this differenceonly approachedsig-
0.0
0
2
8
10 1•)
Age (days)
nificance
(Fig.
5;r5= 0.90,
n= 5,P= 0.10;
two- Fig.
5. Mean +
tailed Spearmanrank correlationtest of means
at each age). The successrate of squawks in
eliciting gapes was relatively low at day 0
SE of proportion of squawksfor
eachfamily that stimulatedgaping in nestlings.Sample size four families for age 0 and six for other ages.
Total number of gapesprovided abovedata points.
(<50%) and then increasedto nearly 90% by
day 4.
There are at least two characteristics
of feed-
ing interactionsthat are sharedwidely among
passerines,including: (1) the use of an adult
Many speciesof passerinesreportedly have vocalizationto stimulatenestling gaping; and
a "special"vocalizationused to stimulate nest- (2) the replacementof a vocal stimulus with
lings to gapeduring feeding. Of the many kinds other kinds of stimuli associated
with the parof vocalizationsproducedby chickadeesnear ent's arrival around the time that the nestlings'
and inside the nesting cavity, only the squawk eyesopen (Kuhlmann 1909,Bengtsson
and Rywas regularly associatedwith the gaping of d•n 1981,Khayutin1985,presentstudy).Other
nestlings.This association
wasbasedin part on commoncharacteristics
are that: (1) the feeding
the frequencyof contextualuse and in part on procedureis slow during the first few dayspostthe frequencyof nestling response.It doesnot hatching,requiringseveralfeedingattemptsby
imply that the only function of the squawk is the parentsbefore the food is successfullydeto elicit nestlinggapingnor that nestlingshave livered; (2) the number of vocalizationsgiven
a specificresponseto the squawk.The squawk by the parents is greatestduring the first few
occurred,though less frequently, in intrapair days posthatching;and (3) the parent is most
interactions
and in situations when the nestlikely to give the vocalizationwhen there are
lings were not present,suggestinga complex no nestlingsgaping(Bengtsson
andRyd•n 1981,
role of the squawkin a variety of intrafamilial presentstudy).
DISCUSSION
interactions (Clemmons 1993). Although the
proportion of gapes following squawks compared with other vocalizationswas not correlated with the frequencyof suchvocalizations,
other reasonscould explain the apparentselec-
One difference
from other studies is that tac-
tile and vibratory stimuli accountedfor a large
proportion of gapes in Black-cappedChickadees at day 0, whereas other specieswere reported to be less responsiveto tactile stimuli
tive responseto the squawk,suchas the prox- until a later age.In Kuhlmann'sstudy(1909)of
imity and orientationof the caller to nestlings, the feeding responsein nestlingsof five pasor the amplitude of the vocalization.Whereas serine species,including the American Robin
one of the obvious functions of the squawk is (Turdusmigratorius),
Chipping Sparrow (Spizella
to elicit nestling gaping, the variable usesand passerina),Rose-breastedGrosbeak (Pheucticus
responsesto the signal require further study ludovicianus),
Red-winged Blackbird (Agelaius
(Clemmons 1993).
phoeniceus
), and BrownThrasher(Toxostoma
ruf-
July1995]
Vocalizations
andNestling
Gaping
um), the parent's vocalization was the most ef-
fectivestimulusduring the first day posthatching and then was replacedby visual and tactile
cuesassociated
with feedingin older nestlings.
Similar findings have been reported with the
Pied Flycatcher (Ficedulahypoleuca),Great Tit
(Parusmajor)and Redstart(Phoenicurus
phoenicurus;Khayutin 1985).
Another apparentdifference from other stud-
iesis the diminishedrole that spontaneous
gaping, or gapingin the absenceof externalstimuli,
playswith hatchlingBlack-cappedChickadees.
For asynchronouslyhatching speciessuch as
the Pied Flycatcher, Great Tit, and European
Blackbird (Turdus merula) (chickadees are also
asynchronous),
it hasbeensuggestedthat spontaneous gaping increasesthe chance that a
youngernestlingwill be fed when the gaping
coincideswith a feeding (Bengtsson
and Ryd•n
1981,Khayutin et al. 1988).Bengtssonand Ryd•n (1981), for example,reported a 40% incidence of spontaneousgaping in the Great Tit
when nestlingswere one to two days of age,
and Khayutin et al. (1988) noted that spontaneousgapingin newly hatchedPied Flycatcher
nestlingsoccurred80%of the time that parents
were away. With chickadees,by contrast,only
13% of gapesoccurred without an observable
611
stimulategaping in the natural setting,or even
what constitutedthe definition of spontaneous
gaping.
Although spontaneousgapingwas not characteristicof newly hatchedBlack-cappedChickadees, at least 40% of all stimuli
that elicited
gaping at day 0 were "irrelevant" or lesspredictive of a feeding.The squawk,therefore,appearsto play a critical role in coupling gaping
with the presentationof food during a period
when nestlingstend to gape inappropriately.
Other studies suggestor demonstratethat
parentsadjusttheir feeding ratesaccordingto
information they receivefrom nestlingsabout
nutritional status (Kluyver 1961, Henderson
1975, O'Connor 1975, Bengtssonand Ryd•n
1983).In my study,parentsmadegreatattempts
to arouse nestlings during the first few days
posthatchingasdemonstratedby the long bouts
of squawksused when nestlingswere unresponsive.Although I did not considerthe de-
greeto which nestlingsregulatedfeedingrate,
the frequency of squawks increased when
hatchlingresponse
decreased
(compareFigs.4
and 5), a resultoppositeto that expectedif nestling responsiveness
regulatedparentalfeeding
rate alone. At leastduring the first few days
posthatchingwhen nestlingswere relatively
stimulus, and this value is inflated because the
inactive,the parent'sfrequent use of squawks
squawk as a stimulus was counted only once and persistentfeedingattemptsappearedto be
per visit. Also, it is possiblethat I did not detect major factorsdriving the feeding interaction.
the external stimulus in some cases.
As Figure4 shows,the number of feeding atSeveral
reasons could
account
for the differ-
ing explanationsamongstudiesaboutthe role
of spontaneous
gaping. Khayutin et al. (1988)
suggestedthat younger nestling Pied Flycatchers gapedspontaneouslybecauseof increased
hungerlevels.If so,ratesof spontaneous
gaping
will depend on food availability in the habitat
or on asymmetryin foodacquisitionamongsiblings (and perhaps,on degreeof hatchingasynchrony).Differencesamongspeciesin their tolerance for human disturbanceduring observation alsomay play a role, thus affectingthe
rate of parental feeding and subsequentlevel
of hunger in the nestlings.For example,Kluyver (1961), who studied both Black-capped
Chickadeesand Great Tits, had the impression
that Black-cappedChickadees were more tolerant
of human
disturbance
at the
nest than
their congenersin Europe.Finally, it is not clear
from
these
other
studies
whether
there
were
specific attempts to document all factors that
tempts when measuredby bill touchesor, in
otherstudies,therateof visitsto thenest(Kluyver 1961, Royama1966) at day 0 doesnot accuratelyreflectthe activerole of the parentsin
regulatingnestling feeding rates.
ACKNOWLEDGMENTS
I am grateful to: JackP. Hailman, JeffreyR. Baylis,
Theodore Garland, Jr., Keith R. Kluender, and Charles
T. Snowdonfor guidanceduring the studyand helpful commentson the manuscript;J. R. Baylisand C.
T. Snowdon for loan of equipment; John E. Dallman,
Kenneth G. Olesen, and Richard J. Ganje for building
nest boxes; Marcel M. Lambrechts for discussions and
comradeship in the field; and Hank, Caroline, and
Henry Clemmonsfor assistancein the field and many
other kinds of invaluablesupport.The studywasaided by grantsfrom JohnJeffersonDavis Funds,a Henry Nathan Netzer and Bernard Netzer Brouchoud
Scholarship,and a Vilas Graduate Fellowship.
612
JANINE
R. CLEMMONS
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