The Auk 113(2):431-440, 1996

POPULATION

FLUCTUATION

HORNBILLS:

IN SULAWESI

TRACKING

FIGS IN SPACE

RED-KNOBBED
AND

TIME

MARGARET F. KINNAIRD , TIMOTHY G. O'BRIEN ,

AND SUER SURYADI 2

WildlifeConservation
Society,185thandSouthern
Blvd.,Bronx,New York10460,USA;and
2Center
for Biodiversity
andConservation
Studies,
Facultyof Mathematics
andSciences,
Universityof Indonesia,
Depok16424,Indonesia

ABSTRACT.--We
studied spatial and temporal variation in a population of SulawesiRedknobbed Hornbills (Aceroscassidix)
in relation to availability of fruit resourcesover a twoyear period in the Tangkoko DuaSudaraNature Reserve,North Sulawesi,Indonesia.Fruit
production did not show any discernablepatternsover 22 months of study, in spite of the
strongseasonalityof rainfall. Figswere availablein all monthsof the year, and fig biomass
exceededripe nonfig-fruit biomassin 10 of 22 months. Hornbill densitiesfluctuated dramatically over time (2 = 51 birds-km-2, range 9.3-82.7) and among habitats. Spatial and
temporal variation in hornbill numbers was best explained by habitat selection and the
abundanceand distributionof figs.Hornbill numberswere higher in thoseareaswith greater
densitiesof fig trees,and monthly hornbill densitiesand mean flock size increasedwith
increasingfig biomass.BecauseSulawesiRed-knobbedHornbills appearto track fig production over potentially large distances,and include a mix of other rainforest tree speciesin
their diet, we hypothesizethat they may play an important role as agentsof rainforest
regeneration.Received
22 June1995,accepted
13 September
1995.

AVIAN

POPULATION FLUCTUATIONS have

been

shown to arise primarily from random demographic processes

(Karr 1982, Boagand Grant
1984,DeSanteand Geupel1987)and movement
of individuals within and among habitats
(Greenberg 1981, Karr and Freemark 1983,
Wheelwright 1983). Individuals move in responseto seasonalclimaticchanges(Root 1988),
breeding(Robinson1992),or the temporaland
spatial variation in food resources (Wheelwright 1983,Levey1988,Blakeand Loiselle1991,
Powell and Bjork 1994). Studies in the New
World tropics emphasizedthe importanceof
fruit-resource availability on the spatial and
temporal population fluctuationsof frugivo-

Communitywide fluctuations in fruit resourcesmay not be sufficient to explain fluctuationsin populationsof avian frugivoresthat
specializeon a subsetof the fruit community,
or arecapableof switchingto invertebrateprey.
Wheelwright (1983) illustrated the importance
of one family (Lauraceae)in the diet of Resplendent Quetzals (Pharomachrus
mocinno);fluctua-

tions in abundanceof Lauraceaetriggers altitudinal migrations in search of these fruits

(Powell and Bjork 1994). Plant taxa that fruit
outsidecommunitypeaksin fruit production,
suchas figs (Ficusspp.) or palms, may be important in maintaining populations of more
sedentaryfrugivores(Terborgh 1986,Lambert

rous birds (Skutch 1967, Karr 1982, Stiles 1985,

and Marshall 1991).

Levey 1988, Blake and Loiselle 1991, Loiselle

and Blake1991).In the Old World tropics,particularlyAsia,studiesproviding concurrentdata
on fluctuationsin both frugivore populations
and fruit abundanceare lacking (but seeLeighton and Leighton 1983).This resultsin part from
extremelylow captureratesfor frugivorousbirds
in Asian forests (Fogden 1972, Wong 1985),
which in turn may be due to the low percentage
of understoryand canopytrees bearing edible
fruit speciesrelative to the Neotropics(Fogden
1972, Medway 1972).

Lambertand Marshall(1991)arguedthat figs

play an important role in maintaining populations of frugivores like flowerpeckers(Dicaeidae)and greenpigeons(Treronspp.)during
periodsof generalfruit scarcity.Leighton(1986)
discussedresponsesto fig availability by a community of Borneanhornbills. Speciesthat include large quantitiesof figs in their diet, such

431

as the Wreathed Hornbill (Acerosundulatus),are

believed to move long distancesin search of

patchy fruit resources,producing local fluctuationsin populationsize.Territorial hornbills,

432

KINNAIRD,O'BPaEN,
AND$URYADI
5OO

[Auk, Vol. 113

bills in North Sulawesi. Concurrently, we collecteddataon fruit productionand askedif population fluctuation and patternsof hornbill distribution could be explainedby the abundance

400

and distribution

of fruit

resources.

Because of

the importance of figs in the Red-knobbed

Hornbill diet (Kinnaird and O'Brien 1993, Sur-

300

yadi et al. 1994),we comparedthe responseof

the hornbill population to fluctuationsin figs
(i.e. synchonia)versusnonfig fruit resources.

200

METHODS
100

Study area.--We conducted our research in the

Tangkoko DuaSudara Nature Reserve on the northernmost tip of the Indonesian island of Sulawesi
(134'N,12514'E).
The Reserveencompasses
approxi-

DJFMAMJ

JASONDJFMAMJ

93

JAS

Month94

Fig. 1. Monthly rainfall (mm) in study area over

22 months.

suchas the Bushy-crestedHornbill (Anorrhinus

galeritus),increase the proportion of invertebrate prey in the diet during periods of fruit
scarcity,and population size remainsrelatively
constant.

The Sulawesi Red-knobbed Hornbill (Aceros

cassidix;formally Rhyticeroscassidixand hereafter referred to as the Red-knobbed Hornbill)

is a large (2.5 kg), canopy-fruit specialistendemic

to the

Indonesian

island

of Sulawesi

(White and Bruce 1986). It is nonterritorial and

sympatricwith only one other hornbill, the Sulawesi Tarictic Hornbill (Penelopides
exarhatus).
Recent studies have focussedexclusively on
breedingbiology (Kinnaird and O'Brien 1993,
Kinnaird in prep.) and feeding ecology(Suryadi et al. 1994). Red-knobbed Hornbills nest in
natural cavities of large forest trees and are ca-

pableof attaining high nestingdensities.Breeding begins in late June during the dry season;
fledging occursfrom late December through
early January, soon after the onset of the wet
season(Kinnaird and O'Brien 1993). Fledging
success
is typicallyhigh (Kinnairdunpubl.data).
Red-knobbedHornbills are a major component
of the Sulawesi frugivore community and, although they prefer ripe fig fruits (Ficusspp.),
they consumefruits and presumablydisperse
the seedsof a wide range of tree species(Kinnaird and O'Brien 1993,Suryadiet al. 1994).
We collecteddata on the spatialand temporal
variationof a populationof Red-knobbedHorn-

mately 8,900ha and is isolatedfrom other forestsby

sea and agricultural lands. Forest ranges from sea
level to 1,350m elevation and is broadly classifiedas
lowland tropical rainforest (International Union for
Conservationof Nature 1991).Rainfall averages1,700
mm per year (1992-1994)and is highly seasonal(Fig.
1), with occasionaldroughts. The reserve is dominated by three volcanoes:Tangkoko, the recent ash
cone Batuangus,and the twin peaks of DuaSudara.
Our studywas conductedwithin a 441-haareaon the
north slope of TangkokoVolcano. The study area is
characterizedby a mosaicof habitat types and disturbanceregimes(O'Brienand Kinnaird unpubl.data).
Disturbanceregimesinclude: (1) heavily burned areas
in which the canopyhasbeen destroyedor severely
disturbed (101 ha); (2) 30-year-old regenerating agricultural plotsdominatedby coconut(Cocos
nucifera)
and mango(Mangiferaindica)treesand early successional forest species(e.g. Anacardiaceaeand Euphorbiaceae;25 ha); and (3) lightly disturbed areaswith
treefall gapsgreaterthan 1 ha in size, or where light
fires passedthrough the understory(271 ha). Forest
conditionin lightly disturbedareasis highly variable,
including broken and closedcanopyforest. Closed
canopy,primary forestaccountsfor approximately44
ha andis characterized
by largePalaquiurn
arnboinensis,
Canangaodorataand Dracontomelurn
daotrees,as well
asfigs(Ficusspp.)andLivistona
rotundifolia
palms.The
study area is gridded with trails at 100-m intervals.
Hornbills.--We used line-transectsurveys to estimate monthly distributionsand densitiesof hornbills
over 24 months(October1992-September1994).Line
transect method is appropriate for Red-knobbed
Hornbills becausethey are large and easily seenand
call loudly; also, during flight they produce a loud
soundasair passesthrough the primariesthat canbe
heard up to 100 m away. Red-knobbedHornbills are
sexually dimorphic in size, plumage, and vocalizations,allowing easyclassificationof sexesduring censuses.One day of eachmonth we surveyed10 trails,
each2 km in length. Surveysbeganat 0600and ended
before 1000. Five observerssimultaneously walked

April 1996]

Resource
Tracking
in Red-knobbed
Hornbills

east-westtrails 200 m apart and noted time, initial

cue(visual,vocalor wing beat),number,ageand sex
(when possible),and estimatedperpendiculardistance from trail to bird or flocks.To prevent double
counting, a maximum strip width was used (100 m

on a side) to map eachbird. All mappeddata were

comparedby location and time of observationand
possibledouble countswere eliminated.
Fruit.--Beginning December 1992, fruit resources
were estimatedeach month just prior to a hornbill
census.We monitored 2,015 trees for fruit, representing about 168 species,in 22 0.25-ha plots. An
additional2.1-kmtransectwasestablished
specifically
to monitorfruiting of fig treesthat were underrepresentedin the plots.For eachfruiting tree, the number

433

Unripe nonfigs

1200

Ripe nonfigs
re.Figs
1000

800

600
400

200

of ripe and unripe fruits was estimatedon an exponential scalefollowing Leighton(1982,1993).Montho

ly biomassof ripe and unripefruit wascalculatedby
DJ FMAMJJASONDJFMAMJJAS
multiplying a species'mean fruit wet mass(O'Brien
93
94
Month
unpubl.data)by its fruit crops,then summingacross
species.We calculatedmonthly fruit biomassfor the
Fig. 2. Monthly estimatesof fruit biomassfor fig
entire community and then partitioned biomasses- and nonfigfruits. Nonfig fruits are partitionedinto
timates for figs and nonfigs.
estimatesof ripe- and unripe-fruit biomass.
Fig census.--Tocalculatedistribution and density
of fig (Ficusspp.)trees,we countedall canopy-sized
figswithin 15 m of either sideof 20 trails for a total of a fruit crop in a given month. Significant differof 42 km. Figswere identifiedby speciesand density encesamonghabitattypesand betweenthe breeding
estimatesfor all speciescombinedwere calculatedfor and nonbreedingseasonswere examinedusing Duneachhectareblock.Ficusvariegatus,
the mostcommon can'smultiple range tests.The ANCOVA model was
fig species,wasnot includedin the censusbecauseit testedusingType III sumsof squares.
was known not to be important to hornbills.
We examined relationships between monthly
Analyses.--Weused the computer program DIShornbill densities and estimates of fruit biomass for
TANCE (Laakeet al. 1993)to calculatemonthly horn- figs and nonfig-fruit treesusing multiple-regression
bill densities.Data were groupedinto 10-mintervals analysis. Becausehornbills feed preferentially on
and evaluated using three models to fit detection- fleshyfruits or huskedfruits with fleshyarils (Leighprobability functions:uniform, half-normal and haz- ton 1982,Suryadiet al. 1994)in the canopyand midard. Eachmodel usedcosine-adjustment
terms;mod- canopy,we eliminatedall wind-dispersed,
understoels were fit sequentiallyuntil no further improve- ry and leguminousspeciesfrom estimatesof monthly
ment was gained by adding cosineterms. We chose nonfig-fruit biomass.The remaining sample commodels

that minimized

the coefficient

of variation

associatedwith density estimates.Data were insufficient to calculatemonthly densitiesby habitatusing

DISTANCE models.To evaluate the monthly distributionof hornbillsby habitat,we calculatedobserved
densitiesper month in eachhabitatby summingall
hornbillsobservedin hectareblocksof a givenhabitat
and divided by the total number of hectaresrepresented by each habitat.
We used analysisof covariance(ANCOVA; Sokal

and Rohlf 1981)to examinethe effectof habitattype

and breeding seasonon monthly hornbill densities,
usingfig-tree densityas a covariate.Fig-treedensity
wasestimatedmonthly for only thosehectareblocks
in which birds were observed. We eliminated hectare
blocks with zero observations because we were con-

prised85 speciesof which 732 individualsof 66 speciesfruited at least once.The fig samplewas comprisedof 18 species,representedby 73 individualsof
which 59 fruited during the study. Nonfig-fruit biomasswas partitioned into ripe and unripe biomass.
Because
fig cropstend to ripen quicklyand simultaneously(Janzen1979,Lambertand Marshall 1991),
estimatesof unripe fig biomasswere not analyzed
separately.We alsoexaminedrelationshipsbetween
mean numbers

of hornbills

in flocks and estimates

of

fruit biomassusing correlationand regressionanalyses. We used StatisticalAnalysis System software

(SASInstitute 1985) for all analyses.
RESULTS

cernedwith habitatchoiceson a monthlybasis.InFruits.--Total fruit biomass varied over time,

clusionof blockswith no birds in the estimateof fig
but
did not show any discernablepatternsover
densitieseliminatesmonthlyvariability.This analysis,therefore,assumes
that birdsare choosinghectare 22 monthsof study,in spite of the strongseablockswithin a habitatthat havea high probability sonality of rainfall (Figs. 1 and 2). Nonfig-fruit

434

KINNAIRD,
O'BRIEN,
AND$URYADI

[Auk,Vol. 113

-1

Figs .ha

1-5

Hornbills

-1
-1
ha. mon

=0.0- 0.2 0.2- 0.4 e>0.4- 0.6 0.6

e6-10 11-20 i20

20
'
'
' '
I111' Illlll
Ill I I1' Ill I1 I' I1

2.0

I I11 IlOI I1' I111I' I I 1 I I11 I

I 111 11 le I[" ]11] ll 1lel.
I I
I Illellll1.111
I .1,11.11-1 el I

.51 Illllel

= .*.
;'';_

Iillll

1111.
Illlel.I' Ilel

1.5

.' -.;..; :;..:

'111 '111' I11' I Illlll?l

Ill 1' I1111 I 1' I Ill'

I' I I I I I {I

1.oll{11
I I Illtlllll'll'lII1'111

'. .".
;.,:

I I'1 I Ill

1.0

;. : :; : :

Illl'l

Il'll'll

I1 I I1

...... ';.., .';';; :. '.

0.5

0.5......,,. ;,,;;;....;:;
.,..... .,,.,...........
o.ol letll I:l I I I'11 I'll
0.0

0.5

1.0

0.0

1.5

0.0

2.0

0.5

1.0

1.5

2.0

Kilometers

Kilometers

Fig. 3. Distributionof Ficustreesand mean monthly hornbill sightingsin studyarea.

productionfluctuatedmorewidely than that for

figs, and these fluctuationssuggesteda weak
association
with monthlyrainfall,althoughthe
associationdid not reachstatisticalsignificance
(Spearman'sr = 0.402, P = 0.06, n = 22). Major

140

120

lOO

6O

4O

2O

peaksin ripe-fruit productionwere lessthan 6

monthsapart,with 10 monthsof generallylow
fruiting beforethe first peak. Unripe-fruit biomasswas higher than ripe-fruit biomassin all
monthsexceptJuly 1994.This reflectsthe dominance of a few specieswith extremely large
cropsthat mature slowly and nonsynchronously within a tree (e.g.Dracontomelum
daoand Palaquiumamboinense).
The fig communityexhibited an asynchronous
fruiting phenology,with
no recurrentannualpattern.Figswereavailable
in all monthsof the year; cropsoften ranged
from100,000to 1,000,000
fruitspertreefor large,
stranglingfigs(e.g.F. virens).Fig-fruit biomass
exceededripe nonfig-fruitbiomassin 10 of the
22 monthsof study.
Fig treesare patchilydistributedthroughout
the study area, with densitiesranging from 0
to 27 trees.ha-' (Fig. 3). Mean fig densitiesare
higher in primary forest( = 10.28trees.ha-z)
than secondaryforests(= 8.28 trees.ha-') or
burned forests (g = 8.25 trees.ha-i), but these

differencesare not significant.Regeneratingagriculturalareashad significantlyfewer fig trees

ONDJ
92

FMAMJ

JASONDJ

93

FMAMJ

JAS

94

Month

Fig.4. Mean(-+SD)monthlyRed-knobbed
Hornbill densities.Horizontal lines denote breeding season.

than all other habitats (= 5.34 trees.ha-'; F =

3.68, df = 3 and 437, P = 0.012).

Hornbills.--Hornbill densitiesvaried spectacularly over time (Fig. 4), ranging from a low of
9.3 birds.km-2 in January1993to a high of 84.1

April 1996]

Resource
Tracking
in Red-knobbed
Hornbills

435

T^nI,E 1. Monthly Red-knobbedHornbill density estimates

a and DISTANCE-model parameterswith associated standard

errors.
No.

Month

Mean

hornbills.km-2

Mean

strip width

clustersize

51.4 + 2.0
50.0 + 0.91
51.1 + 1.9

1.4 + 0.16
1.8 + 0.18
1.7 + 0.17

1992

October
November
December

75
108
68

63.4 + 8.9
84.1 + 9.5
48.1 + 6.8
1993

January
February

24
40

9.3 + 2.2
80.5 + 50.7

100.0 + 0.0
51.0 + 2.5

2.1 + 0.39
7.1 + 4.4

March

45

40.2 + 13.1

67.7 + 8.8

3.1 + 1.2

April
May

56
46

53.8 + 17.1
82.7 + 24.1

71.6 + 7.7
51.7 + 2.8

2.3 + 1.5
5.0 + 1.6

June

35

39.6 + 10.3

79.6 + 4.9

4.5 + 1.3

July
August
September

67
44
70

43.4 +_8.0
58.3 + 23.8
44.2 + 6.6

53.0 + 2.9
40.4 + 4.4
53.1 + 2.8

1.8 + 0.31
3.1 + 1.2
1.6 + 0.17

October
November
December

91
64
42

54.3 + 6.7
51.0 + 7.7
43.9 + 10.8

54.3 + 2.9
50.0 + 1.2
56.9 + 5.2

1.5 + 0.89
1.9 + 0.23
2.6 + 0.67

66.0 + 8.2
54.6 + 4.4

2.6 + 0.74
3.2 + 1.8

1994

January
February

45
40

37.9 + 10.6
44.9 + 18.3

March

38

28.5 + 5.3

50.0 + 1.5

1.6 + 0.22

April
May

68
63

29.4 +_4.1
58.2 +_ 14.5

87.6 + 3.5
55.9 +_3.9

1.7 + 0.15
2.8 + 0.75

June

93

72.5 + 9.5

54.1 + 2.8

1.8 + 0.19

July
August
September

56
52
81

63.0 + 25.9
47.9 + 13.4
55.1 + 8.0

50.0 +- 1.3
52.2 + 2.9
54.9 + 3.2

3.4 + 1.4
2.5 + 0.78
1.5 + 0.19

All calculatedusinguniform model,exceptfor April and June1993and April 1994,which were calculatedusinghazardmodel.

birds.km -2 in November 1992, with an overall

1.4

mean of 51.4 birds.km -2 + SE of 17.7 (Table 1).

We usually chosemonthly density estimates

generatedusinga uniformdensityfunctionwith
a first-ordercosine-adjustment
term for the detection-probabilitymodel;estimatedmeanstrip
width wasrelativelyconstant
within andamong
months,(Table 1). Monthly mean cluster size

0.8

was generally low (1-3 birds/cluster), indicating that hornbills tend to occur as individuals

0.6

(60% records)or pairs (30% records).The remaining 10%of sightingrecordswere of flocks;

flocksrangedin size from 3 birds in October
1993to 10! birdsin February1993.
The sex ratio (female:male) of hornbills fluc-

tuatedamongmonthsandreflectedthe general
chronology
of thebreedingseason
(Fig.5). Sex
ratios were male dominated from June to December when females were sealed in nest cav-

ities, and near unity only during the nonbreeding season(January-earlyJune).

1.2

1.0

0.4

0.2

0.0

92

93

Month

94

Fig.5. Observedsexratio(female:male)by month.

Horizontal lines denotebreedingseason.

436

KINNAIRD,O'BPJEN,AND SURYADI
40-

[Auk, Vol. 113

relationshipsof biomass,hornbill density, and

30'

20.

10-

ass)

do

flocksize,however,are stronglyinfluencedby
unusually high fig production and hornbill
numbersin February 1993 (Fig. 6). Removalof
this month reducesthe fig-hornbill density relationship to a positivebut statisticallynonsignificant association(0.1 > P > 0.05), although
the overall model remains significant.The relationshipbetweenmeanflocksizeand fig biomassalso is reduced to the point at which it is
no longer statisticallysignificant.
The spatialdistribution of hornbills was significantly affectedby habitattype (F = 9.20,df
= 2 and 67, P < 0.001) and the density of reproductivefig trees(F = 5.02, df = 1 and 67, P
= 0.028). Hornbills preferred primary forest (
= 0.41 birds.ha-1) over secondary( = 0.27
birds.ha -) and burned forest (= 0.21 birds.

lOO

40',

ha-). Regenerating gardens were eliminated

from the analysisbecausehornbills were never
detectedin this habitattype. After controlling
for habitat,hornbill densitywashigher in hectare blockswith high fig-treedensities(Fig. 3).
Although hornbill densitieswere higher during the nonbreedingthan during the breeding
season(nonbreeding, = 0.34 birds-ha- vs.
breeding, = 0.25 birds.ha-), the difference
was not statisticallysignificant.

DISCUSSION

Hornbill
density=50.3+O.
16(fig
biomass)
0
Figbiomass
(kg,ha')

Fig. 6. Relationshipof monthly estimatesof figfruit biomass to (A) number of hornbills.kin -2 and

(B) mean flock size.

Hornbillsand fruit resources.--Monthlyestimatesof fruit biomassexplained47%of the temporal variance in hornbill densities(F = 5.33,
df = 3 and 18, P = 0.005). Monthly hornbill
densities increasedsignificantly with increasing fig-fruit biomass(F = 5.43, P = 0.031;Fig.
6), but declined as biomassof unripe nonfigfruits increased (F = -7.18, P = 0.015). There

wasno significanteffectof ripe nonfig-fruitbiomasson monthly hornbill densities. Monthly

estimatesof fig-fruit biomassalso had a significantpositiveeffecton meanmonthly flocksize
(F = 52.02, df = 1 and 20, P < 0.001; Fig. 6).
Estimatesof ripe and unripe nonfig-fruit biomass were

Red-knobbedHornbill densitiesin the Tang-

koko DuaSudara

not correlated

with

flock size. The

Nature

Reserve fluctuate dra-

maticallyover time and space.Our dataindicate

that, although thesefluctuationsare influenced
by breeding, when a large proportion of females enter nest cavities and are removed from

the census population, the distribution and

abundanceof fruiting figs are the overriding
factorsaffectingthesefluctuations.Monthly figfruit biomasswas significantly related to estimatesof hornbill density and the size of hornbill flocks.The importanceof fig productionin
explaining the rise and fall of Red-knobbed
Hornbill numbersis further underscoredby the
lack of relationship between hornbill densities
and ripe-fruit production by the nonfig community.

Nonfig-fruits however are not unimportant

to hornbills.Nearly 20%of the breedingseason
diet is composedof ripe nonfig species(Kinnaird and O'Brien 1993). Although we did not
explorethe possibility,other subsetsof the nonfig communitythat fruit outsidethe community

April 1996]

Resource
Tracking
in Red-knobbed
Hornbills

peak may influencehornbill numbers.For example, Leighton (1982) showed that less than
one-half of the nonfig-treespeciesimportant to
Bornean hornbills fruited during the peak of
community fruiting. Nevertheless,in contrast
to figs, most of these fruiting speciesare rare
and fruit at relatively long intervals(Leighton
andLeighton1983).Nonfig speciesin the TangkokoDuaSudaraNatureReservetypicallyoccur
in smallcropsand matureslowly, suchthat only
a few ripe fruit areavailableon a given dayand
are rapidly selectedby a guild of large frugivores including Red-knobbed Hornbills, imperial pigeons(Duculaspp.), and crestedblack
macaques(Macacanigra).
Our data demonstrate

that the distribution

of

fig trees influencesspatial patternsin hornbill

densities.Red-knobbedHornbills prefer primary habitat over secondaryhabitat, burned
forests,or regeneratingagricultural lands and,
irrespectiveof habitat,they chooseareaswith
high fig-treedensities.Other studieshavedemonstratedsimilar preference among hornbill
species.Kalina (1988) found Black-and-whitecasquedHornbills (Bycanistes
subcylindricus)
at

437

be producingfruits at any given time. On average,19.29 + SD of 4.8 of the figs in our phenologicalsamplewere in fruit eachmonth. With

a mean densityof 8.3 figs-ha , this translates

into 1.6 fruiting figs-mon .ha -, or up to 160
figs.kin-2 with ripe fruit during any given
month.

Fig densitiesand the resulting fruit production in the Reserveare exceptionally high relative to reports from other SoutheastAsian forests.Leighton and Leighton (1983) reported a

meanof 6.6 figs-ha- in primary forestof East

Kalimantan, Lambert (1991) calculated an av-

erageof 2.5 figs.ha- in primary forestof Sabah,

Malaysia,and Johns(1983) estimated2 trees.
ha- in forestsof PeninsularMalaysia.In Kuala
Lornpat,Malaysia,Lambertand Marshall(1991)
estimated

between

1 and

13 Ficus.km -2 with

ripe figs on any particularday.

We believe that high fig densitiesin Tangkoko DuaSudaraNature Reserveare responsible for maintainingthe overall high population
densityof Red-knobbedHornbills. Foresthornbills,in general,arefoundat relativelylow densities.Some of the highest densitiesfor single
significantlyhigher densitiesin primaryforest speciesin Asia havebeenreportedby Leighton
than selectivelyloggedareasin EastAfrica, but (1982) and van Schaik (1991) for the Bushyobservedtemporary influxes of hornbills into crestedHornbill (Table 2). If we compare bioheavily loggedareaswhen two speciesof Ficus mass estimates for entire Asian hornbill com(F.daweiandF. natalensis)
werein fruit. Surveys munities,the TangkokoDuaSudaraNature Reof SoutheastAsian hornbillsin primary and serveranks highest in hornbill biomass(Table
logged forestsshow that hornbills use second- 2). Only biomassestimatesfrom the Kutai comary habitats,but occur at lower densitiesthan munity approachbiomassestimatesfor the Rein comparableprimary habitats (Kemp and serve;this is due primarily to the occurrenceof
Kemp unpubL report, Wilson and Johns1982). large flocks of Wreathed Hornbills and WrinJohns(1983, 1987) documented a numerical de- kled Hornbills (A. corrugatus)
that were becline in some hornbill populationsafter selec- lieved to be tracking fig resources(Leighton
tive logging of forestsin SungaiTekam, Pen- 1982).The Kutai studyareaalsohasthe secondinsularMalaysiaand speculatedthat the decline highestreported fig-tree density next to what
was tied in part to a reduction in densities of
Ficusgrowing on commerciallyimportant hosts
in the logged forests.

we found

in the Reserve.

Figs, combined with numerous tree cavities

may explain the extraordinary Red-knobbed

Hornbill breedingdensitiesin the Reserve.Approximately70%of the Red-knobbedHornbill's
breedingseasondiet is composedof figs (Kinnaird and O'Brien 1993)and the preferrednest
tree,Palaquium
amboinense,
is commonand prone
to heart-rot, resulting in frequent cavity formation.During the 1993-1994breedingseason,
Suryadiet al. 1994).Becausefigs show patterns we counted60 active nest cavitiesin approxiof asynchronous
fruitingbothwithin andamong mately 600 ha, yielding a nestingdensityof 10
species(Janzen 1979, van Schaik 1986, Lambert Red-knobbedHornbill pairs.kin-2. Breeding
and Marshall1991),high fig-treedensityim- studiesof other hornbill specieshave reported
provesthe probabilitythat at leastone fig will lower densities. In Thailand, Poonswad et al.

Although primary habitat in the Tangkoko

DuaSudaraNature Reservedoesnot have significantlymorefig treesrelative to other habitats, primary habitatis characterizedby generally larger canopiedtrees and may contain
largerfigsthat bearlarger crops,or speciesthat
are highly preferreddiet items(e.g.F. altissima;

438

KINNAIRD,
O'BRIIN,
ANDSURYADI

TABLE2. Comparisonof hornbilP densitiesand bio-

massamongfour SouthEastAsianstudysites.
No.

Species

Mean

horn-

body

Hornbill

bills.

mass

biomass.

km-2

(kg)

km-2

Krau Game Reserve,Malaysia (Whitmore 1984)

Helmeted
Hornbill
Rhinoceros Hornbill
Oriental Pied Hornbill

0.5
0.5
1.0

3.10
2.58
0.74

1.55
1.29
0.74

Malay BlackHornbill
Bushy-crestedHornbill

2.0
2.5

1.05
1.17

2.10
2.93

White-crowned
Total

Hornbill

?b

1.31

?
> 8.61

Gunung Leuser National Park, N. Sumatra (van

Schaik unpubl. report)
Helmeted
Hornbill
Rhinoceros Hornbill
Wrinkled
Hornbill
Wreathed Hornbill

0.83
3.11
0.10
1.05

3.1
2.58
1.59
2.54

Bushy-crested
Hornbill

4.28

1.17

Total

2.57
8.02
0.17
2.67

5.02
18.45

Kutai National Park, E. Kalimantan

(Leighton1982)
Helmeted Hornbill
Rhinoceros Hornbill

0.3
1.1

3.1
2.58

0.93
2.84

Malay BlackHornbill
Bushy-crested
Hornbill

2.7
6.2

1.05
1.172

2.84
7.27

White-crownedHornbill
Wrinkled Hornbill
Wreathed Hornbill
Total

4.2
5-21
10-46

1.31
1.59
2.54

5.50
20.67 c
71.12 c
111.17

Tangkoko DuaSudara Nature Reserve,Sulawesi

(this study; O'Brien and Kinnaird 1994)
Red-knobbed Hornbill
Tarictic Hornbill

Total

51.40
2.84

2.36
0.46

120.36
1.30
121.66

' Helmeted Hornbill (Buceros

vigil), RhinocerosHornbill (B. rhinoceros),Oriental Pied Hornbill (Anthracoceros
albirostris),
Malay Black
Hornbill (A. malayanus),
Bushy-crested
Hornbill (Anorrhinus
galeritus),
White-crownedHornbill (Aceroscomatus),
Wrinkled Hornbill (A. corrugatus),Wreathed Hornbill (A. undulatus),Red-knobbed Hornbill (A.
cassidix),
and TaricticHornbill (Penelopides
exarhatus).
bSpeciespresent,but density estimatesnot available.

cDenotesbiomass
calculations
usingmidpointof rangeof densities.

(1987) reporteda nesting density of lessthan 1

pair. kin-2 for four hornbill species.Kalina(1988)
reported maximum densitiesof 5.6 cavities-kin 2

for Black-and-white-casqued
Hornbills of Kibale Forest,Uganda.
The well-documentedaseasonality,intrapopulation asynchrony,and resulting year-round
availability of Ficusoften are cited as the key
factorsallowing figsto gain suchimportanceto
frugivore communities(Foster 1982, Milton et
al. 1982,Leightonand Leighton1983,Terborgh
1986). As Lambert and Marshall (1991) and Kan-

[Auk,Vol. 113

nan (1994) pointed out however, it is not the

intrapopulation asynchrony per se that gives
this taxon such importance, but a combination

of other attributes.Fig cropstend to be large

and frequently are available during periodsof
general fruit scarcity(Lambert and Marshall
1991). Figs also form a unique subsetbecause
of their shortcroppersistenceand synchronous
maturation within a tree. Crop persistenceis an

important indicator of daily fruit availability:

the shorter the duration, the greater the mean
proportion of fruits available per day during
the fruiting period(Lambertand Marshall 1991).
Crop persistencefor figs monitored on daily
basisin the TangkokoDuaSudaraNature Reserve was short, with minimum persistenceas
low as five days. The easeof harvest and nutritional

content of Ficus are added benefits. Most

figs are succulent,soft, and can be easily swallowed. Figs are energy-rich foods and have
higher caloricvaluesthan nonfig-fruits,aswell
asadequateproteinlevels(Wranghamet al. 1993;
but see Bronstein and Hoffmann 1987). Data

from the TangkokoDuaSudaraNature Reserve

demonstratethat figs are an excellentsourceof
natural calcium (Kinnaird et al. unpubl. data)
requiredfor growth and development.The fact
that severalavian frugivoresare capableof subsisting almost entirely on figs (e.g. green pigeons[Treronspp.]and barbets[Megalairna
spp.],
Lambert 1991;Helmeted Hornbills [Buceros
vigil], Leighton 1982;Great Pied Hornbills lB. bicornis],Kannan 1994) supportsthe hypothesis
that, given year-round availability, figs constitute an adequatediet for somefrugivores.
Although the spectrumof fig productiongenerally reflects year-round availability to RedknobbedHornbills, it is apparentfrom the data
that figs may be locally scarceat some times of

the year (Fig 1). During this time Red-knobbed

Hornbills rely more heavily on other fruit resourcesand invertebrateprey, or make largescalemovementsto adjacenthabitatsin search
of figs. Large-scalemovements by Wreathed
Hornbills

in Thailand

have been

documented

by Poonswadand Tsuji (1994), and data from

on goingradio-telemetrystudiesshowthat RedknobbedHornbills coverdaily distancesof up
to 13 km during the nonbreedingseason.Use
by Red-knobbedHornbills of secondaryforests
and burned habitatsin closeproximity to primary forest may promote regeneration of disturbed sites if hornbills are depositing viable
seeds.Although we have not demonstratedseed
viability or effectivenessof dispersal,we hy-

April 1996]

Resource
Tracking
in Red-knobbed
Hornbills

pothesize that Red-knobbed Hornbills may be

important and effectivedispersersbecause:(1)

439

and D. M. Windsor, Eds.). Smithsonian Institu-

tion Press,Washington,D.C.

R. 1981. Frugivory in some migrant

they move seedsaway from seed shadowsof GaEENIEaG,
tropical forest wood warblers. Biotropica13:215parent trees;(2) they are capableof carryingup
223.
to 500g in oneload;(3) fruitsareprocessed
and INTERNATIONAL UNION FOR CONSERVATION OF NATURE.
seedsare spit or defecatedintact; and (4) seeds
1991. Atlas of tropicalrainforests.IUCN Special

of fruits delivered to nestsoften sprout underPublication. Gland, Switzerland.

neath (pers. obs.).Removalof figs (Johns1983, JANZEN,D. H. 1979. How to be a fig. Annu. Rev.
1987, Lambert 1991) or reduction of fig popuEcol.and Syst.10:13-52.
lations to nonviable sizes (McKey 1989) will
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A. 1983. Ecologicaleffectsof selectivelogging in a West Malaysianrain forest.Ph.D. dishave serious repercussionsfor Red-knobbed
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ACKNOWLEDGMENTS

Biol. Conserv.

This work wasconductedunder the auspicesof the

Wildlife ConservationSocietyin collaborationwith
the Indonesian

Directorate

General

for Nature

Pres-

ervation and Forest Protection (PHPA) and Puslit-

bang Biologi of the IndonesianInstitute of Science

(PB/LIPI). Funding was provided by the Wildlife
ConservationSociety, the National GeographicSociety (grant no. 4912-92),and the ConservationFood
and

Health

Foundation.

We

thank

Soetikno

Wir-

yoatmodjo (PB/LIPI), Dedi Darnaedi (PB/LIPI), Romon Palete (PHPA, North Sulawesi), and Jatna Supriatna (University of Indonesia)for their kind help
throughoutour time in Indonesia.Denand Kakauhe,
Nelman Kakauhe,JukberLambaihangand Yopi Manderosare thanked for assistingwith data collection.
Finally, we thank Carlos Martinez, Gary Stiles, and
Adrian

Marshall

for constructive

criticism

of an ear-

lier draft of the manuscript.

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