J. Field Ornithol., 70(4):558-566
BREEDING BIOLOGY OF THE SCARLET IBIS ON CAJUAL
ISLAND,
NORTHERN
BRAZIL
CARLOS MARTINEZ 1
Departamentde BiologiaAnimal (Z. V.)
Fac. Biologia Universitatde Barcelona
Av. Diagonal, 645
08028-Barcelona,Spain
ANTONIO
AUGUSTO
FERREIRA RODRIGUES
Departamentode Biologia
Universidade
Federal
do Maranhdo
Av. dosPortugrueses,
S/N
CampusUniversitYriodo Bacanga
65.080-040, Sdo Luis-MA, Brazil
Abstract.--The reproductivebiologyof the ScarletIbis (Eudocimusruber)and White Ibis (E.
albus) is well known from sites in North America, the Caribbean, and the Venezuelan llanos,
but few data are availableon the statusor breeding patternsof the populationsthat inhabit
SouthAmericanmangroves.From 1992-1997,we monitoredthe statusof a colonyofE. ruber
in an area of mangrovein northern Brazil. The breeding populationnumbered2000-3400
pairs.We did not find any significantpopulationfluctuationsbetweenyears;apparently,most
birds attemptedto breed eachyear,in contrastwith freshwater-breeding
populations.Clutch
sizewas1.97 + 0.17, lower than at more northern saltwatersites.The low variabilityof clutch
sizewassurprising.Whole nest failure from catastrophiceventssuchas storms,human predation, and nest desertionwasresponsiblefor mostegg and nestlingmortality.Partialmortality wasrare. Singletoneggsand nestlingswere frequentlyabandonedby adultsfollowing
the lossof an egg or nestling.We concludethat this population pursueda strategyof brood
survivalrather than brood reduction which is usuallyobservedin Eudocimus.This may have
resultedfrom stableresourceavailabilityat this site. Given that northern populationsoften
do not breed in unfavorableyears, selectionappears to have favored adult survivalover
reproductivecapacityin this species.Human disturbancewas intense, and it can threaten
ibis populationsboth through direct predationand induction of nest desertion.
BIOLOGiA REPRODUCTIVA DE LA POBLACION DE EUDOCIMUS RUBER EN LA
ISLA DE CAJUAL EN EL NORTE DE BRAZIL
Sinopsis.--La biologia reproductivade Eudocimustubery de E. albuses bien conocidaen
localidadesde Norteam6rica,el Caribe y los Llanosde Venezuela,pero existenpocosdata
disponiblessobreel statusy los patronesde reproducci6nde las poblacionesque vivenen
manglaressudamericanos.
Entre 1992y 1997,estudiamosel statuspoblacionalde nrtacolonia
de E. ruberen una regi6n de manglaren el norte de Brasil;en 1995 registramostambidnel
tamafio de puesta,la mortalidad de huevosy pollos (hastalos 20 dias), y el fracasode nidos
enteros.La poblaci6n reproductivarue de 2000-3400 parejas.No rueton encontradasfiuctuacionespoblacionalessistematicas
entre aftos,y la mayoriade las avesintent6 reproducirse
cada afio, en contrastecom lo observadoen poblacionesque se reproducenen agua dulce.
E1tamafiode puestarue 1.97_+0.17,menor queen localidadescosterassituadasmasal norte.
La pequefiavariabilidaddel tamafiode puestaessorprendente.Losfracasosde nidosenteros
debidosa eventoscatastr6ficoscomo tempestaries,predaci6n humana y la deserci6nde nidos
pot los adultos,rueton las principalescansasde mortalidad.La mortalidadparcialrue rata.
Los huevosy pollosfinicosrueton frecuentementeabandonadospot los adultosdespudsde
Current address:Departamentode Biologia,Universidade
Federaldo Maranhdo, Av. dosPortugrueses,
S/N, CampusUniversiteirio
do Bacanga,65.080-040, SdoLuis-MA, Brazil.
558
Vol.70,No.4
Breeding
Biology
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Iln's
[559
la pdrdida de un huevo o pollo, lo que es comdn en ciconiiformes,pero puesto que el
tamafio de la nidada casi siempre fue dos, esto significa que las nidadas fueron, o criadas
enteras,o abandonadas.Conclu/mosque estapoblaci6n se ajust6 milsbien a una estrategia
broodsurvival,que a la estrategiabroodreductionmilscornfinen Eudocimus.
Estopuede haber
resultadode una disponibilidadde recursosestableen esta localidad.Dado que los poblaciones mils nortefias no se reproducen en aftos desfavorables,la selecci6nparece haber
favorecidola supervivenciade los adultossobre la capacidadreproductivaen esta especie.
Las perturbacioneshumanasfueron intensas,y pueden amenazarlas poblacionesde corocoros, tanto a travdsde la predaci6n directa, como induciendo a la deserci6n de los nidos.
The ScarletIbis (Eudocimusruber)occursin both saltwater(Spaans
1990) and freshwater (Ramo and Busto 1985, 1988; Brouwer and Van
Wieringen 1990) ecosystems
in South America. However,most studiesof
ScarletIbis in South America have focusedon freshwatersystems(Ramo
and Busto 1985, 1998; Brouwer and Van Wieringen 1990); studies of
coastalpopulationshavereported only on the statusor locationof breeding populations(e.g., Morrison et al. 1986, Spaans1990, Rodriguesand
Fernandes 1994). This is unfortunate becausethere are often important
differencesin the ecologyof ciconiiformsoccupyingfreshwaterand saltwater ecosystems
(Bildsteinet al. 1990b, Frederick et al. 1992, Hancock
et al. 1992). Thus, more data are needed from mangroveecosystems
to
understand the reproductive biology of Scarlet Ibis at coastalsites in
South America.
Therefore, the objectiveof this studywasdescribethe statusand breeding biology of a population of ScarletIbis breeding on Cajual Island in
the Gulf of Maranh5o,Brazil (Rodrigues1995). Specifically,
we quantified
the size of the adult population as well as clutch size and reproductive
success.
As clutch size and brood reduction patterns differed from those
recorded in other populations,our data form the basefor a discussion
of the role of theseparametersin the breedingstrategyof the population.
Our data will also serve as a basisfor evaluatingthe conservationstatus
of this population.
STUDY
SITE
Cajual Island coversan area of about 6000 ha and is located in the
Gulf of Maranhfio (2ø26'S,44ø30'W),a broad estuaryformed by the confluence of the Itapecuru, Mearim, and Pindar• Riverswith the Atlantic
Ocean (Fig. 1). The siteis part of a major coastalformation characterized
by a highly indented coastline,broad belts of mangrovevegetationup to
several kilometers in width, and extensive intertidal mudflats with dense
populationsof crabs(principally Ucaand Ucides;,
Ocypodidae).Maximum
tidal amplitudein this area is 8.16 m (Mabesooneand Coutinho 1970).
The present studywasfocusedon a colony of ScarletIbis located on
the island'snorthern sector.The nestswere built 5-12 m high in dense
10-15-m tall mangroves(Avicenniagerminans).The colonywas divided
into a number of subcolonies(Fig. 1).
METHODS
Populationstatus.--We censusedthe Scarlet Ibis breeding on Cajual
Islandyearlyfrom 1992-1997.Rodrigues(1995) presenteddatafor 1991.
560]
c. Martinez
andA. A.F. Rodrigues
J.Field
Ornithol.
Autumn 1999
•ARANHAO
GULF
•,/
OCEAN
0
•
5
10 Km
MARAN
02
30'S
FIGURE
1. CajualIslandonthenorthernBrazilian
coast.
Theopencircleindicates
thestudy
site, crosses indicate other subcolonies.
Vol.70,No.4
Breeding
Biology
ofScarlet
Ibis
[561
The number of breeding pairs was estimatedby counting all occupied
nestsin marked quadratsalong parallel transects50 m apart. Transects
were censusedby one observerjust after high tide when adultswere still
presentin the colony;an additionalobserverremainedoutsidethe colony
to count adult birds in flight. Comparisonbetween observer counts
showedapproximately90% similarity.While replacementclutcheswere
probablylaid, and multiple clutchesmay occur,thesephenomenawere
not consideredin our estimates.During the 1996 breeding season(AprilJune), marked quadrat counts were compared with a more extensive
count of the entire colony carried out by a singleobserveron foot. Even
when censuses
of the entire ibispopulationwere not carried out, we made
pre-breedingcountsby boat.
Nestingb/o/ogy.
wWe quantified nestingecologyin detail in 1995 in a
portionof the colonycontaining97 individuallymarkednests.We visited
the colony twice each week from 19 July-6 September(laying through
the first 20 d of life of the chicks) and counted eggsand/or chicksin
each nest from an elevatedpositionseveralmetersfrom the nest. Each
pair was disturbedonly for a few minutes;we never remained in the
colonyfor more than 2 h.
Total nest failure wasdifferentiated from partial losses.As catastrophic
losseswere high, we estimatedreproductivesuccessusing the apparent
mortality method (Johnson and Schaffer 1990). Follow Mock and Parker's (1986) terminology,we refer to nestswith a single nestling as B/l,
and thosewith two nestlingsasB/2. A "primary" B/1 brood is one that
has containeda singlenestlingsincehatching;a "secondary"B/1 brood
previouslycontainedmore chicks.
Survivalrates of broods of different sizeswere not compared by the
nest-casemethod becausein the caseof singletons,there is no difference
betweenindividualmortalityand nestfailure, distortingnestfailure rates.
Therefore, we studiedthe nesdingcase,estimatingthe probabilityof survival of primary B/1 and B/2 nestlings.Survivalrates of B/1 and B/2
chickswere arranged in a contingencytable and comparedusing G-tests
(Sokal and Rohlf 1981). The same test was used to estimate differences
in confidencelimits between mortality rates of eggsand nestlings.We
refer to mortalityratesasthe percentageof total mortalityrecordedduring the given studyperiod (incubation or nestling). All means are reported _ I SD.
RESULTS
Populationstatus.---Thebreeding population on Cajual Island conmined an estimated2000 pairsin 1992, 2500 in 1993, 3000 in 1994, 3400
in 1996,and 2500in 1997.Total adultbirdsin the areawasapproximately
6000-7500 in all yearsof the study.
Nestingbiology.--Nesting
phenologyon CajualIslandwasvariableduring
the studyperiod,with breedingoccurringFebruary-September(Fig. 2).
Mean clutch size was 1.97 _+ 0.17 (n = 97); modal clutch size was 2
(94 of 97 nests).Of 191 eggslaid, 94 (49.2%) hatched;of 94 nestlings
562]
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andA. A. b'.RodriKues
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M
A
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Ornithol.
Autumn
1999
A
S
FIGURE2. ScarletIbis breedingphenologyon CajualIsland, 1991-1997.
hatched,59 (62.8%) fledged.Mean net productivityper nestwas0.61 ___
0.90 chicks(59 fledglingsfrom 97 nests).
Sixty-five(67%) of the 97 nestsfailed to producefledglings.Total nest
failure during incubationwasrecordedfor 46 (47.4%) of the 97 monitored nests.Nineteen (37.3%) of the 51 nestsstill activeat hatchingalso
failed (Table 1). While failure waslower at the nestlingstage,the difference wasnot significant(G = 1.4, df = 1, P > 0.05). Overall, 92.4% of
deaths were due to nest failure; 7.6% occurred in successfulnests (those
fledging at least one young).
TABLEl.
Causesof nestfailure in a •ample of 97 ScarletIbis nestson CajualIsland,Brazil,
1995.
% of total
Cause of failure
Desertion
Predation
Storms a
8
9
12
Unknown
Total failed
n
nests
failures
% of failures with
known
causes
12.31
13.85
18.46
27.59
31.03
41.38
36
55.38
--
65
100.00
--
aNests that disappearedimmediately after storms.The ultimate causescould have been
direct destructionby the stormor desertionby adultsof damagednests,and the latter having
disappearedbefore our next visit.A nestwasconsideredabandonedonlywhen eggsor young
were found
cold or undernourished.
Vol.70,No.4
Breeding
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Ibis
[563
In thoseneststhat hatched at least one egg (n = 51), a mean of 1.84
+--0.36 eggshatched.These nestsoriginallycontained101 eggs,an egg
mortalityof 6.9%. An averageof 1.84 _ 0.36 chicksfledged from successfulnests (n = 32). These nestscontained 62 chicksat hatching, a
nestlingmortalityof 4.8%.
As single eggswere laid in only three nests,it wasnot possibleto compare hatchingratesbetweenclutchesof different size.Only one singleton
egg hatched, and the nestling died during the first week. During the
nestling stage, mortality was significantlylower (G = 5.2, df = 1, P <
0.05) in chicksfrom primary B/2 nests(33.2%, n = 86) in comparison
with that of primary singletons(75.0%, n-- 8).
Causesof mortality.--We were unable to identify the causesof failure
for 36 (55.4%) of the 65 failed nests.Storms,predation,and desertion
were each responsiblefor approximatelyone third of the remainingfailures (Table 1), althoughin a number of casesevidenceof more than one
causeof failure wasfound during successive
visits.Large numbersof human footprintswere found on somevisitsto the colony.We alsoobserved
individualsof both Milvago chimachimaand Cathartesaura feeding on
ibis eggs.
DISCUSSION
Population status.--The Scarlet Ibis population at Cajual Island contained approximately2000-3400 pairs during 1992-1997, and mostindividualsappearedto attempt reproductionat leastonce each season.This
contrastswith the pattern for the closelyrelated (or conspecific;Hancock
et al. 1992). White Ibis (E. albus) at some sitesin North America, where
the bulk of the population may fail to nest in drought years(Bildsteinet
al. 1990a,b;Frederick 1990). ScarletIbis on Cajual Island feed their nestlings principallycrabs (99.7% of the nestlingdiet; C. Martinez, unpubl.
data). The consistentreproductiveactivityin all yearsat Cajualislandmay
reflect a lack of dependence on freshwaterlakes and swamps,whoseannual fluctuationsin water level result in drasticchangesin prey availability. In contrast,Spaans(1990) found that ScarletIbisesoccupiedcolonies
in mangrovesirregularly in the region betweenthe Orinoco and Amazon
Rivers,and attributed this to among-yearvariation in some unidentified
ecologicalcondition.We suggest,however,that mangrovecoloniesmight
appear unoccupied in any given year if they are not monitored consistently becauseof the pronouncedannual variabilityin nestingphenology
(Fig. 2). Rodriguesand Fernandes's(1994) review of the literature also
points to a highly variable breeding seasonin Brazil, a characteristicof
tropical populationsthat would not be apparentfrom studyof more temperate populationsof Eudocimus.
Nestingbiology.--OnCajual Island, modal clutch sizewas two, and no
clutcheshad more than two eggs.This modal value persistedthroughout
brood development;mean brood sizesat hatching and at fledging were
almostidentical. Few nestlingsin successful
nestsdied. This pattern contrastswith other populationsof Eudocimus(Kushlan1977) and other ci-
564]
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andA. A. F. Rodrigues
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Ornithol.
Autumn
1999
coniiforms in which facultative brood reduction occurs (Fujioka 1985,
Mock and Parker 1986, Mock and Ploger 1986). The mean clutch sizeof
Scarlet Ibis at Cajual Island wassmaller than that recorded at other sites,
as might be expected given the latitudinal gradient describedfor other
bird species,and the smaller clutch size recorded for coastalEudocimus
populationsby Hancock et al. (1992). Variability in clutch sizewasalso
low at Cajual (cf. Kushlan1977,Bustoand Ramo 1982).
We might askwhy no clutcheswith three eggswere observed.A stable
resourcebase at Cajual may promote a relativelyinvariable clutch size.
Resourcepredictabilityis probablyalsorelatedto ciconiiformspreference
for coastal colonies (Bildstein et al. 1990b, Frederick et al. 1992). Given
that chicksat Cajual hatch and developwithout any significantasynchrony
(pers. obs.), and that more than 95% of hatchlingsin successful
nests
fledged, the Cajual population fits the definition of a brood-survivalstrategist (Mock and Forbes1994). This contrastswith many other ciconiiform
populations,which are brood-reductionstrategists.
Mock and Forbes (1994) argued that clutch size and brood reduction
can only be fully understoodwhen life-historyselectiveconsequences
are
taken into account.Adult survivalis more important in long-livedbirds.
Even in the very different caseof the coloniesstudiedby Bildsteinet al.
(1990a), a substantialpart of the adult population did not breed during
bad years. This may reflect a selectivepriority for adult survivalwhen
breeding conditions are unfavorable. Despite the fact that most adults at
Cajual attempted to breed, the fact that no more eggswere laid than the
adults were able to rear indicates a relatively small investment in each
successive
breeding attempt. As Mock and Forbes (1994) argued, the
brood-survivalstrategytends to be more advantageous
when the proportion of good yearsin an adult's life is large. The number of bad yearsis
probably relativelylow in mangroves,where Scarlet Ibis use marine resourcesalmost exclusively.
Egg and nestlingmortality in our population washigh, and wasmainly
attributableto failure of entire nests,both during incubationand nestling
development. These results are also consistentwith other studies (e.g.,
Frederick and Collopy 1989a,b; Bildstein et al. 1990a,b;Brouwer and Van
Wieringen 1990). Partial evidenceindicatesthat catastrophicevents,such
as storms and human depredation, may have been the main causesof
failure on Cajual. In a North American population of White Ibis (Fred-
erick and Collopy 1989b), nest desertionaccountedfor 70.3% of total
nest failures and 90.2% of failures of known cause (desertion in this case
included storm-relateddisappearancesand clutchesfound cold). On Cajual, the main causeof nest desertion would appear to be different, especiallyas stormsdestroyednestsdirectly,rather than inducing their desertion. The only common tendencyin the two studiesis for the ibisesto
abandon nestsreadily.
Although Scarlet Ibiseson Cajual Island initiating breeding annually
and appear to enjoy substantialreproductivesuccess,human pressurein
coastalhabitats may disturb this equilibrium and threaten populations,
Vol.70,No.4
Breeding
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[565
both through nest depredation and induction of nest desertions.The
current large population of ScarletIbis is not a guaranteeof survival.In
southern Brazil, where the specieswas once common, the ScarletIbis is
practicallyextinct (Marcondes-Machadoand Monteiro Filho 1989). Prevention of colonydisturbanceby humansmust be given the highestpriority, both at Cajual and at other sitesin Maranh5o, where human disturbance is general.
ACKNOWLEDGMENTS
We are grateful to the Fundagaode Amparo •t Pesquisado Estadodo Maranh5o for financial support; to Domingos Barrosofor his essentialcollaborationin the field work; to Dr.
Xavier Ruiz Gabriel of the Department of Animal Biology of Barcelona University for his
important suggestions
during the initial stagesof the study,and for help with bibliographic
research;to Dr. Silvio GomesMonteiro for providing the softwareusedin the calculationof
statisticaltests;and to FgttimaTeles and RosaHelena Matos for help with the bibliographic
research.Two anonymousreviewershave largelyimporved the quality of the text.
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