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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- than breeders. Our data provide support for the hypothesis
ation among population classessuch as sex and breeding of parental role differentiation as an explanation for
classthat can be consequence of the groups specific reversed sexual size dimorphism in raptors.
constraints and roles. In raptors, differential parental roles
related to foraging have been the main explanation for Keywords Reversed sexual size dimorphism  Breeding
males being smaller than females, as smaller males have constraints  Role differentiation hypothesis  Foraging 
been described to be more efficient foragers. During one Raptor  Floater
phase of breeding, only males forage, requiring them to
feed themselves, females and young. This is expected to Zusammenfassung
induce changes in foraging behavior of breeders compared
to non-breeders. By comparing prey taken by floaters and Geschlecht und Brutstatus beeinflussen die
breeders of Harpy Eagles (Harpia harpyja), we describe Beutezusammensetzung von Harpyien
some effects of breeding and sex on the diet. Here we show
that diet traits differed between male and female floaters, Das Verhalten bei der Nahrungssuche kann sich zwischen
and between floaters and breeders. Juvenile prey was three den Populationsklassenwie beispielweise Geschlecht
times more common in the diet of males than that of und Brutklassebetrachtlich unterscheiden, welches eine
females. Sloths were more common prey among females Folge der spezifischen Beschrankungen und Rollen dieser
than among males (53 vs. 37%). Males preyed four times Gruppen sein kann. Bei Greifvogeln gelten die
more on terrestrial animals than did females, and showed a unterschiedlichen Rollen der Elternvogel bei der
greater niche width than females (6.0 vs. 3.4). The prey of Nahrungssuche als die hauptsachliche Erklarung dafur,
breeders was smaller than that of non-breeders (on average dass die Mannchen kleiner sind als die Weibchen, da die
3.64 vs. 4.24 kg). Non-breeders had a larger niche width kleineren Mannchen als die effizienteren Jager gelten.
Wahrend eines Abschnitts des Brutgeschehens jagen nur
die Mannchen, welche daher nicht nur sich selbst, sondern
Communicated by O. Kruger.
auch noch die Weibchen und die Jungvogel mit Nahrung
Electronic supplementary material The online version of this versorgen mussen. Dies lasst Anderungen im Jagdverhalten
article (doi:10.1007/s10336-017-1482-3) contains supplementary zwischen Brutvogeln und Nichtbrutern erwarten. Im
material, which is available to authorized users. Vergleich von Beutetieren nicht-territorialer Harpyien
& Everton B. P. Miranda
(Harpia harpyja) mit denen von Brutvogeln beschreiben
mirandaebp@gmail.com wir einige Einflusse von Brutstatus und Geschlecht auf die
Nahrungszusammensetzung. Hier zeigen wir, dass sich die
1
ONF Brasil Gestao Florestal, Cotriguacu, MT, Brazil Ernahrungsgewohnheiten nicht-territorialer Mannchen und
2
The Peregrine Fund, 5668 West Flying Hawk Lane, Boise, Weibchen sowie diejenigen der nicht-territorialen Vogel
ID 83709, USA und Brutvogel unterscheiden. Im Nahrungsspektrum der
3
Fundacion Aguilas de Los Andes, Pereira, Colombia Mannchen waren Jungtiere dreimal haufiger vertreten als in

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dem der Weibchen. Faultiere wurden haufiger zur Beute mate for food (Schmutz et al. 2014; Sonerud et al. 2014).
von Weibchen als von Mannchen (53% gegenuber 37%). Therefore, during a key part of their life cycle, male raptors
Mannchen erbeuteten viermal haufiger bodenlebende Tiere must be extraordinarily efficient foragers to feed them-
als die Weibchen und wiesen eine groere Nischenbreite selves, their mates and offspring. Their smaller size gives
auf als diese (6,0 gegenuber 3,4). Die Beutetiere der them more agility compared with females (Andersson and
Brutvogel waren kleiner als die der Nichtbruter (im Schnitt Norberg 1981), and greater energy efficiency when carry-
3,64 kg gegenuber 4,24 kg). Nichtbruter nutzten eine ing heavy prey over long distances between foraging
groere Nischenbreite als Brutvogel. Unsere Daten grounds and the nest (Hakkarainen et al. 1996). In the later
unterstutzen die Hypothese der elterlichen phase of nesting, when nestlings have acquired thermal
Rollenverteilung als Erklarung fur den umgekehrten independence, the female reassumes hunting to recover her
Groendimorphismus bei Greifvogeln. 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-
Introduction feeding or prey delivery; which kind and size of prey to
hunt to maximize energetic gains from larger prey or to
Ever since Darwin (1859), scientists have puzzled about hunt smaller prey to reduce carrying costs (Sonerud et al.
why in many organisms males and females differ (Fisher 2013). These decisions are expected to affect foraging by
1930; Zahavi 1975). Indeed, sexual dimorphism is one of breeding raptors, when compared with non-breeding indi-
the traits without which much of what is most extraordi- viduals free of these constraintsthe floaters (Barrows
nary, beautiful and bizarre in nature would not exist. 1987).
Sexual size dimorphism has generated a still growing body RSD is pronounced in Harpy Eagles (Harpia harpyja).
of knowledge on its origins and consequences (Catry et al. Males average 5.95 kg, and are 19% smaller than females
2016; Andersson 1994), given that body size is a key trait with a mean weight of 7.35 kg, resulting in a female:male
driving organisms fitness (Mayer et al. 2016). In this linear body size ratio of 1.07 (n = 12, Peregrine Fund, unp.
context, foraging behavior has become a focus of attention, data). Furthermore, the Harpy Eagle reproductive cycle is
because it is highly affected by organism size. Foraging exceptionally long (Muniz-Lopez et al. 2007), with an
therefore offers a way of measuring the ecological and average of three years between each successful fledgling,
evolutionary interplay that result in sexual size dimorphism which is expected to be highly demanding on males. Harpy
(Angel et al. 2015). Eagle young depend on females to shred prey for them
While most tetrapods show what is called normal until they are up to ten months of age, they fledge at six
sexual size dimorphismwhere males are larger than months and become independent at 2.53 years (Rettig
femalesin raptors (Accipitriformes, Falconiformes and 1978; Muniz-Lopez et al. 2012). Harpy Eagles occur at low
Strigiformes orders) larger females are the norm. This has densities (de Vargas-Gonzalez and Vargas 2011), formerly
been called reversed sexual dimorphism or RSD (Rey- throughout much of Central and South America. Threat-
nolds 1972). Kruger (2005) used comparative analyses to ened by habitat loss and shooting (Birdlife International
test the three main hypotheses that have been proposed to 2016), range reduction is already impacting its genetic
explain RSD in raptors: (a) niche partitioningwhere size- diversity (Banhos et al. 2016). These problems drove The
divergent sexes are able to reduce intersexual competition Peregrine Fund to test a restoration effort for the species,
for prey; (b) role differentiationwhere larger females are through captive breeding and reintroduction in their former
better brooders and smaller males are better foragers and range (Watson et al. 2016). This kind of initiative is known
territory defenders; (c) behavioralwhere larger females to generate a great deal of information on foraging, since
are dominant over males, aiding in the maintenance of the released animals require intensive monitoring (Hayward
pair-bond and increasing male food-provisioning, or that et al. 2011).
larger females compete more effectively for males. In this With respect to diet, the Harpy Eagle is the most studied
synthesis, the better supported hypothesis was of role dif- of Neotropical raptors. While broad patterns on diet are
ferentiation (b), mainly because small males seem to be known (Aguiar-Silva et al. 2014), important details are not.
more efficient foragers. Nevertheless, raptor RSD is far The half century of systematic work on food habitswhich
from being a closed subject (Slagsvold and Sonerud 2007; resulted in more than 1000 identified prey items from fifty
Olsen et al. 2013). nestsscarcely addressed food habits of floater eagles or
In raptors, although males are smaller, they do most of differences between males and females. Touchton et al.
the hunting during the initial breeding phase when the (2002) offered what may be the best piece of knowledge
females are incubating and brooding and relying on their about Harpy Eagle foraging published to date. Despite

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tantalizing evidence for differential foraging strategies by where there are effects of neither ontogeny nor experience
male vs. female Harpy Eagles in Touchton et al. (2002), the in diet (Electronic Supplementary Material Fig. 1 and 2).
small sample size (two individuals) allowed limited infer- We therefore consider foraging by reintroduced Harpy
ence over the subjects discussed here. Would the con- Eagles to be identical to that of floater Harpy Eagles in
straints of breeding and the size difference between sexes general. We acknowledge that in more social raptors ver-
affect prey taken by this top predator? tical knowledge transmission can shape predation patterns
Our goal in this study is to address two questions (Kitowski 2008).
regarding prey composition of Harpy Eagles: (i) do males
and females differ in their diet? (2) Do breeders have a diet Study site
that is different from that of floaters to deal with repro-
duction constraints? Implications of our findings are rele- Acclimation of released Harpy Eagle was executed at
vant for improving understanding of raptor biology under Soberania National Park, a 19,545 ha moist tropical forest
the hypotheses of role divergence between males and in central Panama (9.07N, 79.65W), bordering the
females, and the changes that breeding may induce on prey Panama Canal (ANAM 2016). Annual rainfall averages
composition. 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.
Methods Forest age ranges from 80 to 150 years, though some small
patches of old growth forest, estimated to be 400 years old,
The Harpy Eagle restoration program remain (Heckadon et al. 1999). This park is home to many
species known to be the main prey of Harpy Eagles
Reintroduction to the wild of captive or rehabilitated wild (Aguiar-Silva et al. 2014), including sloths (Bradypus tri-
Harpy Eagles is complex; see Muela et al. (2003) for dactylus and Choloepus hoffmanni), monkeys (Alouatta
hacking protocols (defined as a falconry technique that palliata and Cebus capucinus), porcupines (Sphiggurus
helps young raptors reach their hunting potential by mexicanus, Coendou rothschildi), and coatis (Nasua
allowing them to exercise and to begin foraging indepen- narica).
dently over time), Campbell-Thompson et al. (2012) for
reintroduction protocols and Watson et al. (2016) for Comparisons between Harpy Eagle breeders
general restoration results and management of captive and floaters
breeders. Harpy Eagles were equipped with radio and GPS
tags. During soft release, they were fed with thawed rats We summarized available data on prey of breeding Harpy
and rabbits, always using a blind to avoid association of Eagles from the available literature in order to compare it
food with humans. Independence was determined based on with prey of floaters. This search was done using Google
the eagle being able to make two successive kills in Scholar, combining the vernacular and scientific names of
20 days or to survive 30 days without food provisioning, the species with diet, dieta, food habits and
proving that it was able to self-feed. Radio-tracking leading habitos alimentarios. This allowed us to find published
to visual contact with the telemetered animal was needed to and unpublished studies in English, Spanish and Por-
check individual condition. During tracking, animals were tuguese. For all comparisons between breeders and floaters,
seen hunting and eating prey. At each predation record, we used a null-model approach. We chose this approach to
field attendants recorded the species killed (when identifi- avoid any bias in our results due to the differences in
cation to the species level was possible) and its age class, sample sizes and geographic areas.
roughly divided into adult and juvenile. Field attendants To see if the difference in the geometric means of prey
were instructed to remain as inconspicuous as possible and mass between breeders and floaters were larger than
leave the eagles alone as soon as required notes were taken. expected by chance, we used 1000 iteration of geometric
All applicable international and institutional guidelines for means of randomly labeled groups (i.e. random catego-
the care and use of animals in research were followed. rization of breeding condition), later comparing them with
Learning from parents has a limited role in shaping the the real differences. While bootstrapping samples to each
food habits of Harpy Eagles, as juveniles remain in close simulation we used the n of the smallest group (floaters).
vicinity of the nest during their first two years (Muniz- We used mean adult body mass at the species level for all
Lopez et al. 2012), with parents bringing food at decreasing prey, except ungulates for which we used 1/5 of adult body
rates, while juveniles learn to hunt by trial, with no role for mass, because all known records involve predation of
vertical knowledge transmission of hunting behavior. This newborns. When lacking identification at species level, we
led to a very homogeneous diet during the study period used the body mass of the smallest species of the genus

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occurring in the area and discarded data when identification male Harpy Eagle prey with available age. We calculated
was above genus (e.g., unidentified primates, unidentified Piankas niche overlap between male and female Harpy
birds). Eagles using the null-model approach (Gotelli and
To compare standardized Levins niche widthgiven Entsminger 2006), which allowed the calculation of niche
by Bsta = B - 1/(n - 1), where B is Levins index overlap and the probability of it being higher or lower than
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 Eagles with respect to predation of sloths, juvenile prey,
species (Krebs 1999)of Harpy Eagle breeders and floa- terrestrial prey and unknown prey. This was done by a null-
ters, we used the same null model approach, with prey model approach, using bootstrap sampling to compare
species at the genus level. Therefore we compared breeders differences in the frequencies of these prey species
vs. floaters by: (1) jackknifing one sample of 25 prey between males and females to the differences between prey
records of breeders and another sample of 25 prey records samples unlabeled for eagle sex and standardizing sample
of floaters; (2) calculating niche width for each one using size by the sex with the fewest samples (i.e., males). Niche
niche breadth measure; (3) creating a pairwise difference in width between sexes was compared by setting the differ-
niche width between breeders and floaters; and (4) seeing if ences between ten thousand bootstrapped iterations
the difference in niche width found between breeders and (n = 25) for each sex, and later comparing this difference
floaters was larger than expected by chance by comparing to randomly labeled sexes in another ten thousand itera-
differences between two randomly labeled jackknifed tions. Prey size comparison was identical to that used
samples (n = 25). Our sample size of floaters allowed 10 between breeders and floaters, but in this case we had
iterations to be taken to calculate niche width between information on the age class of prey (juveniles and adults),
treatments, and 1000 were taken to see how far it was from which were accounted by using 3/4 of adult body mass for
random. We chose 25 as a sample size after previous work most juveniles, with the exception of ungulates for which
showed this sample as enough to adequately represent all we used 1/5 of mean adult body mass. Alpha levels where
prey species with frequencies [5% in tropical forests set at 0.05, and statistical analyses and figures were per-
(Miranda 2015). formed with R using Vegan, EcoSim and SPSS packages
We used prey identification at the genus level to make (Gotelli and Entsminger 2006; Oksanen et al. 2007; Zhang
meaningful comparisons of diet diversity between breeders et al. 2013).
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 Results
monkeys (Alouatta belzebul, A. macconnelli, A. palliata,
A. pigra, A. seniculus) and all others were treated at the Two hundred predation records were obtained from 33
genus level in the analysis comparing prey diversity (for floaters Harpy Eagles during this study, 69 by males and
niche width) and prey size between breeders and floaters. 131 by females, from which 172 were identified to the
This prevents misconceptions of a hyper-diverse diet when species level. Main prey of released Harpy Eagles were
analyzing diet across Central and South America, since remarkably consistent with previously published literature,
allopatric speciation induced by the Panama isthmus represented mainly by medium-sized arboreal mammals.
caused several prey to split at the species level, otherwise Brown-throated Sloth (Bradypus variegatus) was the most
being consistent at genus level (e.g., Tamadua mexicana important prey species for both sexes. Combined with
vs. T. tetradactyla, N. narica vs. Nasua nasua). Only two Hoffmanns two-toed Sloth (C. hoffmanni) and unidentified
species were evaluated over the genus level: Sapajus and sloths, they represented more than 50% of Harpy Eagle
Cebus (capuchin monkeys) and Sphiggurus and Coendou prey. Sloths were followed by White-nosed coati (N. nar-
(porcupines), which although in different levels, are close ica) and Northern lesser anteater (Tamandua mexicana) in
genera with consistent general biology throughout their frequency (Table 1).
distributions. The review of prey data for Harpy Eagle breeders
included a total of 50 nests, which accounted for more than
Comparisons between floater males and females 1000 prey records (Table 2). Body mass of prey captured
by floaters was larger (p = 0.009; Fig. 1), with a geometric
We used data from two other Harpy Eagles mentioned in mean mass of 4.24 kg (SD = 1.85, n = 198) than mean
Touchton et al. (2002) as floaters, that were collected with prey mass of breeders (3.64 kg, SD = 1.27, n = 1024).
similar methods as part of the same restoration project. We Niche width of floaters was 3.94, while that of breeders
adopted this procedure because of our small sample size of 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 aged prey only, the geometric mean of Harpy Eagle prey
female Harpy Eagles was 0.79 and larger than expected by size was 3.78 kg (SD = 1.47, n = 40) for males and
chance (p = 0.008 for the upper tail). Combining data 4.06 kg (SD = 1.52, n = 88) for females, presenting no
from our work and Touchton et al. (2002), we obtained 128 significant difference (p [ 0.05; Fig. 2). Prey of male
predation records for which prey age was estimated. This Harpy Eagles was less identifiable, resulting in 12.2% of
showed that among prey consumed by males and females, unidentified items compared with 2.9% for females
57 and 17%, respectively, were juvenile prey (p \ 0.01; (Table 4).
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 Discussion
by 53% in female diet compared to 37% in male diet
(p = 0.014). Males preyed more on terrestrial animals (11 We show that sex and breeding status were associated with
vs. 2%) than females (p \ 0.01), and had a greater niche several modifications affecting diet of Harpy Eagles. Males
width (6.0 vs. 3.4) than females (p \ 0.05). Considering 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 trait. It has been suggested that large size in female raptors
age (Watson et al. 2016), and did not accept supplementary may afford better performance in shredding prey for nest-
food as sub-adults, contrary to females (Campbell- lings (Slagsvold and Sonerud 2007). This would be par-
Thompson et al. 2012). Our study adds to this showing that ticularly true in Harpy Eagles because sloths have tough
male Harpy Eagles fed on more diverse prey, as their niche skin and muscles, requiring considerable power to be
width was double that of females. Their smaller size also shredded for nestlings. Furthermore, male raptors are
allowed them to hunt more terrestrial prey, and probably inefficient in shredding food for nestlings (Schmutz et al.
afforded them better agility to swoop between lianas and 2014). Considering the many cited factors that create
branches throughout the several layers that separate the selection pressure for Harpy Eagle females being large, and
canopy from the ground. Terrestrial prey consumption by the abundance on their main prey source (sloths), they
males can be detrimental to population sex-ratio, since grow larger than most other extant eagles.
predation of livestock (terrestrial prey) may be more While our data offer support for role differentiation
common for males, resulting in retaliatory shooting by between males and females as an explanation of RSD, no
local people. Juvenile prey consumption by male Harpy support can be given to niche differentiation. In this
Eagles was triple that of females. Although lacking sta- hypothesis, differently sized males and females would
tistical significance, males prey was smaller in size than relieve competition by targeting different prey (Kruger
females. We believe that the following factors contribute to 2005). Niche overlap between males and females was high,
this lack of statistical significance: (1) Smaller prey are suggesting competition. Even if accounting for aspects in
consumed faster than larger prey, reducing chances of which male and female diet differs (juvenile vs. adult prey,
proper identification (Slagsvold et al. 2010); (2) The pro- for instance), high niche overlap would still lead to
portion of prey remains left uneaten increases with prey scramble competition. Another putative source of demand
body mass, also reducing identification chances for small for hunting small prey in males is that large prey cannot be
prey (Slagsvold et al. 2010); (3) Our scoring of a prey item consumed efficiently; a large carcass will decompose to the
as unidentified was due to the fact that little remained of it, point of not being more consumable by the female and
hence it probably had been consumed fast, and therefore young at the nest. However when females resume hunting,
probably was small; (4) Males had a four times higher the young is already large and hungry, therefore making
proportion of unidentified prey compared to females, so large prey more profitable. This increases selection pres-
they probably took smaller prey. Some prey items taken sure for females preying on larger animals, which is the
mainly by malessuch as agoutis, monkeys and small case in female Harpy Eagle floaters. This hypothesis could
peccariesare the most agile, creating selection pressure be tested by using camera traps to monitor changes in
for smaller body size in males until it reaches a tradeoff delivery frequency and prey size in Harpy Eagle nests.
limit, where the handicaps of subduing and carrying prey Breeding pressure induces a series of modifications in
will not pay off for decreasing Harpy Eagle body size. Harpy Eagle diet. Harpy Eagles are known to apply some
On the other hand, sloths were consumed more fre- processing of prey to maximize energetic profit of carrying
quently by females. Whereas common sense suggests them to the nest: monkeys are decapitated, and frequently
sloths as defenseless animals, they readily swung claws just hind limbs and tail reach the nest, while sloths are
over predators, and two-toed sloths are highly inclined to eviscerated and often only the rear limbs and head are car-
bite. This lead researchers that witnessed interactions ried to the nest (Aguiar-Silva et al. 2014). This suggests that
between sloths and Harpy Eagles to depict sloths as for- prey mass is a constraint. When free of the constraint to
midable prey (Touchton et al. 2002; Touchton 2010). If carry prey to the nest, Harpy Eagles targeted larger prey.
failing to avoid detection, sloths also rely on anchoring to Golden Eagles (Aquila chrysaetus) have a similar pattern of
branches, through which they can avoid 45% of Harpy consuming larger prey on the ground outside the breeding
Eagle predation attempts (Touchton et al. 2002). Large size season (Watson 2010). Ground feeding is a behavior that
may allow females to succeed in detaching sloths from also exists in Harpy Eagles (Rettig 1978; Springer et al.
branches more effectively than males do. Besides an 2011). Niche width of breeders was nearly twice that of
extraordinary ability to avoid detection, sloths have large floaters. Foraging becomes restricted to the vicinity of the
claws, thick skin, and 1/3 of mass represented by undigested nest in breeding raptors, sometimes exhausting local prey
leaves (Goffart 1971). Considering these traits, it is hard to populations (Rutz and Bijlsma 2006) and leading to preying
suggest another reason for sloths being so frequent in upon less profitable and more diverse prey. Even though
Harpy Eagle diet other than their high abundance (Taube porcupines are one of the most dangerous prey for raptors
et al. 1999). Bearing in mind sloths cryptic habits, the fact (Katzner et al. 2015), they are common prey of Harpy Eagle
that Harpy Eagles are highly dependent on sound and breeders (Alvarez-Cordero 1996; Piana 2007) but nearly
vision to detect prey may also play a role in this dietary absent from the prey of floaters.

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A possible caveat of our analysis is that the data on enterprise. Victor Landeiro and Marcelo Salsicha Segall provided
breeders pertain to a much larger area, and this may par- useful discussions on data analysis and theory. All research protocols
and capture procedures applied for Harpy Eagles in Soberania
tially explain our finding of a larger niche width in National Park were approved by the National Environmental
breeders. However, we believe that by analyzing data using Authority of Panama Committee on Animal Care and were in
prey above genus level and by doing extensive bootstrap- accordance with the Guidelines of The Peregrine Funds Council on
ping to avoid problems of different samples sizes circum- Animal Care. The Peregrine Fund s Harpy Eagle Restoration Program
complied with the laws of Panama during the time in which the
vents this limitation. One could argue that differences project was carried out. We also thank staff and volunteers who have
between floaters and breeders are a result of foraging participated in The Peregrine Funds Harpy Eagle Restoration
during breeding being performed essentially by males. Program.
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 References
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