J Ornithol
DOI 10.1007/s10336-017-1482-3
ORIGINAL ARTICLE
Sex and breeding status affect prey composition of Harpy Eagles
Harpia harpyja
Everton B. P. Miranda1,2 Edwin Campbell-Thompson2,3 Angel Muela2
Felix Hernan Vargas2
Received: 31 December 2016 / Revised: 17 July 2017 / Accepted: 31 July 2017
Dt. Ornithologen-Gesellschaft e.V. 2017
Abstract Foraging behavior may show considerable vari-
ation among population classessuch as sex and breeding
classthat can be consequence of the groups specific
constraints and roles. In raptors, differential parental roles
related to foraging have been the main explanation for
males being smaller than females, as smaller males have
been described to be more efficient foragers. During one
phase of breeding, only males forage, requiring them to
feed themselves, females and young. This is expected to
induce changes in foraging behavior of breeders compared
to non-breeders. By comparing prey taken by floaters and
breeders of Harpy Eagles (Harpia harpyja), we describe
some effects of breeding and sex on the diet. Here we show
that diet traits differed between male and female floaters,
and between floaters and breeders. Juvenile prey was three
times more common in the diet of males than that of
females. Sloths were more common prey among females
than among males (53 vs. 37%). Males preyed four times
more on terrestrial animals than did females, and showed a
greater niche width than females (6.0 vs. 3.4). The prey of
breeders was smaller than that of non-breeders (on average
3.64 vs. 4.24 kg). Non-breeders had a larger niche width
Communicated by O. Kruger.
Electronic supplementary material The online version of this
article (doi:10.1007/s10336-017-1482-3) contains supplementary
material, which is available to authorized users.
& Everton B. P. Miranda
mirandaebp@gmail.com
1
ONF Brasil Gestao Florestal, Cotriguacu, MT, Brazil
2
The Peregrine Fund, 5668 West Flying Hawk Lane, Boise,
ID 83709, USA
3
Fundacion Aguilas de Los Andes, Pereira, Colombia
than breeders. Our data provide support for the hypothesis
of parental role differentiation as an explanation for
reversed sexual size dimorphism in raptors.
Keywords Reversed sexual size dimorphism  Breeding
constraints  Role differentiation hypothesis  Foraging 
Raptor  Floater
Zusammenfassung
Geschlecht und Brutstatus beeinflussen die
Beutezusammensetzung von Harpyien
Das Verhalten bei der Nahrungssuche kann sich zwischen
den Populationsklassenwie beispielweise Geschlecht
und Brutklassebetrachtlich unterscheiden, welches eine
Folge der spezifischen Beschrankungen und Rollen dieser
Gruppen sein kann. Bei Greifvogeln gelten die
unterschiedlichen Rollen der Elternvogel bei der
Nahrungssuche als die hauptsachliche Erklarung dafur,
dass die Mannchen kleiner sind als die Weibchen, da die
kleineren Mannchen als die effizienteren Jager gelten.
Wahrend eines Abschnitts des Brutgeschehens jagen nur
die Mannchen, welche daher nicht nur sich selbst, sondern
auch noch die Weibchen und die Jungvogel mit Nahrung
versorgen mussen. Dies lasst Anderungen im Jagdverhalten
zwischen Brutvogeln und Nichtbrutern erwarten. Im
Vergleich von Beutetieren nicht-territorialer Harpyien
(Harpia harpyja) mit denen von Brutvogeln beschreiben
wir einige Einflusse von Brutstatus und Geschlecht auf die
Nahrungszusammensetzung. Hier zeigen wir, dass sich die
Ernahrungsgewohnheiten nicht-territorialer Mannchen und
Weibchen sowie diejenigen der nicht-territorialen Vogel
und Brutvogel unterscheiden. Im Nahrungsspektrum der
Mannchen waren Jungtiere dreimal haufiger vertreten als in
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dem der Weibchen. Faultiere wurden haufiger zur Beute
von Weibchen als von Mannchen (53% gegenuber 37%).
Mannchen erbeuteten viermal haufiger bodenlebende Tiere
als die Weibchen und wiesen eine groere Nischenbreite
auf als diese (6,0 gegenuber 3,4). Die Beutetiere der
Brutvogel waren kleiner als die der Nichtbruter (im Schnitt
3,64 kg gegenuber 4,24 kg). Nichtbruter nutzten eine
groere Nischenbreite als Brutvogel. Unsere Daten
unterstutzen die Hypothese der elterlichen
Rollenverteilung als Erklarung fur den umgekehrten
Groendimorphismus bei Greifvogeln.
Introduction
Ever since Darwin (1859), scientists have puzzled about
why in many organisms males and females differ (Fisher
1930; Zahavi 1975). Indeed, sexual dimorphism is one of
the traits without which much of what is most extraordi-
nary, beautiful and bizarre in nature would not exist.
Sexual size dimorphism has generated a still growing body
of knowledge on its origins and consequences (Catry et al.
2016; Andersson 1994), given that body size is a key trait
driving organisms fitness (Mayer et al. 2016). In this
context, foraging behavior has become a focus of attention,
because it is highly affected by organism size. Foraging
therefore offers a way of measuring the ecological and
evolutionary interplay that result in sexual size dimorphism
(Angel et al. 2015).
While most tetrapods show what is called normal
sexual size dimorphismwhere males are larger than
femalesin raptors (Accipitriformes, Falconiformes and
Strigiformes orders) larger females are the norm. This has
been called reversed sexual dimorphism or RSD (Rey-
nolds 1972). Kruger (2005) used comparative analyses to
test the three main hypotheses that have been proposed to
explain RSD in raptors: (a) niche partitioningwhere size-
divergent sexes are able to reduce intersexual competition
for prey; (b) role differentiationwhere larger females are
better brooders and smaller males are better foragers and
territory defenders; (c) behavioralwhere larger females
are dominant over males, aiding in the maintenance of the
pair-bond and increasing male food-provisioning, or that
larger females compete more effectively for males. In this
synthesis, the better supported hypothesis was of role dif-
ferentiation (b), mainly because small males seem to be
more efficient foragers. Nevertheless, raptor RSD is far
from being a closed subject (Slagsvold and Sonerud 2007;
Olsen et al. 2013).
In raptors, although males are smaller, they do most of
the hunting during the initial breeding phase when the
females are incubating and brooding and relying on their
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mate for food (Schmutz et al. 2014; Sonerud et al. 2014).
Therefore, during a key part of their life cycle, male raptors
must be extraordinarily efficient foragers to feed them-
selves, their mates and offspring. Their smaller size gives
them more agility compared with females (Andersson and
Norberg 1981), and greater energy efficiency when carry-
ing heavy prey over long distances between foraging
grounds and the nest (Hakkarainen et al. 1996). In the later
phase of nesting, when nestlings have acquired thermal
independence, the female reassumes hunting to recover her
depleted fat reserves, and shreds food hunted by her and by
the male until nestlings are able to tear food themselves
(Sonerud et al. 2014). Under these constraints, breeding
raptors have to make important decisions between self-
feeding or prey delivery; which kind and size of prey to
hunt to maximize energetic gains from larger prey or to
hunt smaller prey to reduce carrying costs (Sonerud et al.
2013). These decisions are expected to affect foraging by
breeding raptors, when compared with non-breeding indi-
viduals free of these constraintsthe floaters (Barrows
1987).
RSD is pronounced in Harpy Eagles (Harpia harpyja).
Males average 5.95 kg, and are 19% smaller than females
with a mean weight of 7.35 kg, resulting in a female:male
linear body size ratio of 1.07 (n = 12, Peregrine Fund, unp.
data). Furthermore, the Harpy Eagle reproductive cycle is
exceptionally long (Muniz-Lopez et al. 2007), with an
average of three years between each successful fledgling,
which is expected to be highly demanding on males. Harpy
Eagle young depend on females to shred prey for them
until they are up to ten months of age, they fledge at six
months and become independent at 2.53 years (Rettig
1978; Muniz-Lopez et al. 2012). Harpy Eagles occur at low
densities (de Vargas-Gonzalez and Vargas 2011), formerly
throughout much of Central and South America. Threat-
ened by habitat loss and shooting (Birdlife International
2016), range reduction is already impacting its genetic
diversity (Banhos et al. 2016). These problems drove The
Peregrine Fund to test a restoration effort for the species,
through captive breeding and reintroduction in their former
range (Watson et al. 2016). This kind of initiative is known
to generate a great deal of information on foraging, since
released animals require intensive monitoring (Hayward
et al. 2011).
With respect to diet, the Harpy Eagle is the most studied
of Neotropical raptors. While broad patterns on diet are
known (Aguiar-Silva et al. 2014), important details are not.
The half century of systematic work on food habitswhich
resulted in more than 1000 identified prey items from fifty
nestsscarcely addressed food habits of floater eagles or
differences between males and females. Touchton et al.
(2002) offered what may be the best piece of knowledge
about Harpy Eagle foraging published to date. Despite
J Ornithol
tantalizing evidence for differential foraging strategies by
male vs. female Harpy Eagles in Touchton et al. (2002), the
small sample size (two individuals) allowed limited infer-
ence over the subjects discussed here. Would the con-
straints of breeding and the size difference between sexes
affect prey taken by this top predator?
Our goal in this study is to address two questions
regarding prey composition of Harpy Eagles: (i) do males
and females differ in their diet? (2) Do breeders have a diet
that is different from that of floaters to deal with repro-
duction constraints? Implications of our findings are rele-
vant for improving understanding of raptor biology under
the hypotheses of role divergence between males and
females, and the changes that breeding may induce on prey
composition.
Methods
The Harpy Eagle restoration program
Reintroduction to the wild of captive or rehabilitated wild
Harpy Eagles is complex; see Muela et al. (2003) for
hacking protocols (defined as a falconry technique that
helps young raptors reach their hunting potential by
allowing them to exercise and to begin foraging indepen-
dently over time), Campbell-Thompson et al. (2012) for
reintroduction protocols and Watson et al. (2016) for
general restoration results and management of captive
breeders. Harpy Eagles were equipped with radio and GPS
tags. During soft release, they were fed with thawed rats
and rabbits, always using a blind to avoid association of
food with humans. Independence was determined based on
the eagle being able to make two successive kills in
20 days or to survive 30 days without food provisioning,
proving that it was able to self-feed. Radio-tracking leading
to visual contact with the telemetered animal was needed to
check individual condition. During tracking, animals were
seen hunting and eating prey. At each predation record,
field attendants recorded the species killed (when identifi-
cation to the species level was possible) and its age class,
roughly divided into adult and juvenile. Field attendants
were instructed to remain as inconspicuous as possible and
leave the eagles alone as soon as required notes were taken.
All applicable international and institutional guidelines for
the care and use of animals in research were followed.
Learning from parents has a limited role in shaping the
food habits of Harpy Eagles, as juveniles remain in close
vicinity of the nest during their first two years (Muniz-
Lopez et al. 2012), with parents bringing food at decreasing
rates, while juveniles learn to hunt by trial, with no role for
vertical knowledge transmission of hunting behavior. This
led to a very homogeneous diet during the study period
where there are effects of neither ontogeny nor experience
in diet (Electronic Supplementary Material Fig. 1 and 2).
We therefore consider foraging by reintroduced Harpy
Eagles to be identical to that of floater Harpy Eagles in
general. We acknowledge that in more social raptors ver-
tical knowledge transmission can shape predation patterns
(Kitowski 2008).
Study site
Acclimation of released Harpy Eagle was executed at
Soberania National Park, a 19,545 ha moist tropical forest
in central Panama (9.07N, 79.65W), bordering the
Panama Canal (ANAM 2016). Annual rainfall averages
2226 mm and four dry months occur annually (Wishnie
et al. 2007). Vegetation of Soberania National Park con-
sists of a mixture of secondary and old growth forest.
Forest age ranges from 80 to 150 years, though some small
patches of old growth forest, estimated to be 400 years old,
remain (Heckadon et al. 1999). This park is home to many
species known to be the main prey of Harpy Eagles
(Aguiar-Silva et al. 2014), including sloths (Bradypus tri-
dactylus and Choloepus hoffmanni), monkeys (Alouatta
palliata and Cebus capucinus), porcupines (Sphiggurus
mexicanus, Coendou rothschildi), and coatis (Nasua
narica).
Comparisons between Harpy Eagle breeders
and floaters
We summarized available data on prey of breeding Harpy
Eagles from the available literature in order to compare it
with prey of floaters. This search was done using Google
Scholar, combining the vernacular and scientific names of
the species with diet, dieta, food habits and
habitos alimentarios. This allowed us to find published
and unpublished studies in English, Spanish and Por-
tuguese. For all comparisons between breeders and floaters,
we used a null-model approach. We chose this approach to
avoid any bias in our results due to the differences in
sample sizes and geographic areas.
To see if the difference in the geometric means of prey
mass between breeders and floaters were larger than
expected by chance, we used 1000 iteration of geometric
means of randomly labeled groups (i.e. random catego-
rization of breeding condition), later comparing them with
the real differences. While bootstrapping samples to each
simulation we used the n of the smallest group (floaters).
We used mean adult body mass at the species level for all
prey, except ungulates for which we used 1/5 of adult body
mass, because all known records involve predation of
newborns. When lacking identification at species level, we
used the body mass of the smallest species of the genus
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occurring in the area and discarded data when identification
was above genus (e.g., unidentified primates, unidentified
birds).
To compare standardized Levins niche widthgiven
by Bsta = B - 1/(n - 1), where B is Levins index
B 1=Rp2j , pj is the frequency of occurrence of each expected by chance. We compared male and female Harpy
group of prey species, and n is the total number of prey
species (Krebs 1999)of Harpy Eagle breeders and floa-
ters, we used the same null model approach, with prey
species at the genus level. Therefore we compared breeders
vs. floaters by: (1) jackknifing one sample of 25 prey
records of breeders and another sample of 25 prey records
of floaters; (2) calculating niche width for each one using
niche breadth measure; (3) creating a pairwise difference in
niche width between breeders and floaters; and (4) seeing if
the difference in niche width found between breeders and
floaters was larger than expected by chance by comparing
differences between two randomly labeled jackknifed
samples (n = 25). Our sample size of floaters allowed 10
iterations to be taken to calculate niche width between
treatments, and 1000 were taken to see how far it was from
random. We chose 25 as a sample size after previous work
showed this sample as enough to adequately represent all
prey species with frequencies [5% in tropical forests
(Miranda 2015).
We used prey identification at the genus level to make
meaningful comparisons of diet diversity between breeders
and floaters from widely separated sites. Their prey, two-
toed sloths (C. hoffmanni and C. didactylus), three-toed
sloths (Bradypus variegatus and B. tridactylus), howler
monkeys (Alouatta belzebul, A. macconnelli, A. palliata,
A. pigra, A. seniculus) and all others were treated at the
genus level in the analysis comparing prey diversity (for
niche width) and prey size between breeders and floaters.
This prevents misconceptions of a hyper-diverse diet when
analyzing diet across Central and South America, since
allopatric speciation induced by the Panama isthmus
caused several prey to split at the species level, otherwise
being consistent at genus level (e.g., Tamadua mexicana
vs. T. tetradactyla, N. narica vs. Nasua nasua). Only two
species were evaluated over the genus level: Sapajus and
Cebus (capuchin monkeys) and Sphiggurus and Coendou
(porcupines), which although in different levels, are close
genera with consistent general biology throughout their
distributions.
Comparisons between floater males and females
We used data from two other Harpy Eagles mentioned in
Touchton et al. (2002) as floaters, that were collected with
similar methods as part of the same restoration project. We
adopted this procedure because of our small sample size of
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male Harpy Eagle prey with available age. We calculated
Piankas niche overlap between male and female Harpy
Eagles using the null-model approach (Gotelli and
Entsminger 2006), which allowed the calculation of niche
overlap and the probability of it being higher or lower than
Eagles with respect to predation of sloths, juvenile prey,
terrestrial prey and unknown prey. This was done by a null-
model approach, using bootstrap sampling to compare
differences in the frequencies of these prey species
between males and females to the differences between prey
samples unlabeled for eagle sex and standardizing sample
size by the sex with the fewest samples (i.e., males). Niche
width between sexes was compared by setting the differ-
ences between ten thousand bootstrapped iterations
(n = 25) for each sex, and later comparing this difference
to randomly labeled sexes in another ten thousand itera-
tions. Prey size comparison was identical to that used
between breeders and floaters, but in this case we had
information on the age class of prey (juveniles and adults),
which were accounted by using 3/4 of adult body mass for
most juveniles, with the exception of ungulates for which
we used 1/5 of mean adult body mass. Alpha levels where
set at 0.05, and statistical analyses and figures were per-
formed with R using Vegan, EcoSim and SPSS packages
(Gotelli and Entsminger 2006; Oksanen et al. 2007; Zhang
et al. 2013).
Results
Two hundred predation records were obtained from 33
floaters Harpy Eagles during this study, 69 by males and
131 by females, from which 172 were identified to the
species level. Main prey of released Harpy Eagles were
remarkably consistent with previously published literature,
represented mainly by medium-sized arboreal mammals.
Brown-throated Sloth (Bradypus variegatus) was the most
important prey species for both sexes. Combined with
Hoffmanns two-toed Sloth (C. hoffmanni) and unidentified
sloths, they represented more than 50% of Harpy Eagle
prey. Sloths were followed by White-nosed coati (N. nar-
ica) and Northern lesser anteater (Tamandua mexicana) in
frequency (Table 1).
The review of prey data for Harpy Eagle breeders
included a total of 50 nests, which accounted for more than
1000 prey records (Table 2). Body mass of prey captured
by floaters was larger (p = 0.009; Fig. 1), with a geometric
mean mass of 4.24 kg (SD = 1.85, n = 198) than mean
prey mass of breeders (3.64 kg, SD = 1.27, n = 1024).
Niche width of floaters was 3.94, while that of breeders
was significantly wider at 5.55 (p \ 0.001).
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Table 1 Prey species, mean

Prey Habit Prey mass (kg) Males % (n) Females % (n) Overall %
body mass and frequency of
predation associated with non- Brown-throated sloth Arboreal 4.34 17.30 (12) 35.80 (47) 29.5
breeding Harpy Eagle males and
females reintroduced to Bradypus variegatus
Soberania National Park, Hoffmanns two-toed sloth Arboreal 5.72 13.00 (9) 14.50 (19) 14
Panama Choloepus hoffmanni
Unidentified sloth Arboreal 15.90 (11) 12.90 (17) 14
White-nosed coati Scansorial 3.05 5.79 (4) 6.87 (9) 6.5
Nasua narica
Northern lesser anteater Scansorial 4.60 1.44 (1) 7.63 (10) 5.5
Tamandua mexicana
Mantled howler monkey Arboreal 7.00 5.79 (4) 3.81 (5) 4.5
Alouatta palliata
Green Iguana Scansorial 2.29 2.89 (2) 3.05 (4) 3
Iguana iguana
Common opossum Scansorial 1.08 1.44 (1) 2.29 (3) 2
Didelphis marsupialis
White-headed capuchin Arboreal 3.92 2.89 (2) 1.52 (2) 2
Cebus capucinus
Collared peccary Terrestrial 3.68 4.34 (3) 0.00 (0) 1.5
Tayassu tajacu
Nine-banded armadillo Terrestrial 4.60 0.00 (0) 1.52 (2) 1
Dasypus novemcinctus
Central American agouti Terrestrial 2.95 2.89 (2) 0.00 (0) 1
Dasyprocta punctata
Crab-eating raccoon Terrestrial 10.10 0.00 (0) 0.76 (1) 0.5
Procyon cancrivorus
Tayra Scansorial 3.75 0.00 (0) 0.76 (1) 0.5
Eira Barbara
Black vulture Scansorial 1.64 1.44 (1) 0.00 (0) 0.5
Coragyps atratus
Unidentified prey 15.9 (11) 3.81 (5) 8
Unidentified mammal 5.79 (4) 4.58 (6) 5
Unidentified parrot Arboreal 1.44 (1) 0.00 (0) 0.5
Unidentified monkey Arboreal 1.44 (1) 0.00 (0) 0.5
Total 69 131

Piankas niche overlap between released male and
female Harpy Eagles was 0.79 and larger than expected by
chance (p = 0.008 for the upper tail). Combining data
from our work and Touchton et al. (2002), we obtained 128
predation records for which prey age was estimated. This
showed that among prey consumed by males and females,
57 and 17%, respectively, were juvenile prey (p \ 0.01;
Table 3). All prey records resulted in 261 samples, from
which we show that male and female Harpy Eagles present
differences in the frequency of sloth predation, represented
by 53% in female diet compared to 37% in male diet
(p = 0.014). Males preyed more on terrestrial animals (11
vs. 2%) than females (p \ 0.01), and had a greater niche
width (6.0 vs. 3.4) than females (p \ 0.05). Considering
aged prey only, the geometric mean of Harpy Eagle prey
size was 3.78 kg (SD = 1.47, n = 40) for males and
4.06 kg (SD = 1.52, n = 88) for females, presenting no
significant difference (p [ 0.05; Fig. 2). Prey of male
Harpy Eagles was less identifiable, resulting in 12.2% of
unidentified items compared with 2.9% for females
(Table 4).
Discussion
We show that sex and breeding status were associated with
several modifications affecting diet of Harpy Eagles. Males
fed on prey that was numerically smaller (although not

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Table 2 Number of nests monitored, study location, species richness and prey sample size (n) of Harpy Eagle breeders through South and
Central America
Site and country Nests Prey species Prey items Prey identified Sources

Bladen Nature Reserve, Belize 1 9 17 17 Rotenberg et al. (2012)

Cauaxi Farm, Brazil 1 3 21 21 Galetti and de Carvalho (2000)
Sierra Imataca, Venezuela 1 2 23 14 Seymour et al. (2010)
Kanaku Montains, Guyana 1 15 58 58 Rettig (1978)
Manaus, Brazil 1 6 26 25 Sanaiotti et al. (2001)
Kanaku Montains, Guyana 1 10 16 16 Izor (1985)
Esmeraldas, Ecuador 2 3 130 122 Muniz-Lopez (2008)
Kanaku Montains, Guyana 2 6 27 27 Fowler and Cope (1964)
Darien, Panama 3 19 97 91 Alvarez-Cordero (1996)
Comunidad de Infierno, Peru 4 14 80 79 Piana (2007)
Parintins, Brazil 5 14 253 240 Aguiar-Silva et al. (2014)
Xingu River, Brazil 6 19 165 147 Aguiar-Silva et al. (2015)
Sucumbios, Ecuador 10 14 53 47 Muniz-Lopez et al. (2007)
Guayana, Venezuela 12 19 139 125 Alvarez-Cordero (1996)
Total 50 1116 1024
Data from published literature

Fig. 1 Histogram of
differences in prey body mass of
Harpy Eagle breeders and
floaters. The line represents the
adjustment of a normal curve to
the data. As shown by arrows,
mean geometric prey body mass
of breeders (3.64 kg) is smaller
than that of floaters (4.24 kg)
the latter being larger
(p = 0.009)

significantly so), more varied and frequently terrestrial, support the hypothesis that breeding-related constraints
requiring more agility and therefore a smaller body size induced changes in prey composition: prey of breeders was
than females. This confirms the role separation hypothesis smaller than that of floaters, as has been shown for other
for the function of RSD (Kruger 2005). Our results also raptors (Caro et al. 2010, 2011). This probably reflects food

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Table 3 Predation of Harpy Eagle floaters by sex (males and Table 4 Percentage occurrence and respective sample size of several
females) on adult and juvenile prey species after reintroduction to prey categories and their associated increases for Harpy Eagle males
Soberania National Park, and Barro Colorado Island, Panama or females reintroduced to Soberania National Park
Prey Males Females Prey Male n Female n p
Juveniles Adults Juveniles Adults Sloths (%) 37.7 90 53.2 171 0.014
Brown-throated sloth 6 2 6 35 Terrestrial (%) 11.6 90 2.1 171 \0.01
Hoffmanns two-toed sloth 1 12 2 7 Unknown (%) 12.2 90 2.9 171 \0.01
Mantled howler monkey 4 0 3 13 Juveniles (%) 57.5 40 17.0 88 \0.01
White-nosed coati 5 0 1 5 Size (kg) 3.7 40 4.0 88 0.357
Green Iguana 0 0 0 6 Niche width 6.0 67 3.4 144 \0.01
Collared peccary 5 0 0 0 Prey size and niche width differences between sexes are also
White-headed capuchin 0 1 0 3 described
Common opossum 0 0 0 3
Central American agouti 1 1 0 0 rats and rabbits, their prey composition in the wild was
Northern lesser anteater 0 0 1 1 typical of Harpy Eagles. This strengthens our notion that
Brocket deer 1 0 1 0 captive-bred and released Harpy Eagles had feeding habits
Tayra 0 0 1 0 similar to the wild-hatched floaters. With some caveats, the
Kinkajou 0 1 0 0 data available warrant some tentative conclusions: our
Sum 23 17 15 73 results are the first to reveal significant differences in diet
as a product of sex and breeding in a large raptor with a
robust sample size.
stress related with overhunting around the vicinity of the Small size increases hunting success in some raptors
nest (Nilsson et al. 1982; Bonal and Aparicio 2008), (Hakkarainen and Korpimaki 1991; Hakkarainen et al.
leading to a more diverse diet that relies on less prof- 1996). As male Harpy Eagles take prey more frequently
itable but still abundant prey. Despite the fact that captive- than females (Touchton et al. 2002), male Harpy Eagles
bred and released individuals were fed with laboratory bred seem to be able to obtain more energy per time invested in

Fig. 2 Histogram of
differences between prey body
mass between Harpy Eagle
males and females. The line
represents the adjustment of a
normal curve to the data. As
shown by arrows, mean
geometric prey body mass of
males (3.78 kg) is smaller than
that of females (4.06 kg) but
this difference lacks statistical
significance (p [ 0.05)

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foraging. Furthermore, males started hunting at an earlier
age (Watson et al. 2016), and did not accept supplementary
food as sub-adults, contrary to females (Campbell-
Thompson et al. 2012). Our study adds to this showing that
male Harpy Eagles fed on more diverse prey, as their niche
width was double that of females. Their smaller size also
allowed them to hunt more terrestrial prey, and probably
afforded them better agility to swoop between lianas and
branches throughout the several layers that separate the
canopy from the ground. Terrestrial prey consumption by
males can be detrimental to population sex-ratio, since
predation of livestock (terrestrial prey) may be more
common for males, resulting in retaliatory shooting by
local people. Juvenile prey consumption by male Harpy
Eagles was triple that of females. Although lacking sta-
tistical significance, males prey was smaller in size than
females. We believe that the following factors contribute to
this lack of statistical significance: (1) Smaller prey are
consumed faster than larger prey, reducing chances of
proper identification (Slagsvold et al. 2010); (2) The pro-
portion of prey remains left uneaten increases with prey
body mass, also reducing identification chances for small
prey (Slagsvold et al. 2010); (3) Our scoring of a prey item
as unidentified was due to the fact that little remained of it,
hence it probably had been consumed fast, and therefore
probably was small; (4) Males had a four times higher
proportion of unidentified prey compared to females, so
they probably took smaller prey. Some prey items taken
mainly by malessuch as agoutis, monkeys and small
peccariesare the most agile, creating selection pressure
for smaller body size in males until it reaches a tradeoff
limit, where the handicaps of subduing and carrying prey
will not pay off for decreasing Harpy Eagle body size.
On the other hand, sloths were consumed more fre-
quently by females. Whereas common sense suggests
sloths as defenseless animals, they readily swung claws
over predators, and two-toed sloths are highly inclined to
bite. This lead researchers that witnessed interactions
between sloths and Harpy Eagles to depict sloths as for-
midable prey (Touchton et al. 2002; Touchton 2010). If
failing to avoid detection, sloths also rely on anchoring to
branches, through which they can avoid 45% of Harpy
Eagle predation attempts (Touchton et al. 2002). Large size
may allow females to succeed in detaching sloths from
branches more effectively than males do. Besides an
extraordinary ability to avoid detection, sloths have large
claws, thick skin, and 1/3 of mass represented by undigested
leaves (Goffart 1971). Considering these traits, it is hard to
suggest another reason for sloths being so frequent in
Harpy Eagle diet other than their high abundance (Taube
et al. 1999). Bearing in mind sloths cryptic habits, the fact
that Harpy Eagles are highly dependent on sound and
vision to detect prey may also play a role in this dietary
123
J Ornithol
trait. It has been suggested that large size in female raptors
may afford better performance in shredding prey for nest-
lings (Slagsvold and Sonerud 2007). This would be par-
ticularly true in Harpy Eagles because sloths have tough
skin and muscles, requiring considerable power to be
shredded for nestlings. Furthermore, male raptors are
inefficient in shredding food for nestlings (Schmutz et al.
2014). Considering the many cited factors that create
selection pressure for Harpy Eagle females being large, and
the abundance on their main prey source (sloths), they
grow larger than most other extant eagles.
While our data offer support for role differentiation
between males and females as an explanation of RSD, no
support can be given to niche differentiation. In this
hypothesis, differently sized males and females would
relieve competition by targeting different prey (Kruger
2005). Niche overlap between males and females was high,
suggesting competition. Even if accounting for aspects in
which male and female diet differs (juvenile vs. adult prey,
for instance), high niche overlap would still lead to
scramble competition. Another putative source of demand
for hunting small prey in males is that large prey cannot be
consumed efficiently; a large carcass will decompose to the
point of not being more consumable by the female and
young at the nest. However when females resume hunting,
the young is already large and hungry, therefore making
large prey more profitable. This increases selection pres-
sure for females preying on larger animals, which is the
case in female Harpy Eagle floaters. This hypothesis could
be tested by using camera traps to monitor changes in
delivery frequency and prey size in Harpy Eagle nests.
Breeding pressure induces a series of modifications in
Harpy Eagle diet. Harpy Eagles are known to apply some
processing of prey to maximize energetic profit of carrying
them to the nest: monkeys are decapitated, and frequently
just hind limbs and tail reach the nest, while sloths are
eviscerated and often only the rear limbs and head are car-
ried to the nest (Aguiar-Silva et al. 2014). This suggests that
prey mass is a constraint. When free of the constraint to
carry prey to the nest, Harpy Eagles targeted larger prey.
Golden Eagles (Aquila chrysaetus) have a similar pattern of
consuming larger prey on the ground outside the breeding
season (Watson 2010). Ground feeding is a behavior that
also exists in Harpy Eagles (Rettig 1978; Springer et al.
2011). Niche width of breeders was nearly twice that of
floaters. Foraging becomes restricted to the vicinity of the
nest in breeding raptors, sometimes exhausting local prey
populations (Rutz and Bijlsma 2006) and leading to preying
upon less profitable and more diverse prey. Even though
porcupines are one of the most dangerous prey for raptors
(Katzner et al. 2015), they are common prey of Harpy Eagle
breeders (Alvarez-Cordero 1996; Piana 2007) but nearly
absent from the prey of floaters.
J Ornithol
A possible caveat of our analysis is that the data on
breeders pertain to a much larger area, and this may par-
tially explain our finding of a larger niche width in
breeders. However, we believe that by analyzing data using
prey above genus level and by doing extensive bootstrap-
ping to avoid problems of different samples sizes circum-
vents this limitation. One could argue that differences
between floaters and breeders are a result of foraging
during breeding being performed essentially by males.
Though, most data regarding breeding Harpy Eagles are
from late breeding phase, when both parents hunt. Another
caveat that further research may tackle is modeling bird
identity for accounting with intra-individual variation and
further avoiding pseudo replication. In our case, the num-
ber of prey items per bird (or per nest in the data from the
literature) was too small to include bird identity as a ran-
dom factor (and not possible to track in most of the pub-
lished data).
In conclusion, our data suggest that Harpy Eagle diet
can be affected by two dependent mechanisms: sex and
breeding condition. Our data provide support for the
hypothesis of parental role differentiation (Kruger 2005) as
an explanation for RSD in raptors. Breeding imposes a
number of constraints on Harpy Eagles, inducing hunting
of smaller prey, and also increasing their niche width.
These have been observed in other raptors and can prob-
ably be generalized (Collopy 1984; Watson 2010). As a
result, the data provided here presents a case study which
may help to understand the relationship of RSD and
breeding to raptor feeding ecology. If our hypotheses sur-
vive to further research, questions remain regarding how
the strong diet variation among these groups (sex and
breeding classes), affect population dynamics of this key-
stone species and its prey.
Acknowledgements We thank the many donors who supported The
Peregrine Funds Harpy Eagle Restoration Program: The U.S. Agency
for International Development (USAID), Archie W. and Grace Berry
Foundation, Burns Family Foundation, Butler Foundation, CEMEX
Panama, Jim and Barbara Cimino, Liz Claiborne and Art Ortenberg
Foundation, Disney Worldwide Conservation Fund, Walt Disney
Company Foundation, Evie Donaldson, Charles Engelhard Founda-
tion, ExxonMobil Foundation, Greater Los Angeles Zoo Association,
Howard Gilman Foundation, Houston Zoo, Diane A. Ledder Chari-
table Trust, Ledder Family Charitable Trust, Mr. and Mrs. Peter
Manigault, Ruth O. Mutch, Newmans Own Organics, Norcross
Wildlife Foundation, Offield Family Foundation, Paxson H. Offield,
Pennzoil-Quaker State Company, Don Tyson, Wallace Genetic
Foundation, Julie A. Wrigley, Wolf Creek Charitable Foundation,
Zoological Society of San Diego, and other important donors. EBPM
thanks Rufford Small Grants (Grant no. 18743-1), Rainforest Biodi-
versity Group, Idea Wild and The Explorers Club Exploration Fund
Mamont Scholars Program for their financial support. EBPM
received logistical support from the Peugeot-ONF Carbon Sink
Reforestation Project, based at the Sao Nicolau Farm in Cotriguacu,
Mato Grosso, Brazil. This Project is a Peugeot initiative to fulfill
some of the Kyoto Protocol directions and is run by the ONF-Brasil
enterprise. Victor Landeiro and Marcelo Salsicha Segall provided
useful discussions on data analysis and theory. All research protocols
and capture procedures applied for Harpy Eagles in Soberania
National Park were approved by the National Environmental
Authority of Panama Committee on Animal Care and were in
accordance with the Guidelines of The Peregrine Funds Council on
Animal Care. The Peregrine Fund s Harpy Eagle Restoration Program
complied with the laws of Panama during the time in which the
project was carried out. We also thank staff and volunteers who have
participated in The Peregrine Funds Harpy Eagle Restoration
Program.
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