Sexual segregation in tropical seabirds: drivers of sex-specific foraging in the Brown Booby Sula leucogaster

Abstract

Sexual segregation in the behaviour, morphology or physiology of breeding seabirds can be related to divergent parental roles, foraging niche partitioning or sex-specific nutritional requirements. Here, we combine GPS tracking, dietary and nutritional analysis to investigate sex-specific foraging of Brown Boobies breeding on Raine Island, Great Barrier Reef, Australia. We observed sex-specific segregation in: (1) foraging location: females undertook longer trips, foraging at more distant locations than males; (2) foraging time: male activity and foraging occurred throughout the day, while female activity and foraging increased from midday to an afternoon peak; and (3) prey type, females mostly consumed flying fish, whereas males consumed equal proportions of flying fish and squid. Brown Booby diets contained five tropical prey species that significantly differed in their nutritional composition (Protein, Lipid and Water, wet mass). Despite this variation we found no differences in the overall nutritional content of prey caught by each sex. The observed sex-specific differences in prey type, location and time of capture are likely driven by a combination of a division of labour, risk partitioning and competition. However, Brown Boobies breeding on Raine Island, and other populations, might flexibly partition foraging niches by sex in response to varying competitive and environmental pressures. In light of such potential foraging dynamism, our inconclusive exploration of nutritional segregation between sexes warrants further investigation in the species.

Full text

Vol.:(0123456789)
1 3
J Ornithol
DOI 10.1007/s10336-017-1512-1
ORIGINAL ARTICLE
Sexual segregation intropical seabirds: drivers ofsex‑specific
foraging intheBrown Booby Sula leucogaster
MarkG.R.Miller1· FabiolaR.O.Silva2· GabrielE.Machovsky‑Capuska2,3·
BradleyC.Congdon1
Received: 10 April 2017 / Revised: 28 September 2017 / Accepted: 26 October 2017
© Dt. Ornithologen-Gesellschaft e.V. 2017
prey type, location and time of capture are likely driven by
a combination of a division of labour, risk partitioning and
competition. However, Brown Boobies breeding on Raine
Island, and other populations, might flexibly partition for-
aging niches by sex in response to varying competitive and
environmental pressures. In light of such potential forag-
ing dynamism, our inconclusive exploration of nutritional
segregation between sexes warrants further investigation in
the species.
Keywords Foraging strategy· Great Barrier Reef· Prey·
Right-angle mixture triangle (RMT)· Sexual segregation·
Sula leucogaster
Zusammenfassung
Sexuelle Segregation bei tropischen Seevögeln: Einflussfak
toren geschlechtsspezifischer Nahrungssuche bei Weißbau
chtölpeln Sula leucogaster
Sexuelle Segregation in Verhalten, Morphologie oder
Physiologie brütender Seevögel kann mit unterschiedlichen
Elternrollen, Nah rungsnischendifferenzierung oder
geschlechtsspezifischem Nährstoffbedarf zusammenhängen.
Hier kombinieren wir GPS-Ortung mit Nahrungs-
und Nährstoffanalysen, um die geschlechtsspezifische
Nahrungssuche bei auf Raine Island im australischen Great
Barrier Reef brütenden Weißbauchtölpeln zu untersuchen.
Wir haben geschlechtsspezifische Segregation gefunden
in Bezug auf (a) den Ort der Nahrungssuche: Weibchen
unternahmen längere Suchflüge als Männchen, da sie an
weiter entfernten Orten nach Nahrung suchten; (b) den
Zeitpunkt der Nahrungssuche: Männchen waren den ganzen
Tag über aktiv und suchten nach Nahrung, während bei
Weibchen die Aktivität und Nahrungssuche von mittags an
Abstract Sexual segregation in the behaviour, morphol-
ogy or physiology of breeding seabirds can be related to
divergent parental roles, foraging niche partitioning or
sex-specific nutritional requirements. Here, we combine
GPS tracking, dietary and nutritional analysis to investi-
gate sex-specific foraging of Brown Boobies breeding on
Raine Island, Great Barrier Reef, Australia. We observed
sex-specific segregation in: (1) foraging location: females
undertook longer trips, foraging at more distant locations
than males; (2) foraging time: male activity and foraging
occurred throughout the day, while female activity and for-
aging increased from midday to an afternoon peak; and (3)
prey type, females mostly consumed flying fish, whereas
males consumed equal proportions of flying fish and squid.
Brown Booby diets contained five tropical prey species that
significantly differed in their nutritional composition (Pro-
tein, Lipid and Water, wet mass). Despite this variation we
found no differences in the overall nutritional content of prey
caught by each sex. The observed sex-specific differences in
Communicated by C. Barbraud.
Electronic supplementary material The online version of
this article (https://doi.org/10.1007/s10336-017-1512-1) contains
supplementary material, which is available to authorized users.
* Mark G. R. Miller
mark.gr.miller@gmail.com
1 College ofScience andEngineering andCentre forTropical
Environmental andSustainability Science, James Cook
University, Cairns, Australia
2 School ofLife andEnvironmental Sciences, The University
ofSydney, Sydney, Australia
3 Charles Perkins Centre, The University ofSydney, Sydney,
Australia

J Ornithol
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zunahmen und am Nachmittag ihren Höhepunkt erreichten;
(c) Beutetyp: Weibchen fraßen hauptsächlich fliegende
Fische, während Männchen zu gleichen Teilen fliegende
Fische und Kalmare verzehrten. Die Weißbauchtölpel
nutzten fünf tropische Beutearten, die sich signifikant in ihrer
Nährstoffzusammensetzung (Proteine, Lipide und Wasser
in der Feuchtmasse) unterschieden. Trotz dieser Variation
fanden wir keine Unterschiede im Gesamtnährstoffgehalt der
von männlichen und weiblichen Tölpeln gefangenen Beute.
Die beobachteten geschlechtsspezifischen Unterschiede
im Beutetyp sowie Ort und Zeitpunkt des Beutefangs
kommen wahrscheinlich durch eine Kombination von
Arbeitsteilung, Risikoaufteilung und Konkurrenz zustande.
Bei den auf Raine Island sowie in anderen Populationen
brütenden Weißbauchtölpeln könnten die Geschlechter
die Nahrungsnische flexibel unter sich aufteilen, abhängig
von wechselnden Konkurrenz- und Umweltdrücken.
Angesichts von solchem potenziellen Nahrungsdynamismus
rechtfertigt unsere nicht beweiskräftige Erforschung der
geschlechtsspezifischen Nahrungssegregation weitere
Untersuchungen an Weißbauchtölpeln.
Introduction
Sexual segregation of foraging in breeding birds has been
observed in many terrestrial groups, including warblers
(Morse 1968; Petit etal. 1990), woodpeckers (Selander
1966) and raptors (Newton 1979). Sex-specific foraging
has also been observed in many seabirds, with the proposed
causal factors varying between studies. For example, niche
partitioning and inter-sexual competition are suggested as
drivers of sexual segregation in foraging Northern Giant
Petrels Macronectes halli (González-Solís etal. 2000)
and albatrosses Thalassarche spp. (Stahl and Sagar 2000;
Phillips etal. 2004). Whereas a division of labour, where
partners assume different reproductive roles, is considered
the principal driver of sex-specific foraging in the Alcini
(Uria, Alca, and Alle; Elliott etal. 2010) and Masked Boo-
bies Sula dactylactra (Weimerskirch etal. 2009a; Sommer-
feld etal. 2013). Seabird species can also display varying
levels of sexual size dimorphism, which is considered an
important influence upon sexual segregation in Wander-
ing Albatrosses Diomedea exulans (Shaffer etal. 2001),
boobies Sula spp. (Zavalaga etal. 2007; Weimerskirch
etal. 2009a) and frigatebirds Fregata spp. (Congdon and
Preker 2004). However, sexual segregation also occurs in
monomorphic seabirds, such as Wedge-tailed Shearwaters
Ardenna pacifica (Peck and Congdon 2006) and gannets
Morus spp. (Lewis etal. 2002; Ismar etal. 2017), ques-
tioning the importance of sex-specific size differences. A
proposed alternative explanation for sex-specific foraging
is that male and female seabirds have differing nutritional
requirements (Lewis etal. 2002; Elliott etal. 2010) that
can only be met by each sex foraging on different prey
types, size classes and/or at locations where prey avail-
ability differs.
There is a poor consensus on the drivers of sex-specific
foraging in Sulids (gannets and boobies), primarily due to
the varying levels of sexual size dimorphism within and
between species. While gannets are considered sexually
monomorphic (although females can be up to~10% heavier
than males; Cleasby etal. 2015), boobies show reverse sexual
dimorphism (RSD), where females are~14% (Red-footed
Sula sula and Masked Boobies; Weimerskirch etal. 2006,
2009a),~31% (Blue-footed Booby Sula nebouxii; Guerra
and Drummond 1995), or between 27 and 38% heavier than
males (Brown Booby Sula leucogaster; Nunes etal. 2016;
Lewis etal. 2005). The greater weight of female boobies has
been used as a mechanistic explanation for them diving deeper
(Weimerskirch etal. 2006; Zavalaga etal. 2007), while lower
flight costs attributed to the smaller body size of male Brown
Boobies has been used to explain their greater foraging range
(Lewis etal. 2005). The larger female has been observed to
take a greater responsibility for chick provisioning (larger
meals), while the smaller male specializes in nest defence in
Masked Boobies (Weimerskirch etal. 2009a) and to a lesser
extent in Red-footed Boobies (Lormee etal. 2005) and Blue-
footed Boobies (Guerra and Drummond 1995). However,
in these studies a division of labour did not appear to foster
sexual segregation in foraging behaviour.
Intra-specific competition is known to drive foraging site
segregation in Sulids, with competition pressure in larger
populations forcing individuals to forage further from the
colony (Lewis etal. 2001; Oppel etal. 2015). However, little
support for inter-sexual competition as a driver of foraging
segregation exists in either monomorphic Northern Gannets
Morus bassanus (Lewis etal. 2002; Cleasby etal. 2015) or
sexually dimorphic boobies (Pontón-Cevallos etal. 2017;
Weimerskirch etal. 2009a). This is surprising as the larger
size of female boobies could enable local dominance and
exclusion of males as seen in other seabirds (González-Solís
etal. 2000; Stahl and Sagar 2000). A potential explanation
is that different booby species often breed sympatrically and
that inter-specific competition is more significant than intra-
specific competition (Young etal. 2010; Pontón-Cevallos
etal. 2017; but see Weimerskirch etal. 2009b).
Nutritional segregation between sexes is an often dis-
cussed, but rarely tested, driver of seabird foraging differ-
ences (Lewis etal. 2002, 2005; Peck and Congdon 2006;
Sommerfeld etal. 2013). Multiple studies have compared
prey items captured by male and female boobies, most
finding high overlap (Weimerskirch etal. 2006; Zavalaga
etal. 2007; Weimerskirch etal. 2009a) or small differences
(Castillo-Guerrero etal. 2016). However, these studies did
not explore potential sexual differences in the nutritional

J Ornithol
1 3
composition of prey consumed. In a wide range of species,
foraging goals are related to a specific amount or proportion
of nutrients (Raubenheimer etal. 2015). Within Sulid spe-
cies, nutritional requirements could vary between sexes to
offset sex-specific physiological costs, such as female ovipo-
sition compensation (Lewis etal. 2002; Ismar etal. 2017).
Such demands could lead to foraging segregation, so as to
allow each sex to obtain prey of appropriate nutritional qual-
ity. Right-angled mixture triangle modelling (RMT) enables
researchers to explore the relationships among the propor-
tional content of nutrients in foods and diets, through visual-
isation in two-dimensional space (Raubenheimer 2011). To
date RMTs have provided novel insights into the nutritional
ecology of two Sulid species in the wild, Australasian Gan-
nets Morus serrator (Tait etal. 2014; Machovsky-Capuska
etal. 2016b) and Masked Boobies Sula dactylatra tasmani
(Machovsky-Capuska etal. 2016a). These studies high-
lighted the nutritional complexities of marine environments
and provide the only evidence of sex-specific nutritional
foraging strategies in seabirds. Recently, RMT models were
also used to integrate food-level approaches in a multi-nutri-
ent framework to provide fresh insights into dietary breadth
and niche theory (Machovsky-Capuska etal. 2016c). Using
this multi-nutrient framework, the dietary niche of species
can be characterized across three levels: (1) the “funda-
mental nutritional niche” known as the nutritional diet that
a population needs to persist; (2) the “realised nutritional
niche” defined as the observed diet of a population that can
be subject to ecological constraints such as prey availability
or competition, and (3) the “prey composition niche” con-
sidered as the range of ecological and physical attributes of
prey that the species is able to consume.
The Brown Booby (hereafter boobies) shows consist-
ent RSD and high local adaptation across its global range
(Morris-Pocock etal. 2011; Nunes etal. 2016), making it
a good model for studying drivers of sex-specific foraging
(Castillo-Guerrero etal. 2016). Locally adapted popula-
tions demonstrate different sex-specific foraging strategies:
males undertake longer foraging trips than females while
incubating at Johnston Atoll, Central Pacific (Lewis etal.
2005) and while chick-rearing at Dog Island, Anguilla
(Soanes etal. 2015). Conversely females forage further
from the colony while chick-rearing at Clipperton Island,
Eastern Pacific (Gilardi 1992) and undertake longer forag-
ing trips while chick-rearing at Isla San Ildefonso, Mexico
(Weimerskirch etal. 2009b). The plasticity of sex-specific
foraging behaviour shown by these Brown Booby popula-
tions is unlikely to be explained by a single underlying
driver (e.g., competition, sexual size dimorphism or a divi-
sion of labour). As such, sex-specific nutritional demands
warrant investigation as a potential explanation for sexual
segregation in this species.
Here, we combined the use of global position satellite
(GPS) data loggers, morphometric measurements, dietary
analysis, nutritional composition of prey and nutritional
modelling (RMT) to gain a better understanding of the driv-
ers of sexual segregation in Brown Boobies from the Far
Northern Great Barrier Reef (GBR), Australia. Based on a
synthesis of previously available information we predict that
Brown Boobies from this GBR population should: (1) dis-
play RSD; (2) show sexual segregation in foraging grounds;
(3) show sex-specific differences in the timing of foraging
activities; (4) consume different prey based on sex; and (5)
have sex-specific realised nutritional niches.
Methods
Study area, capture andhandling
This study was carried out on Raine Island (144°02′E,
11°35′S), a 28-hectare, vegetated coral cay on the outer edge
of the Northern GBR, Australia. The Brown Booby popula-
tion on Raine Island was last estimated at 2642 individuals
between 1994 and 2003 (Batianoff and Cornelius 2005) and
breeds year-round with a peak in November and Decem-
ber (Blaber etal. 1998). GPS tracking of Brown Boobies
was undertaken during the chick-rearing phase in Decem-
ber 2014, when chicks were~1month old. I-gotU GT-120
GPS loggers (Mobile Action Technology) were programmed
to obtain fixes every minute and sealed in heat-shrink tub-
ing. Birds were captured by hand at dusk and loggers were
attached to three central tail feathers using Tesa® 4651 Tape
(Weimerskirch etal. 2005). Devices weighed~17g and
remained on the birds for several days so as to gather data
on consecutive foraging trips (Oppel etal. 2015). Birds were
recaptured at dusk for logger retrieval. Body mass and mor-
phometric measurements, including flattened wing chord,
tarsus and culmen lengths were obtained. Additionally, for
chicks associated with adults carrying loggers, we obtained
chick tarsus and body mass measurements upon adult recap-
ture. Handling of adults and chicks was limited to<10min.
Boobies were sexed using facial skin, bill and foot coloura-
tion (Nelson 1978). Diet samples were opportunistically col-
lected from adults that regurgitated upon handling and stored
in polyethylene bags at −20°C.
Diet composition
Prey obtained from the regurgitations were individually
weighed (±0.1g), total length measured (±0.1cm) and
identified to the lowest possible taxonomic level using pub-
lished guides (Allen 2009). For each prey species the per-
centage contribution of the individual to the total weight was
calculated as a mass percentage (M%, Duffy and Jackson

J Ornithol
1 3
1986). The total number of prey items contributed by an
individual of a particular species was calculated as a percent-
age termed numerical abundance (N%), and the frequency of
occurrence (F%) was calculated as the percentage of birds
that had one particular species present in the regurgitation
(Schuckard etal. 2012). The above metrics were summarised
using the index of relative importance (IRI), calculated for
each prey species as IRI=F%×(M%+N%) and expressed
as a percentage (IRI%) by dividing by the sum of IRI values
from all prey species (Cortés 1997).
Nutritional composition ofprey anddiet
To measure the nutritional composition of prey species and esti-
mate the nutritional composition of boobies’ diets, only undi-
gested prey was selected for nutritional composition analyses
(Tait etal. 2014). The most representative prey samples selected
included flying fish (Cypselurus spp., n=6), Blue Sprat (Spra-
telloides robustus, n=8), Smooth belly Sardine (Amblygaster
leiogaster, n=2), Leatherjacket (Catherhines fronticinctus,
n=2) and squid (Sthenoteuthis spp., n=8). Prior to analysis,
each sample was partially thawed and weighed (±0.1g), dried
for 5days in a freeze dryer and ground in a laboratory mill.
We measured total nitrogen (N) using Kjeldahl analysis and
estimated crude protein by multiplying N by a factor of 6.25
(AOAC method 981.10; AOAC 2005). We used the Mojonnier
method to measure total lipid (ether extract) (AOAC 954.02;
Min and Steensen 1998). Ash was measured by ignition in
a furnace at 550°C (AOAC method 920.15; AOAC 2005).
Finally, we measured moisture (hereafter water) by drying the
sample in a convection oven at 125°C (AOAC method 950.46;
AOAC 2002) and combining this moisture loss with initial loss
from the overnight dry down.
GPS data analyses
All data handling and statistical analyses were performed
in the statistical software environment program R version
3.2.4 (R Core Team 2017). Tracking data were speed filtered
(removal of points>75km/h), and gap filled (interpolation
to 1min interval) prior to analyses. Individual foraging trips
were extracted from multi-day tracks using BirdLife Inter-
national’s ‘marine IBA’ R package (Lascelles etal. 2016).
We also calculated time spent on the colony between suc-
cessive foraging trips for birds that were tracked for several
days. To identify behavioural states, we applied Hidden
Markov Models (HMM) to the GPS data. We constructed a
single HMM using the full GPS tracking dataset, including
an identifier for each trip, using the ‘moveHMM’ R pack-
age (Michelot etal. 2016). For each consecutive GPS point
the step length and turning angle were calculated, produc-
ing three distributions consistent with foraging, resting and
transiting behaviours observed in HMM studies on Sulids
(Boyd etal. 2014; Oppel etal. 2015). To visualise foraging
areas of sexes, we estimated 99 and 50% utilization distribu-
tions (UDs) using kernel analysis of foraging locations from
the HMM, in the ‘adehabitatHR’ R package (Calenge 2006).
Difference inmovements anddaily activity
We estimated a range of movement parameters for each
foraging trip including maximum distance away from the
colony (MDC), mean foraging distance from the colony
(MFD), total foraging path (TFP), foraging trip duration
(FTD), foraging time (FT), transiting time (TT), resting time
(RT square-root transformed) and time on colony, from the
GPS data and HMM results. We constructed separate linear
mixed models (LMMs) in which each movement parameter
was fitted against a single predictor for sex, adult body mass,
chick condition (chick mass/tarsus) and date, with individual
bird as the random effect, in the ‘lme4’ R package (Bates
etal. 2015). Bonferroni-corrected p-values for multiple
comparisons were used to test for significant differences
(α=0.05). We used linear models (LMs) and quasibinomial
generalized linear models (GLMs) to test for sex-specific
differences in: colony departure and return times; the per-
centage of boobies at-sea between morning (hour<12), and
afternoon (hour≥12); and the number of foraging locations
between morning and afternoon.
Difference inprey species
We tested for an association between prey species occur-
rence and sex of birds using Chi squared analysis. To evalu-
ate sex-specific differences in the number of prey items and
the mass of regurgitate collected from adults, we fitted each
as a response against bird sex in a quasipoisson GLM. Simi-
larly, to evaluate variation in prey species weight and length,
two LMs were constructed, where the log-transformed
weight and length of prey were fitted against bird sex.
Nutritional composition ofprey anddiets
To assess differences in the nutritional composition of prey
(comprised of different species), LMs were constructed
using protein (P), lipid (L), water (W), protein-to-lipid
ratio (P:L) or water-to-lipid ratio (W:L) as responses fitted
against bird sex and prey species. We present the differences
in the proportional wet mass contribution of the nutritional
compositions of prey items and diets using RMT modelling
(Raubenheimer 2011). To estimate energy (E) supplied by
nutrients in each prey, we converted macronutrient masses
to energy using conversion factors of 17 kJ/g for P, and 37
kJ/g for L (NRC 1989). The data on the proportion of prey

J Ornithol
1 3
species enabled us to estimate the nutritional composition
for 91.3% (wet mass) of the diet of Brown Boobies.
Foraging performance
To evaluate the efficiency of nutrient gains, the foraging per-
formance parameters TFP, FTD and FT obtained for each
foraging trip were divided by the quantity of each nutri-
ent obtained, as per Machovsky-Capuska etal. (2016a). For
example, P (g) divided by FTD (h) was to establish intake of
P (g/h). Separate LMs using each combined nutrient/perfor-
mance parameter were fitted against sex and the individual
bird, accounting for interactions. All results are presented as
mean±standard deviation (SD).
Results
Adult morphometric measurements andmovement
Female boobies were 16.3% heavier than males, and had longer
tarsi, wings and culmens (n female=15, n male=11; Table1).
In total, 19 individuals (female=10, male=9) were success-
fully tracked, comprising 58 individual trips. Almost all trips
foraged outside the reef, most over pelagic waters (depths
1000–2000m) and some at the reef edge (Fig.1a). All individ-
uals made a single foraging trip each day, except for three males
that undertook a second short trip, before dusk (FTD<2.5h).
The mean MDC that boobies travelled was 57±22km (maxi-
mum of 113km) with a mean MFD of 47±18km from the
colony. The mean TFP that boobies covered was 150±59km,
taking an average FTD of 5.42±2.06h. During trips, boobies
spent a mean time of 1.84±0.8h foraging, a mean time of
2.84±1.21h transiting, and a mean time of 0.75±0.63h rest-
ing. We detected significant variation between sexes in move-
ment parameters MDC, MFD and TFP (Table1). This trans-
lated spatially into a general core-foraging area shared by sexes,
but with the female distribution more distant from the colony
relative to the male distribution (Fig.1b). Adult body mass,
chick condition and date did not vary significantly in relation
to any movement parameters. Variance was detected within the
individual bird random effect for movement parameters MFD,
RT and time on colony but not MDC, TFP, FTD, FT and TT.
Daily activity budget
Boobies spent a mean time on the colony of 18.64±2.92h
between successive trips, both parents returned to the colony
at night and males spent longer guarding the chick during
the day than females, but not significantly so (Table1).
Boobies were active at-sea from 05:26 to 20:57 with birds
departing and returning to the colony throughout the day
(Fig.2). On average, sexes departed the colony at the same
time (females, 11.12±2.53h, males 11.25±4.18h; LM,
F=0.021, df=1, p=0.886). However, female departure
was concentrated in the morning (Fig.2a) whereas male
departure spread throughout the day (Fig.2b). Females
returned to the colony at a mean time of 17.38±2.10h,
whereas males returned significantly earlier at a mean time
of 15.94±2.82h (LM, F=4.73, df=1, p=0.034). The
mean percentage of female boobies at-sea during the morn-
ing (24.63±18.98%), was significantly lower than during
the afternoon (66.38±32.73%; GLM, F=2.54, df=1,
p=0.135; Fig.2a). The mean percentage of male boobies
at-sea was no different during the morning (32.38±14.18%)
or afternoon (44.29±13.25%; GLM, F=2.54, df=1,
p=0.135; Fig.2b). The average number of female booby
foraging locations during the morning (85±74) was sig-
nificantly lower than during the afternoon (338±230; LM,
F=8.75, df=1, p=0.011). The average number of male
booby foraging locations did not differ during the morning
(207±115) or afternoon (244±136; LM, F=0.32, df=1,
p=0.578).
Table 1 Morphological (n=26 birds; female=15, male=11) and
movement parameter (n= 19 birds; female = 10, male=9) differ-
ences between males and female Brown Boobies, rearing chicks on
Raine Island in December 2014
Mean±1 standard error for each sex is given, corresponding test sta-
tistics from ANOVA (F value) or Welch’s t test (t value), and signifi-
cance (Bonferroni-corrected p value)
For each parameter MDC maximum distance from the colony, MFD
mean distance of foraging from the colony, TFP total foraging path,
FTD foraging trip duration, FT foraging time, TT transiting time, RT
resting time
Parameter Females Males Statistic p
Mass (g) 1430±147 1197±65 t=5.41 <0.001
Tarsus (mm) 50.73±1.16 48.36±2.46 t=2.96 0.054
Culmen length
(mm)
97.66±2.61 93.27±3.00 t=3.89 0.004
Culmen height
(mm)
34.60±1.88 33.45±1.29 t=1.83 0.392
Wing chord (cm) 41.27±1.13 40.36±1.05 t=2.09 0.238
MDC (km) 65.84±4.12 50.33±3.72 F=7.80 0.049
MFD (km) 54.82±3.22 40.51±2.9 F=10.92 0.012
TFP (km) 173.61±11 131.71±9.9 F=8.05 0.044
FTD (h) 6.18±0.38 4.8±0.35 F=7.10 0.070
FT (h) 1.95±0.16 1.75±0.14 F=0.89 1
TT (h) 3.25±0.23 2.51±0.2 F=5.82 0.133
RT (h) 0.92±0.08 0.69±0.08 F=4.54 0.289
Time on colony
(h)
17.6±0.83 19.58±0.74 F=3.15 0.101

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Diet composition
A total of 19 regurgitations were collected (n=9 females,
n= 8 males, n=2 sex unknown) with a mean mass of
96.20±13.80g. Of 134 individual prey items, 127 were
identifiable and were comprised of four species of fish, flying
fish Cypselurus spp., Blue Sprat S. robustus, Smooth belly
Sardine A. leiogaster and Leatherjacket C. fronticinctus, and
one species of squid Sthenoteuthis spp. Only one prey spe-
cies was present in 52.6% of regurgitates, 36.8% had two
prey species present, and 10.5% had three species present.
Flying fish was the most important prey species (most fre-
quent and most abundant by mass, IRI%) in the diet of boo-
bies and females, in particular; whereas squid was the most
important prey (IRI%) in the diet of males (Table2). Overall,
prey items had a mean weight of 18.55±3.32g and a mean
length of 11.59±0.93cm. No differences were detected
in number of prey items that individual foragers brought
back to the colony (GLM, F=0.01, df=1, p=0.917). We
observed a significant association between prey occurrence
and sex, where flying fish was the most frequent (66.7%)
for females, while squid and flying fish were equally fre-
quent (75%) for males (Chi square test, χ2=13.805, df=4,
p<0.05, Table2). However, no differences were observed
in the total mass of regurgitate by males or females (GLM,
F=0.0004, df=1, p=0.984). Similarly, no differences
were detected in weight (LM, F=1.30, df=1, p=0.257)
and length (LM, F=1.73, df=1 p=0.192) of prey items
between sexes of birds.
Nutritional composition ofprey anddiets
P, L and W wet mass proportions varied significantly
between prey species (P: LM, F=3.69, df=4, p<0.05;
L: LM, F=8.65, df=4, p<0.05; W: LM, F=10.51,
df=4, p<0.001). Blue Sprat had the highest mean L
(1.9±0.43%) and highest W (77.35±0.91%), Smooth
Belly Sardine had the highest P (21.78±0.33%) and the
lowest W (70.94±0.88%) and Leatherjacket had the low-
est P (17.32±0%) and L (1±0%; see ESM Appendix1).
There were no significant differences in the wet mass
nutritional composition of prey captured by each sex (P:
Fig. 1 GPS tracking of 19 (n female=10, n male=9) chick-rearing Brown Boobies from Raine Island in December 2014. Foraging locations
(a) and kernel density based utilization distributions (UDs) of foraging locations (b) are shown for each sex

J Ornithol
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LM, F=0.01, df=1, p=0.906; L: LM, F=0.05, df=1,
p= 0.827; W: LM, F=0.002, df=1, p=0.969), P:L
(LM, F=0.20, df=1, p=0.660) and W:L (LM, F=2.27,
df=1, p=0.134). The RMT shows that P:L of the different
prey species consumed varied from 3.7:1.0 (Blue Sprat),
8.3:1.0 (Leatherjacket), 11.6:1.0 (squid), 12.2:1.0 (Smooth
Belly Sardine) to 16.9:1.0 (flying fish) and provides an
estimate of the Brown Booby minimal realised nutritional
niche and minimal prey composition niche (Fig.3). The
W:L also varied considerably from 7.1:1.0 (Blue Sprat),
Fig. 2 Daily activity data for female (a) and male (b) chick-rearing
Brown Boobies from Raine Island in December 2014. The histo-
gram gives the percent of booby foraging trips (female n=26, male
n=32) at-sea in each hour, the black line is a density plot of time-
stamped foraging locations from active booby trips, scaled from 0
to 100. The black circles are the number of foraging trips departing
and black triangles the number of foraging trips returning within each
hour
Table 2 Composition of the
diet of chick-rearing Brown
Boobies, reflected by analysis
of regurgitations collected from
Raine Island in December 2014
M% mass, N% numerical abundance, F% frequency of occurrence, IRI% index of relative importance. Prey
Species: S squid Sthenoteuthis spp., FF flying fish Cypselurus spp., BS Blue Sprat S. robustus, SS Smooth
Belly Sardine A. leiogaster, L Leatherjacket C. fronticinctus. Regurgitations were collected from 19 birds
(females=9, males=8, unknown sex=2)
Prey species Females n=9 Males n=8 Total birds n=19
M%N%F%IRI% M%N%F%IRI% M%N%F% IRI%
S 10.89 19.05 33.33 11.45 56.59 44.44 75.00 52.97 33.35 31.50 52.63 31.01
FF 47.31 50.79 66.67 75.03 41.53 46.30 75.00 46.05 47.78 49.61 73.68 65.19
BS 11.91 22.22 22.22 8.70 0.99 7.41 12.50 0.73 5.56 14.17 15.79 2.83
SS 28.82 6.35 11.11 4.48 0.00 0.00 0.00 0.00 12.46 3.15 5.26 0.75
L 1.08 1.59 11.11 0.34 0.89 1.85 12.50 0.24 0.84 1.57 10.53 0.23

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36.4:1.0 (Leatherjacket), 40.5:1.0 (squid), 39.7:1.0 (Smooth
Belly Sardine) to 58.6:1.0 (flying fish) (Fig.3). No differ-
ences between sexes were observed in the wet mass nutri-
tional ratios (males, P:L=13.2:1.0 and W:L=45.4:1.0
and females, P:L=13.2:1.0 and W:L=44.6:1.0, P:L, LM,
F=0.002 df=1, p=0.963 and W:L, LM, F=0.011 df=1,
p=0.917, respectively) (Fig.3) or in the overall dietary
energy consumption (males=399.05±289.95 kJ/g and
females=362.70±257.10 kj/g, LM, F=0.07, df=15,
p=0.79).
Foraging performance
Of the 19 regurgitations collected, only six were from birds
carrying GPS data loggers. Therefore, these samples were
used to establish foraging performance in relation to the
nutritional intake (Table3). No significant differences in
the costs of nutrient gains (wet mass P, L, W) or in P:L or
W:L, in relation to the TFP, FTD, and FT, were observed
between sexes or individual birds (Table4).
Fig. 3 Right-angled mixture triangle (RMT) showing proportional
data on three mixture components [here protein (P), lipid (L) and
water (W)] in two dimensional graphs. To plot the nutritional com-
positions (P, L and W) in the RMT, each nutrient was expressed as
a wet mass percentage of the sum of the three (Raubenheimer 2011).
The circles represent prey species consumed by chick-rearing Brown
Boobies from Raine Island in 2014. Grey filled circle= Blue Sprat
S. robustus (19.1% P, 1.9% L, 79.0% W); Black filled circle=Leath-
erjacket C. fronticinctus (18.4% P, 1.1% L, 80.6% W); Circle filled
with lines=flying fish Cypselurus spp. (22.0% P, 1.3% L, 76.7% W);
Black hollow circle=Smooth Belly Sardine A. leiogaster (23.0% P,
1.9% L, 75.1% W); Black and grey filled circle=squid Sthenoteu-
this spp. (21.9% P, 1.9% L, 76.2% W). Black triangle= male mini-
mal realised nutritional niche (21.9% P, 1.7% L, 76.5% W) and black
square=female minimal realised nutritional niche (21.7% P, 1.6% L,
76.8% W), both constrain within the minimal prey composition nutri-
tional niche (black dot-dash line)

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Discussion
As predicted, the Brown Booby population of Raine island
displays RSD and, during our study period, segregated the
timing and location of foraging between sexes. However,
while our prediction that male and female boobies would
consume different prey items was proved correct, our expec-
tation that this would translate into sex-specific realised
nutritional niches was not observed.
Firstly, the temporal differences in foraging behav-
iour we observed between Brown Booby sexes could be
due to a division of labour (Weimerskirch etal. 2009a).
The~1month old chicks of our sampled boobies were
always guarded by at least one parent (MGRM pers. obs.),
suggesting this behaviour may be obligatory for reproduc-
tive success. Males spent more time than females at the nest,
possibly because they are better suited to territory defence
(Weimerskirch etal. 2006, 2009a), or to increase opportuni-
ties for extra-pair copulations (Gilardi 1992), while females
made longer foraging trips. This division of labour, which
provides greater foraging opportunities for females, may also
allow them to recover from oviposition costs (although this
is more likely during incubation than chick-rearing; Ismar
etal. 2017), or to accumulate a large food payload for the
chick (Weimerskirch etal. 2009a).
Alternatively, Brown Booby pairs could temporally parti-
tion foraging to minimise the risk of kleptoparasitism (Elli-
ott etal. 2010). The observed sexual differences in Brown
Booby foraging activity mirror sexual differences in the
timing of chick provisioning in Lesser Frigatebirds Fregata
ariel at the same breeding location during the December
period (Congdon and Preker 2004). Raine Island supports
Table 3 Foraging performance and nutritional intake from single foraging trips made by six Brown Boobies, while rearing chicks on Raine
Island in December 2014
MDC Maximum distance from colony, TFP total foraging path, FTD foraging trip duration, FT foraging time, TT transiting time, RT resting
time, P protein, L lipid, W water, P:L protein-to-lipid ratio, and W:L water-to-lipid ratio
Bird Sex MDC (km) TFP (km) FTD (h) FT (h) TT (h) RT (h) P (g) L (g) W (g) P:L W:L
23 M 13.33 39.52 1.47 0.82 0.65 0.02 27.53 1.63 95.26 16.89 58.44
17 F 69.86 182.34 6.52 2.22 3.65 0.67 13.50 1.04 46.88 12.98 45.08
26 M 77.44 213.22 6.93 2.07 4.38 0.50 6.71 0.58 23.35 11.57 40.26
11 F 66.11 188.32 8.57 2.85 3.37 2.37 8.70 0.51 30.12 16.93 58.59
1 M 38.95 93.80 2.80 1.02 1.73 0.07 4.93 0.42 17.16 11.74 40.86
35 F 33.20 79.47 4.47 2.00 1.23 1.25 26.38 6.90 54.02 3.82 7.83
Table 4 Differences in the
foraging performance of single
foraging trips made by six
Brown Boobies, while rearing
chicks on Raine Island in
December 2014
Variation by bird sex and between the six individual birds is shown with mean±1 standard error
F (F value), and p (p value). For each parameter P protein, L lipid, W water, P:L protein-to-lipid ratio, W:L
water-to-lipid ratio, TFP total foraging path, FTD foraging trip duration, and FT foraging time
Parameter Female Male F p Individual
birds F p
P/TFP (g/km) 0.15±0.03 0.26±0.22 0.0004 0.979 0.21±0.11 1.341 0.311
L/TFP (g/km) 0.03±0.03 0.01±0.01 0.405 0.448 0.02±0.01 4.928 0.091
W/TFP (g/km) 0.37±0.16 0.90±0.76 0.028 0.876 0.63±0.37 0.867 0.405
P:L/TFP (g/km) 0.07±0.01 0.20±0.12 1.272 0.323 0.14±0.06 0.325 0.599
W:L/TFP (g/km) 0.22±0.06 0.70±0.39 1.794 0.252 0.46±0.21 0.715 0.445
P/FTD (g/h) 3.00±1.48 7.17±5.81 0.092 0.777 5.08±2.84 0.877 0.402
L/FTD (g/h) 0.59±0.48 0.45±0.33 0.058 0.822 0.52±0.26 3.750 0.125
W/FTD (g/h) 7.60±2.48 24.82±20.08 0.257 0.639 16.21±9.83 0.438 0.545
P:L/FTD (g/h) 1.61±0.38 5.79±2.95 2.953 0.166 3.70±1.63 0.708 0.447
W:L/FTD (g/h) 5.17±1.71 20.08±10.20 2.953 0.161 12.63±5.70 1.159 0.342
P/FT (g/h) 0.07±0.05 0.31±0.27 0.293 0.617 0.19±0.13 0.653 0.464
L/FT (g/h) 1.37±1.05 0.89±0.55 0.167 0.709 1.13±0.54 4.239 0.109
W/FT (g/h) 19.57±4.81 48.09±34.08 0.313 0.606 33.83±16.66 0.414 0.555
P:L/FT (g/h) 4.57±1.33 12.57±4.37 3.514 0.134 8.57±2.71 1.578 0.278
W:L/FT (g/h) 14.92±5.51 43.59±15.06 3.196 0.148 29.26±9.62 0.378 0.572

J Ornithol
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the largest Lesser Frigatebird colony on the GBR and chick-
rearing Brown Boobies are their preferred target for piracy
(Batianoff and Cornelius 2005). Therefore, to minimise the
impact of kleptoparasitism on chick provisioning, male boo-
bies may risk the piracy of meals obtained on shorter, morn-
ing trips, while females return en-mass at sunset to avoid
frigatebird attacks (Cruz etal. 2013).
Finally, the observation that females forage more in the
afternoon could simply be a product of spatial niche par-
titioning (Phillips etal. 2004), where longer transit times
and late arrival at the colony are a consequence of females
using more distant foraging grounds not accessed by males.
Females foraged for approximately the same duration while
at-sea and caught the same sized prey as males. There-
fore, to sustain their larger body mass and increased flight
costs relative to males, females must access areas where
they capture more prey items at a faster rate than males.
Although we did not observe complete spatial or temporal
foraging segregation between sexes, the combination of
females foraging at greater distance from the colony and
more often during the afternoon may allow them to feed
under reduced inter-sexual and inter-specific competition,
affording higher prey availability (Ashmole and Ashmole
1967; Lewis etal. 2001; Oppel etal. 2015). This may be
particularly important given the potential additional for-
aging competition associated with the 13 other seabird
species breeding on Raine Island (Batianoff and Cornelius
2005; Pontón-Cevallos etal. 2017).
Our results that males consumed more squid and females
more flying fish could be explained by sexes foraging in
different habitats (Cleasby etal. 2015), or at different times
of day (Lewis etal. 2002). Differing spatio-temporal prey
encounter rates between sexes could simply be a product of
constraints imposed by niche partitioning, risk avoidance or
divisions of labour. Shorter male trips, whether constrained
by a higher nest attendance role or competition with females,
could increase encounters with juvenile squid which are
evenly distributed across lagoon, passage, reef and open
ocean habitats of the GBR (Moltschaniwskyj and Doherty
1995). While longer, afternoon female trips, potentially
timed to protect a greater food payload from kleptoparasit-
ism, could increase encounters with pelagic-dwelling flying
fish (Randall etal. 1997). Additionally, female foraging in
late afternoon could exploit a concurrent peak in subsurface
predator activity (Clua and Grosvalet 2001), making particu-
lar prey more easily captured due to facilitated foraging with
predatory fish and cetaceans (Ashmole and Ashmole 1967;
Spear etal. 2007).
Alternatively, prey species could be distributed homo-
geneously across the seascape used by Raine Island Brown
Boobies, and differences in prey capture relate to mor-
phological differences between the sexes (Zavalaga etal.
2007). Male Brown Boobies have been shown to dive more
frequently than females, on account of reduced energetic
costs from their smaller body size (Lewis etal. 2005), while
female Blue-footed Boobies dive deeper than males due to
their greater body size (Zavalaga etal. 2007). In our study,
a higher male diving rate is hinted at by lower at-sea resting
times relative to females, and, although we did not collect
data on dive depths, we speculate that body size somehow
influences flying fish and squid capture. Our inter-sex Brown
Booby prey differences mirror inter-species differences
between tropical Sulids: the largest bodied, the Masked
Booby, predominantly catches flying fish, whereas the small-
est bodied, the Red-footed Booby, predominantly catches
squid (Blaber etal. 1995; Weimerskirch etal. 2006, 2009a).
Our results showed that Brown Boobies from Raine
Island consumed prey that differed in their nutritional
composition supporting previous suggestions that marine
predators forage in a nutritionally complex environment
(Machovsky-Capuska etal. 2016a, b; Denuncio et al.
2017). We have also estimated, for the first time, the mini-
mal range of prey that contributes to the food composi-
tion niche and the minimal realised nutritional niche of
the Brown Booby. Our findings on the realised nutritional
niches between sexes revealed no significant differences
in mass or energy, and they are inconsistent with previ-
ous suggestions that males and females differ in their
nutritional requirements (Lewis etal. 2002; Machovsky-
Capuska etal. 2016b). However, these results could be
subject to potential caveats related to our relatively small
sample size and difficulties in collecting regurgitations
from foragers upon arrival at the colony. The latter led to
the possibility that adults had already fed a portion of their
foraging gains to chicks directly influencing our estimates
of the prey composition and realised nutritional niches.
Such caveats likely contributed to the similarities in real-
ised nutritional niches observed between sexes, in spite of
male preference for higher lipid prey (squid) relative to
females. Considering that Brown Boobies at Raine Island
have a dynamic diet, dominated at different times by squid,
Blue Sprat and goatfish Mulloides spp. (Blaber etal. 1995),
we suggest that future studies aiming to describe the prey
composition and nutritional niches of Sulids should collect
a large number of regurgitations over a broad temporal
scale.
Brown Boobies display high levels of local adapta-
tion (Morris-Pocock etal. 2011; Nunes etal. 2016) which
makes them useful for understanding connections between
sex-specific foraging and size dimorphism. The size of
Brown Boobies has been shown to vary with primary
productivity: populations of larger birds being found in
productive waters and populations of smaller birds in oli-
gotrophic waters (Nunes etal. 2016). Despite this local
adaptation, RSD was consistent across the six populations
sampled with females 5.2% larger and 21.0% heavier. It

J Ornithol
1 3
seems very unlikely that consistent RSD could regulate
consistent sex-specific foraging strategies across the differ-
ent populations in the Nunes etal. (2016) study, given the
differing geographic locations (continental shelf vs. oce-
anic island), and productivity regimes of sampled colonies
(Weimerskirch etal. 2009b; Castillo-Guerrero etal. 2016).
As such, segregation in male and female foraging may
operate independently of size-dimorphism (Lewis etal.
2002), as a flexible response to resource availability (Paiva
etal. 2017). Our findings of foraging niche partitioning (by
location, time of day and prey type) between sexes con-
trast with those of Pontón-Cevallos etal. (2017), that found
no evidence of inter-sexual niche partitioning in breeding
Brown Boobies on Raine Island. The differences could be
explained by competition pressure, as Pontón-Cevallos etal.
(2017) collected samples during July when breeding effort
was low, whereas our study was during December and coin-
cided with peak summer breeding activity for Brown Boo-
bies and the majority of Raine Island seabirds (Batianoff
and Cornelius 2005). By modifying their foraging behav-
iour (such as partitioning by sex), Brown Boobies could
offset higher competition for resources at times of peak
breeding (Lewis etal. 2001; Oppel etal. 2015). Being able
to flexibly partition foraging niche by sex in response to
poor ocean conditions (Paiva etal. 2017), could also assist
Brown Boobies to overcome periodic environmental vari-
ability (Castillo-Guerrero etal. 2016). This plasticity in the
Brown Booby foraging strategy likely explains the dispar-
ity between various sex-specific foraging studies across the
species range.
In conclusion, our study found evidence for multi-
ple drivers of sex-specific foraging in the Brown Booby
population at Raine Island. Our exploration of nutritional
segregation between sexes, although inconclusive, pro-
vides a stepping-stone towards understanding the nutri-
tional requirements for this species and warrants further
investigation. We suggest that a combination of a division
of labour, risk partitioning and competition likely drives
sexual segregation in this population. More widely, RSD
likely prescribes different breeding roles in the Brown
Booby (larger female can deliver larger meals) but is
maintained in the species as a mechanism to overcome
resource variability. By being different sizes, male and
female Brown Boobies have different mechanical forag-
ing advantages and are thus able to partition more eas-
ily during reduced resource conditions. The oligotrophic
waters and peak breeding season of Raine Island in
December exemplify such conditions and our observed
sex-specific partitioning of foraging niche (by location,
time of day and prey type) demonstrated the Brown Boo-
bies’ response.
Acknowledgements We would like to thank Damon Shearer,
Andrew Dunstan and crew of the QPWS Reef Ranger for transport,
accommodation and logistical support on and off of Raine Island. We
also thank two anonymous reviewers, whose comments significantly
improved the manuscript. This research was funded by the Australian
Research Council (ARC) LP 0562157, the Marine and Tropical Sci-
ences Research Facility (MTSRF), the Great Barrier Reef Marine Park
Authority (GBRMPA) and National Environmental Research Program
(NERP). Fieldwork procedures were authorised under James Cook Uni-
versity Ethics Approval A1992. GEMC is supported by the Loxton
research fellowship from The University of Sydney.
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