July2001]
APPENDIX.
ShortCommunications
785
Basalmetabolicrate (BMR) and body mass(rob)in herbivorousbirds.
BMR
mb (g)
(mL/O2
/g h)
Anasplatyrhyncos
Anasgibberifrons
Anas rhynchotis
741
391
480
0.82
0.77
0.80
Anas aucklandica chlorotis
Species
References
Anatidae
529
0.79
Anas castaneas
Anser anser
944.1
3250
0.78
0.60
Aythyafuligula
Anaspenelope
Tadornavariegata
Cygnusbuccinator
611
723
1199
8880
0.86
0.70
0.61
0.41
1253
0.87
96
412
519
944
1.47
0.89
0.87
0.66
Branta bernicla
Ralidae
Crex crex
Fulica atra
Gallinula tenebrosa
Gallinula mortierii
Porphyrio
porphyrio
Porphyrio
mantelli
Daan et al. (1990)
McNab (1994)
McNab (1994)
McNab (1994)
Hinds et al. (1993)
Kendeighet al. (1977)
Daan et al. (1990)
Kendeighet al. (1977)
McNab (1994)
Benedict and Fox (1927)
Daan et al. (1990)
Kendeighet al. (1977)
Kendeighet al. (1977)
973
2764
0.71
0.44
McNab
McNab
McNab
McNab
(1994)
(1994)
(1994)
(1994)
598
0.48
Grajal A. (1991)
2500
0.52
Vehrencampet al. (1989)
Cuculidae
Opisthocomus
hoazin
Tetraonidae
Centrocerus
urophasianus
Emberezidae
Saltator coerulescens
Saltator orenocensis
47
32.7
1.49
1.72
Bosqueet al. (1990)
Bosqueet al. (1990)
Phytotomidae
Phytotomarara
41.6
2.47
this study
TheAuk 118(3):785-789, 2001
Functionand TemporalVariation in Use of Ossuariesby BeardedVultures
(Gypaetusbarbatus)During the Nestling Period
ANTONI MARGALIDA• AND JOAN BERTRAN
Groupof StudyandProtection
of theBearded
Vulture,Apdo.43, E-25520El Pontde$uert(Lieida),Spain
ABSTRACT.--We
analyzethe useand functionality
of ossuariesby the Bearded Vulture (Gypaetusbarbatus)in the Pyreneesduring the nestlingperiod. In
71% of cases,the ossuarywas used to prepare food
for chicks,in 11% for storingfood, and only in 18%
for preparing the adults' own food. Pairsused an average of two ossuariesat a mean distancefrom the
nest of 789 m (SE _+377). The averagetime dedicate
to breaking bone was 5.3 min (SE _+4.2) and 4.5
throws (SE _+5.8) for each sessionin the ossuarie(n
= 86). The temporalvariationfound in the useof the
ossuaries,with maximum frequenciesbetween 31-
90 days of age of chicks,may be due to a possible
qualitative variation in chicks'diets. Ossuariesare
also used to store food, this being a differentiating
and advantageoustrait with respectto feeding behavior developedby other meat scavengers.
BeardedVultures(Gypaetus
barbatus)
feed mainly
on the carcasses of medium-sized
E-mail: [email protected]
domestic and wild
ungulates(Hiraldo et al. 1979).Althoughmostof the
786
ShortCommunications
[Auk,Vol. 118
TABLE1. Useof bonebreakingsitesor ossuaries
by BeardedVulturesin relationto the ageof their chick
Percentagesappearsin parentheses.
Food-handling
sequence
Searching-breakingnests
Nest-breaking-nest
Ossuary-breakingnest
Searching-breakingconsumptionby adult
Nest-breakingconsumptionby adultabandoned
food
1-30 days
31-60 days
61-90 days
91-fledging
Total
2 (12)
7 (41)
30
28
6 (46)a
1 (8)
14 (48)
8 (27.5)
8 (23)
12 (34)
2 (15)
4 (14)
3 (9)
0
1 (8)
1 (3.5)
4 (11)
4 (23)
10
1 (8)
1 (3.5)
3 (9)
2 (12)
7
9
at
ossuary
Total
2 (15)
13
1 (3.5)
5 (14)
29
2 (12)
35
10
17
94
Seetext for explanation.
skeletonof thosespeciesmay be consumed,vultures
preferentiallyselectthe longerbones.Adult individuals ingest bonesup to 250 mm long and 35 mm
wide without apparentdifficulty(Brown1988).They
resolvethe problemof ingestinglargerbonesby the
use of bone-breakingsites,or ossuaries.
Thosesites
are rocky surfaceswhere BeardedVultures deliberately and repeatedlythrow the remainsfrom the air
until theybecomefragmentedor disjointed(Huxley
and Nicholson1963).Although someossuariesmay
be usedonly occasionally,
individualstypicallyhave
specificsites at their disposal, close to the nest,
where bonebreakingtakesplaceregularly.
Althoughossuariesare used year round by territorial adults,the importanceof thosesitesis heightened during nestling(Heredia 1991).Studiesof vulture activity at ossuariesincludegeneraldescriptions
of behavior(Boudoint1976),the physicalcharacteristicsof the ossuaries(Brown 1988,Heredia 1991),the
kinds of remains encountered(Heredia 1974, Brown
and Plug 1990),and the intra- and interspecies
interactionsthat occurthere(Bertranand Margalida1996,
methodfor determiningthe possibletemporalvariation in the diet, on which no information exists.
Here we analyze the function of ossuariesand
quantifytheir usein relationto the ageof chicks.
Studyareaandmethods.--This
studywasconducted
in the centralPyreneesin northeastSpain,from 1992
to 1997.Data obtainedduring the study of the species'breedingbehavior(BertranandMargalida1999,
Margalidaand Bertran2000a,b) correspondto observationsmade on sevenbreedingpairs (265 _+SD
= 157 h/pair, range 50 to 492 h). This area has one
of the highest densitiesof Bearded Vultures in the
Pyrenees(Garcfaet al. 1996),and apparentlyhassuf-
ficientfood resources
to coverthe annualenergetic
needsof the breedingpairs (Margalidaet al. 1997).
BeardedVultures are solitary breedersthat nests
on large rocky outcrops(Hiraldo et al. 1979).Each
pair generally has one to four ossuariesavailable
within its territory (Heredia 1991).
Observationstotalling 1,852h were made using
20-60x field telescopes
from vantagepointsdominating the nestingsitesat 300 to 600 m from the cliff,
1997).
from
Although it is generallyassumedthat 70 to 90% of
BeardedVultures'foodis composedof boneremains
(Brownand Plug 1990),49% of the remainsbrought
to onenesthad a high proportionof meat(Margalida
and Bertran1997).Likewise,Brownand Plug (1990)
observedthat 12%of the remainsbroughtto thenest
were from meat (n = 65) and that 73% of those remains were broughtduring the first three weeksafter hatching.Thoseauthorsalsoobservedthat 6% of
remainscollectedby adults at feeding stations(n =
viewed simultaneously.Given the distanceat which
70) were from meat and that all of them were selected
which
both
ossuaries
and
nests
could
be
observations
weremade,it wasnot possibleto identify the differenttypesof remainsdroppedontoor
gatheredfrom thebone-breaking
sites.Thenestling
period was considered as the time period from
hatching(Februaryto March) until fiedging(Juneto
July).In the studiedpairs,themeanageof thechicks
at fiedgingwas 117.6_+3.2 days(range113to 122,n
= 7).
To examine
variation
in use of ossuaries in relation
to ageof chicks,the nestlingperiodwassubdivided
during the breedingseason.Thoseresultssuggest into four 30 day periods.The activitiesdevelopedby
existence
of differences
betweendietduringnestling the adults at the ossuarieswere groupedas follows
period and the remainder of the year. However, in- (Table1): SBN:Returnfrom foodsearching
with food
formationon diet of chicksis scarce(BrownandPlug remains,breakingfood, and bringing it to the nest.
1990, Thibault et al. 1993, Margalida and Bertran NBN: Leaving the nestwith food remains, breaking
1997)and the studyof activityat the ossuaries
is one food, and bringing it back to the nest.OBN: Collec-
July2001]
ShortCommunications
787
lOO
90
80
70
=
60
o•
50
•
40
30
20
10
I
II
IV
III
Nestling period (month)
FIG. 1. Temporalvariationin the useand functionalityof the bone-breakingsites,or ossuaries,for preparing food. White columns:preparationof food for the chick;grey columns:preparationof food for the
adult; black columns:storageof food. Chi-squaretest:*** P < 0.01;* P < 0.05.
tion of remains from the ossuary,breakingfood, and
bringingit to the nest;or collectionof remainsfrom
the ossuaryand bringingthem to the nest.SBCA:Return from food searching
with remains,breakingfood,
and consumption
by the adult;or collectionof remains
from the ossuary,breaking them, and consumption
by the adult; or collectionof remains from the ossuaryand consumptionby the adult. NBCA:Leaving
the nestwith food remains, breakingfood, and consumptionby the adult.AO: Abandoning
food remains
at the ossuary,or breaking the remainsand abandoning food at the ossuary.The remains abandoned
couldbe recoveredthe sameday or severaldayslater
and that behaviorwas consideredfood caching.
Observation times were standardized among
pairs. For comparisonsbetween periods, we determined a rate of daily useof the ossuary(numberof
bone-breakingsessionsper hour) for eachobservation day and pair. Forthe statisticaltreatmentof the
data we used nonparametrictests (Sokal and Rohlf
1981).
Results.--We
witnessed
94 visits
to the ossuaries
(Table1), 71%of whichwere relatedto chickfeeding,
18%of which were relatedto adult feeding,and 11%
of which involved food storage(Fig. 1). Monitored
pairs usedan averageof 2 + 0.58 ossuaries(range1
to 3, n = 7) at a mean distance from the nests of 789
+ 377 m (range 175 to 2,400,n = 14).
It took BeardedVultures an average5.3 + 4.2 min
(range1 to 17, n = 50) to break bones.During those
sessions,vultures dropped bones an average4.5 +
5.8 times (range 1 to 35, n = 86).
Bearded
Vultures
used ossuaries
less in the first
and fourth month of life of the chick (0.023 + 0.059
and 0.027 + 0.052 sessionsh-q/day, respectively)
than during the secondand third month (0.072 +
0.123 and 0.073 + 0.108 sessionsh •/day, respectively) (Kruskall-WallisH = 8.35, df = 3, P = 0.04).
Comparisonof the first and secondhalf of nestling
period (1 to 60 daysvs. 61 daysto fledging)showed
significantinversetendenciesin the proportionsof
the SBN an NBN scenarios (Fisher's exact test, P =
0.02).Although the mean time at bonebreakingsites
dedicatedto the preparationof food during the first
half of the nestlingperiodwaslower than during the
secondhalf (<60 days: 4.48 + 3.77 min, n = 27 vs.
>61 days to fledging:6.04 + 4.54 min, n = 23), the
difference was not statisticallysignificant (MannWhitney U-test, U = 231, NS).
Discussion.•Our observationssuggestthat during
the nestlingperiod, ossuariesare used mainly for
adapting the size of the food items to the needsof
the chickand, to a lesserdegree,for the preparation
of the adults'
own food.
The temporalvariationin use of ossuariesmay be
due to a possiblequalitativevariation in chicks'diets. In captivity, chicksingestsmall bone fragments
combined
with meat within
a few hours after hatch-
ing (H. Frey pers. comm.).In the wild, meat as opposed to bone probably acquiresspecial relevance
788
ShortCommunications
during the first month of life. Mammalianbonehas
a higherenergeticcontentthan muscletissue(6.7vs.
5.6 kJ/g, Brown 1988) so selectionof meat as food
probablyis due to the chicks'limited ingestivecapacity. Although prey predictability also would
seemto conditionthepatternof selection(Margalida
and Bertran 1997) during the first few weeksafter
hatching,prey items delivered to the nest are generallyfoodremainscontainingfreshmeat.Thoseobservationsare consistentwith publisheddata (Brown
and Plug 1990),which,togetherwith the significantly lower frequencyof visits to the ossuariesduring
the first month of chickrearing, suggestthe presence
of meatprey itemsin the diet. In that respect,feeding
time investedby adults during the two weeksafter
hatchingis significantlylower (Margalidaand Bertran 2000a).
The fact that the use of the ossuaries
decreases
sharply in the fourth month of chickrearing might
be relatedto two factors.(1) The capacityof the chick
for ingesting bones is considerableat that time,
which would allow the adults to reducethe preparation time at the ossuaries;or (2) during that phase,
the seasonalmovementof livestockto new pastures
takesplace,making it the periodwhen the availability of foodis highest(Margalidaet al. 1997).The relative abundanceof food and the consequentspatial
and temporal predictability of searching for it,
would permit vultures to selectthe most adequate
types of remains,which might reducetime needed
for their preparation at ossuaries.
The hypothesisof temporalvariationin food quality also is supportedby the differencesobservedin
the behavior of the adults at ossuaries.Although
during the first two monthsfood is morefrequently
preparedbeforebeingcarriedto the nest(SBN),during the last two monthsit is usually prepared once
the remains have been brought to the nest (NBN).
Those differencescould reflect the fact that during
the first half of nestlingperiod, limitationsof the
chickfor ingestingbonesforcethe adult to prepare
the food prior to enteringthe nest.Meat remainsand
smallbonefragmentsare consumed
by the chickbut
generallyit is the adult who ingeststhe bones(A.
Margalida pers.obs.).The lowerproportionof bones
in the diet and use that the adults make of those,
mean t_hatthey accumulatelessin the nestand that
the NBN
scenario
is observed
less often. Neverthe-
[Auk, Vol. 118
ond half of the nestling period may be related to
chicks'higher energeticneeds and to the time investedin searchingfor food (Margalida and Bertran
2000a). The accumulationof food remains at the nest
and in ossuariesmakesthe adults' feeding easierand
allows them to maximize the time spent searching
for food for the chick.
Bearded Vultures occasionallyabandonfood remains
at ossuaries.
Traditional
ossuaries
allow
in-
dividuals to deposit and to recover remains when
food is scarce or when
adverse
weather
conditions
(principallysnowfall)limit flightsin searchof food.
Thus, ossuarieswould serveas predictablealternative food sources.That is possibledue to the maintenanceof that type of food in an edible condition,
whichhasbeenestimatedto be ten timeslongerthan
soft tissues(Houston and Copsey1994). That representsan important advantagewith regard to the
feedingbehaviorof othermeatscavengers.
However,
given the risk of piracy by conspecifics,
storageof
food in ossuariesis not very frequentand probably
occurs at ossuaries close to the nest which would al-
low them to be surveyedand defendedby the breeding pairs (seeBertran and Margalida 1996).
Our observations
may allowbettermanagementof
feedingstations,whichare usuallyprovisionedwith
boneremains.Although quantityof food availableis
not a limiting factor for breedingsuccess(Margalida
et al. 1997),food quality might be one.Provisionof
food to the feeding stationswith a higher meat content during the first weeks after hatching may increasebreeding success,given that most breeding
failuresin that speciestake placeduring that period
(A. Margalida pers. obs.).
Acknowledgments.--We
are grateful to J. Boudet,D.
Garcia, R. Heredia, and P. Romero for their assis-
tancein the field, and to H. Frey for contributinghis
observationson and experiencewith captive birds.
We are also grateful to K. Bildstein,A. Gamauf,J.J.
Negro, K. G. Smith, and an anonymousreviewerfor
commentson the manuscript.S. Cahill, J. Cancalosi
and S. Hardie translatedthe text into English.This
study was supportedby Departamentd'Agricultura
Ramaderiai Pescaof the Generalitatde Catalunya,
Fundaci6Territori i Paisatge,Minuartia EstudisAmbientals and a Life Project of the European Union
(94/E/A221/E/01126/ASJ).
less,during the secondhalf of the nestlingperiod,
increase in bone remains
in the diet leads to their ac-
cumulationin the nest. The greatercapacityof the
chickto ingestbonefragmentsmakestheprior preparation of bones at the ossuariesunnecessary,and
the increasedfrequencyof observationof the NBN
scenario would
be related
to the accumulation
of re-
mains at the nest and to the total use that the chick
can make of those.
The nonsignificantincreasein the use of ossuaries
by adults to prepare their own food during the sec-
LITERATURE
CITED
BERTRAN,
J., AND A. MARGALIDA.1996. Patr6n anual
de observacionesde Quebrantahuesos(Gypaetus
barbatus)de diferentesgrupos de edad en los
sectores de nidificaci6n.
Alauda
64:171-178.
BERTRAN,J., AND A. MARGALIDA.1997. Griffon Vul-
tures (Gypsfulvus) ingestingbonesat the ossuaries of Bearded Vultures (Gypaetusbarbatus)
Journalof Raptor Research31:287-288.
July2001]
ShortCommunications
BERTRAN,
J., AND A. MARGALIDA.1999. Copulatory
behavior
of the Bearded
Vulture.
Condor
789
HOUSTON, D.C.,
101:
AND J. A. COPSEY. 1994. Bone di-
gestionand intestinalmorphologyof the Bearded Vulture. Journalof Raptor Research28:73-78.
164-168.
BOUDOINT,
Y. 1976. Techniquesde vol et de cassage HUXLEY, J., AND E. M. NICHOLSON. 1963. LammerMeierGypaetusbarbatus
breaking bones.Ibis 105:
d'os chez le gypa•te barbu (Gypaetusbarbatus).
Alauda
106-107.
44:1-21.
BROWN,C. J. 1988. A study of the Bearded Vulture MARGALIDA,A., AND J. BERTRAN.1997. Dieta y selecci6nde alimento de una pareja de QuebranGypaetusbarbatusin southernAfrica. Ph.D. distahuesos
(Gypaetus
barbatus)
en los Pirineosdursertation,Universityof Natal, Pietermaritzburg,
ante la crianza.
South Africa.
BROWN,C. J., AND I. PLUG. 1990. Food choice and diet
of the Bearded Vulture Gypaetusbarbatusin
southern Africa. South African Journal of Zoology 25:169-177.
GARCfA, D., A. MARGALIDA, X. PARELLADA,AND J.
CANUT.1996. Parametrosreproductoresy evol-
Ardeola
44:191-197.
MARGALIDA,A., AND J. BERTRAN.2000a. Breeding
behaviourof the BeardedVulture (Gypaetus
barbatus):Minimal sexual differencesin parental
activities.
Ibis 142:225-243.
MARGALIDA,A., AND J. BERTRAN.2000b. Nest-build-
ing behaviourof the BeardedVulture (Gypaetus
barbatus).Ardea 88:259-264.
uci6n del Quebrantahuesos(Gypaetusbarbatus) MARGALIDA, A., D. GARCIA, AND R. HEREDIA. 1997.
en Catalufia(NE Espafia).Alauda 64:229-238.
Estimaci6nde la disponibilidadtr6fica para el
HEREDIA, R. 1974. Nota sobre la alimentaci6n del
Quebrantahuesos
(Gypaetus
barbatus)
en CataluQuebrantahuesos(Gypaetusbarbatus).Ardeola
fia (NE Espafia) e implicacionessobre su conservaci6n.
19:345-346.
Dofiana
Acta Vertebrata
24:235-243.
HEREDIA,R. 1991. Alimentaci6ny recursosalimen- SOKAL,R. R., AND E J. ROHLF.1981. Biometry.W. H.
Freeman and Co., San Francisco, California.
ticios.Pages79-89 in E1Quebrantahuesos(Gypaetusbarbatus)en los Pirineos (R. Heredia and THIBAULT,J. C., J. D. VIGNE, AND J. TORRE.1993. The
diet of youngLammergeiersGypaetus
barbatus
in
B. Heredia, Eds.).Instituto para la Conservaci6n
Corsica:Its dependenceon extensivegrazing.
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Ibis 135:42-48.
HIRALDO, E, M. DELIBES,AND J. CALDERON.1979. E1
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Associate Editor: K. Bildstein
The Auk 118(3):789-795, 2001
Individual
and Seasonal
Variation
in External
MICHAEL
Genitalia
of Male
Tree Swallows
P. LOMBARDO 1
Department
of Biology,
GrandValleyStateUniversity,
Allendale,
Michigan49401,USA
ABSTRACT.--The
cloacalprotuberance(CP) of passerines functions primarily to store spermatozoa.
When gently squeezed,the CP of male Tree Swallows (Tachycineta
bicolor)evertsto exposea smallpapilla from which semencanbe expressed.
From1994
to 1999, I examined individual
and seasonal varia-
tion in CP dimensionsand papilla length of mated
male Tree Swallowsin westernMichigan. Male CP
volumeswere greatestwhen their mateswere laying
eggs and declined to the nestling period. Papilla
lengthsdid not vary over the courseof the breeding
season.Cloacalprotuberancedimensionsand papilla length were not associatedwith the age classof a
i E-mail: lombardm@gvsu.
edu
male'smate,the dateshestartedlaying eggs,or number of eggsshelaid. The decreasein CP sizeoverthe
courseof the breeding seasonis consistentwith the
steady decreasein reproductive opportunities for
male swallows.Although it seemslikely, whetheror
not the papilla of Tree Swallowsfunctionsas an intromittent organ awaitsfurther study of the anatomical mechanicsof copulationin thesebirds.
During the breedingseason,the distal endsof the
ductusdeferens(seminalglomera)of male passerinesfill with newly formedspermatozoaresultingin
a swellingof the cloacacommonlyreferredto as the
cloacalprotuberance(CP) (King 1981). The CP can
be consideredas the externalmale Menitalia.The di-