Prey Composition of Harpy Eagles ( Harpia harpyja ) in Raleighvallen,Suriname

Abstract

Apex predators are in widespread decline, in many occasions as a consequence of the demise of their prey. Harpy Eagles (Harpia harpyja) are the largest extant eagles on Earth and keystone predators in the tropical forests they inhabit. Although Harpy Eagle prey composition has been described by a number of studies, diet data from primary forests are rare on the literature. Here, I describe the diet of Harpy Eagles living in the Central Suriname Reserve primary forests and review literature data to provide an accessible reference to all known reports of Harpy Eagle prey species. In Central Suriname Nature Reserve, Harpy Eagles made frequent use of game prey such as large primates, large birds, and terrestrial animals, besides what is considered their staple prey, sloths. Nine new prey species were recorded, most of them game animals. This totals 102 prey species when summed with literature data. This information provides new insights into the autecology of Harpy Eagles in Neotropical forests, enabling a better understanding of the ecological effects of apex predator.

Keywords

apex predator primate predation primary forest nonhunted forest aerial predator canopy

Introduction

Predators have widespread regulatory potential over the biological landscapes they inhabit (Newsome et al., 2017) and are thus prioritized in the conservation biology agenda (Sérgio, Newton, Marchiesi, & Pedrini, 2006). An adequate prey basis is one of the most important determinants of predator persistence (Barber-Meyer et al., 2013; Lamichhane et al., 2018). To better understand the importance of predator–prey interactions, we need to understand composition of the prey base in detail (Uulu, Wegge, Mishra, & Sharma, 2014). Indeed, prey composition is a trademark of apex predator’s scientific literature (Hayward & Kerley, 2005; Schweiger, Fünfstück, & Beierkuhnlein, 2015).

The Harpy Eagle (Harpia harpyja; Figure 1) is the largest extant eagle on Earth, weighting from 4.9 to 6.9 kg in males and from 5.9 to 9.1 kg in females. They hunt by sight and hearing, carefully scanning the canopy for prey species (Touchton, Hsu, & Palleroni, 2002). Harpy Eagles have been recognized as keystone predators, and in their absence, overgrown prey populations can cause trophic cascades (Orihuela, Terborgh, Ceballos, & Glander, 2014; Terborgh et al., 2001). Harpy Eagles are threatened by habitat loss and shooting (Muñiz-López, 2017). While they have disappeared from much of their former distribution (Vargas-González et al., 2006), Amazonia remains their last stronghold. Harpy Eagles have been described as sloth (Pilosa order) specialists in Amazonia (Aguiar-Silva, Sanaiotti, & Luz, 2014; Miranda, 2015), preying extensively on them wherever they occur together. Sloths are the most abundant vertebrates in Neotropical forests (Taube, Vie, Fournier, Genty, & Duplantier, 1999). Nonetheless, Harpy Eagles also rely upon other prey, such as large-sized monkeys (Barnett, Schiel, & Deveny, 2011), large birds, and some terrestrial animals (Alvarez-Cordero, 1996). There is currently no catalog of Harpy Eagles’ prey species diversity in the scientific literature.

Figure 1.

Harpy Eagle eating a Howler monkey in Suriname (Photo credit: Rienus Van Der Wal, Kabalebo Nature Resort).

The most common method used to characterize Harpy Eagle prey composition is to search their nests for prey remains. However, finding Harpy Eagle nests is a challenging task. Densities as low as 3 to 6 nests per 100 km² (Vargas-González & Vargas, 2011) make the ornithological community celebrate every nest discovery (Pereira & Salzo, 2006; Rotenberg, Marlin, Pop, & Garcia, 2012; Ubaid, Ferreira, de Oliveira, & Antas, 2011). Half a century of research on the species has identified over 50 nests that allowed the collection of more than one thousand individual prey remains (Miranda, Campbell-Thompson, Muela, & Vargas, 2017). Nevertheless, these discoveries were made by indigenous people, poachers, loggers, and other people involved in a diverse range of land uses. Those nests are therefore mostly located in modified landscapes. Hence, prey composition of Harpy Eagles in primary forests is still poorly known.

Here, I report the prey composition of a pair of Harpy Eagles in a primary forest site, the Central Suriname Reserve, and collate a complete prey species list for this key raptor. With this, I plan to advance the knowledge of Harpy Eagle prey composition in primary forests and to provide contemporary researchers with a single, accessible reference to all known reports of species used as prey by Harpy Eagles.

Methods

Study Site

Raleighvallen (4°39′30.6″N 56°10′43.4″W) is part of the larger Central Suriname Nature Reserve, which consists of 1.6 million ha of primary and tropical forest that has not been hunted for several decades. The site is limited on the northwestern part by the eastern bank of the Coppename River and has a mean altitude of 30 m. Rainfall averaged 1967 mm between 2000 and 2005. Rainfall shows multimodal seasonality, with a brief rainy season in December to January, a brief dry season in February to March, a long wet season in April to July, and a long dry season in August to November. Minimum and maximum temperatures, noted daily, averaged 23.7°C and 28.9°C, respectively, during the study period (Vath, 2008).

Data Collection and Identification

Workers of the Monkey-Forest Project discovered a Harpy Eagle nest in 2002. A field crew visited the site once a week to monitor activity and to retrieve bones and other prey body parts beneath the nest. This continued up to a second nesting cycle in 2004. Bones and other materials were identified by comparison with reference collections: Southern Illinois University for primates and other mammals, and Florida Museum of Natural History for birds and reptiles.

Literature Review

I conducted an extensive literature search concerning interactions between Harpy Eagles and their prey using Google Scholar, Web of Science, Scopus, and Scielo search engines. I also consulted other researchers for unpublished studies and literature unrevealed by online searches. In my search, I used the following keywords: Harpy Eagle, Harpia harpyja, harpia, águila arpía, and águila harpía combined with diet, feeding habits, food habits, habitos alimentarios, and dieta. This allowed me to find published and unpublished data in English, Portuguese, and Spanish.

Biomass Calculation

As differently sized prey offer different energetic contributions to predators, I added a biomass calculation to prey composition. All prey individuals were considered average sized adults, and whereas it is known that Harpy Eagles prey over juveniles of many species (Aguiar-Silva et al., 2014), the proportions of adults and juveniles were not known in data presented here. An exception was made for ungulates, which are known to be preyed exclusively when young and were therefore considered to weight one fifth of total adult body mass. As undigested leaves inside sloths average one third of their body mass (Goffart, 1971), this reduction was applied on their biomass score. Biomass proportion of tortoises was reduced to two thirds, given that this is the proportion of edible tissue (Emmons, 1989). A complete list of bibliographical records used to obtain prey average body mass and their respective sample sizes is given in Table 1.

Table 1.

Body Mass, Sample Sizes, and Sources Used in the Consumed Biomass Calculation.

Species	Mass (kg)	Sample size (N)	Source
Tayassu tajacu	18.40	9	Richard-Hansen, Vié, Vidal, and Kéravec, 1999
Ateles paniscus	9.02	8	Parry, Barlow, and Peres, 2009
Choloepus didactylus	6.07	21	Wetzel and Montgomery, 1985
Chelonoidis denticulatus	5.90	50	Moskovits, 1985
Alouatta macconnelli	5.35	7	Ford and Davis, 1992
Boa constrictor	5.08	106	Bertona and Chiaraviglio, 2003
Tamandua tetradactyla	4.80	43	Richard-Hansen et al., 1999
Dasypus novemcinctus	4.60	19	McDonough, 2000
Dasyprocta leporina	4.37	62	Richard-Hansen et al., 1999
Bradypus tridactylus	4.01	7	Wetzel and Montgomery, 1985
Coendou prehensilis	3.60	70	Richard-Hansen et al., 1999
Cabassous unicinctus	3.44	2	Richard-Hansen et al., 1999
Crax alector	2.87	10	Dunning, 1992
Chiropotes chiropotes	2.85	33	Ford and Davis, 1992
Sapajus apella	2.71	203	Peres, 1997
Cebus olivaceus	2.60	3	Koster, 2008
Leopardus wiedii	2.40	9	Carvajal-Villarreal et al., 2012
Iguana iguana	2.29	54	Koster, 2008
Pithecia pithecia	2.10	9	Ford and Davis, 1992
Potos flavus	1.76	12	Richard-Hansen et al., 1999
Penelope sp.^a	1.32	–	Dunning., 1992
Tupinambis teguixin	1.09	110	Herrera and Robinson, 2000
Didelphis marsupialis	1.08	131	Richard-Hansen et al., 1999
Psophia crepitans	1.03	14	Dunning, 1992
Saimiri sciureus	0.87	20	Ford and Davis, 1992
Didelphis imperfecta	0.76	18	Catzeflis, Richard-Hansen, and Fournier-Chambrillon 1997
Saguinus midas	0.54	40	Ross, 1991
Aratinga sp.^a	0.10	–	Dunning, 1992

Note. ^aAveraged body masses of the species in the genus occurring at the study site.

Results

Remains collected under the Harpy Eagle nest at the Raleighvallen primary forest revealed 220 individual prey records, of a minimum of 26 species. Prey remains were mainly composed of sloths, which represented 39.1% of prey frequency and 43.6% of biomass consumed. From these, 19.5% were two-toed sloths, 10.45% unknown sloths, and 9.1% tree-toed sloths. Primates were the following most important prey, representing 34.5% of prey frequency and 40.4% of biomass consumed. The remaining prey were primarily medium-sized mammals, followed by large-sized birds and finally large reptiles (Table 2). The literature review revealed a total of 93 prey species, totalizing a prey list of 102 species given the 9 new prey records presented here (Table 3).

Table 2.

Prey Composition of Harpy Eagles in Raleighvallen, Suriname.

Prey species	Body mass (kg)	Frequency % (N)	Biomass %
Two-toed sloth Choloepus didactylus	6.07	19.54 (43)	24.90
Red howler monkey Alouatta macconnelli	5.35	12.27 (27)	20.88
Unidentified sloths^a	5.04	10.45 (23)	11.06
Pale-throated sloth Bradypus tridactylus	4.01	9.09 (20)	7.65
White-faced saki Pithecia pithecia	2.10	9.09 (20)	6.07
Red-backed saki Chiropotes chiropotes	2.85	4.54 (10)	4.12
Red-faced spider monkey Ateles paniscus	9.02	1.36 (3)	3.91
Green iguana Iguana iguana	2.29	5 (11)	3.64
Tufted capuchin Sapajus apella	2.71	2.72 (6)	2.35
Kinkajou Potos flavus	1.76	4.09 (9)	2.29
Wedge-capped capuchin Cebus olivaceus	2.60	2.72 (6)	2.25
Nine-banded armadillo Dasypus novemcinctus	4.6	0.90 (2)	1.33
Red-humped agouti Dasyprocta leporina	4.37	0.90 (2)	1.26
Yellow-footed tortoise Chelonoidis denticulatus	5.90	0.90 (2)	1.13
Lowland paca Cuniculus paca	6.25	0.45 (1)	0.90
Black curassow Crax alector	2.87	0.90 (2)	0.83
Red-tailed boa Boa constrictor	5.075	0.45 (1)	0.73
Lesser anteater Tamandua tetradactyla	4.80	0.45 (1)	0.69
Grey-winged trumpeter Psophia crepitans	1.49	1.36 (3)	0.65
Collared peccary Tayassu tajacu	3.68	0.45 (1)	0.53
Brazilian porcupine Coendou prehensilis	3.60	0.45 (1)	0.52
Naked-tailed armadillo Cabassous unicinctus	3.44	0.45 (1)	0.50
Squirrel monkey Saimiri sciureus	0.87	1.36 (3)	0.38
Unidentified small cat Leopardus sp.^b	2.40	0.45 (1)	0.35
Guianan opossum Didelphis imperfecta	0.76	1.36 (3)	0.33
Gold tegu Tupinambis teguixin	1.09	0.90 (2)	0.32
Unidentified guan Penelope sp.^c	1.317	0.45 (1)	0.19
Common opossum Didelphis marsupialis	1.08	0.45 (1)	0.15
Red-handed tamarin Saguinus midas	0.54	0.45 (1)	0.08
Unidentified conure Aratinga sp.^c	0.10	0.45 (1)	0.01
Unidentified primates	–	2.72 (6)	-
Unidentified birds	–	1.81 (4)	-
Unidentified fish	–	0.45 (1)	-
Unidentified crab	–	0.45 (1)	-
Total		(220)

Note. ^aMean mass of the two other sloth species.

^bBody mass of Leopardus wiedii, smallest cat in the study site.

^cAveraged body masses of all species in the genus occurring in the study site.

Table 3.

Harpy Eagle Prey Species Recorded in the Literature and the Number of Predation Records (n).

Order	Species	n
Mammals
Pilosa	Bradypus trydactylus	74
Pilosa	Bradypus variegatus	256
Pilosa	Choloepus didactylus	366
Pilosa	Choloepus hoffmanni	80
Pilosa	Tamandua mexicana	12
Pilosa	Tamandua tetradactyla	18
Primates	Alouatta arctoidea	1
Primates	Alouatta belzebul	10
Primates	Alouatta macconnelli	16
Primates	Alouatta palliata	25
Primates	Alouatta pigra	3
Primates	Alouatta seniculus	62
Primates	Aotus azarae	1
Primates	Ateles geoffroyi	1
Primates	Ateles paniscus	4
Primates	Cacajao ouakary	1
Primates	Callicebus brunneus	1
Primates	Callicebus discolor	7
Primates	Callicebus hoffmannsi	10
Primates	Callicebus lucifer	3
Primates	Callicebus moloch	1
Primates	Cebus albifrons	9
Primates	Cebus capucinus	7
Primates	Cebus olivaceus	66
Primates	Cebus yuracus	7
Primates	Chiropotes albinasus	3
Primates	Chiropotes chiropotes	1
Primates	Chiropotes satanas	16
Primates	Chiropotes utahicki	1
Primates	Lagotrix lagotricha	13
Primates	Pithecia aequatorialis	1
Primates	Pithecia irrorata	1
Primates	Pithecia milleri	1
Primates	Pithecia monachus	3
Primates	Pithecia pithecia	34
Primates	Saguinus graellsi	5
Primates	Saguinus midas	1
Primates	Saguinus nigricollis	4
Primates	Saimiri macrodon	17
Primates	Saimiri sciureus	14
Primates	Sapajus apella	32
Primates	Sapajus cay	1
Primates	Sapajus robustus	2
Primates	Sapajus xanthosternos	1
Primates	Sapajus nigritus	1
Carnivora	Bassaracyon alleni	6
Carnivora	Cerdocyon thous	1
Carnivora	Eira barbara	4
Carnivora	Leopardus pardalis	1
Carnivora	Leopardus wiedii	1
Carnivora	Nasua narica	20
Carnivora	Nasua nasua	17
Carnivora	Potos flavus	56
Carnivora	Procyon cancrivorus	1
Cingulata	Cabassous centralis	1
Cingulata	Cabassous unicinctus	2
Cingulata	Dasypus novemcinctus	9
Rodentia	Agouti paca	1
Rodentia	Coendou bicolor	20
Rodentia	Coendou koopmani	5
Rodentia	Coendou mexicanus	1
Rodentia	Coendou prehensilis	45
Rodentia	Coendou spinosus	1
Rodentia	Dasyprocta fuliginosa	6
Rodentia	Dasyprocta leporina	14
Rodentia	Dasyprocta punctata	2
Rodentia	Sphiggurus melanurus	1
Rodentia	Sphiggurus insidiosus	1
Didelphimorphia	Didelphis albiventris	4
Didelphimorphia	Didelphis marsupialis	27
Didelphimorphia	Didelphis imperfecta	1
Didelphimorphia	Philander opossum	1
Artiodactyla	Mazama americana	2
Artiodactyla	Mazama guazoubira	1
Artiodactyla	Mazama temama	2
Artiodactyla	Tayassu tajacu	6
Birds
Psittaciformes	Amazona farinosa	1
Psittaciformes	Amazona spp.	3
Psittaciformes	Anodorhyncus hyacinticus	1
Psittaciformes	Ara ararauna	2
Psittaciformes	Ara chloropterus	1
Psittaciformes	Aratinga sp.	1
Galliformes	Aburria cumanensis	1
Galliformes	Crax alector	3
Galliformes	Crax fasciolata	1
Galliformes	Crax rubra	3
Galliformes	Penelope sp.	1
Galliformes	Pipile pipile	3
Passeriformes	Cacicus haemorrhous	4
Gruiformes	Psophia crepitans	1
Gruiformes	Psophia leucoptera	3
Piciformes	Ramphastos culminatus	1
Piciformes	Ramphastos tucanus	1
Suliformes	Anhinga anhinga	1
Opisthocomiformes	Opisthocomus hoazin	2
Cariamiformes	Cariama cristata	1
Reptiles
Squamata	Amphisbaena alba	1
Squamata	Boa constrictor	1
Testudines	Chelonoidis denticulatus	2
Squamata	Iguana iguana	29
Squamata	Tupinambis merianae	1
Squamata	Tupinambis teguixin	2

Note. Given the very large number of references, a complete version of the table with all literature can be found in Supplementary Material Table 1.

Discussion

The feeding habits of Harpy Eagles in the Raleighvallen primary forest are characterized by a high diversity of prey species—chiefly sloths and primates. Sloths are the most abundant folivore in the canopy of Neotropical forests. Primates, on the other hand, have an important role as prey in the primary forest of the study site because of their high energetic contribution to Harpy Eagle diet. The extensive trophic links between this apex predator and its highly diverse prey have tempting implications for the functioning of tropical ecosystems.

Sloths may appear ideal prey for a giant raptor, given their body size and slow-moving habits associated with heterothermy and low metabolism. A close examination of sloth biology suggests otherwise: (a) Sloths feed mainly on leaves, which average one third of their body mass (Goffart, 1971), reducing edible tissue availability for carnivores; (b) sloths have half the muscular mass (i.e., meat) of a mammal of comparable size (Britton & Atkinson, 1938), further constraining energetic availability to predators. (c) Contrary to popular perception, sloths are formidable prey (Touchton, 2010), ready to swing claws against predators, and two-toed sloths are vicious biters. Consequently, sloths are less cost effective when compared with primates but otherwise easier to catch (55% vs. 17% success rate by Harpy Eagles; Touchton et al., 2002). Higher predation rates over sloths is a possible result of more sophisticated methods of predation avoidance by primates (Barnett et al., 2017; Mourthé & Barnett, 2014). In addition, sloths are more abundant, they outnumber even the most abundant primate species (the folivore-frugivore howler monkey, Aloutatta spp.) from a two-to-one (Alho, 2011) up to a seven-to-one ratio (Sergio et al., 2014). Sloths are therefore abundant but of low energetic cost effectiveness.

Harpy Eagle prey diversity encompasses 102 known prey species, a number that will rise steadily in the forthcoming years given the poorly explored species’ autecology in tropical forests. Data reviewed here show that they prey over many of the largest species on Neotropical canopies, as Hyacinth macaws, Great curassows, Spider monkeys, and Green iguanas, as well as over smaller passerines and parakeets. Comparatively, the widespread and best studied predator of the Neotropics, the jaguar (Panthera onca), preys on 84 vertebrate species (Nowell & Jackson, 1996). The publication of detailed prey inventories and diet composition are important initial steps in conservation and management.

I emphasize that primary forest nests of Harpy Eagles—as the one described here—are mostly absent from the literature, given the idiosyncrasies that constrain nest finding. In summary, I have shown that Harpy Eagle prey composition in the Raleighvallen primary forest is mainly formed by sloths and primates. At Raleighvallen, Harpy Eagle diet includes a comparatively high amount of game species such as terrestrial mammals, large primates, and game birds, some recorded here for the first time. While the connection of human overhunting to the dietary traits described here cannot be straightly established, the multiple research groups that are working with dozens of Harpy Eagle nests may have an opportunity to advance on this question.

Implications for Conservation

Large primates, game birds, and terrestrial mammals such as armadillos and pacas are among the most persecuted prey by poachers in Amazonia, having disappeared from vast forest tracts (Jerozolimski & Peres, 2003; Peres & Palacios, 2007) but are abundant in Central Suriname Reserve (Vath, 2008). Five of the nine new prey records presented here are from widespread vertebrates that are game species, such as the lowland paca, the grey-winged trumpeter, and the yellow-footed tortoise. Despite limited direct evidence, poaching seems a remarkable phenomenon which led to the greater role of game prey species on the diet of Harpy Eagles in Raleighvallen when compared with other study sites. The same applies for the higher amounts of large primates on eagle diet. If my hypothesis survives further research, future efforts may address if trophic restructuring in secondary landscapes is in fact related with forest vertebrate elimination through hunting.

Supplemental Material

Supplemental material for Prey Composition of Harpy Eagles (Harpia harpyja) in Raleighvallen, Suriname

Supplemental material for Prey Composition of Harpy Eagles (Harpia harpyja) in Raleighvallen, Suriname by Everton B. P. Miranda in Tropical Conservation Science

Supplemental Material

Supplemental material1 - Supplemental material for Prey Composition of Harpy Eagles (Harpia harpyja) in Raleighvallen, Suriname

Supplemental material, Supplemental material1 for Prey Composition of Harpy Eagles (Harpia harpyja) in Raleighvallen, Suriname by Everton B. P. Miranda in Tropical Conservation Science

Supplemental Material

Supplementary Information Table 1 - Supplemental material for Prey Composition of Harpy Eagles (Harpia harpyja) in Raleighvallen, Suriname

Supplemental material, Supplementary Information Table 1 for Prey Composition of Harpy Eagles (Harpia harpyja) in Raleighvallen, Suriname by Everton B. P. Miranda in Tropical Conservation Science

Footnotes

Acknowledgments

I wish to express my sincere gratitude to Dr. Sue Boinski, whose sheer generosity allowed the publication of this data. Logistical support was given by the Peugeot-ONF Carbon Sink Reforestation Project, based at the São Nicolau Farm in Cotriguaçu, 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. Luísa Genes and Bruno Moraes provided thoughtful discussions that improved an earlier version of this manuscript. Bernardo Araujo performed the English polishing improving an earlier version of this manuscript. Finally, I would like to thank the many participants of Monkey-Forest Project for their crucial field effort.

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: I greatly appreciate the generous financial support of the following donors: Rufford Small Grants Foundation (18743-1 and 23022-2), Rainforest Biodiversity Group, Idea Wild, The Mamont Scholars Program of the Explorer’s Club Exploration Fund, Cleveland Metroparks Zoo, and the SouthWild.com Conservation Travel System.

Supplemental Material

Supplemental material for this article is available online.

References

Aguiar-Silva

F. H.

Sanaiotti

T. M.

Luz

(2014). Food habits of the Harpy Eagle, a top predator from the Amazonian rainforest canopy. Journal of Raptor Research, 48(1), 24–45. doi:10.3356/JRR-13-00017.1

Alho

(2011). Environmental effects of hydropower reservoirs on wild mammals and freshwater turtles in Amazonia: A review. Oecologia Australis, 15(3), 593–604. doi:10.4257/oeco.2011.1503.11

Alvarez-Cordero

(1996). Biology and conservation of the harpy eagle in Venezuela and Panama (doctoral thesis). University of Florida, FL, USA.

Barber-Meyer

S. M.

Jnawali

S. R.

Karki

J. B.

Khanal

Lohani

Long

Wikramanayake

(2013). Influence of prey depletion and human disturbance on tiger occupancy in Nepal. Journal of Zoology, 289(1), 10–18. doi:10.1111/j.1469-7998.2012.00956.x

Barnett

A. A.

Schiel

Deveny

(2011). Predation on Cacajao ouakary and Cebus albifrons (Primates: Platyrrhini) by harpy eagles. Mammalia, 75(2), 169–172.

Barnett

A. A.

Silla

J. M.

de Oliveira

Boyle

S. A.

Bezerra

B. M.

Spironello

W. R.

Pinto

L. P.

(2017). Run, hide, or fight: Anti-predation strategies in endangered red-nosed cuxiú (Chiropotes albinasus, Pitheciidae) in southeastern Amazonia. Primates, 58(2), 353–360. doi:10.1007/s10329-017-0596-9

Bertona

Chiaraviglio

(2003). Reproductive biology, mating aggregations, and sexual dimorphism of the argentine boa constrictor (Boa constrictor occidentalis). Journal of Herpetology, 37(3), 510–516. doi:10.1670/122-02A

Britton

S. W.

Atkinson

W. E.

(1938). Poikilothermism in the Sloth. Journal of Mammalogy, 19(1), 94. doi:10.2307/1374287

Carvajal-Villarreal

Caso

Downey

Moreno

Tewes

M. E.

Grassman

L. I.

(2012). Spatial patterns of the margay (Leopardus wiedii; Felidae, Carnivora) at “El Cielo” Biosphere Reserve, Tamaulipas, Mexico. Mammalia, 76, 237–244. doi:10.1515/mammalia-2011-0100

10.

Catzeflis

Richard-Hansen

Fournier-Chambrillon

(1997). Biométrie, reproduction et sympatrie chez Didelphis marsupialis et D. albiventris en Guyane française (Biometry, reproduction and sympatry at Didelphis marsupialis and D. albiventris in French Guiana.) (Didelphidae: Marsupialia). Mammalia, 61, 231–244.

11.

Dunning

J. B.

Jr. (1992). CRC handbook of avian body masses. Boca Ratón, FL: CRC Press.

12.

Emmons

(1989). Jaguar predation on chelonians. Journal of Herpetology, 23(3), 311–314. doi:10.2307/1564460

13.

Ford

S. M.

Davis

L. C.

(1992). Systematics and body size: Implications for feeding adaptations in New World monkeys. American Journal of Physical Anthropology, 88, 415–468. doi:10.1002/ajpa.1330880403

14.

Fowler

Cope

(1964). Notes on the Harpy Eagle in British Guiana. Auk, 81(3), 257–273. doi:10.2307/4082683

15.

Galetti

de Carvalho

Jr. (2000). Sloths in the diet of a harpy eagle nestling in Eastern Amazon. The Wilson Bulletin, 112(4), 535–536.

16.

Goffart

(1971). Function and form in the sloth. New York, NY: Pergamon Press.

17.

Hayward

M. W.

Kerley

G. I. H.

(2005). Prey preferences of the lion (Panthera leo). Journal of Zoology, 267(3), 309–322. doi:10.1017/S0952836905007508

18.

Herrera

E. A.

Robinson

M. D.

(2000). Reproductive and fat body cycles of the tegu lizard, Tupinambis teguixin, in the Llanos of Venezuela. Journal of Herpetology, 34(4), 598–601. doi:10.2307/1565277

19.

Jerozolimski

Peres

C. A.

(2003). Bringing home the biggest bacon: A cross-site analysis of the structure of hunter-kill profiles in Neotropical forests. Biological Conservation, 111(3), 415–425. doi:10.1016/S0006-3207(02)00310-5

20.

Koster

(2008). The impact of hunting with dogs on wildlife harvests in the Bosawas Reserve, Nicaragua. Environmental Conservation, 35(3), 211–220. doi:10.1017/S0376892908005055

21.

Lamichhane

B. R.

Pokheral

C. P.

Poudel

Adhikari

Giri

S. R.

Bhattarai

Subedi

(2018). Rapid recovery of tigers Panthera tigris in Parsa Wildlife Reserve, Nepal. Oryx, 52(1), 16–24. doi:10.1017/S0030605317000886

22.

McDonough

(2000). Social organization of nine-banded armadillos (Dasypus novemcinctus) in a riparian habitat. The American Midland Naturalist, 144(1), 139–151. doi:10.1674/0003-0031(2000)144[0139:SOONBA]2.0.CO;2

23.

Miranda

E. B. P.

(2015). Conservation implications of harpy eagle Harpia harpyja predation patterns. Endangered Species Research, 29(1), 69–79. doi:10.3354/esr00700

24.

Miranda

E. B. P.

Campbell-Thompson

Muela

Vargas

F. H.

(2017). Sex and breeding status affect prey composition of Harpy Eagles Harpia harpyja. Journal of Ornithology, 159, 141–150.

25.

Moskovits

D. K.

(1985). The behavior and ecology of the two Amazonian tortoises, Geochelone carbonaria and Geochelone denticulata, in northwestern Brasil (doctoral thesis). University of Chicago, IL.

26.

Mourthé

Í.

Barnett

A. A.

(2014). Crying tapir: The functionality of errors and accuracy in predator recognition in two Neotropical high-canopy primates. Folia Primatologica, 85(6), 379–398. doi:10.1159/000371634

27.

Muñiz-López

(2008). Revisión de la situación del Águila Harpía Harpia harpyja en Ecuador. Cotinga, 29, 42–47.

28.

Muñiz López

(2016). Biología y conservación del Águila Harpía (Harpia harpyja) en Ecuador. Universidad de Alicante, Spain.

29.

Muñiz-López

(2017). Harpy Eagle (Harpia harpyja) mortality in Ecuador. Studies on Neotropical Fauna and Environment, 30(1), 1–5. doi:10.1080/01650521.2016.1276716

30.

Newsome

T. M.

Greenville

A. C.

Ćirović

Dickman

C. R.

Johnson

C. N.

Krofel

Wirsing

A. J.

(2017). Top predators constrain mesopredator distributions. Nature Communications, 8, 15469. doi:10.1038/ncomms15469

31.

Nowell

Jackson

(1996). “Panthera Onca”. Wild Cats. Status survey and conservation action plan. Gland, Switzerland: IUCN/SSC Cat Specialist Group.

32.

Orihuela

Terborgh

Ceballos

Glander

(2014). When top-down becomes bottom up: Behaviour of hyperdense howler monkeys (Alouatta seniculus) trapped on a 0.6 Ha island. PloS One, 9(4), e82197. doi:10.1371/journal.pone.0082197

33.

Parry

Barlow

Peres

C. A.

(2009). Allocation of hunting effort by Amazonian smallholders: Implications for conserving wildlife in mixed-use landscapes. Biological Conservation, 142(8), 1777–1786. doi:10.1016/j.biocon.2009.03.018

34.

Pereira

A. D. M. M.

Salzo

(2006). Primeiro registro da nidificação de Harpia harpyja (Falconiformes, Accipitridae) na Serra da Bodoquena, First record of the nesting of Harpia harpyja (Falconiformes, Accipitridae) in Bodoquena Ridge (Mato Grosso do Sul, Brasil). Revista Brasileira de Ornitologia, 14(2), 157–160.

35.

Peres

C. A.

(1997). Effects of habitat quality and hunting pressure on arboreal folivore densities in Neotropical forests: A case study of howler monkeys (Alouatta spp.). Folia Primatologica, 68(3), 199–222. doi:10.1159/000157247

36.

Peres

C. A.

Palacios

(2007). Basin-wide effects of game harvest on vertebrate population densities in Amazonian forests: Implications for animal-mediated seed dispersal. Biotropica, 39(3), 304–315. doi:10.1111/j.1744-7429.2007.00272.x

37.

Piana

(2007). Anidamiento y dieta de Harpia harpyja Linnaeus en la Comunidad Nativa de Infierno, Madre de Dios, Perú. Revista Peruana de Biología, 14(1), 135–138. doi:10.15381/rpb.v14i1.2178

38.

Rettig

(1978). Breeding behavior of the harpy eagle (Harpia harpyja). The Auk, 95(4), 629–643.

39.

Richard-Hansen

Vié

J. C.

Vidal

Kéravec

(1999). Body measurements on 40 species of mammals from French Guiana. Journal of Zoology, 247(4), 419–428. doi:10.1017/S095283699900401X

40.

Ross

(1991). Life history patterns of New World monkeys. International Journal of Primatology, 12(5), 481–502. doi:10.1007/BF02547635

41.

Rotenberg

Marlin

Pop

Garcia

(2012). First record of a Harpy Eagle (Harpia harpyja) nest in Belize. The Wilson Journal of Ornithology, 124(2), 292–297. doi:10.1676/11-156.1

42.

Schweiger

Fünfstück

H.-J.

Beierkuhnlein

(2015). Availability of optimal-sized prey affects global distribution patterns of the golden eagle Aquila chrysaetos. Journal of Avian Biology, 46(1), 81–88. doi:10.1111/jav.00396

43.

Sérgio

Newton

Marchiesi

Pedrini

(2006). Ecologically justified charisma: Preservation of top predators delivers biodiversity conservation. Journal of Applied Ecology, 43(6), 1049–1055. doi:10.1111/j.1365-2664.2006.01218.x

44.

Sergio

Schmitz

O. J.

Krebs

C. J.

Holt

R. D.

Heithaus

M. R.

Wirsing

A. J.

Korpimäki

(2014). Towards a cohesive, holistic view of top predation: A definition, synthesis and perspective. Oikos, 123(10), 1234–1234. doi:10.1111/oik.01468

45.

Taube

Vie

J.-C.

Fournier

Genty

Duplantier

J.-M.

(1999). Distribution of two sympatric species of sloths (Choloepus didactylus and Bradypus tridactylus) along the Sinnamary River, French Guiana1. Biotropica, 31(4), 686–691. doi:10.1111/j.1744-7429.1999.tb00418.x

46.

Terborgh

Lopez

Nunez

Rao

Shahabuddin

Orihuela

Balbas

(2001). Ecological meltdown in predator-free forest fragments. Science, 294(5548), 1923–1926. doi:10.1126/science.1064397

47.

Touchton

(2010). The Harpy Eagle. In Tingay

Katzner

(Eds.), The eagle watchers: Observing and conserving raptors around the world (1st ed., p. 264). Ithaca, NY: Cornell University Press.

48.

Touchton

Hsu

Palleroni

(2002). Foraging ecology of reintroduced captive-bred subadult harpy eagles (Harpia harpyja) on Barro Colorado Island, Panama. Ornitología Neotropical, 13(4), 365–379.

49.

Ubaid

F. K.

Ferreira

L. P.

de Oliveira

S. B.

Antas

P. D. T. Z.

(2011). Primeiro registro de Harpia harpyja para o bioma Pantanal, com dados sobre atividade reprodutiva. (First Harpy harpyja record for the Pantanal biome, with breeding activity data), Revista Brasileira de Ornitologia, 19, 88–92.

50.

Uulu

Wegge

Mishra

Sharma

(2014). Large carnivores and low diversity of optimal prey: A comparison of the diets of snow leopards Panthera uncia and wolves Canis lupus in Sarychat-Ertash Reserve in Kyrgyzstan. Oryx, 48(4), 529–535. doi:10.1017/S0030605313000306

51.

Vargas-González

J. de. J.

Vargas

F. H.

(2011). Nesting density of Harpy Eagles in Darien with population size estimates for Panama. Journal of Raptor Research, 43(3), 199–210. doi:10.3356/JRR-10-57.1

52.

Vargas-González

J. de. J.

Whitacre

Mosquera

Albuquerque

Piana

Thiollay

J.-M.

Sanaiotti

T. M.

(2006). Estado y distribucion actual del aguila arpia (Harpia harpyja) en Centro y Sur America. (Status and current distribution of the harpy eagle (Harpia harpyja) in Central and South America), Ornitologia Neotropical, 17, 39–55.

53.

Vath

C. L.

(2008). Species richness and habitat preference of large vertebrates in the Central Suriname Nature Reserve. Gainesville, FL: University of Florida.

54.

Wetzel

Montgomery

(1985). The evolution and ecology of armadillos, sloths and vermilinguas. Washington, DC: Smithsonian Institution.

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