PLASMA LUTEINIZING
BEHAVIORAL
COOPERATIVELY
HORMONE, STEROID HORMONES,
ROLE, AND NEST STAGE IN
BREEDING HARRIS' HAWKS
(PARABUTEO UNICINCTUS)
NORA A. MAYS,• CAROL MASTERSVLECK,1 AND JAMESDAWSON2
•Departmentof EcologyandEvolutionary
Biology,Universityof Arizona,
Tucson, Arizona 85721 USA, and
2School
of Renewable
NaturalResources,
Universityof Arizona,Tucson,
Arizona85721USA
ABSTRACT.--We
measuredplasmalevels of testosterone(T), estradiol 17fl(E), corticosterone,
and luteinizing hormone(LH) in adult breeders,adult-plumagedhelpers,and juvenal-plumagedhelpersof the cooperativelybreedingHarris' Hawk (Parabuteo
unicinctus)
in southeastern
Arizona. In the males,both adult breedersand mostadult-plumagedhelpershad elevatedT
and LH during February and March, when nest building occurs,whereasmost juvenalplumagedhelpersshowedno changein LH, T, or E throughouttheyear.Thusadult-plumaged
helpers,usuallynot relatedto the breeders,are hormonallyreadyto breedin the spring.We
suggestthat thesehelpersattainbreedingreadinessbecause
potentialbenefitsthey canderive
from either occasionalsuccessful
copulationsor possibleattainmentof the breedingposition
make reproductivereadinessadvantageous.
In contrast,mostjuvenal-plumagedhelpersare
aiding their own parentson their natal territory and are not hormonallyreadyto breed,and
thus they physiologicallyavoid the potential for inbreeding. An exceptionto this was a
juvenal-plumagedmale helper with elevatedtestosteronelevels who was not helping his
parents.The female breederswe examinedhad elevatedT, LH, and E during the nest-building
period, whereasthe helpers(both adult- and juvenal-plumaged)did not show elevationsat
any time of the year. During the early part of the nestingcycle,the adult-plumagedfemale
helpersweighed significantlyless(ca. 10%)than the breeders.It is possiblethat poor body
condition,subordinatestatusto the breedingfemales,or both were related to their lack of
breedingreadiness.In all birds,corticosterone
levelsincreasedwith handling time, andwere
higherduring the nestingperiodsthan during non-nestingperiods,but showedno consistent
relationwith helper or breederstatus.As in other speciesthat are relatively social,maintain
long-term pair bonds, or are tropical in distribution, plasmaconcentrationsof LH and sex
steroidsin Harris' Hawks, even when elevated,were relatively low. Received
10 May 1990,
accepted13 January1991.
COOPERATIVE
breeding, in which more than breeding(Ligon et al. 1988).In this study we
two adultsassistin raisingyoung, occursin at present endocrine evidence for reproductive
least222 speciesof birds and is taxonomically readinessin breedersand helpersin the Harris'
widespread among altricial species (Brown
Hawk (Parabuteo
unicinctus)
and discusspossible
1987).Although the evolutionaryoriginsof co- proximate and ultimate causesfor lack of breedoperativebreedingsystemsremain unclear (see ing in helpers.In an accompanying
paper(Vleck
Brown 1983, Emlen 1984, Jamiesonand Craig et al. 1991),we discussthe physiologicalbasis
1987, Jamieson1989) many authors have dis- of parental or helping behavior in the Harris'
Hawk.
cussedthe ecologicalfactorsthat promote the
developmentof cooperativebreedingin differHarris'Hawk breeding
biology.--Harris'Hawks
ent species(e.g. Emlen and Vehrencamp 1983) breed cooperativelyin New Mexico, Texas,and
and the potentialadvantagesaccruedby non- Arizona (Mader 1975a, Griffin 1976, Brannon
breeding helpers (e.g. Ligon and Ligon 1978; 1980,Whaley 1986,Bednarz1987a,Dawsonand
Woolfenden and Fitzpatrick 1978, 1984;Brown Mannan 1989). The mean number of hawks asand Brown 1981). Few studies, however, have
addressedeither the physiologicalbasisof this
type of behavior (Reyer et al. 1986, Wingfield
et al. in press,Schoechet al. 1991)or physiological constraints involved in cooperative
619
sociatedwith a nest in the population we studied was 3.8 (+1.3 SD) and ranged from 2 to 7
birds.Harris' Hawks may be polyandrous(Mader 1979), but behavioral and electrophoretic
evidencesuggeststhat groupsgenerallyconsist
The Auk 108:619-637. July 1991
620
M^¾s,VLECK,
,•'qDD^WSON
of 1 breeding pair and 1-5 nonreproducingbirds
(Bednarz 1987a; Dawson and Mannan 1991a, b)
[Auk, Vol. 108
son and Mannan 1991a). Approximately three
fourths of observedjuvenal-plumagedgamma
that may or may not be relatedto the breeders.
DNA analysisof all membersof severalHarris'
Hawk groupsindicatesthat polygynyand polyandry, as well as monogamy,occur in the Arizona population (Sheehyet al. MS), but the frequency of each of these mating systemsin the
population is unknown.
helperswere bandedoffspringof the breeders
the groups also have another alpha-level fe-
persedgammahelpers.In Arizona <6% of female offspring remain on natal territories by
they were helping, and about one fourth were
immigrants. Furthermore, no birds banded in
the nest were observed to attain alpha or beta
statuswithin their natal group or territory, although three males were observed to do so
within unrelated groups. Adult male helpers
The behavioral roles of different members of
can be older than 4 yr; three adult beta helpers
the group have been describedin detail else- on the study area had been banded more than
where (Dawson and Mannan 1991a) for this Ar8 yr previously by earlier workers (Dawson unizona population. The dominant pair in each publ. data).
We did not divide our helpers into beta and
group (termedthe alpha male and female)progamma types becausewe did not always have
vides direct care of the eggs and young, including nest building, egg laying, incubation enough information to do so. Rather, we clasand brooding, and shading and feeding the sified them as either in adult plumage or in
nestlings.The dominant pair also participates juvenal plumage (Table 1). Basedon the above
in group hunting although the alpha female information, however, the probability that our
rarely leavesthe nest area during the breeding adult-plumaged male helpers were of the unseasonand is usually supplied with food by the related, beta type is ca. 80%; the other 20% of
alpha male or helpers. (Approximately 9% of adult-plumaged helpers were probably nondismale, an alpha-2 bird, but none of the females
we capturedin this study were of this type.) In
Harris' Hawks, alpha breeders remain on the
sameterritory year after year; thus helpers that
remain on natal territoriesare likely to be help-
ing their parentsand those that disperseare
likely to be helping birdsthat are not their parents. The helpers' major contributionsto the
breedingeffortare to captureand transportprey
to the nest area, detect and harass predators,
and help with defenseof the nesting territory.
Bednarz (1988) and Bednarz and Ligon (1988)
suggestedthat cooperativehunting may be the
basisfor the social organization of the Harris'
Hawk and participationin hunting may be one
of the largestcontributionsthat helpersmake
to the breeding effort.
Based on behavior,
Dawson
and Mannan
(1991a)distinguishtwo typesof helpersin Harris' Hawks: beta malesand gammamalesor females. They find that approximately 80% of
adult-plumaged male helpers are beta birds
their second year (after molting into adult
plumage),and none remain by their third year
(Dawson and Mannan 1991a). Thus, the adult
femalehelperswe caughtwere even lesslikely
to havebeen offspringof the breedersthey were
helping. All of our juvenal-plumagedbirdswere
gammahelpers (no juvenal-plumagedbeta birds
have been observed). Approximately 75% of
them were probably helping their parents,and
25% were
not.
Endocrinemechanisms
and lack of breedingin
helpers.--Elevationsin reproductive hormones
are commonly interpreted as an indication of
readinessto breed. In all seasonallybreeding
birds in which annual cycles in reproductive
hormones have been studied, there are seasonal
increasesin plasmalevels of gonadotropinand
sexsteroidsassociated
with gonadalmaturation
or recrudescence(Wingfield and Farner 1980,
Wingfield and Moore 1987). The extent of the
elevation varies between species,however, and
hormone
levels
often
decline
after
the initia-
(Dawson and Mannan 1991a: table 3) and are
not related to the breeders.Gamma helpers may
be in adult plumage (•22%) but are more frequently in juvenal plumage (• 78%).They may
tion of breeding cycles.If gonadotropin and sex
steroid levels in a speciesare not elevated in
helpers at the same time that they are elevated
be either male (•63%)
in breeders, then it seems reasonable that lack
or female (•37%) and
of breeding in helpersmust be causallyrelated,
at least in part, to this hormonal difference.
We use analysesof hormonesknown to be
of helpers comesfrom 4 yr of group-composition analysis,banding,and dispersaldata(Daw- involved in avian breeding cyclesand acom-
are usuallyoffspringof the breeding pair. The
evidence for the relatedness of these two types
July1991]
Hormones
inCooperative
Breeders
621
TABLE1. Categoriesand sample size for each sex of the compositevariable called nestrole used in the
statisticalanalysisof hormone levels in Harris' Hawks. The 12 categoriesof nest role for each sex are
determinedby the individual'sbehavioralrole and stageof the nestwhen the bloodsamplewas taken.
Behavioral
Adult breeders
Nest stage
M
F
Nonbreeding
Nest building
-5
Adult-plumaged
helpers
role
Juvenal-plumaged
helpers
M
F
M
F
4
10
3
7
I
5
3
4
Total
M
F
1
9
6
16
6
24
Incubation
9
7
3
1
1
1
13
9
Feeding young
9
12
6
1
2
1
17
14
19
8
10
12
Total
23
33
capturedbirds with a heparinized syringe and 25gauge %-in needle. Handling time was then calculated as maximum possible time on trap plus processingtime. The mean maximum handling time was
70 +- 61 min. Bloodwas stored on ice in heparinized
test tubesuntil the end of the field day when it was
tradiol-17•3 (E), and corticosterone vary with
centrifuged.The plasmawasthen removedand stored
season, behavior, social status and relatedness
at -20øC until analyzed.
amongindividualHarris'Hawks.We measured
We banded each bird with a unique combination
parisonof levelsbetweenhelpersand breeders
to investigatewhether or not Harris' Hawk
helpersare physiologicallyreadyto breed.We
describethe way that plasmaconcentrationsof
luteinizing hormone(LH), testosterone
(T), es-
corticosterone
levels as an indicator
of stress
(e.g. Wingfield, Smith, and Farner 1982, Deviche 1983,Harvey et al. 1984,Wingfield 1985,
Wingfield and Silverin 1986),in order to explore the possibilitythat lack of breedingby
helpers is due to high stresslevels associated
with
their subordinate
social status.
METHODS
Studyareas.--Thisstudy was conductedfrom May
1985throughAugust1987on an approx.200-km2site
north of Tucson, Arizona, and south of Florence, Ar-
izona. Approx. 25% of the site overlapsthat used by
Dawson and Mannan (1991a, b). Harris' Hawks com-
monlynestin saguarocactusandpaloverdeandmesquite treesin this habitat.
Fieldmeasurements.--To
capture 157 Harris' Hawks
(n = 157),we set a balchatri trap (Bergerand Mueller
1959)near a perchedbird and watchedfrom 300-400
m until the bird wascaught,or we stakedtrapswithin
200 m of active nestsand checkedtraps every 1-2 h.
Birdsusuallydonot hunt when closelyobservedand
will not approacha trap if humansare within sight.
We were thus forced to remain away from the traps
for long periodsof time to increasethe probability
of capturinga bird. The maximum possibletime a
bird could have been ensnaredon a trap was recorded
as time elapsedsincethe trap was set until the bird
was removed from the trap. Mean (+SD) maximum
time birds spenton the trap was55 +58 min (median
time = 30 min).
We withdrew 3 ml of blood from a wing vein of
of three colored
bands and a numbered
aluminum
USFWSserviceband (permit no. 09335).Morphological measurements were taken, and each bird was
weighed. A 2,000-g pesolascalewas used to weigh
eachbird to +_25g.
To assessthe breeding condition of males, we examined the cloacalcontentsof 26 males for the presence or absenceof sperm. The cloacalcontentswere
extruded onto a slide (Bird et al. 1976), the slide was
air-dried and later examinedfor the presenceof sperm
under a phase contrast light microscope.We found
spermin 4 of 8 breedingmalesand no spermin the
cloacalcontentsof 7 adult helpers, 4 juvenal-plumagedhelpers,and 7 maleswhoserole wasunknown.
We believe, however, that detectionof cloacalsperm
in Harris' Hawks by the "stripping" techniquemay
reflectonly the remnantsof a recentsperm ejaculation, rather than evidence of spermatogenesis.For
instance, we found no sperm in the cloaca of one
alpha breeder5 daysbeforethe first egg. This male
was the only male at a nest lacking helpers,and the
eggsin the nest hatched.When sperm were present,
we found only a few per microliter.Othershave also
noted low levelsof spermin cloacalsamplescollected
from breeding raptors(Corten 1973).
Age andsexof individuals.--Based
on their appearance, we identified banded hawks as belonging to
one of two agecategories:adult or juvenal-plumaged.
The juvenal plumage is retained through one breeding seasonafter fledging (Brown and Amadon 1968).
The sexesare monomorphic in plumage coloration.
We assigneda sexto eachindividual in the field (after
separationby age) on the basisof mass(Hamerstrom
and Hamerstrom 1978). Mass of adult males (range:
622
MAYS,VI•EClC,
ANI• DAWSON
610-900g;• = 726g) overlappedthat of adult females
(range:900-1,225g; • = 1,046g) in only one male.
The next largestmale weighed 825 g, and the sexof
the one unusuallylarge male was supportedusing
principalcomponents
analysisof sevenmorphological measurements(Mays 1989).The massof juvenal-
plumagedmales(range:650-800g; œ= 706 g) did
not overlapthat of juvenal-plumagedfemales(range:
850-1,086 g; • = 942 g).
Field observations.--We
identified
a hawk as a mem-
ber of a groupif it wastrappedor seenwithin 300 m
of an active nest. Harris' Hawks actively expel trespassersfrom within at least 500 m of an active nest
(Dawson and Mannan 1991b);therefore trapping a
nonmember within this zone is unlikely.
Most behavioral information on color-marked birds
[Auk, Vol. 108
45 dayspost-hatch(Mader 1975a),and group memberscontinueto feed the young for severalmonths
after fledging (pets.obs.).
Hormone
assays.--Testosterone
(T) and Estradiol-17/•
(E) in 200 •1 plasmawere assayedafter extractionin
2.5 ml diethyl etherand chromatographic
separation
on celite columnsby radioimmunoassay
(RIA) fol-
lowingthe methodsof Abraham(1974)with modificationsdescribedby Wingfield and Farner (1975)
for usewith avianplasma.For the corticosterone
RIA,
the hormonewasextractedfrom 30 •1 plasmain 3 ml
dichloromethane,and it was then assayedin duplicate. Least detectableconcentrationswere 15 pg/ml
for T, 1 ng/ml for corticosterone,
and 12 pg/ml for
E.Interassay
variabilityandintraassay
variability(SD/
mean x 100) for T were 10.8%and 7.0%; for cortico-
was gatheredfrom fully enclosed,elevatedblinds, sterone, 7.0% and 10.9%;and for E, 23.2% and 8.7%,
respectively.
We assayedluteinizing hormone (LH) in the laboratoryof JohnWingfield (Univ. Washington,Seattle,
Washington)with a double-antibody,postprecipita9 x binocularsto identify and observethe behavior tion RIA for avian LH developedby Follett et al.
of marked birds. We recordedbehavioral activity of (1972) and modified by Follett et al. (1975). Luteinmarked individuals for a minimum of 10 h at each
izing antiserum(anti 3/ 3) andLH standard(PRC-AEInest (see Dawson and Mannan 1989, 1991a, b). At
I) were kindly provided by Peter Sharp (Poultry Resomenests,we useda fully enclosedcloth blind erect- searchCentre, Roslin Edinburgh). The least detected on the groundwithin 10 m of active nestsand able concentrationwas approx. 0.1 ng/mL
Statistical
analysis
ofeffectofseason.--Allvalueswere
recordedbehavioralactivityof markedindividualsat
the nestfor 3-16 h per nest.Behavioralobservations first transformedwith natural logs to minimize the
at 47 different nests allowed us to identify the be- effects of outliers and normalize the data. Statistical
havioral role (breeder or helper) of 105 of the 157 tests were performed using general linear models
trappedindividualsfor whomwe hadbloodsamples. contained in SAS statisticalpackage(SAS 1984). To
Neststage.--Weclassifiedthe nest stagefor each elucidateseasonalpatternsin hormonelevels,we did
hawk for the time the blood sample was taken by three-wayANOVAs for eachhormoneafter separatcountingforward or backwardfrom the estimated ing samplesby sex.To testfor the effectof ageof the
dateof the first-laidegg.The dateof the first-laidegg bird, month of year, and maximumpossiblehandling
was either observeddirectly, calculatedfrom obser- time on hormone levels, we used samplesfrom all
vations of the first-hatched chick, or calculated from
yearscombined(Table2A). All 157samplescouldbe
estimatesof the ageof the nestlingsbasedon plumage used for this analysis.Two-way ANOVAs were perdevelopment(Bednarz1987a).Nest building begins formed (after separationof the data by sexand age)
approx.36daysbeforeegglaying(Mader1975b).De- to determinewhether valueschangedsignificantlyin
fense of a nest site from human intruders (circling a given month from the previousmonth. Handling
and screaming)beginsapproximatelythe sametime time was included in all two- and three-way ANOVAs
as nestbuilding, and we observedit a maximumof becausehandling times were long. A pilot study
66 daysbeforethe first-laidegg(œ= 32 + 16 days,n showed that testosterone and corticosterone levels in
= 14 nests).We used the mean time of nest-sitede- serial samplestend to increasewith handling time,
fenseplusoneSD to indicatethe earlybeginningof althoughestradioland luteinizinghormonelevelsdo
the nestingcycle.Thus samplescollected>50 days not change(Maysand Vleck 1987;unpubl. data).We
beforethe first-laidegg were consideredto be from excludedhandling time from one-wayANOVAs only
the nonbreedingstageof the annualcycles(approx- after it showedno significanteffectin two- or threeimatelyAugustthroughearlyJanuary).Samplescol- way ANOVAs.
Statistical
analysis
ofeffectofnestrole.--Harris'Hawks
lected50 daysbeforethe first egg up to the dateof
the first egg were consideredto be from the nest- do not breed synchronously;first-eggdatesranged
buildingand gamete-production
stage.Samplescol- from 21 Februarythrough5 May. Hormonelevelsare
with neststagethan
lectedfrom the date of the first-laidegg to 35 days probablymorecloselycorrelated
later were from the incubationstage(Mader 1975b), with day of the year. Thus,we analyzedseparately
and thosecollectedfrom 36 to 100daysafter the first- the data from the 105 hawks for which we knew the
laid eggwerefrom the stagewhenyoungwerebeing behavioralrole and the stageof its associatednest.
fed. The chicksremain in or near the nestfor approx. Due to the incompletedesigninherent in our study,
which were erected3-10 m from the nest gradually
over a period of severaldays.Blindswere entered
either before dawn or by two people,one of whom
later left the area.We useda 20 x spottingscopeand
July1991]
Hormones
in Cooperative
Breeders
we designateda compositevariable that we called
nest role for use in the ANOVA.
variable based on the combined
We defined
behavioral
this
role of the
individual at the nest, the stageof the nest,and the
ageof the bird. Nest role separatesthe valuesfor each
sexinto 12 possiblecategories;samplesizesfor each
nest role are shown in Table 1.
For the 105 hawks for whom we knew nest role,
we examined the effects of sex, nest role, and han-
dling time on the levels of eachof the hormoneswith
a three-way ANOVA (statisticsnot shown).After separation by sex,we testedthe 105 samplesfor the combined effectsof nest role and handling time with a
two-way ANOVA (Table 2B). For casesin which handling time showedno effect,we did one-wayANO-
VAs for eachrole category,to test whether means
differedbetweenneststagesfor eachbehavioralrole
(Table 2C). One-way ANOVAs were also done for
eachnest stage,to test whether hormone levelsdifferedbetweenrolesduring the sameneststage(Table
2D). Eachvariablethat showeda significanteffect(P
< 0.05) wasfurther examinedusingBonferronimultiple-comparisontests(BON) to indicatewhich means
differed (SAS 1984).
RESULTS
TESTOSTERONE
Effectof season
in males.--MeanplasmaT concentrationsvaried significantly by month in
maleHarris Hawks(Fig. la), but handlingtime
did not significantlyaffectT levels (Table 2A).
In adult-plumagedmales exclusively,mean T
levels differed significantlybetween months
(two-way ANOVA, F = 4.94, P = 0.007, n = 33).
Levelsrose during Februaryand remained elevatedduring March (nest-buildingperiod for
mostbirds).Levelsof T declinedin April, which
coincidedwith incubationat mostnests.In juvenal-plumagedmales,T levels did not vary
amongmonths.Adult levels were higher than
those in juvenal-plumagedbirds, but the differencesin T betweenagegroupsdid not quite
623
egg date for both study sites and all 3 yr was
30 March (+ 17 days,n = 113nests)and previous
studies(Balthazart 1983;Wingfield and Farner
1978a,b; Fivizzani and Oring 1986; Wingfield
and Moore 1987;Wingfield 1984a)have shown
that thesetwo hormonesare highestin the period before egg laying in most species.During
March, T levels were significantly higher in
adult males than in juvenal-plumaged males
(one-way ANOVA, F = 5.68, P = 0.038, n = 12).
Effectof nestrolein males.--AverageplasmaT
levelsdifferedsignificantlydependingon nest
roles (Fig. lb, Table 2B). In adult breeders,T
was significantlyhigher during the nest-building stagethan during incubation or feeding of
young (BON, t = 2.63, P < 0.05, n = 22). In the
adult helpers, T was also significantlyhigher
during the nest-building stagethan during incubation (BON, t = 3.07, P < 0.05, n = 18). There
were no statisticallysignificant changesin T
betweenneststagesin juvenal-plumagedhelpers (Table 2C). Sample sizeswere small for juvenal-plumaged helpers (total n = 10), but T
levels were low in all but the individual
who
was not on his natal territory (Fig. lb).
We also examinedthe effect of role during
each nest stage (Table 2D). During the nestbuilding stage, T levels in breeder and adult
helper were similar to each other and higher
thanjuvenal-plumaged
helpers,but this differencewas not significant.Excludingthe T value
for the one male helper that was not on his
parents' territory decreasedthe mean T value
for juvenal-plumaged helpers during nest
building, and the differencesin breedersand
adult helpersfrom the threeremainingjuvenalplumagedhelpersapproachedsignificance(F =
2.24, P = 0.08, n = 14). Nest role did have a
significanteffectin the two-wayANOVA (Table
2B), so the inability of the one-way ANOVA to
detect significant differences between the
groupsduring the nest-buildingstagewaspresumablydue to smallsamplesizesthat resulted
from partitioning the databy neststages.
Effectof season
in females.--Levelsof T in the
82 femalesdiffered significantlybetween age
groupsand months,and due to handling time
(Table2A); averageT levelswere lower than in
males(three-wayANOVA, F = 10.66,P = 0.002,
reach significance(Table 2A). One juvenalplumagedmale plotted individually (Fig. la)
hadan elevatedT level latein February,30 days
beforethe first eggwaslaid in the nestat which
he helped.This individualwas the only juvenal-plumagedmale sampledduring the nestbuilding stagethat wasknown to be helpingat
a nest not belonging to his parents.The other n = 101). In adult females, T levels differed
three had been bandedin the previousyears' significantlyamongmonths(two-wayANOVA,
nestsof the birdsthey were currentlyhelping. F = 2.94,P = 0.005,n = 67),rising during March
We examined the male T and LH data from
(Fig. lc), but there were no significantchanges
March in more detail becausethe averagefirst- betweenmonthsin juvenal-plumagedfemales.
624
MAYS,VLœClC,
ANDDAWSON
[Auk,Vol. 108
v
v
v
ddddddd
July1991]
Hormones
inCooperative
Breeders
625
Levels
ofT in adultS
females
weresignificantly
higherthan thosein juvenal-plumaged
females
(Table 2A).
Effectof nestrole in females.In femalesthere
were also significantdifferencesin plasma T
levels between nest roles and due to handling
time (Table2B).Breedingadult femaleshad the
highestT levels during the nest-building stage
(Fig. ld). We think that the higher levels of T
in breedingfemaleswhen comparedwith helper femalesduring nestbuilding are unlikely to
be solelydue to handlingtime becausethe mean
handling time for the adult breeding females
during this nest stagewas less (œ= 62 min, n
= 10) than that for the adult helper females (œ
= 90 min, n = 5), and similar to that for the
juvenal-plumagedhelper females(œ= 57 min,
n = 9).
Handling time (maximum time on trap plus
processingtime) significantlyaffectedT levels
in females (Table 2: A and C), but not in males.
Previously, we reported that T levels increase
with handling time in serially sampledHarris'
Hawk males(Mays and Vleck 1987). Stressdue
to handling time may causean adrenalcortical
release of T as well
as corticosterone.
The max-
imum T valuesresultingfrom this stress-related
releasearean orderof magnitudelessthan those
in males during nest building and territorial
defense,so it is not surprisingthat there were
no statisticaleffectsof handling time on male
T, but there were effects on female T.
ESTRADIOL
Effectofseason
infemales.--MeanplasmaE lev-
els variedsignificantlyover the year in female
Harris Hawks (Fig. 2a) and were significantly
higher in adultsthan in juvenal-plumaged
birds
(Table 2A). Plasma E levels in adults rose in
¸
o
March just before egg laying, but not significantly so, whereas in juvenal-plumagedbirds,
there were no changes in levels during the
months when birds were sampled.
Effectof nestroleinfemales.--Nestrole, but not
handling time, had a significanteffecton E levelsin females(Table2B,Fig. 2b).In adult breeders, E levels were significantlyhigher during
the nest-buildingstagethan during incubation
and feeding of young and were lower during
feeding of the young than during the nonbreeding stage(BON, t = 2.83, P < 0.05, n =
626
MAYS,VLECK,
ANDDAWSON
[Auk, Vol. 108
Males
C
&
r• Adult
Juv
800
4oo
O
N
Non-
Breedin
O
J
F
M
Nest
A
Building
d ....
J
J
A
O N D J F M A M' J J
Feeding
bating
,
.i6o' ' ' •s'o....
M
Incu-
Young
Breeding
Buildin
bating
Young
,
6'0' ' ' i'o
Time relative to first •99, da•s
.•oo
.so
o
so
•oo
Time relative to first •99•
Fig. 1. Meanplasmatestosterone
levelsin Harris'Hawk males(a andb) and females(c andd). The top
panelsindicatethemeanlevelforall adult-plumaged
andjuvenal-plumaged
birdsin eachmonth.Thebottom
panelsplotthe meanvaluesd•ing eachneststagefor thoseindividuals
forwhomnest-role
is known.The
nonbreeding
se•on extends&omapproximately
AugustthroughearlyJanua•.Ad Br = adultbreeder,Ad
H = adult-plumaged
helper,andJuvH = juvenal-plumaged
helper.Errorbarsindicateß 1 SE.Lackof error
barsindicatesno variance,sometimes
becausen = 1 (seeTable1).The open•iangle (in a) andclosed•iangle
(in b) showthe testosterone
v•ue for the one juvenal-plmagedmalehelperwho wasnot on his parent's
te•ito•; thisvaluewasnot includedin the meanfor juvenal-plmageda•iliafies for thatinte•al. Within
eachneststagethe meanhormonevalueis plottedon the meandayon whichsamples
werecollected.
34). Estradiol-17•Slevels did not differ signifi-
cantly between nest stagesin either adult or
juvenal-plumagedhelpers(Table2C).
During the nest-buildingstage,levelsof E in
breedingfemaleswere significantlyhigherthan
in either adult helpers or juvenal-plumaged
helpers(Table 2D, BON, t = 2.60, P < 0.05, n =
24). Adult- and juvenal-plumagedhelper fe-
LUTEINIZING
HORMONE
Effectof season
in males.--PlasmaLH levelsin
males differed from month to month (Fig. 3a,
Table 2A). In adult-plumagedmales,LH rosein
January and fell in May (two-way ANOVA, F
= 8.54, P = 0.0001, n = 52). In contrast to the
stages.Malesexhibitedno variation in E with
timeof yearor nestrole,andvalueswerealways
seasonalpattern in T, LH levels remained high
throughout April (during incubation). Plasma
LH did not vary significantly with month in
juvenal-plumaged birds, where levels were
lower overall than in adults, but not significantly so (Table 2A). In March, during nest
building and mateguarding,LH levelsin adults
were significantlyhigher than in juvenal-plumaged males (one-way ANOVA, F = 8.26, P =
low (Table 2A).
0.017, n = 12).
male levelsdid not differ significantlyfrom each
other. This is in contrastto the pattern of T in
malesin which both breeder and helper adults
had higher levelsthan juvenal-plumaged
helpers. There were no significant changesin E in
femalesof different roles during the other nest
July1991]
Hormones
inCooperative
Breeders
Effectof nestrolein males.--Plasma
LH levels
differed significantly between nest roles (Fig.
3b, Table 2B). In adult breeders,LH was significantly higher during nestbuilding and incubation than during feeding of young (Table
2D; BON, t = 2.64, P < 0.05, n = 22). For adult
helpers,LH was highest during nest building
but not significantly so. There were no significant changesin LH levels of juvenal-plumaged
helpers between nest stages.Luteinizing hormone levels in breedersand adult helperswere
similar during eachneststageand higher than
thosein juvenal-plumagedhelpers(exceptduring feedingof young),but thesedifferenceswere
not statisticallysignificant(Table 2D). Overall,
LH levels were lower
100'
o
ß
8O
(three-way ANOVA, F = 5.26, P = 0.024, n =
Effectof season
in females.--Inplasmasamples
of females, LH levels differed significantly
among months (Fig. 3c), but there were no statistically demonstrabledifferencesdue to age
or handling time (Table2A). In adult-plumaged
females,LH levelsdifferedamongmonths(twoway ANOVA, F = 2.16, P = 0.036, n = 62); they
rose in January and remained relatively high
throughApril. The one femalesampledduring
November had a high level of LH (1.68 ng/ml),
which may indicate an undiscovered autumn
nest (Radke and Klimosewski 1977, Bednarz
Adult
Juv
60'
40'
2O
O I N 'D •J ' F ' M 'A ' M'J
in males than in females
98).
627
120
Non-
Nest
Breeding
Building
T
!
b
100
Incubating
Feeding
Young
•
•
[] Ad Br
' AdH
/ :
80
•
•
40
•
•
'J ' A
ß auvH
20
0
-' 00
,
-50
I
0
-
-
-'o
-
5'0
-
1987b). There was no statisticallysignificant
Time relative tr, first egg, days
seasonalpattern detectedin the plasmaLH valFig. 2. Meanplasmaestradiollevelsin female
ues from juvenal-plumagedfemales,and their
Harris'Hawks.The(a)panelindicates
themeanlevel
levels did not differ significantlyfrom thoseof
for all adultsand juvenal-plumaged
birds in each
adults.
month,whereas(b)plotsthemeanvalueduringeach
Effectof nestrolein females.--Therewere no neststagefor thoseindividualsfor whomnestrole
significantdifferencesin female plasmaLH lev- is known.Symbolsand statistics
asin Figure1.
els between nest roles or due to handling time
(Fig. 3d, Table 2B). In breeding females, LH
levelswere significantlyhigher during the nest- there were also significanteffectsof age and
building stagethan during feeding of young monthof yearin males(Fig.4a, Table2A). Cor(Table 2C; BON, t = 2.83, P < 0.05, n = 34). ticosteronelevels were generally lower in juAdult breeders had higher levels of LH than venal-plumagedmalesthan in adultsand were
either adult or juvenal-plumagedhelpers dur- higher in adults during the breeding season
ing all nest stages,but these differenceswere than during the nonbreeding season.In fenot significant(Table 2D). The adult helper fe- males, corticosteronelevels differed signifimales had lower levels of LH than either adult
breederor juvenal-plumagedfemalesduring all
stagesexceptnonbreeding(Fig. 3d).
CORTICOSTERONE
cantlyfrommonthto monthandwith handling
time (Fig. 4b); however,there were no significant differences between adult- and juvenal-
plumagedbirds (Table2A). As with the males,
corticosteronelevels in females were higher
during the breedingseasonthan during the
Effectof season.--Although
mostof the variancein corticosteronewas due to handling time,
nonbreeding season.
Effectof nestrole.--Averageplasmacortico-
628
MAYS,VLECK,ANDDAWSON
Males
[Auk, Vol. 108
Females
2.0'
2.5
c
i• Adult
;] Adult
AJuv
2.0
e
o
o
0,5
e
0.5
o.g
O;N•D•J
•F •M•A
Non2.5
Breeding
•M•J
Neet
Innu-
Building
batlnu
•J •A
Neet
Incu-
BreedingBuildln•lbating
Young
b
Feeding
Young
2.0
=AdBr,
A Juv H
Non-
Feeding
I
:
,
T
{).5'
0.5
0.0
-50
0
50
Time relative to first egg, days
Fig.3. Meanplasmaluteinizinghormonelevelsin Harris'Hawk males(a andb) andfemales(c andd)
in eachmonth(top)or duringeachneststagefor thoseindividualsfor whom nestrole is known(bottom).
Symbolsand statisticsas in Figure 1.
sterone levels did not differ significantly between nest roles.The only statisticallysignificant variation
in corticosterone
levels we could
accountfor in this data setwas due to handling
time (Table 2B), although the effectof nest role
approachedsignificancein males (P = 0.052).
Corticosteroneis the major adrenocorticoidin
birds associated with stress, and an effect of
handling time has been demonstratedin several other species(reviewed in Harvey et al.
1984).
BODY MASS
affectedbody mass.Breedingadults were significantly heavierthan adult helpers(BON, t =
2.03, P < 0.05). During the nonbreedingand
nest-buildingstages,breeding femaleshad a
mean massof 1,100 g (n = 10, range:975-1,225
g), but the helper femalesaveragedonly 990 g
(n = 7, range:925-1,050g). Aswith males,body
massdecreasedthough the breeding seasonin
the adult breeding females(Fig. 5b).
DISCUSSION
INTERSPECIFIC COMPARISONS
PlasmaLH levels in breeding male and female Harris' Hawks are generally lower than
levels in breeding membersof the samesex in
nificant effect (Table 2E). Males were heaviest most other speciesstudied (e.g. Lincoln et al.
during the nonbreeding seasonand massde- 1980, Silverin and Wingfield 1982, Dufty and
creasedthroughout the nesting seasonin both Wingfield 1986,Hiatt et al. 1987). In addition,
helpersand breeders(Fig. 5a).In adult females, T levels in breeding male Harris' Hawks were
both behavioralrole and neststagestatistically lower than thosein breeding malesduring the
In adult male Harris' Hawks, there were no
differencesbetween the body massesof the
helpers and breeders,but nest stagehad a sig-
July1991]
Hormones
in Cooperative
Breeders
100
a
629
Non-
Melee
Nest
Breeding
{3 Adult
ß
80
Incu-
Building
Feeding
bating
Young
I
Males
Juv
Ad Br
800
Ad H
Juv H
60'
40'
700.
20'
0
O
N
D
J
F
M
A
M
J
J
A
600
-100
-50
0
50
100
Femelee
Adult
NonBreeding
Nest
Building
Incubating
Feeding
Young
b
t2oo.
Females
o
Ad Br
i
Ad H
30ttO0.
i
!
I
10'
tOO0
O
N
D
J
F
M
A
M
J
J
A
Fig. 4. Mean plasma corticosteronelevels in male
(a) and female (b) Harris' Hawks in each month. Val-
ues for adult-plumagedand juvenal-plumagedbirds
are plotted separately.Symbols and statisticsas in
Figure 1.
nesting seasonin most monogamousand polygamousspecies(e.g. Wingfield and Farner
900
,.
-100
-50
.
ß ....
0
,
....
50
100
Time relative to first egg, days
Fig. 5. Mean bodymassin male (a) and female(b)
Harris' Hawks during eachnest stagefor thoseindividualsfor whom nestrole is known.Symbolsand
statisticsas in Figure 1.
1978b, 1980; Lincoln et al. 1980; Silverin and
Wingfield 1982;Wingfield 1984a,b; Fivizzani
et al. 1986;Fivizzani and Oring 1986;Hegner
and Wingfield 1986a, b; Ball and Wingfield
1987). Low LH levels, similar to those in Harris'
Hawks,arefoundin breedingpolyandrous
male
Spotted Sandpipers (Actitis macularia;Rissman
Relatively low lvels of LH and sex steroids
seemto be found in those speciesthat are not
strongly territorial such as the Spotted Sandpiper and Mallard or those that pair for life or
return to the sameterritory year after year, such
as the Western Gull. For instance,Wingfield et
and Wingfield 1984)and in Pied Flycatcherfemales(Ficedulahypoleuca;
Silverin and Wing-
al. (1987) correlated the low T levels found in
field 1982). Levels of T in Harris' Hawks are
only slightly lower than concentrationsin the
Spotted Sandpiper and are similar to levels re-
tition
portedin the Mallard (Anasplatyrhynchos;
Donham 1979) and male Western Gulls (Larusoccidentalis
wymani;Wingfield,Newman, Hunt, and
Farner 1982). Plasma T and E levels are lower
male Western Gulls with low levels of compebetween
males
for mates and nest sites.
Relatively low levels of LH and sexsteroidsare
alsofound in sometropicalspecies(e.g. Dittami
and Gwinner 1985, Dittami 1986, Reyer et al.
1986).Severalof thesecharacteristics
apply also
to the Harris' Hawk, such as their generally
tropical distribution (southwestern United
in breedingHarris' Hawks than in the captive- Statesto Argentina and Chile), year-round resbreeding American Kestrel (Falcosparverius; idency,and long-term pair bondsbetweenbirds.
Rehder et al. 1986, 1988).
Bednarz (1987a) described the Harris' Hawk
630
MAYS,
VLECK,
ANDDAWSON
in New Mexico as not obviouslyterritorial. In
contrast,Dawsonand Mannan (1991b)reported
that groupsin Arizona resideon nestingterritoriesall yearand continuouslydefendat least
a portion of their territory, and that all group
[Auk,Vol. 108
ENDOCRINE DIFFERENCES BETWEEN
HELPERS AND BREEDERS
Understandingwhy (both mechanistically
andfunctionally)helpersdo not breediscentral
members participate in this defense to some to understandingthe evolution of cooperative
degree.Aggressiveencounters(attacking,chas- breedingsystems,
becausethe lackof breeding
ing, and foot grabbing)occurbetweenmembers would seemto producea heavy costin terms
of differentgroupsduring the winter (Dawson of direct fitness(Woolfendenand Fitzpatrick
and Mannan 1991b)but to a lesserdegreethan 1977, Brown 1978, Emlen 1984). We first exin intraspecificterritorial disputesin other rap- amineseveralalternative,but not mutuallyextors (de Vries 1975, Newton 1979). Members clusive,hypothesesthat could accountfor the
from morethan onegroupmay hunt, feed,and lack of breeding in helper Harris' Hawks and
perchtogetherduring the winter (Mader 1975b, then discussour interpretationof our hormonal
Whaley 1986,Dawsonand Mannan 1991b).The datafrom breedingand helping Harris' Hawks
relatively low amplitude of T cyclesin male in the light of these hypotheses.We propose
breeding Harris' Hawks comparedwith other that the proximate and ultimate causesfor the
speciesmaypartly reflectthe relativelylow lev- lack of breeding in Harris' Hawks are not the
el of conflictpresentin territorialdisputes.The samefor all helpersin the group.
rise in T during the nest-buildingstageis preReproductive
maturity.--Absenceof breeding
sumablyassociated
primarilywith nestdefense, by helpers could be due to incompletematusperm production and copulatorybehavior.
ration and not a particular socialfactor.Lack of
Among female Harris' Hawks, T levels are breedingand low reproductive-hormonelevels
elevatedonlyin alphafemalesandonly during found in mostjuvenal-plumagedhelperscould
the nest-building stage. In other species,fe- be simply due to their age.Both sexesof Harris'
malesshowelevatedT levelsonly when they Hawks, however,have been reportedto breed
participatein territorialdefense(Wingfieldand while still in juvenal plumage (Mader 1975a,
Farher 1978b,Rissmanand Wingfield 1984). Whaley 1986,Dawsonand Mannan 1991a,Lett
Harris' Hawk breeding females participate in pets. comm.), and one juvenal-plumagedmale
territorial defenseand are especiallylikely to we sampledhad a T level higher than the mean
exhibit aggressive behavior toward other
value for breedingmales(Fig. 1). Clearly posbreedingfemalesor nestpredators(Dawsonand sessionof juvenalplumagedoesnot necessarily
Mannan 1991b). Unlike Western Gulls, in which
mean that a bird is sexuallyimmature.
femaleshavelevelsof T equivalentto thoseof
Reyeret al. (1986)rejectedthe hypothesisthat
the males, T levels in Harris' Hawk females, the low T levelsin (usuallyyounger)primary
althoughelevated,are significantlylower than helpers of the cooperativelybreeding Pied
thoseof the males.Levelsof T in female helpers Kingfisher(Cerylerudis)were due to incomplete
are not elevatedduring nest building, and fe- maturation. They found that T levels did not
male helpersare muchlesslikely to defendthe necessarilycorrelatewith age but with helper
nest (Dawson and Mannan 1991b).
status.In addition, some primary helpers are
As in mostmonogamousspeciesstudied,ste- failed breeders that have returned to their natal
roid levels fell in breeding Harris' Hawks of territories. In other cooperatively breeding
both sexes at the onset of incubation. Elevated
speciesthat previouslywere thought to exhibit
T levels are thought to be incompatiblewith delayed maturation, it is now known that firstparentalcarein males(Silverin and Wingfield year individuals can and do breed under ap1982; Hegner and Wingfield 1986a, 1987a; propriate circumstances(Stallcup and WoolfenWingfield and Moore 1987). Estradiol-17fllev- den 1978, Koenig and Mumme 1987).
els decreasefollowing egg laying in the AmerBehavioral
suppression.--Helpers
may not breed
ican Kestrel(Rehderet al. 1986),as they do in because of behavioral interactions with the
breedingfemaleHarris'Hawks,althoughE does breeders(e.g.mateguarding)eventhoughthey
not necessarilydecreaseat the onset of incu- are physiologicallyreadyto do so.The ultimate
bation in all species(Donham 1979,Schwablet reasonfor this may be that dominant breeders
al. 1980,Wingfield 1984a).
have an interestin protectingtheir geneticin-
July1991]
Hormones
in Cooperative
Breeders
631
vestmentby interfering with, or not cooperating in, mating attemptsby helpers. Most, but
not all, adult-plumagedmale Harris' Hawks-whetherbreedersor helpers--haveelevatedLH
and T during the nest-buildingstage.Thus,most
adultmalehelpersappearreproductivelyready,
basedon LH and T levelsindistinguishable
from
vary with the relatednessof the helper to the
breedersbecauserelatednessaffectsthe prob-
those in breeders at the same time. In fact, adult
A helper relatedto the breederof the opposite
sex should not ascendto breeding statusbecausedoing so would risk inbreeding and po-
helpermalesoftenattemptto copulatewith the
alphafemale,and their apparentlackof success
is due mainly to her lack of cooperation.In 46
observationsof mounting of the alpha female
by the alpha male, copulationwas completed
in 44, whereasonly 1 in 22 observedmountings
by beta malesappearedto be successful(Daw-
ability that a helper can becomea breeder in a
nonconsanguineousmating. In monogamous
groups,a helper unrelatedto the breederof the
oppositesexcouldascendto breedingstatuson
the departureof the alpha bird of the samesex.
tentially reduce the inclusive fitness of both
birds (although the adverseeffectsof inbreeding in birds are controversial;cf. Greenwood et
al. 1978,Craig and Jamieson1988). If inbreeding is avoided, ascent of a related helper to
sonand Mannan 1991a,pers.obs.).Femaleswill breeding statuswould require the lossof both
occasionallycopulatewith more than one male, breedersfrom the group: lossof one to free a
which results in some polyandrousmating breeding slot and loss of the other to avoid
groups(Mader 1979,Whaley 1986,Sheehyet inbreeding.Thus, while the energeticcostsof
al. MS).
becomingphysiologicallyready to reproduce
Physiologicalsuppression.--Alternatively,
helpersmay be sexuallymaturebut not physiologicallyreadyto breed(i.e.with inactivegonadsand low levelsof reproductivehormones).
In Harris' Hawks, all helper femalesand most
juvenal-plumagedmale helpers appear to be
physiologically
unpreparedfor breeding,based
would
on very low levelsof LH, T, and E. At the same
time, these hormones were elevated in breeders
and adult-plumagedmale helpers.Physiological readinessto breedcouldbe constrainedby
factorssuchaspoorbodycondition,or it could
be the result of social interactions between birds.
For instance,physiologicalinhibition could re-
suitfromstressdueto dominationby the breeder of the samesexto assureits geneticparentage
(Reyeret al. 1986).Forexample,an alphafemale
might dominate a potentially competingfemale, causing hormonal suppressionin the
helper and preventing breeding.On the other
hand, physiologicalinhibition couldoccurdue
to the presenceof the parentof the opposite
sex,
be the same for both related and unre-
latedhelpers,the probabilityof receivingany
benefit from this readiness would be much low-
er for a helper related to the breeder of the
oppositesex.This leadsto a prediction:if we
assumethat opportunitiesto breed outsidethe
breedingunit are few, helpersthat are related
to the breederof the oppositesexshouldbe less
likely to invest in reproductivereadiness(gonad growth, gamete production,costsof carrying and maintainingreproductivetissues,etc.)
than helpersthat are unrelatedto the breeders.
(This energeticargument is analogousto that
which wasbeenusedto explainthe regression
of gonadsin seasonal
breedersduring the nonbreeding seasonwhen chancesof successfulreproduction are slim).
The pattern of LH and sex steroid levels we
observedin Harris' Hawk helpersis consistent
with the hypothesisthat inbreedingavoidance
is an important ultimate selectivefactor determining their reproductivereadiness(exceptin
presumablyas a result of selectionto avoid in- adult femalehelpers,seebelow).Mostjuvenalbreeding.Under this hypothesis,physiological plumagedHarris' Hawks (•75%) are helping
readinessto breed would dependprimarily on theirownparentsandarenothormonallyready
the relatedness
betweenhelpersand breeders, to breed with the opposite-sex
parent even if
rather than on age or statuswithin the domi- the same-sexbreederdisappeared.In contrast,
nancehierarchy.Of course,physiological
sup- mostadult-plumagedmalehelpersarenot helppressionof reproductioncouldbe due to a com- ing their own parents(• 80%).We suggestthat,
bination
of these factors.
for thesebirds,the costof becomingreproduc-
Behavioralvs. physiological
suppression.--We tively readyduring the breedingseasonis more
suggestthat whether behavioralor physiolog- than offsetby the potentialbenefitsto be deical suppression
of breedingoccursis likely to rived from either occasionalsuccessfulcopu-
632
MAYS,VLECK,
ANDDAWSON
lations with the breeding female or attainment
of alpha status.Thoseadult helperswhoseLH
and T levels were not elevated during the nestbuilding stagewere presumablynot reproductively ready, and they were possibly related
gammahelpersrather than unrelatedbetahelpers.For instance,one of the six adult-plumaged
male helperswe sampledduring the nest-building stagehad a T value in the samerange(<15
pg/ml) as all the juvenal-plumagedmale help-
[Auk, Vol. 108
er than that for the male helpers in Harris'
Hawks. The costof recrudescencein a 1,000 g
female bird (growth of oviduct and functional
but nonovulating ovary) is probably ca. 100150%of a single day'sbasalenergyexpenditure,
whereas
estimates
of the costs of testicular
re-
crudescence
in male birds range from only 7%
to 40%(basedon data in Walsberg 1983). Helpersin other cooperativelybreedingspeciesmay
be constrainedto help rather than breed beers on their natal territories.
The other adultcausethey are energeticallyincapableof attainplumaged males,whether helpers or breeders, ing breeding condition (Brown 1983). Unsuchad T values 2-70 times higher than related cessfulbreeding has been attributed to a less
juvenal-plumagedhelpers.We do not know the than adequateweight gain in femalesfor many
relatedness
of thisadult-plumagedhelperwhose wild and captive species including raptors
T value was low. We do know that the only (Newton 1979, Hardy et al. 1981, Rehder et al.
juvenal-plumagedhelper who was known not 1986), and reduced food intake has dramatic
to be helping on its parents'territory was the antigonadal effects(see Wingfield 1983 for reonly such bird with high sex steroid levels (T view) or results in lower reproductive output
> 900 pg/ml).
(Drent and Daan 1980) in all avian speciesinvestigated.For instance,poor body condition
(i.e. low fat depositsand body mass)resultsin
MECHANISMS FOR PHYSIOLOGICAL
low circulating levels of T in male Song Sparrows (Melospizamelodia;Wingfield 1985).
Poorbodycondition.--Adultfemale helpersdo
Dominancesuppression.--Onthe other hand,
not appearto be reproductivelyready to breed dominancebehaviorby alphafemalescouldreeven though they are unlikely to be on their sult in physiologicalsuppressionof reproducnatal territory. These birds also weigh signifi- tion in adult female helpers either directly or
cantly less than breeding females. In contrast, indirectly. For instance, subordinate females
male adult helpers and breedersdo not differ may have low accessto resourcesdue to their
in mass. In fact, these female helpers weigh low rank in the dominancehierarchy.An adult
• 10%lessthan the breeding femalesduring the female helper that is capable of reproducing
6-7 weeks before the first egg, when gonadal may pose a greater threat to the alpha female
developmentis probablyoccurringin thosefe- or to groupstabilitythan a reproductivelyready
males that becomebreeders.The greater mass adultmalehelper,possiblybecausetwo or more
in the female breeders comparedwith female laying femaleswould increasethe number of
helpersis not likely to be simply due to having chicksto be raised.One normal-sizedbroodmay
eggs in the oviduct. Body massesof laying be all a Harris' Hawk group can care for (FaaAmerican Kestrelsexhibited distinct peaksrel- borg and Bednarz 1990). In the Acorn Woodcompetition
ative to nonlaying females, but only for ap- pecker (Melanerpesformicivorous),
proximately 1 week before and 1 week after egg among communally nesting females is greater
laying (Rehder et aL 1986). The low hormone than that among males and decreasesthe relevels in the adult female helpers during the production of groups significantly more than
early nesting stagesmay be due to poor body doesmale-malecompetitionin the group (Koeconditionrather than to any socialsuppression. ning et al. 1983). Dominant females in a group
Adult-plumaged female helpers do not usually can suppressreproductiveoutput in birds (e.g.
remain with a group for > 1 yr, and have never Jamiesonand Craig 1987), and a similar phebeen observedto replacean alpha female(Daw- nomenon is seen in some mammals (Wasser and
sonand Mannan 1991a).It maybe that they join Barash 1983 and references therein).
a group primarily to benefit from group huntMechanisms by which breeding females
ing (Bednarz and Ligon 1988) rather than to might suppressreproduction in adult female
actively participate in reproduction.
helpers are not clear. One might predict that
The cost/benefitratio of becomingreproduc- the mechanism of (or a correlate of) dominancetively readyin femalehelpersis probablygreat- induced hormonal suppressionwould involve
SUPPRESSIONOF REPRODUCTION
July1991]
Hormones
in Cooperative
Breeders
633
the adrenocorticoids,which are normally ele-
peckers(Koenig and Pitelka 1979,Koenig et al.
1983) and Florida Scrub Jays (Aphelocoma
coerone levels in females did not differ between
rulescens;
Woolfenden and Fitzpatrick 1978)
breedersand helpers,however, and thus levels show well-developed behavioral patterns to
were not correlated with the subordinate status
avoid closeconsanguineous
matings,but nothand reproductivehormonesuppression
of adult ing is known of the hormonalstatusof the nonfemalehelpers.If reproductive-hormone
levels breeders in these species.The likelihood that
are suppressedin helpersbecauseof their sub- othermaleswill cuckoldthe alphamale,or othordinate status it must work via some mechaer females will parasitize the alpha female,
nism other than adrenocorticoid-induced
inshould be greater when the individuals inhibition.
volvedareunrelated(Koenig1981,Faaborgand
vated with stress (Deviche 1983). Corticoste-
In juvenal-plumaged
helpers,we suggestthat
the breeding birds do not directly causehormonal suppressionvia dominance.Rather, we
Bednarz 1990). Whether this results from a hor-
monal suppressionin relatedbirdsis unknown.
Hormone data for Pied Kingfisherhelpersare
believe that relatedjuvenal-plumagedhelpers alsoconsistentwith inbreedingavoidance.The
remain reproductively inactive to avoid in- Pied Kingfisherhas two types of helpers:pribreeding.Lackof evidencefor dominancesup- mary and secondary (Reyer 1980). Primary
pressionis of two types. First, corticosterone helpersare offspringof the breeding pair from
levelsin thejuvenal-plumaged
maleswerelow- a previous year, whereassecondaryhelpers are
er, not higher, than those in the adults, which not related to the breeders(Reyer 1986). Priagain does not support their involvement in mary helpers are associatedwith the breeders
hormonalsuppression.
Second,moststudiesthat throughoutthe entire nestingcycle.In contrast,
correlatehormonelevels with degree of dom- secondary
helpersaretoleratedby the breeders
inance have indicated that subordinate individonly after the younghatchand then only when
uals do not differ from dominant individuals in
the parents' feeding capacitiesare exceeded
sex-steroidlevels once socialrelationshipsbe- (Reyer1984,Reyerand Westerterp1985).Reyer
tween birds have become well established, alet al. (1986) found that before egg laying, secthough they can differ in corticosteroidlevels ondary helpers have T levels similar to the
(Balthazart et al. 1979, Tsutsui and Ishii 1981, breeders,whereasprimary helpers have T levRohwer and Wingfield 1981). Similar condi- els significantlylower. They attributed the low
tionshavebeenfoundin free-rangingoliveba- levelsof T in the primary helpersto dominance
boons(Papioanubis;Sapolsky1987). Levels of suppressionby the breeding males.Their hortestosteronecan play an important role in de- monedata are alsoconsistentwith the hypothtermining statusin the first place(Ramenofsky esisthat reproductive hormonesare suppressed
1984,Hegner and Wingfield 1987b)and T levels in the primary helpers becausethe potential
increasein male birds following repeatedin- mate is also a parent. Primary helpers are, of
tense aggressiveinteractions with other males course,alsosubordinateto their parents,sothese
(Searcy and Wingfield 1980, Wingfield and two hypothesescannotbe distinguishedin this
Moore 1987). Harris' Hawk group hierarchies, case.
Reyer's (1986) behavioral data provide addihowever,arewell established
andstableby the
nestingseasonin March with little aggression tional support for inbreeding avoidance.In 7
displayed between members (Dawson and casessecondaryhelpershad an opportunityto
Mannan 1991b).
breedin a slotvacatedby the malebreederthey
Inbreeding
avoidance.--Iflow T levels in birds helped. In each of the 7 casesthe secondary
helping on their natal territories are related to male helper moved into the vacated slot and
inbreeding avoidance,it shouldbe possibleto bred with the widowed female that was not his
identify a link betweenkin recognitionand re- mother. In 6 casesprimary helpers had an opproductiveinhibition, but little is known about portunityto moveinto a slotvacatedby a breedhow birdsrecognizerelativesor how this affects er. In 4 of the 6 casesthe primary helper disphysiologicalprocesses.In Harris' Hawks, LH persedandultimatelybredwith anotherfemale,
concentrations
in differenttypesof helperspar- and in 2 caseshe moved into the vacated poallel concentrations of T, thus the mechanism sition. In the 4 casesof dispersal,if the helper
is presumablycentral and actsabove the ante- had assumed the vacated slot, he would have
rior pituitary/hypothalamic axis.Acorn Wood- mated with his mother; in the 2 cases where
634
MAYSß
VLECK,
ANDDAWSON
the primary helper bred with the widowed female, she was not his mother.
The hormone
levels of these individuals are not known, but
it may be that primary helpers have high T
levels,similarto the secondary
helpers,if they
are not helping their own mothers.
[Auk,Vol. 108
steroid hormonesin relation to multiple-broodedness and nest-site density in male starlings.
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In Harris' Hawks,physiologicalsuppression --,
R. MASSA,& P. NEGRI-CEsI.1979. Photopeof reproductivereadinessin helperson their
riodic controlof testosteronemetabolismß
plasma
natal territoriesand the lack of suchsuppresgonadotrophins,cloacal gland growth and reproductivebehaviourin the JapaneseQuail. Gen.
sionin helpersnot on their natal territoriesare
Comp. Endocrinol.39: 222-235.
consistentwith the hypothesisof inbreeding
avoidance.Physiological
readiness
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success,
polyandry,and cooperativebreedingin
but not sufficientfor a helper to breed.ReproHarris' Hawks. Auk 104: 393-404.
ductively ready male helpersare presumably
1987b. Successivenesting and autumnal
not often able to breed because of behavioral
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Mannan 1991a).In our study,the one juvenalplumaged male with high T did not breed after
leaving his natal territory, presumablybecause
of his low socialstatusin his new group. Inbreeding avoidance also does not account for
breeding in HarrisßHawks. Auk 104: 85-96.
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breedersin the group. Either poor body con-
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1191.
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J. D. 1980. The reproductiveecologyof
a Texas Harris ßHawk (Parabuteounicinctusharrisi)
ACKNOWLEDGMENTS
We thank all thoseindividualswho helpedwith
the fieldworkßincluding Rick Bowers,Ellen Weintraub, JeffWhite, Lynn Oliphant, BobScheibe,and
other membersof the TucsonAudubonSociety.We
acknowledgethe loan of equipmentfrom OscarWard,
Holly Hobart,Mable Mays,and StephenRussell.Bill
Mannan, Dave Vleck, StephenRussell,John B. Dun-
population.M.S. thesisßAustinßUniv. Texas.
BROWN,J. L. 1978. Avian communalbreeding systems.Annu. Rev. Ecol.& Syst.9: 123-156.
1983. Cooperation--a biologistßsdilemma.
Adv.
Stud. Avian
Biol. 13: 1-37.
ß 1987. Helping and communalbreeding in
birds. Princeton, Princeton Univ. Press.
., & E. R. BROWN. 1981. Kin selection and in-
dividual fitnessin babblers.Pp. 244-256 in Nat-
ningßRon Mumme, Jetram Brown, Jim Bednarz, and
ural selection
M. E. Morbeckcriticallyreadthe manuscript.
Richard
and new theory (R. D. Alexander and D. W. Tin-
Strauss offered invaluable
kle, Eds.). New Yorkß Chiron Press.
advice on statistics. We are
and social behavior:
recent results
L. H., & D. AMADON. 1968. Eagles,hawks
indebtedto JohnC. Wingfield in whoselaboratory BROWNß
the luteinizing hormone measurementswere made.
Early in the study,fundswere providedby Arizona
Wildlife
Foundation, James R. Silliman Memorial
Fund, SigmaXi, and WesternBird BandingAssociation to Nora Mays. Major funding was provided by
NSF grant BSN-8606548to Carol Vleck.
and falconsof the world. London, Country Life
Books.
CORTEN,P. J. M. 1973. Through method and machination. Captive Breeding Diurnal Birds of Prey
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CRmG, J. L., & I. G. JAMmSON. 1988. Incestuous mat-
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