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

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.

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.

Table 3.

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

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

Supplemental Material