HORMONAL
CORRELATES
BEHAVIOR
OF PARENTAL
IN COOPERATIVELY
AND
HELPING
BREEDING
HARRIS' HAWKS (PARABUTEO UNICINCTUS)
CAROL MASTERSVLECK,• NORA A. MAYS,t JAMESW. DAWSON,2
AND ARTHUR g. GOLDSMITH 3
•Departmentof EcologyandEvolutionary
Biology,Universityof Arizona,Tucson,
Arizona85721 USA,
2School
of Renewable
Natural Resources,
Universityof Arizona,Tucson,
Arizona85721 USA, and
3Agricultural
andFoodResearch
Council,Research
Groupon Photoperiodism
andReproduction,
Department
of Zoology,
University
of Bristol,BristolBS8lUG, UnitedKingdom
ABSTRACT.--We
measuredplasmalevelsof progesteroneand prolactinin free-living adult
breeders,adult-plumagedhelpers,and juvenal-plumagedhelpersof the cooperativelybreeding Harris' Hawk, Parabuteo
unicinctus,
at different stagesof the nestingcycle.Overall, progesteronelevels did not vary significantlywith sex,neststage,or behavioralrole, but they
increasedsignificantlywith handling time. Progesterone
levelswere highest(2-4 ng/ml) in
breedingfemalesjust beforeegg laying. Prolactinlevelsdid not vary with handlingtime
but were significantlyelevatedin breedingfemalesduring the nest-buildingstage(14.1ng/
ml) and in both breedingmales(8.4 ng/ml) and females(25.5 ng/ml) during incubation.
Bothsexesof breedersincubatethe eggs,but the femalesdo the bulk of incubationand only
they developa broodpatch.Prolactinlevelsin the breedersdeclinedimmediatelyafter the
eggshatched,in contrastto the patternseenin many other altricial species.Prolactinlevels
in the adult-plumagedmale helpersrosesignificantlyafter the eggshatched(9.1 ng/ml). At
this time thesebirdsbring morefooditemsfrom groupkills to the nestlingsthan any other
group members.The elevatedprolactinlevels in the adult-plumagedhelpersmay facilitate
the helpingbehaviorthat they exhibittowardthe nestlingsand fledglings.Received
8 August
1991, acceptedI April 1991.
HELPINGbehavior conventionally refers to
parentlikebehaviordirectedtowardyoungthat
are not the offspringof the bird displayingthe
behavior.
It has been
one of the main
foci of
studies on cooperativelybreeding speciesbecausehelping behavior seemsto entail costs,
often without clear-cutbenefits(seereviewsby
Woolfenden and Fitzpatrick 1984, Brown 1987,
Koenig and Mumme 1987). Investigatorshave
soughtto explainnot only the presentselective
advantagesof helping behavior, but also the
ological level to augment the behavior. This
would supportthe hypothesisthat helping behavior is adaptive.
The socialsystemin the Harris' Hawk is com-
plex and hasbeen describedin detail for populationsin Arizona (Dawsonand Mannan 1991a)
and New Mexico (Bednarz 1987). In Arizona,
evolutionaryoriginsof helper systems,and it
groupsizerangesfrom a breedingpair to 7 birds
(meangroupsize= 3.8).The breedingmaleand
female (or alphabirds)build the nest,the female
lays the eggs,both male and female incubate,
shadeor brood the nestlings,and feed the nest-
remains controversialwhether helping behavior is selectedfor, or is simply a result of mis-
cubateapproximatelyone-fourthasmuch asfe-
directed parental behavior (cf. Jamieson and
Craig 1987, Jamieson 1989, Ligon and Stacy
1989). The proximate mechanismsthat control
such parentlike behaviors,however, have not
been investigated in any cooperativelybreed-
lings and fledglings.Breedingmalesonly inmales (Dawson and Mannan 1991a), and the
maledoesnot developa broodpatch(pets.obs.).
The alpha female rarely leavesthe nest area
during the nestingseasonand is providedfood
fromgroupkillsby her mateandthe otherbirds
ing species.We investigatedthe hormonalcor- in the group.
relatesof parentalbehaviorin the cooperatively
We call all other birds in the group helpers
breeding Harris' Hawk (Parabuteounicinctus). even though the extent to which individual
Evidencefor an endocrinesystemthat promotes hawks help differs (see Dawson and Mannan
helping behavior in nonbreedingbirds would 1991a for details) and some of them breed
suggestthat selectionhas operatedat a physi- ($heehyet al. MS).In particular,few groups(0638
The Auk 108:638-648. July 1991
July1991]
Prolactin
ina Cooperative
Breeder
639
11%,depending on the year studied) contain and, in particular, we comparehormone levels
another breeding female (termed an alpha-2fe- of breederswith thoseof helpers. We choseto
male;Dawsonand Mannan 1991a),but this type examine the levels of these two hormones bewas absentfrom the groupswe studied. Two causethey (often in synergywith estrogenand
classesof helpers have been described,distin-
testosterone) are the hormones most often as-
guished by behavior (Dawson and Mannan
1991a):betamalesand gammabirds,who may be
sociatedwith parentalcare(incubationand care
of young)in birds(reviewedin Balthazart1983,
either males or females. Beta males are the most
Goldsmith 1983,Silver and Cooper 1983,Brown
common,are found in approx. 62% of groups,
and are alwaysin adult plumage.Gammabirds
are usuallyin juvenalplumage(1 yr old or less)
and may be either male (66%)or female (34%).
They are in adult plumage(> 1 yr old) approx.
32% of the time. Gamma birds are usually, but
not always, offspring of the breeders in the
group,whereasbetamalesare not relatedto the
breeders. We did not divide our helpers into
beta and gamma types becausewe did not always have enough information, but classified
them as either in adult plumage or in juvenal
1985, Buntin 1985).
Helpers rarely comeinto direct contactwith
the eggsor young (Dawsonand Mannan 1991a).
Betamalesare allowed to bring food to within
50 m of the nest before transferring it to one of
the alpha birds, who delivers it to the incubating female or the nestlings.Gammabirds bring
food to the nest areabut transfer it to the alpha
birdsat least150m from the nest.Occasionally
the beta males will incubate or bring food directly to the nest, and gamma birds will also
occasionallyattempt to incubate and feed the
young directly, but they are usuallysupplanted
from the nestby the breeding pair. All birds in
the group detect and harasspredators,defend
the nesting territory from both predatorsand
conspecifics(Dawson and Mannan 1991b),and
take part in group hunting. Participationin cooperativehunting efforts(Mader 1975,Bednarz
1988, Bednarzand Ligon 1988) and delivering
prey items to the nest area are probably the
largest contributions that helpers make to the
breeding effort.
In the accompanyingpaper(Mays et al. 1991),
were
METHOD•
Fieldmethods.--Thestudyareas,animals,blood collection, field measurements, and observations were
describedin detailelsewhere(Mayset al. 1991).Briefly, we usedbal-chatritraps(Bergerand Mueller 1959)
to capture 157 hawks north of Tucson,Arizona, in
uplandSonoranDeserthabitatbetweenMay 1985and
August 1987. Most hawks were trapped during their
nestingseason(Februaryto July). Bloodsamplesfor
hormonalanalyseswere takenfrom a wing vein, and
plumage. Approximately80% of adult-plum- eachbird wasbandedwith a unique color-bandcomaged males were probably beta birds, and all binationand weighedbeforerelease.Approx.80%of
adult-plumagedfemale helpersand all juvenal- bloodsampleswere collectedbetween0530and 1300,
plumagedbirdswere probablygammabirds(see but becauseof the difficulty in trapping birds, we did
some trapping in the afternoon and three samples
details in Mays et al. 1991).
we described how testosterone, estradiol-17•,
collected
after
1800.
Most birds during the breeding seasonwere examined for evidence of a brood patch, which was
scoredas 0 = absent:breastcompletely feathered; 1
= developing:breastbeginningto losefeathers;2 =
present: breast fully defeathered, but not vascularized;3 = functional:breastfully defeatheredand vas-
cularized;or 4 = regressing:
breastdefeathered,but
no longervascularizedand beginningto sproutnew
feathers.In 1985we noticed reddening and swelling
of the outercloacaof somefemalesduring the breeding seasonvery similar to that describedin Alpine
Accentor (Prunella collaris) females (Nakamura 1990:
fig. 2c).In 1986and 1987we recordedthe appearance
of the cloacalopeningof all hawksas either dry and
small, or red and swollen.
Blood sampleswere stored on ice in the field and
centrifugedlater the sameday.The plasmawasstored
at -20øC until analyzed by radioimmunoassay.We
recordedthe maximum possibletime the hawk was
ensnaredon the trap and the time taken to obtain the
bloodsample,and their sumis the maximumpossible
handling time for that bird. The mean maximumhandling time was 70 min (+61 min SD). Maximum possiblehandlingtimeswerehighbecause
we wereforced
to remain away from the traps for long periodsof
time to increasethe probabilityof capturinga bird.
and luteinizing hormone (LH) levels are corWe identified hawks as either male or female, based
relatedwith breeder/helperstatusand neststage on body mass,and as either in juvenal or adult plumin both
males
and females.
Here
we describe
the correlationbetween progesteroneand prolactinand parentalbehaviorin individual birds
age.Femalesare approx.30%larger,and there is essentially no overlap between the sexes(Hamerstrom
and Hamerstrom1978).Birdsretainthe juvenalplum-
640
VrECK•r AL.
age until after the next year's breeding season.We
identified the behavioralrole (helper or breeder)and
stage of the nesting cycle for 105 of the hawks for
which we had bloodsamplesby observingthe hawks
from enclosedblinds near the nests(details in Mays
et al. 1991).The neststagewas calculatedrelative to
the date of the first-laid egg. Samplescollected>50
daysbeforethe first-laidegg were consideredto be
from the nonbreedingstageof the annual cycles(approx. August through early January),thosecollected
during the 50 daysbeforethe first egg were from the
nest-building and gamete-productionstage, those
collectedduring the next 35 days were from the incubationstage(Mader 1975),and thosecollectedfrom
36 to 100 days after the first-laid egg were from the
stagewhen young were being fed. The chicksremain
in or near the nest for approx.45 daysafter hatching
(Mader 1975),and group memberscontinuedto feed
the young after fledging for several months (pets.
obs.).The meandateof the first-laideggwas30 March
(+17 days SD), and the range was from 21 February
through 5 May.
Radioimmunoassay
of hormones.--Plasma
samplesfor
progesteroneanalysis(150-200 •1) were equilibrated
overnight with approximately 1,000 cpm of 3H-progesteronefor determination of recoveryand then extracted in 4 ml hexane:ethyl acetate(98:2). The extractwasdried under nitrogen and then resuspended
in phosphatebuffer. Duplicate samplesof the resuspensionwere analyzedby radioimmunoassay
following the procedureof Wingfield and Farner (1975).
The progesteroneantiserum used was Pl1-192 (En-
[Auk, Vol. 108
categories(see Mays et al. 1991: table 1). We used
three-way analysis of variance (ANOVA) on logtransformed
data to test for the effects of sex, nest
role, and handling time on hormone levels in each
blood sample(data from all years combined).After
separationby sex we used a two-way ANOVA to examine the effectsof nest role and handling time (Table 1A). For the prolactin data in which there wasno
significanteffectof handling time, we then did oneway ANOVAs on eachbehavioralrole category,testing whether meansdiffered betweenneststagesfor
each role (Table lB). One-way ANOVAS were also
done for each nest stage,testing whether prolactin
levels differed between behavioral roles during the
sameneststage(Table 1C).Eachvariable that showed
a significanteffect (P < 0.05) was further analyzed
with Bonferroni multiple comparisontests(BON) to
find which meansdiffered. We used Spearman'scoefficientof rank correlation(rs)to analyzebroodpatch
scoresor cloacalswellingand hormonedata.For these
testswe used only brood patch scoresbetween 0 and
3, indicative of progressingdevelopment.
RESULTS
Progesterone.--Progesteronelevels did not
differ between males and females (three-way
ANOVA, F = 1.29, P = 0.26, n = 97). In both
sexesthere were significantdifferencesin progesteronelevels in different individuals, but
the
differencescanbe statisticallyaccountedfor
docrine Sciences). The standard curve covered the
by
handling
times (Fig. 1 and Table 1A). For
rangefrom 1.96to 1,000pg and wasrun in triplicate.
Lowestdetectableconcentrationwas 64 pg/ml plas- example, an exceptionallyhigh progesterone
ma.Intrasssayand interassaycoefficientsof variation level in the plasmaof the onejuvenal-plumaged
(SD/mean x 100) were 7.6% and 9.7%, respectively. male helper sampledduring the incubationpeMean recovery was 49%.
riod was correlatedwith a long handling time
Prolactin concentrationsin plasma from 102 birds (180 min) for this individual. Plasma progesfor which we knew the neststageand behavioralrole terone levels increasewith handling time in
were measuredat the University of Bristol using a serially bled Harris' Hawks (Mays and Vleck
heterologous
radioimmunoassay
systemdevelopedby
1987),probablydue to progesteronereleasefrom
McNeilly et al. (1978)and modifiedby Goldsmithand
the adrenal cortex where it is produced as a
Hall (1980). After confirming that a plasma sample
(Assenmacher
1973),
from a Harris' Hawk assayedat five doubling dilu- precursorto corticosterone
a
hormone
released
in
response
to
stress
(Hartions gave a dilution curve parallel to that of the
standard(NIADDK ovine prolactin PS-12), all sam- vey et al. 1984).
In femalesduring the nest-building stage,the
ples were assayedin duplicate 20 •1 volumes. Intraand interassaycoefficientsof variation were 5.2% (n mean progesteronelevel in the breeding birds
= 10) and 12.3%(n = 10), respectively,and the lowest was about twice that found in adult or juvenaldetectableconcentrationwas 2.0 ng/ml.
plumagedhelpers(Fig. 1). We do not think these
Statistical
analysis.--Foranalysiswe useda variable differencescan be accountedfor solely by difcalled nestroleto group the data. This grouping variferences in handling time becausethe mean
able is a compositeof stageof the nest with which
eachbird wasassociated(nonbreeding,nestbuilding, handling time during the nest-building stage
incubatingeggs,or feedingyoung)and that individu- for the breeding femaleswith high progesteral'srole andage(adultbreeder,adult-plumagedhelp- one (62 min) wassimilar to that for the juvenaler, or juvenal-plumagedhelper). This compositevari- plumagedhelpers(59 min) and actuallylower
ableseparatesthe valuesfor eachsexinto 12 possible than that for the adult helpers (90 min), al-
July1991]
Prolactin
in a Cooperative
Breeder
641
642
VLECK
ETAL.
Non
4
Neet
Feedin
Incube-
Non
Young
Breedin;
[Auk,Vol. 108
Neet
Incube-
BreedIn.
• Buildingting
Feeding
Youn=
,,
-150
-100
Time
-50
relative
0
to
first
50
egg
100
-100
(days}
-50
o
50
100
Tlms relative to first egg (days)
Fig. 1. Mean plasma progesteronelevels in Harris' Hawk males (left panel) and females (right panel)
during each nest stage.Key: [] = adult breeder,ß = adult-plumagedhelper, and /x = juvenal-plumaged
helper. Error bars indicate + 1 SE. Sample sizesand statisticalsignificanceare in Table 1.
though the handling times do not differ significantlyamongthesegroups(one-wayANOVA, F = 0.05, P > 0.59).
Prolactin.--Prolactin levels varied significantly with sexand nest role in the ANOVAs,
but not with handling time (Fig. 2 and Table
1A). We could detect no tendencyin our data
for prolactinlevels to increasewith handling
time. A regressionof prolactinlevels from 97
birds plotted againstmaximumpossiblehandling time for eachsample(5-225 min) had a
slope(0.001)not significantlydifferentfrom 0
(t = 0.14, P > 0.89). Overall, values were lower
in males than in females (three-way ANOVA,
F = 8.33, P < 0.005, n = 91). In the breeding
were no significantchangesin prolactin with
neststagein the juvenal-plumagedbirdsnor in
the adult-plumagedfemale helpers (Table lB).
We do not think the differences in prolactin
levels between the breedersand helpers during
incubation or care of young are due to an undetectedeffect of the long handling times for
the different groupsbecausethe meanhandling
times did not differ among the nest roles for
both sexes(one-wayANOVA, F = 0.53,P > 0.74
for incubation;F = 0.81, P > 0.55 for feeding
young). In addition, it seemsunlikely that differencesin the time of day sampleswere collected
for the different
nest roles could
have
biasedour interpretationbecauseall but one of
birds, prolactin levels varied with nest stage 31 samplesfrombirdsin groupscaringfor young
(Table lB), and rosesignificantlyduring incu- were collected before 1200.
bation in both males (BON, t = 2.63, P < 0.05)
Broodpatch and cloacalswelling.--Although
and females(BON, t = 2.87, P < 0.05). The mean breedingmalesincubate,none of the 58 males
level in female breedersduring incubationwas examined showed any sign of a brood patch
significantlyhigherthanthatin helperfemales exceptone breeding male, who had slight, nonat this stage(Table1C;BON, t = 3.53,P < 0.05). vascularizeddefeathering of the breast at the
Prolactinwasalsoelevatedin breeding females end of incubation(stage1). Only breeding feduring the nest-buildingstagecomparedwith malesdevelopedbrood patches(n = 23); none
helperfemalesat the samestage(Table1C;BON, of the 16 female helpers examined before or
t = 2.60, P < 0.05).
during incubationhad a broodpatch.Breeding
Levelsof prolactinfell in both breedingmales femalesbeganto showa developingbroodpatch
and femalessoonafter hatchingof the eggs,but asearlyas55 daysbeforethe firstegg,and most
there wasa significantelevationin prolactinin had a fully functionalbrood patchby the time
the adult male helpers during care of young the eggs were laid, although two incubating
(Table lB; BON, t = 2.05, P < 0.05). During this femalesshowedonly a stage-2brood patchdurstage, the prolactin levels in the adult male ing incubation. The brood patch began to rehelperswere significantlyhigher than thosein gresswithin a few daysafter hatching.In breedthe other males (Table 1C; BON, t = 2.05, P <
ing females during the nest-building and
0.05), whereas the prolactin levels in the fe- incubating stages,there was a positive corremales did not differ from one another. There
lation between the extent of development of
July1991]
Prolactin
in a Cooperative
Breeder
Non
Breeding
Nest
Building
Incubiting
Feeding
Young
5O
_=
Non
Nest
Breeding
Building
'
Incubering
Feeding
Young
30-
ß
t.......
643
/_
_e
•
,
Time relative to first egg (days)
Time relative to firat egg (days)
Fig. 2. Plasmaprolactinlevelsin Harris'Hawk males(left panel)and females(right panel)duringeach
nest stage.Symbols(seeFig. 1 legend) representvaluesfrom individuals.The mean levels for individuals
with the samebehavioralrole during eachneststageare connectedwith lines(solidline for adult breeders;
dottedline for adult-plumaged
helpers;dashedline for juvenal-plumaged
helpers);errorbarsindicate_+1 SE.
the brood patchand prolactinlevels (rs= 0.66, ing female Harris' Hawks were found in the
P < 0.001,n = 14), althoughwe cannotdeter- week beforeegglaying (LH datain Mayset al.
mine whether this relationshipis independent 1991),althoughthe effectsof handlingtimeand
of the effectof time on brood-patch
develop- probablediel rhythmsin hormonelevelsmake
ment and prolactin levels over the sameintervalssincethe partial correlationbetweenbrood
patchand prolactin,holdingthe effectof time
constant,is lower (r = 0.47, P > 0.05).
interpretation of the data difficult. In captivebreeding American Kestrels(Falcosparverious),
peaksin progesteronereaching 2-4 ng/ml are
closelyassociatedwith egg laying (Rehder et
Cloacalswellingalsooccurredin breeding al. 1986).
females at about the same time that the brood
patchwas developing.Of 13 female breeders,
10showedcloacalswellingfrom57daysbefore
the firsteggto 17daysafterthe firstegg.None
showedany cloacalswellingafter the incubation period (n = 4). The presenceof cloacal
swellingwaspositivelycorrelatedwith prolactin levels (rs = 0.58, P = 0.022, n = 15), but it
wasnot significantlycorrelatedwith neststage
or the levelsof luteinizing hormone,testosterone, estradiol(datafrom Mays et al. 1991)or
with progesterone.Only 1 of 10 adult female
helpersshowedany cloacalswelling,and no
malesdid at any time (n = 41).
Our
data
indicate
no correlation
between
plasma progesterone and parental behaviors
suchas incubationor careof young in Harris'
Hawks. Plasmaprogesteroneis not elevatedin
breedingmalehawksthat incubateand carefor
young, although a changein progesterone-receptordensity,possiblymediatedby the previously elevatedtestosteronelevels (seeBrown
1985),might have altered the effectof proges-
terone even if plasmalevels did not change.
There doesnot seemto be an importantrole for
progesteronein incubation in domestic fowl
(Bedrak et al. 1981), but it does influence the
timing of incubation bouts in African Turtle
Doves (Streptopelia
roseogrisea;
Silver and NorDISCUSSION
gren 1987).In the Harris' Hawk, progestrone
couldbe involved in brood-patchformationas
Progesterone.--In birds, progesterone is suggested
by Jones(1971),possiblyin conjuncthought to be involved in ovulation. For ex- tion with elevated estradiol since only the
ample,in the domesticfowl (Gallusgallus)there breeding femalesdevelop a brood patch, and
isa positivefeedbackrelationshipbetweenpro- only they have elevatedestradiol(Mays et al.
gesterone
andLH thatdetermines
theovulatory 1991) and progesteronebefore incubationbesequence;progesteronelevels usually peak 4gins.
6 h beforeovulation(reviewedin Kamiyoshi Prolactin.--Therolesof prolactinin avian reandTanaka1983).A similarrelationshipprob- productionand the mechanismsthat control its
ably existsin Harris' Hawks. All elevatedlevels secretionare not well understoodand appear
(2-4 ng/ml) of progesterone
and LH in breed- to vary among species.Prolactin has been im-
644
VrECK
ETAI..
plicatedin the developmentof the broodpatch
(Jones1971),the developmentof photorefractoriness (Ebling et al. 1982, Goldsmith and
Nicholls 1984), migration, molt, and fat deposition (Meier 1975)aswell asparentalbehavior
(Balthazart 1983, Goldsmith 1983, Silver and
Cooper 1983, Brown 1985, Buntin 1985). Elevationsin prolactin have been correlatedwith
incubation and brooding in many species,as
well aswith feeding of young in the European
Starling (Sturnusvulgaris;Dawson and Goldsmith 1982) and columbiformbirds that producecropmilk (Goldsmithet al. 1981),andwith
the displayof antipredatorybehaviorin Willow
Ptarmigan(Lagopus
I. lagopus;
Pedersen1989).
Elevatedprolactin is clearly associatedwith
incubation
behavior
in birds. Whether
or not
prolactininitiatesparentalbehavioror simply
maintains it, however, has been of interest. In
addition, whether elevated prolactin levels are
the cause or the result of incubation
behavior
is not always clear. In some species,artificial
extensionor termination of the incubationperiod affectsprolactinlevels,which suggests
that
the act of incubation influences prolactin secretion (Silverin and Goldsmith 1984,Oring et
[Auld,
VoL108
involved in developmentof a functionalbrood
patch and incubation in this species.Prolactin
is alsoelevatedin breeding male Harris' Hawks
during incubation,although not as much as in
females.The significant elevation in prolactin
we detected in all incubating hawks implies
that our methods allow us to detect functional
changesin plasma prolactin levels associated
with the breedingcycles,even thoughthe long
handling times for many of thesebirds might
be expectedto have changedprolactin levels
independentlyof the breedingcycle.Elevated
prolactin levels may also be involved in the
developmentof the swellingand reddeningof
the cloacalregion in the females,but the functional significanceof this in Harris' Hawks is
unknown.Nakamura(1990)suggested
a display
of cloacalswelling was used by female Alpine
Accentorsto solicit copulationsfrom the male.
Prolactinlevelsin the breedingHarris' Hawks
decreaseimmediately after incubationto levels
not different from those found in the nonbreed-
ing season.In other altricial and semiprecocial
species,prolactin levels usually remain relatively elevatedaslong asthe birdsare brooding
nonthermoregulating young (Dawson and
al. 1988).Similarly,manipulationof chickages Goldsmith 1982; Goldsmith 1982; Hector and
caninfluenceprolactinlevelsin broodingPied Goldsmith1985;Oring et al. 1986,1988;Myers
Flycatchers(Ficedulahypoleuca;Silverin and et al. 1989; Ketterson et al. 1990). Levels may
Goldsmith1990).In otherspecies,prolactinlev- decrease at about the same time that the chicks
els seem to be determined by an endogenous begin to thermoregulateand no longer require
scheduleor by day length, relatively indepen- extensivebroodingby the parent(Silverinand
dently of the bird's exposureto nest and eggs Goldsmith 1984, 1990;Oring et al. 1986, 1988),
(Eblinget al. 1982,HectorandGoldsmith1985). but prolactinlevelsoften remainelevatedcomUsuallylevelsof prolactinarehigherin females pared with nonbreedinglevels as long as the
than in males,whether or not the male partic- parentsare caring for young. Prolactin levels
ipatesin incubation(Dawsonand Goldsmith remain elevated between broods in multiple1982,Hiatt et al. 1987).Prolactinlevelsare high- broodedWhite-crownedSparrows(Zonotrichia
pugetensis;
Hiatt et al. 1987)and Song
er in malesthan in femalesin speciesin which leucophrys
the male incubatesmore than the female, e.g. Sparrows (Melospizamelodia;Wingfield and
the SpottedSandpiper(Actitismacularia;
Oring Goldsmith 1990), although not in multipleet al. 1986) and Wilson's Phalarope (Phalaropus
tricolor;Oring et al. 1988). On the other hand,
prolactinlevelsneed not necessarilybe elevated for incubationbehaviorto be expressed.Turkeys(Meleagris
gallopavo)
deprivedof their nest
show a decline in prolactin levels, but will in-
brooded canaries (Serinus canaria; Goldsmith
1982).The pattern of prolactinchangeswe observedin breedingHarris'Hawksresembles
that
in precocialgalliform and anseriformspecies
(reviewed in Goldsmith 1983) in which the
young can thermoregulateand leave the nest
soonafter hatching.In thesespecies,prolactin
thoughprolactinlevelsdo not becomeelevated usually falls to nonbreeding levels as soon as
the young are hatched.
until later (Zadworny et al. 1985).
The fall in prolactin in breeding Harris'
In Harris' Hawks, prolactin levels are elevated in breeding femalesbefore egg laying and Hawks after the eggshatch, even though the
during incubationin a mannersimilarto other altricial young remain in the nestapproximatebirds.Presumably,high levelsof prolactinare ly 45 days,suggeststhat the high levelsof procubate as soon as returned to their nest, even
July1991]
Prolactin
in a Cooperative
Breeder
lactin associated with incubation
need not be
maintainedto ensurebroodingand feedingof
the young.The chicksare altricialand the parentswill broodthe youngin the nestat night,
but relativelylittle broodingoccursduringthe
daybecause
ambienttemperatures
in May and
June(the normal monthsfor hatchlingsto be
in the nest)are relativelyhigh comparedwith
higher-latitudespecies.In fact, the chicksare
645
ng/ml) was higher than that in either male (5.6
ng/ml) or female (7.3 ng/ml) breeders at the
same time. This increase occurs at a time when
the male beta helpers,if presentin a group,
actually provide more food for the nestlings
than either of the breedingbirds. For example,
Dawson and Mannan (1991a) determined which
individualsbroughtfoodto the nestareain four
Harris'Hawk groupsof fiveindividualsmatched
often shadedby the parentsrather than brood- for groupcomposition(a breedingpair, a beta
ed, presumablyto keep chicksfrom overheat- male, and a male and female gammabird). In
ing. In addition,becausefooditemsbroughtto 136 food deliveries, the adult beta male transthe nestlingsare large (e.g. parts of rabbits), ported the food 37% of the time, whereas the
adultsmakerelativelyfew feedingtripsto the breeding male performed this task only apnest per day (Dawson and Mannan 1991a, refproximately 30% of the time, the breeding feerencestherein). Consequentlythe intensity of male only 3% of the time, and the two other
parentalbehaviordisplayedby an individual gamma helpers combined, >30% of the time.
Harris'Hawk (in termsof timespentin the nest
We havefew samplesfromadultfemalehelpand feedingtrips to the nest)may be low com- ers during incubation and care of young, but
paredwith altricialspecies
in general,especial- their prolactin levelsdo not seemto be elevated
ly thosewithout helpers,and could accountfor as in adult male helpers. This may not be surthe relatively low levelsof prolactinfound in prising becausefemale gamma helpers spend
the parents at this time.
the leastamount of time of any group member
The contributionthat the helpersmake to- near the nest or feeding young, althoughthey
ward provisioningthe youngmaydecreasethe participate in group hunting (Dawson and
effort the breedingpair mustexpendto raise Mannan 1991a).
The rise in prolactin in the adult-plumaged
theyoung.In a surveyof feedingratesof young
in 15 cooperativelybreeding species,Reyer male helper Harris' Hawks indicates that ele(1990)foundthat in speciesthatmakefew feed- vationin prolactinassociated
with careof young
ing trips (<10 per hour), the contribution the canbe uncoupledfrom the earlier prolactinelparentsmaketo feedingyoungisreducedwhen evation associatedwith nest building and inhelpersare present.In speciesthat make >20 cubationin thiscooperativelybreedingspecies.
feedingtrips per hour, parentsdo not reduce We cannotrule out a relation between previtheir effortwhen helpersare present.If Harris' ously elevated sexsteroidsand the subsequent
Hawkbreeders
providelesscareforyoungwhen elevation in prolactin (see Goldsmith 1983 and
helpersare present,one might expectan in- Buntin 1985), becausethese adult-plumaged
earverserelationshipbetweengroupsizeandpro- helpershaveelevatedLH and testosterone
lactin levels in the breedersduring the nest- lier in the nestingcycle(Mays et al. 1991).Luling/fledgling stage.We couldnot demonstrate teinizing hormones and testosteronedecrease
sucha relationship(Fig. 3). In Pied Flycatchers in both the adult malehelpersand the breeders
(Silverin and Goldsmith1984)and Dark-eyed during the incubation stage.This seemsto folJuncos(Juncohyemalis;Ketterson et al. 1990), low the pattern describedby Brown (1985) for
there is alsono discernabledifferencein pro- many speciesin which both sexesshowparenlactinlevelsin femalesthat raiseyoungalone tal behavior. Elevated testosterone in males is
and thosethat are aided by a mate. Thus the probablyassociated
with defenseand courtship
level of prolactinsecretiondoesnot seemto be earlyin the nestingseason,and it possiblyacts
modulatedin any preciseway by the level of as a primer for parental behavior;but later as
parental effort expended.
the level of prolactinrises(possiblystimulated
The mostsurprisingthing that we foundwas by the presenceof eggsor young),the testosthat prolactin levels rose significantlyin the teronelevel falls. The effectsof exogenousproadult male helpersduring the nestling/fledg- lactin on behaviorin nonbreedingindividuals
ling stage;at the sametimeprolactindecreased have been demonstrated before (reviewed in
in thebreedingbirds(Fig.2). In fact,the mean Goldsmith 1983,Buntin 1985),but we are aware
level at thistime in the adultmalehelpers(9.1 of no previous report of a correlationbetween
646
VLEaC
E'r^L.
[Auk,Vol. 108
12
[]
Females
ß
Males
10
ß
[]
ß
[]
ß
ß
ß
ß
[]
ß
2
3
4
5
[]
6
7
8
Group Size
Fig. 3. Plasmaprolactinlevelsin breedingmaleand femaleHarris' Hawksduring the stagewhen groups
are caring for their young (36-100 daysafter the first-laid egg) plotted in relation to group sizes.Symbols
represent values from individuals.
endogenousprolactin levels and parentlike be-
havior in a free-living, nonbreedingbird. Kettersonet al. (1990)measuredprolactinin DarkeyedJuncosduring the nestlingstagein natural
fathersand in maleswho had replacedthe original male in a pair after the young hatched.
They reported that prolactin levels in two replacementmales that were helping the female
raise young were not different from those in
replacementmalesthat were not feeding adopted young. The natural fathers who fed their
own young had levels of prolactinhigher than
thoseof the replacementmales.Interpretation
of the data was confoundedby seasonaleffects
sight or sound of young birds in the nest as
suggestedby Woolfendenand Fitzpatrick1984),
the elevated prolactin may increasethe probability that thesehelperswill exhibit parentlike
behaviors even though they are not likely to
be closelyrelated to the young they help. It
would be interestingto know whether helpers
display this rise in prolactin when caring for
young in cooperativelybreedingspeciesin general, and if this differs from the responseof
nonbreeding individuals to eggs or young in
noncooperativelybreeding species.If this were
the case,it is likely that selection has acted at
a physiological level to alter behavior in coon prolactin levels.
operativelybreedingspecies,althoughthis does
If prolactin functions to facilitate provision- not allow us to saywith certainty whether care
ing of the hatchlingsand fledglingsin Harris' of young by helpersis a uniquely evolved charHawks, we suggestthat there is a physiological acteristicof cooperativebreeders, nor specifibasisfor helping behavior in this cooperatively cally why helping behavioris adaptive.Experbreeding bird. Although we don't know what imental manipulation of prolactin levels in
the environmental
stimulus is for the rise in
helpers may provide a tool to alter helping beprolactin in adult male helpers (it may be the havior and therebyallow direct testingof hy-
July1991]
Prolactin
ina Cooperative
Breeder
647
nusvulgaris)during the annual cycleand in re-
pothesesconcerningcostsand benefitsof helping behavior.
lation to nesting,incubationand rearing young.
Gen. Comp. Endocrinol.48: 213-221.
DAWSON,J. W., & R. W. MANNAN. 1991a. Dominance
ACKNOWLEDGMENTS
hierarchiesand helper contributionsin Harris'
Hawks.
We thank all those individuals who helped with
the fieldwork, including Rick Bowers,Ellen Weintraub, Jeff White, Lynn Oliphant, Bill Mannan, Bob
Scheibe
and other
members
of the Tucson Audubon
Society.We acknowledgethe loan of equipmentfrom
OscarWard, Holly Hobart,Mable Mays,and Stephen
Russell.Dave Vleck and Mike Moore critically read
the manuscript, and Richard Straussoffered advice
on statistics.Early in the study,fundswere provided
by Arizona Wildlife Foundation,JamesR. Silliman
Memorial Fund, Sigma Xi, and the Western Bird
Banding Associationto Nora Mays. Major funding
was provided by NSF grant BSN-8606548to Carol
Vleck.
Auk 108: 649-660.
,&
. 1991b. The role of territoriality in
the socialorganizationof Harris' Hawks.Auk
108: 661-672.
EnLING,F. J.P., A. R. GOLDSMITH,• B. K. FOLLETT.
1982. Plasmaprolactinandluteinizinghormone
during photoperiodically induced testicular
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in starlings(Sturnus
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GOLDSMITH,A. R. 1982. Plasma concentrations of
prolactinduringincubation
andparentalfeeding
throughoutrepeatedbreedingcyclesin canaries
(Serinus
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