ArticlePDF Available

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

Authors:

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.
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
1 3
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°02E,
11°35S), 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
J Ornithol
1 3
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
1 3
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
J Ornithol
1 3
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)
J Ornithol
1 3
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
1 3
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.
References
Allen G (2009) Field guide to marine fishes of tropical Australia. West-
ern Australian Museum, Perth
AOAC (2002) Official methods of analysis of AOAC International,
17th edn. Association of Official Analytical Chemists, Washing-
ton DC
AOAC (2005) Official methods of analysis of AOAC International,
18th edn. Association of Official Analytical Chemists, Arlington
Ashmole NP, Ashmole MJ (1967) Comparative feeding ecology of
sea birds of a Tropical Oceanic Island. Peabody Mus Nat Hist
Bull 24:1–131
Bates D, Maechler M, Bolker BM, Walker S (2015) Fitting linear
mixed-effects models using lme4. J Stat Softw 67:1–48
Batianoff GN, Cornelius NJ (2005) Birds of Raine Island: population
trends, breeding behaviour and nesting habitats. Proc R Soc Qld
112:1–29
Blaber SJM, Milton D, Smith GC, Farmer MJ (1995) Trawl discards in
the diets of tropical seabirds of the Northern Great Barrier Reef,
Australia. Mar Ecol Prog Ser 127:1–13
Blaber SJM, Milton D, Farmer MJ, Smith GC (1998) Seabird breeding
populations on the far Northern Great Barrier Reef, Australia:
trends and influences. Emu 98:44–57
Boyd C, Punt AE, Weimerskirch H, Bertrand S (2014) Movement mod-
els provide insights into variation in the foraging effort of central
place foragers. Ecol Model 286:13–25
Calenge C (2006) The package ‘adehabitat’ for the R software: a tool
for the analysis of space and habitat use by animals. Ecol Model
197:516–519
Castillo-Guerrero JA, Lerma M, Mellink E, Suazo-Guillén E,
Peñaloza-Padilla EA (2016) Environmentally-mediated flexible
foraging strategies in Brown Boobies in the Gulf of California.
Ardea 104:33–47
Cleasby IR, Wakefield ED, Bodey TW, Davies RD, Patrick SC, Newton
J, Votier SC, Bearhop S, Hamer KC (2015) Sexual segregation in
a wide-ranging marine predator is a consequence of habitat selec-
tion. Mar Ecol Prog Ser 518:1–12
Clua É, Grosvalet F (2001) Mixed-species feeding aggregation of dol-
phins, large tunas and seabirds in the Azores. Aquat Living Resour
14:11–18. https://doi.org/101016/S0990-7440(00)01097-4
Congdon BC, Preker M (2004) Sex-specific chick provisioning and
kleptoparasitism in the Least Frigatebird, Fregata ariel. Emu.
104:347–351. https://doi.org/10.1071/MU03008
Cortés E (1997) A critical review of methods of studying fish feeding
based on analysis of stomach contents: application to elasmo-
branch fishes. Can J Fish Aquat Sci 54:726–738
Cruz SM, Hooten M, Huyvaert KP, Proaño CB, Anderson DJ, Afa-
nasyev V, Wikelski M (2013) At-sea behavior varies with Lunar
Phase in a Nocturnal Pelagic Seabird, the Swallow-tailed gull.
PLoS One 8:1–8
Denuncio P, Viola M, Machovsky-Capuska GE, Raubenheimer D,
Blasina G, Machado R, Polizzi P, Gerpe M, Cappozzo HL,
J Ornithol
1 3
Rodriguez DH (2017) Population variance in prey, diets and their
macronutrient composition in an endangered marine predator,
the Franciscana dolphin. J Sea Res. https://doi.org/10.1016/j.
seares.2017.05.008
Duffy DC, Jackson S (1986) Diet studies of seabirds: a review of meth-
ods. Colon Waterbirds 9:1–17
Elliott KH, Gaston AJ, Crump D (2010) Sex-specific behavior by a
monomorphic seabird represents risk partitioning. Behav Ecol
21:1024–1032
Gilardi JD (1992) Sex-specific foraging distributions of Brown Boobies
in the Eastern Tropical Pacific. Colon Waterbirds 15:148–151
González-Solís J, Croxall JP, Wood AG (2000) Sexual dimorphism
and sexual segregation in foraging strategies of Northern giant
petrels, Macronectes halli, during incubation. Oikos 90:390–
398. https://doi.org/10.1034/j1600-07062000900220x
Guerra M, Drummond H (1995) Reversed size dimorphism and
parental care: minimal division of labour in the blue-footed
Booby. Behaviour 132:479–797
Ismar SMH, Raubenheimer D, Bury SJ, Millar CD, Hauber ME
(2017) Sex-specific foraging during parental care in a size-
monomorphic seabird, the Australasian Gannet (Morus
serrator). Wilson J Ornithol 129:139–147. https://doi.
org/10.1676/1559-4491-1291139
Lascelles B, Taylor P, Miller MGR, Dias MP, Oppel S, Torres L, Hedd
A, Le Corre M, Phillips RA, Schaffer S, Weimerskirch H, Small C
(2016) Applying global criteria to tracking data to define impor-
tant areas for marine conservation. Divers Distrib 22:422–431
Lewis S, Sherratt TN, Hamer KC, Wanless S (2001) Evidence of
intra-specific competition for food in a pelagic seabird. Nature
412:816–819
Lewis S, Benvenuti S, DallAntonia L, Griffiths R, Money L, Sherratt
TN, Wanless S, Hamer KC (2002) Sex-specific foraging behaviour
in a monomorphic seabird. Proc R Soc Lond B 269:1687–1693.
https://doi.org/10.1098/rspb20022083
Lewis S, Schreiber E, Daunt F, Schenk G, Orr K, Adams A, Wan-
less S, Hamer KC (2005) Sex-specific foraging behaviour in
tropical Boobies: does size matter? Ibis 147:408–414. https://doi.
org/10.1111/j1474-919x200500428x
Lormee H, Barbraud C, Chastel O (2005) Reversed sexual size dimor-
phism and parental care in the Red-Footed Booby Sula sula. Ibis
147:307–315. https://doi.org/10.1111/j1474-919x200500404x
Machovsky-Capuska GE, Priddel D, Leong PH, Jones P, Carlile N,
Shannon L, Portelli D, McEwan A, Chaves AV, Raubenheimer D
(2016a) Coupling bio-logging with nutritional geometry to reveal
novel insights into the foraging behaviour of a plunge-diving
marine predator. NZ J Mar Freshwat Res 8330:1–15. https://doi.
org/10.1080/0028833020161152981
Machovsky-Capuska GE, Senior AM, Benn EC, Tait AH, Schuckard
R, Stockin KA, Cook W, Ogle M, Barna K, Melville D, Wright
B, Purvin C, Raubenheimer D (2016b) Sex-specific macronutri-
ent foraging strategies in a highly successful marine predator: the
Australasian Gannet. Mar Biol 163:1–14. https://doi.org/10.1007/
s00227-016-2841-y
Machovsky-Capuska GE, Senior AM, Simpson SJ, Raubenheimer D
(2016c) The multi-dimensional nutritional niche. Trends Ecol
Evol 31:355–365. https://doi.org/10.1016/jtree201602009
Michelot T, Langrock R, Patterson TA (2016) moveHMM: an R pack-
age for the statistical modelling of animal movement data using
hidden Markov models. Methods Ecol Evol 7:1308–1315
Min D, Steensen D (1998) Crude fat analysis. Food Anal 2:201–216
Moltschaniwskyj N, Doherty P (1995) Cross-shelf distribution patterns
of tropical juvenile cephalopods sampled with light-traps. Mar
Freshw Res 46:707–714
Morris-Pocock JA, Anderson DJ, Friesen VL (2011) Mechanisms
of global diversification in the brown booby (Sula leucogaster)
revealed by uniting statistical phylogeographic and multilocus
phylogenetic methods. Mol Ecol 20:2835–2850
Morse DH (1968) A quantitative study of foraging of male and female
spruce-woods warblers. Ecol Soc Am 49:779–784
Nelson B (1978) The Sulidae: gannets and boobies. Oxford University
Press, Oxford
Newton I (1979) Population ecology of raptors. T. & A.D. Poyser,
Berkhamsted
NRC (1989) Recommended dietary allowances, 10th edn. National
Academy Press, Washington DC
Nunes GT, Mancini PL, Bugoni L (2016) When Bergmann’s rule
fails: evidences of environmental selection pressures shaping
phenotypic diversification in a widespread seabird. Ecography
40:365–375
Oppel S, Beard A, Fox D, Mackley E, Leat E, Henry L, Clingham E,
Fowler N, Sim J, Sommerfeld J, Weber N, Weber S, Bolton M
(2015) Foraging distribution of a tropical seabird supports Ash-
moles hypothesis of population regulation. Behav Ecol Sociobiol
69:915–926
Paiva VH, Pereira J, Ceia FR, Ramos JA (2017) Environmentally
driven sexual segregation in a marine top predator. Sci Rep 7:2590
Peck DR, Congdon BC (2006) Sex-specific chick provisioning and div-
ing behaviour in the wedge-tailed shearwater Puffinus pacificus. J
Avian Biol 37:245–251
Petit LJ, Petit DR, Petit KE, Fleming W (1990) Intersexual and tempo-
ral variation in foraging ecology of Prothonotary warblers during
the breeding season. Auk 107:133–145
Phillips RA, Silk JRD, Phalan B, Catry P, Croxall JP (2004) Seasonal
sexual segregation in two Thalassarche albatross species: com-
petitive exclusion, reproductive role specialization or foraging
niche divergence? Proc R Soc Lond B 271:1283–1291. https://
doi.org/10.1098/rspb20042718
Pontón-Cevallos J, Dwyer RG, Franklin CE, Bunce A (2017) Under-
standing resource partitioning in sympatric seabirds living in
tropical marine environments. Emu Austral Ornithology. https://
doi.org/10.1080/0158419720161265431
R Core Team (2017) R: a language and environment for statistical
computing. R Foundation for Statistical Computing, Vienna
Randall J, Allen G, Steene R (1997) Fishes of the Great Barrier Reef
and Coral Sea. University of Hawaii Press, Hawaii
Raubenheimer D (2011) Toward a quantitative nutritional ecology: the
right-angled mixture triangle. Ecol Monogr 81:407–427
Raubenheimer D, Machovsky-Capuska GE, Chapman CA, Rothman
JM (2015) Geometry of nutrition in field studies: an illustration
using wild primates. Oecologia 177:223–234
Schuckard R, Melville D, Cook W, Machovsky-Capuska G (2012) Diet
of the Australasian Gannet (Morus serrator) at Farewell Spit, New
Zealand. Notornis 59:66–70
Selander RK (1966) Sexual dimorphism and differential niche utiliza-
tion in birds. Condor 68:113–151
Shaffer SA, Weimerskirch H, Costa DP (2001) Functional significance
of sexual dimorphism in wandering albatrosses, Diomedea exu-
lans. Funct Ecol 15:203–210
Soanes LM, Bright JA, Bolton M, Millett J, Mukhida F, Green JA
(2015) Foraging behaviour of Brown Boobies Sula leucogaster
in Anguilla, Lesser Antilles: preliminary identification of at-
sea distribution using a time-in-area approach. Bird Conserv Int
25:87–96. https://doi.org/10.1017/S095927091400001X
Sommerfeld J, Kato A, Ropert-Coudert Y, Garthe S, Hindell MA
(2013) The individual counts: within sex differences in foraging
strategies are as important as sex-specific differences in Masked
Boobies Sula dactylatra. J Avian Biol 44:531–540. https://doi.
org/10.1111/j1600-048X201300135x
Spear LB, Ainley DG, Walker WA (2007) Foraging dynamics of
seabirds in the eastern tropical Pacific Ocean. Stud Avian Biol
35:1–99
J Ornithol
1 3
Stahl JC, Sagar PM (2000) Foraging strategies and migration of
southern Bullers albatrosses Diomedea b. bulleri breeding on the
Solander Is, New Zealand. J R Soc N Z 30:319–334. https://doi.
org/10.1080/0301422320009517625
Tait A, Raubenheimer D, Stockin K, Merriman M, Machovsky-
Capuska GE (2014) Nutritional geometry and the macronutrient
variation in the diet of Gannets: the challenges in marine field
studies. Mar Biol 12:2791–2801
Weimerskirch H, Le Corre M, Jaquemet S, Marsac F (2005) Foraging
strategy of a tropical seabird, the Red-footed Booby, in a dynamic
marine environment. Mar Ecol Prog Ser 288:251–261. https://doi.
org/10.3354/meps288251
Weimerskirch H, Le Corre M, Ropert-Coudert Y, Kato A, Marsac F
(2006) Sex-specific foraging behaviour in a seabird with reversed
sexual dimorphism: the Red-footed Booby. Oecologia 146:681–
691. https://doi.org/10.1007/s00442-005-0226-x
Weimerskirch H, Le Corre M, Gadenne H, Pinaud D, Kato A, Rop-
ert-Coudert Y, Bost CA (2009a) Relationship between reversed
sexual dimorphism, breeding investment and foraging ecology in
a pelagic seabird, the Masked Booby. Oecologia 161:637–649.
https://doi.org/10.1007/s00442-009-1397-7
Weimerskirch H, Shaffer S, Tremblay Y, Costa DP, Gadenne H, Kato
A, Ropert-Coudert Y, Sato K, Aurioles D (2009b) Species- and
sex-specific differences in foraging behaviour and foraging zones
in Blue-footed and Brown Boobies in the Gulf of California. Mar
Ecol Prog Ser 391:267–278. https://doi.org/10.3354/meps07981
Young HS, McCauley DJ, Dirzo R, Dunbar RB, Shaffer S (2010)
Niche partitioning among and within sympatric tropical seabirds
revealed by stable isotope analysis. Mar Ecol Prog Ser 416:285–
294. https://doi.org/10.3354/meps08756
Zavalaga CB, Benvenuti S, Dall’Antonia L, Emslie SD (2007) Diving
behavior of Blue-footed Boobies Sula nebouxii in Northern Peru
in relation to sex, body size and prey type. Mar Ecol Prog Ser
336:291–303. https://doi.org/10.3354/meps336291
... Intra-specific competition can exist in large seabird colonies, especially during breeding seasons when adult seabirds are constrained by central place foraging [4,10], with breeders of some species segregating sexually. This type of segregation can usually be explained by three factors: (1) Anatomic differences between males and females (sexual dimorphism) [11][12][13][14], most frequently related to size of seabird species [12,14], influencing flight speed, foraging range and flapping frequency, as well as diving depth and duration induced by body mass [15]; ...
... (2) Divergent parental roles, influencing nest fidelity; and (3) nutritional requirements [13]. Thus, some sulids exhibit Reversed Sexual Dimorphism (RSD), where the bigger females are the main chick provisioners and the smaller males invest more in nest attendance and defence [13][14][15][16][17][18]. ...
... (2) Divergent parental roles, influencing nest fidelity; and (3) nutritional requirements [13]. Thus, some sulids exhibit Reversed Sexual Dimorphism (RSD), where the bigger females are the main chick provisioners and the smaller males invest more in nest attendance and defence [13][14][15][16][17][18]. Here, size difference, when present, work as a limiting factor, by excluding the smaller gender from productive areas closer to the colony or competing for better resources. ...
Article
Full-text available
In the oligotrophic tropical marine environment resources are usually more patchily distributed and less abundant to top predators. Thus, spatial and trophic competition can emerge, especially between related seabird species belonging to the same ecological guild. Here we studied the foraging ecology of two sympatric species–brown booby (BRBO) Sula leucogaster (breeding) and red-footed boobies (RFBO) Sula sula (non-breeding)–at Raso islet (Cabo Verde), across different seasons. Sexual segregation was only observed during Jun-Oct, when RFBO were present, with larger females BRBO remaining closer to the colonies, while males and RFBO travelled further and exploited different habitats. Overall, species appeared to prefer areas with specific oceanic features, particularly those related with oceanic currents and responsible for enhancing primary productivity in tropical oceanic areas (e.g. Sea Surface Height and Ocean Mixed Layer Thickness). Female BRBOs showed high foraging-site fidelity during the period of sympatry, while exploiting the same prey species as the other birds. However, during the months of co-existence (Jun.-Oct.), isotopic mixing models suggested that female BRBO would consume a higher proportion of epipelagic fish, whereas female RFBO would consume more squid compared to the other birds, possibly due to habitat-specific prey availability and breeding energy-constraints for BRBO. We conclude that divergent parental roles, environmental conditions, habitat preference and competition could be mechanisms simultaneously underlying sexual segregation for BRBO during a period of co-existence, while inter-specific foraging differences appear to be more affected by habitat preference and different breeding stages. These results support previous statements that BRBO can adapt their foraging ecology to different circumstances of environmental conditions and competition, and that marine physical features play an important role in foraging decisions of boobies.
... Yet these environments, characterised by low productivity and limited seasonal variability [31], support diverse communities of marine vertebrates including large populations of seabirds [32]. In comparison to the impressive dive depths common amongst temperate and polar seabirds, many tropical species feed at or near the ocean's surface, where social and commensal foraging in mixed aggregations is common [33][34][35]. This propensity for coexploitation of resources contrasts with predictions of ecological niche divergence, and highlights a need for improved knowledge of multi-species interactions in these systems. ...
... Thus, understanding the mechanisms by which these sulids coexist requires consideration of factors in both marine and terrestrial habitats. While RFBs and BBs have received considerable attention for tropical species, with some interspecific differences in foraging ecology reported [35,[40][41][42][43][44], the degree to which they coexploit and/or partition marine resources, both in terms of space use and diet, remains poorly understood [36,45]. ...
... Higher provisioning requirements may cause female BBs to remain closer to the nest, a response likely not required in RFBs that vary only slightly in their parental participation [41]. Some BB populations show an opposite pattern of foraging differentiation to those found here, with males remaining closer to shore than females [83,84], or spending more time at the nest [35]. These cases have been attributed to selection on males to defend nest sites, and females to undertake greater roles in chick provisioning (i.e. through increased food payload capacity or more extensive travel [85,86]). ...
Article
Full-text available
Background Social interactions, reproductive demands and intrinsic constraints all influence foraging decisions in animals. Understanding the relative importance of these factors in shaping the way that coexisting species within communities use and partition resources is central to knowledge of ecological and evolutionary processes. However, in marine environments, our understanding of the mechanisms that lead to and allow coexistence is limited, particularly in the tropics. Methods Using simultaneous data from a suite of animal-borne data loggers (GPS, depth recorders, immersion and video), dietary samples and stable isotopes, we investigated interspecific and intraspecific differences in foraging of two closely-related seabird species (the red-footed booby and brown booby) from neighbouring colonies on the Cayman Islands in the Caribbean. Results The two species employed notably different foraging strategies, with marked spatial segregation, but limited evidence of interspecific dietary partitioning. The larger-bodied brown booby foraged within neritic waters, with the smaller-bodied red-footed booby travelling further offshore. Almost no sex differences were detected in foraging behaviour of red-footed boobies, while male and female brown boobies differed in their habitat use, foraging characteristics and dietary contributions. We suggest that these behavioural differences may relate to size dimorphism and competition: In the small brown booby population ( n < 200 individuals), larger females showed a higher propensity to remain in coastal waters where they experienced kleptoparasitic attacks from magnificent frigatebirds, while smaller males that were never kleptoparasitised travelled further offshore, presumably into habitats with lower kleptoparasitic pressure. In weakly dimorphic red-footed boobies, these differences are less pronounced. Instead, density-dependent pressures on their large population ( n > 2000 individuals) and avoidance of kleptoparasitism may be more prevalent in driving movements for both sexes. Conclusions Our results reveal how, in an environment where opportunities for prey diversification are limited, neighbouring seabird species segregate at-sea, while exhibiting differing degrees of sexual differentiation. While the mechanisms underlying observed patterns remain unclear, our data are consistent with the idea that multiple factors involving both conspecifics and heterospecifics, as well as reproductive pressures, may combine to influence foraging differences in these neighbouring tropical species.
... For example, brown boobies (Sula leucogaster) are considered to show sex differences in foraging, as competition for resources suggests that males exclude females from foraging on squid, and this exclusion may change with different levels of foraging resources available. [22] Foraging theory states that animals attempt to intake food in the most optimal manner possible [23][24][25] to ensure that net energy gain exceeds gross energy expenditure. However, accurately measuring energy intake and expenditure remains a challenge, especially in free-ranging animals [26,27]. ...
Article
Full-text available
Many animals show sexually divergent foraging behaviours reflecting different physiological constraints or energetic needs. We used a bioenergetics approach to examine sex differences in foraging behaviour of the sexually monomorphic northern gannet. We derived a relationship between dynamic body acceleration and energy expenditure to quantify the energetic cost of prey capture attempts (plunge dives). Fourteen gannets were tracked using GPS, time depth recorders (TDR) and accelerometers. All plunge dives in a foraging trip represented less than 4% of total energy expenditure, with no significant sex differences in expenditure. Despite females undertaking significantly more dives than males, this low energetic cost resulted in no sex differences in overall energy expenditure across a foraging trip. Bayesian stable isotope mixing models based on blood samples highlighted sex differences in diet; however, calorific intake from successful prey capture was estimated to be similar between sexes. Females experienced 10.28% higher energy demands, primarily due to unequal chick provisioning. Estimates show a minimum of 19% of dives have to be successful for females to meet their daily energy requirements, and 26% for males. Our analyses suggest northern gannets show sex differences in foraging behaviour primarily related to dive rate and success rather than the energetic cost of foraging or energetic content of prey.
... In Abrolhos, estimated population size is about 300 pairs for brown boobies and 200 pairs for red-billed tropicbirds with breeding activity throughout the year (ICMBio, 2019). Foraging areas are located around colonies, but brown boobies tend to explore the immediate colony surroundings (Weimerskirch et al., 2009;Miller et al., 2018a), while tropicbirds tend to travel further and make longer foraging trips (Diop et al., 2018). Both species are primarily plunge divers and feed on fish occurring at the sea surface, but brown boobies can also interact with fisheries and use discards as a food source (Alves et al., 2004;Castillo-Guerrero et al., 2011). ...
Article
Human-induced rapid environmental changes can disrupt habitat quality in the short term. A decrease in quality of habitats associated with preference for these over other available higher quality is referred as ecological trap. In 2015, the Fundão dam containing iron mining tailings, eastern Brazil, collapsed and released about 50 million cubic meters of metal-rich mud composed by Fe, As, Cd, Hg, Pb in three rivers and the adjacent continental shelf. The area is a foraging site for dozens of seabird and shorebird species. In this study, we used a dataset from before and after Fundão dam collapse containing information on at-sea distribution during foraging activities (biologging), dietary aspects (stable isotopes), and trace elements concentration in feathers and blood from three seabird species known to use the area as foraging site: Phaethon aethereus, Sula leucogaster, and Pterodroma arminjoniana. In general, a substantial change in foraging strategies was not detected, as seabirds remain using areas and food resources similar to those used before the dam collapse. However, concentration of non-essential elements increased (e.g., Cd and As) while essential elements decreased (e.g., Mn and Zn), suggesting that the prey are contaminated by trace elements from tailings. This scenario represents evidence of an ecological trap as seabirds did not change habitat use, even though it had its quality reduced by contamination. The sinking-resuspension dynamics of tailings deposited on the continental shelf can temporally increase seabird exposure to contaminants, which can promote deleterious effects on populations using the region as foraging sites in medium and long terms.
... However, this tactic is likely to be colony specific and dependent on resource availability (Baduini 2002;Congdon et al. 2005;McDuie et al. 2015). Another common feature involves sex-specific foraging, which has been described in many seabird species, where differences are often associated with size-mediated competitive exclusion or habitat specialization (Lewis et al. 2005;Phillips et al. 2006;Gonzalez-Solis et al. 2007;Miller et al. 2018b;Austin et al. 2019;Clay et al. 2020;Orgeret et al. 2021). ...
Article
Full-text available
Seabirds are distributed widely over the world’s oceans and have adopted a range of foraging tactics to secure food resources necessary for survival and reproduction. To better understand the foraging tactics and at-sea distribution of tropical seabirds, 38 Wedge-Tailed Shearwaters, Ardenna pacifica (WTS) from Réunion Island (21.375° S; 55.569° E) were tracked during 81 foraging trips using GPS loggers deployed over three breeding seasons (2016–2019). Clustering algorithms, kernel density estimation and habitat models were applied to this tracking dataset. During incubation, WTS foraged in the open ocean towards the southeast of Madagascar. During chick rearing, however, WTS restricted their distribution and implemented a dual foraging tactic, where they executed several short trips near the colony before performing a single long trip (> 200 km) in a similar south-westerly direction observed for incubating birds. Birds did not seem to show a strong preference for specific environmental conditions or habitat features and arguably cue on marine predators, conspecifics, or fish-aggregating devices to find productive foraging grounds. This study confirmed that WTS foraged in areas that have previously been identified as ‘hotspots’ for other marine species which are threatened by anthropogenic pressures; further highlighting that these areas are important from a conservation perspective.
... Brown boobies Sulo leucogaster are philopatric, mono gamous tropical seabirds (Nelson 1978) that exhibit RSD, with females significantly larger than males both morphometrically and in terms of ab solute mass (Croxall 1995, Lewis et al. 2005, Weimerskirch et al. 2009a, Nunes et al. 2017. Dietary studies undertaken at various brown booby colonies globally have yielded mixed results for intersexual dietary segregation, with segregation at some colonies (Young et al. 2010, Miller et al. 2018) but not at others (Weimerskirch et al. 2009a, Mancini et al. 2013, Pontón-Cevallos et al. 2017. Interestingly, recent modelling has identified several criteria which promote SSD, including a narrow individual niche width for each sex (not only with respect to prey resource, but also differences in habitat use and even feeding techniques), monogamy in an exclusive territory (be cause the fitness of a male is reflected by the reproductive success of his female partner) and a number of prey resources being reliably present (Li & Kokko 2021). ...
Article
The causes of intraspecific variation in diet and isotopic niche width can provide important insights into the local food resource requirements for a population. This information is particularly important for highly philopatric colonially nesting species, where local competition for food resources may be high. We investigated the relative influence of environmental, temporal and spatial attributes on intraspecific variation in the diet of colonially nesting brown boobies Sula leucogaster using both regurgitant samples and stable isotope analysis of blood and feathers. Diet analyses revealed that Indian anchovy Stolephorus indicus was the predominant prey species in brown booby diet. Despite the predominance of Indian anchovy, there was significant populationlevel intraspecific variation in diet. Our results supported the intersexual competition hypothesis, with female diet not only exhibiting greater species richness, but non-breeding females likely to feed in a different habitat. The isotopic niche also varied according to life-history stage, with individuals utilising different food sources between the breeding and non-breeding seasons. Additionally, there were significant inter-annual differences in diet composition associated with warmer sea surface temperatures. Furthermore, we identified sub-colony differences in the nonbreeding diet. The different patterns of food intake represent those typical of a central place forager: during the non-breeding season (when adults were not area-restricted due to breeding activity), the width of the isotopic niche of both sexes increased. This study has revealed multiple causes of intraspecific variation in diet and isotopic niche and highlights the need for comprehensive dietary analyses to manage seabird populations effectively within specific locations.
... This nutritionally explicit framework is particularly relevant to marine apex predators known to forage in complex and fluctuating marine environments (Machovsky-Capuska et al., 2016a;Machovsky-Capuska and Raubenheimer, 2020). While the characterization of nutritional niche breadths of marine predators has shown to be critical to trophic interactions, marine pollution, aquaculture, captivity and rehabilitation, climate change, and conservation and management of endangered species (Machovsky-Capuska and , yet the field remains poorly characterized to few species of seabirds (Machovsky-Capuska et al., 2016c, 2016dMiller et al., 2018;Tait et al., 2014), sharks (Grainger et al., 2020;Machovsky-Capuska and Raubenheimer, 2020), turtles , cetaceans (Denuncio et al., 2017;Machovsky-Capuska et al., 2019) and pinnipeds . ...
Article
Niche segregation has been recognized as a valuable mechanism for sympatric species to reduce interspecific competition and facilitate coexistence. The differential use of habitats is one of the behavioural mechanisms that may shape coexistence among marine predators. In this study, we provide a dietary and nutritional assessment of two pinnipeds, the South American sea lion (SASL) and the South American fur seal (SAFS) and explore their sympatric coexistence within the Warm Temperate Southwestern Atlantic biogeographic province (WTSA province). Pelagic prey species within the WTSA province showed significantly higher proportional composition of lipids than demersal counterparts, evidencing a nutritional variability in a vertical dimension accessible to marine predators. By modelling the dietary niches of these pinnipeds through a nutritional lens, we showed high overlapping prey composition niche breadths suggesting that both species consumed prey with similar nutritional composition; however, distinct realized nutritional niches showed that diets are likely shaped by differences in foraging behaviours. The SAFS combined pelagic and demersal prey, whereas SASL mostly preyed upon demersal species. This paper provides crucial information on how nutritional variability in the water column likely drives the feeding strategies of both pinnipeds in the WTSA province. Given that this variation can influence the stability of the contrasting population trends shown by these two pinnipeds, nutritional dynamics must be taken into consideration when defining conservation strategies.
... This indicates that females dive more frequently than males between 10:00 and 17:00 (Additional file 1: Figure S1 and Additional file 2: Figure S2 ). The differences in diurnal modes between males and females have been often observed in seabirds [27], which was interpreted as a result of sexual size dimorphism or sex-specific roles. In the case of Streaked Shearwaters, females conduct relatively short trips for chicks, suggesting that they dive soon after initiating foraging trips (i.e., in the morning). ...
Article
Full-text available
Background Recent advances in sensing technologies have enabled us to attach small loggers to animals in their natural habitat. It allows measurement of the animals’ behavior, along with associated environmental and physiological data and to unravel the adaptive significance of the behavior. However, because animal-borne loggers can now record multi-dimensional (here defined as multimodal) time series information from a variety of sensors, it is becoming increasingly difficult to identify biologically important patterns hidden in the high-dimensional long-term data. In particular, it is important to identify co-occurrences of several behavioral modes recorded by different sensors in order to understand an internal hidden state of an animal because the observed behavioral modes are reflected by the hidden state. This study proposed a method for automatically detecting co-occurrence of behavioral modes that differs between two groups (e.g., males vs. females) from multimodal time-series sensor data. The proposed method first extracted behavioral modes from time-series data (e.g., resting and cruising modes in GPS trajectories or relaxed and stressed modes in heart rates) and then identified two different behavioral modes that were frequently co-occur (e.g., co-occurrence of the cruising mode and relaxed mode). Finally, behavioral modes that differ between the two groups in terms of the frequency of co-occurrence were identified. Results We demonstrated the effectiveness of our method using animal-locomotion data collected from male and female Streaked Shearwaters by showing co-occurrences of locomotion modes and diving behavior recorded by GPS and water-depth sensors. For example, we found that the behavioral mode of high-speed locomotion and that of multiple dives into the sea were highly correlated in male seabirds. In addition, compared to the naive method, the proposed method reduced the computation costs by about 99.9%. Conclusion Because our method can automatically mine meaningful behavioral modes from multimodal time-series data, it can be potentially applied to analyzing co-occurrences of locomotion modes and behavioral modes from various environmental and physiological data.
Thesis
Full-text available
Reproductive senescence is common in seabirds; however, the underlying causes remain elusive. Because reproductive success and foraging performance of seabirds are often linked, a decline in foraging performance with age may underlie reproductive senescence. Environment, too, affects breeding, with high prey availability and/or quality improving reproductive outcomes. For seabirds, foraging, such as the flapping flight required to reach a foraging location, is physically demanding. Senescent decline in a seabird’s ability to match the costs of foraging might cap delivery of food to young at the nest, and provide a proximate explanation for poor breeding success in old age. I evaluated the relationship between age, sex, environment, and three aspects of foraging (flight, foraging, and diving performance) in a tropical seabird, the Nazca booby (Sula granti), on Isla Española, Galápagos, Ecuador. I predicted poor performance by old Nazca boobies compared to young or middle-aged adults, contributing to observed patterns of reproductive senescence in this species. Young adults may still lack the foraging ability of middle-aged birds, contributing to overall age-related variation in foraging performance. Biologgers (GPS in 2011–2012 / 2014–2016, GPS/accelerometer in 2015–2016) were deployed during the incubation period on male and female adults of young, middle, and old age classes that correspond to poor, peak, and senescing reproductive success, respectively. I tested the ability of age and sex to explain variation in flight performance (e.g., airspeed) in Chapter 2. In Chapter 3, I evaluated foraging traits (e.g., mass gained during a foraging absence) by age and environment, and in Chapter 4, diving performance (e.g., dive depth) was evaluated by age. Of the commuting flight traits linked to physiology, only airspeed varied with age. However, sex-specific patterns of aging emerged for foraging performance: only females incurred longer foraging absences, while males showed early-life improvement in flight speed. Age affected female diving traits, with younger females not diving as deep, and flapping slower when taking off from the water after a dive. These varied, but cumulative, aging results emphasize the need for studies to examine a large suite of traits to dissect complicated aging patterns in wild populations.
Article
Full-text available
Flexibility in foraging strategy is an important mechanism by which seabirds cope with spatiotemporal heterogeneity in food availability and the variable energetic constraints of their annual life cycle. Foraging strategy flexibility was investigated in the grey-faced petrel Pterodroma gouldi breeding on Ihumoana Island (36°53′S, 174°26′E) using stable isotope analyses. Intra- and inter-annual variations in stable isotope values, isotopic niches and diet inferred from isotope mixing models were studied by analysing δ15N and δ13C in adult wing feathers and blood, chick down and body feathers, and muscle from spontaneously regurgitated prey, collected during 2013 and 2014 breeding seasons. Grey-faced petrels exhibited variations in stable isotopes, isotopic niches and diet more markedly throughout their annual life cycle than between years. A trophic segregation occurred between adults and chicks presumably from adults feeding inshore and chicks being fed more oceanic prey of higher trophic level. Stable-isotope mixing models revealed that adult diet during the breeding season could consist mainly of ram’s horn squids Spirula spirula and chick diet of crustaceans, fish and other cephalopods being secondary prey throughout the breeding season. Adult male and female isotopic niches slightly differed. Finally, isotopic niche in adults during non-breeding was similar to that during breeding, suggesting non-breeding foraging areas located off the eastern Australian coast, around the limit between the Tasman and Coral seas. Our results demonstrated plasticity in the foraging strategy of grey-faced petrels in response to the changing nutritional demands of their annual cycle and to changes in oceanographic conditions likely driven by El Niño Southern Oscillation.
Article
Full-text available
Sexual segregation in foraging occurs in many animal species, resulting in the partitioning of resources and reduction of competition between males and females, yet the patterns and drivers of such segregation are still poorly understood. We studied the foraging movements (GPS-tracking), habitat use (habitat modelling) and trophic ecology (stable isotope analysis) of female and male Cory’s shearwaters Calonectris borealis during the mid chick-rearing period of six consecutive breeding seasons (2010–2015). We found a clear sexual segregation in foraging in years of greater environmental stochasticity, likely years of lower food availability. When food became scarce, females undertook much longer foraging trips, exploited more homogeneous water masses, had a larger isotopic niche, fed on lower trophic level prey and exhibited a lower body condition, when compared to males. Sexual competition for trophic resources may be stronger when environmental conditions are poor. A greater foraging success of one sex may result in di erential body condition of pair mates when enduring parental e ort, and ultimately, in an increased probability of breeding failure.
Article
Full-text available
Sexual segregation, common in many species, is usually attributed to intra-specific competition or habitat choice. However, few studies have simultaneously quantified sex-specific foraging behaviour and habitat use. We combined movement, diving, stable isotope and oceanographic data to test whether sexual segregation in northern gannets Morus bassanus results from sex-specific habitat use. Breeding birds foraging in a seasonally stratified shelf sea were tracked over 3 consecutive breeding seasons (2010-2012). Females made longer trips, foraged farther offshore and had lower δ13C values than males. Male and female foraging areas overlapped only slightly. Males foraged more in mixed coastal waters, where net primary production (NPP) was relatively high (>3 mg C m-2 d-1) and sea-surface temperature (SST) was relatively low (15°C) more than females, possibly as a consequence of foraging in productive mixed waters over offshore banks. Females foraged most frequently in stratified offshore waters, of intermediate SST (12-15°C), but exhibited no consistent response to NPP. Sex-specific differences in diving behaviour corresponded with differences in habitat use: males made more long and deep U-shaped dives. Such dives were characteristic of inshore foraging, whereas shorter and shallower V-shaped dives occurred more often in offshore waters. Heavier birds attained greater depths during V-shaped dives, but even when controlling for body mass, females made deeper V-shaped dives than males. Together, these results indicate that sexual segregation in gannets is driven largely by habitat segregation between mixed and stratified waters, which in turn results in sex-specific foraging behaviour and dive depths.
Article
Full-text available
Due to the substantial progress in tracking technology, recent years have seen an explosion in the amount of movement data being collected. This has led to a huge demand for statistical tools that allow ecologists to draw meaningful inference from large tracking data sets. The class of hidden Markov models (HMMs) matches the intuitive understanding that animal movement is driven by underlying behavioural modes and has proven to be very useful for analysing movement data. For data that involve a regular sampling unit and negligible measurement error, these models usually are sufficiently flexible to capture the complex correlation structure found in movement data, yet are computationally inexpensive compared to alternative methods. The R package moveHMM allows ecologists to process GPS tracking data into series of step lengths and turning angles, and to fit an HMM to these data, allowing, in particular, for the incorporation of environmental covariates. The package includes assessment and visualization tools for the fitted model. We illustrate the use of moveHMM using (simulated) movement of the legendary wild haggis Haggis scoticus. Our findings illustrate the role our software, and movement modelling in general, can play in conservation and management by illuminating environmental constraints.
Article
Full-text available
The Brown Booby Sula leucogaster is a seabird with a pantropical distribution across a wide variety of oceanic environments. Sexual size dimorphism in Brown Boobies has been proposed as an explanation for intersexual differences in foraging, but results have been inconsistent. We investigated whether there is context-dependent foraging behaviour driven by local environmental conditions. In this study, we evaluated (1) inter-sex differences in foraging behaviour (by capillary tubes, temperature and depth recorders, and diet) at two colonies in the Gulf of California: Isla San Jorge (ISJ) and Farallón de San Ignacio (FSI) and, (2) intercolonial and interannual differences in foraging behaviour, and (at ISJ) their relationship with local-scale environmental variation, using 5-day composite images of sea surface temperature (SST) and primary productivity (PP) as proxies. Inter-sex differences were few and inconsistent between years, and smaller than overall differences between years and localities. At ISJ, Brown Boobies included more prey species in their diet (27 vs. 19 spp.) and dove shallower (2.3 vs. 3.14 m) than at FSI. At ISJ, Brown Boobies exhibited adjustments in diving depth and prey size as a function of environmental variation: shallower plunge dives and smaller prey items were related with lower SST and higher PP values, whereas deeper dives and larger prey items were related with higher SST and lower PP values. Our results confirmed that the Brown Booby is highly plastic in its foraging ecology, which explains its ability to live in places with large-scale environmental variation (intercolony and interannual), such as tropical areas worldwide.
Article
Full-text available
Organisms tend to exhibit phenotypes that can be shaped by climate, commonly demonstrating clinal variations along latitudinal gradients. In vertebrates, air temperature plays a major role in shaping body size in both ectothermic and endothermic animals. However, additional small-scale environmental factors can also act as selection pressures in the marine ecosystem (e.g. primary productivity), evidencing multi-scale processes acting on marine organisms. In this study, we tested Bergmann’s rule in a widely distributed seabird, the brown booby Sula leucogaster , in addition to evaluating the relationship of sea surface temperature and chlorophyll α with phenotypes. We used traits from a morphometric dataset (culmen, wing chord, and tarsus length) and body mass of 276 brown boobies distributed on six breeding sites along a latitudinal gradient in the South Atlantic Ocean (0 – 27 ° S). We found signifi cant diff erentiation among colonies, but phenotypic similarities were observed between colonies located at the extremes of the latitudinal gradient. As the colony nearest to the Equator, Saint Peter and Saint Paul archipelago, had the largest and heaviest individuals, the model containing only air temperature explained 5% of the allometric variation, providing no substantial support for Bergmann’s rule. However, when we added the interaction of chlorophyll α and sea surface temperature the deviance explained rose to over 80%. Primary productivity and sea surface temperature do not follow a latitudinal gradient in the ocean and, therefore, the role of small-scale oceanographic processes in shaping body size and the importance of considering additional environmental variables when testing Bergmann’s rule in marine organisms are evident.
Article
The avifauna recorded from Raine Island between 1843 and 2003 comprises 84 species. Of the 16 species recorded as breeding on Raine Island, five are seabird species considered to be uncommon and/or rare in Queensland i.e. Herald Petrel, Red-tailed Tropicbird, Red-footed Booby, and Great and Lesser Frigatebirds. The Red-tailed Tropicbird’s conservation status in Queensland is Vulnerable, whilst the Herald Petrel is listed as Critically Endangered in Australia. The waterbird species breeding on the island are the Nankeen Night Heron and the Buff-banded Rail. The terrestrial ecological factors that affect the birds breeding on Raine Island are examined. Annual seabird population counts taken between 1979-1993 and 1994-2003 are reported. Comparisons of bird populations between the two periods suggest population decline in 13 of the 16 species over the last 24 years. The combined averages for all 16 species indicate a total population reduction of the rookery by 16,347 birds, or 69.7%. Five species with >60% reductions in the mean population estimates are: Red-footed Booby (67.9%), Lesser Frigatebird (67.6%), Bridled Tern (69.1%), Sooty Tern (84.4%) and Common Noddy (95.5%). There is no evidence of significant human disturbance, no habitat loss and/or deterioration of nesting habitat conditions on the island over the period in which the population has declined.
Article
Sex differences in foraging behavior are typically studied in size-dimorphic taxa. Data on sex-specific behavior in monomorphic taxa are needed to test theories of reproductive investment. It has been suggested that in seabirds foraging niche separation may be related to decreased intersexual competition for food between cooperating pair-bonded individuals. Alternatively, sex differences in foraging niches may be driven by different nutritional requirements of females associated with the reproductive costs of egg production and oviposition. To assess these possibilities, we studied a size-monomorphic colonial seabird, the Australasian Gannet (Morus serrator) at the Cape Kidnappers gannetry, New Zealand. We recorded maximum dive depths, and distinct diet composition of incubating females as indicated by stable isotopic signatures. Results suggested greater female foraging effort during early times of incubation, indicated by significantly deeper maximum dives. Sex-specific foraging patterns across other breeding stages were more variable. Nitrogen stable isotopic values showed that incubating females occupied a different trophic position compared to males at the same breeding stage, and also from those of gannets of both sexes at later stages of parental care. Overall, the data are consistent with cost-of-oviposition compensation in females necessitating male-bias in parental care in biparental breeders. Further research is needed to unravel the implications of nutritional needs for the evolution of sex differences in behavior in this and other monomorphic taxa.