Apex predators room threatened globally, and their regional extinctions are often driven by failures in sustaining food acquisition under contexts of significant prey scarcity. The harpy eagle Harpia harpyja is Earth’s largest eagle and the apex aerial predator of Amazonian forests, however no ahead study has actually examined the affect of woodland loss on their feeding ecology. Us monitored 16 active harpy eagle nests embedded in ~ landscapes that had actually experienced 0 to 85% of woodland loss, and also identified 306 recorded prey items. Harpy eagles might not move to open-habitat prey in deforested habitats, and also retained a diet based on canopy vertebrates also in deforested landscapes. Feeding rates diminished with forest loss, with three fledged individuals dying of scarcity in landscapes that succumbed to 50–70% deforestation. Because landscapes deforested by > 70% supported no nests, and also eaglets can not be provisioned to freedom within landscapes > 50% woodland loss, we established a 50% woodland cover threshold for the reproductive viability the harpy eagle pairs. Our scaling-up estimate shows that 35% that the entire 428,800-km2 Amazonian ‘Arc that Deforestation’ study an ar cannot support reproduction harpy eagle populations. Our results imply that restoring harpy eagle population viability within extremely fragmented forest landscapes critically counts on decisive forest conservation action.
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Securing an adequate food it is provided is a biological imperative the drives fundamental elements that a species biology, including mating1, danger assessment2, survivorship3 and also geographic selection boundaries4. Consequently, feeding ecology studies have become central to populace ecology3, and also have presented how consumer density is linked to food abundance5 and why some types can persist in human-dominated landscapes6,7,8, while rather cannot9,10,11. Apex predators are specifically sensitive to changes in the spectrum and availability of food because of their high metabolic requirements12. They count on stable and also secure prey populations to fuel their relatively high day-to-day survival and also breeding requirements13.
Anthropogenic habitat degradation and prey scarcity induced by poaching forces predators to adapt to feeding on alternative prey species to accomplish their straightforward metabolic needs. There room several instances of food switching as a consequence, including jaguars (Panthera onca) the feed mostly on armadillos (Cingulata) in semi-defaunated habitats14, and gold eagles (Aquila chrysaetus) the feed generally on mesopredators in ~ sites doing not have their normal lagomorph prey15. Some herbal predators may switch to residential livestock8,16,17,18, yet once exacerbated through habitat loss, these human-wildlife conflicts often drive the landscape-scale extirpation the apex predators9,10. Predators may change to these changes and also thrive in anthropogenic landscapes conquered by an agricultural matrix as an ideal prey continues to be abundant, and humans show tolerance19,20,21. Consequently, the threshold that minimum food availability—which deserve to be offered to guess the population viability and persistence of apex predators and also their coexistence through humans—has been extensively investigated in degraded landscapes22,23,24.
The harpy eagle (Harpia harpyja; Fig. 1) is an apex predator the feeds mostly on forest canopy vertebrates25,26. As among the Earth’s largest eagles (males and females averaging 5.9 and 7.3 kg, respectively), they have stringent ecological requirements27 the include ~ 800 g the food per day for adults28 and also emergent swarm trees taller 보다 40–45 m29. Harpy eagles have actually a 30–36-month-long reproduction cycle, lay two eggs however fledge only a solitary eaglet30,31,32,33. Harpy eagles space typically an extremely long-lived; a 54 years-old wild-caught adult individual was still alive through the publishing of the latest studbook34. They usually display strict nest site fidelity, breeding in the same certain T-shaped emergent nest tree for several consecutive decades35,Harpia harpyja). Auk 95, 629–643 (1978)." href="/articles/s41598-021-92372-z#ref-CR36" id="ref-link-section-d120897831e932">36. These trees are commonly of commercial attention to the logging industry29,37. Studies of their reproduction biology room still considered a high study priority33. Their an international distribution has actually contracted by 41% due to the fact that the nineteenth century, and currently, 93% of your distribution selection is in ~ Amazonian Forests, your last stronghold10. Leading reasons explaining your rapid decrease are habitat loss10, and also shooting by inhabitants and, come a lesser extent, reprisal because that killing livestock38,39.
Harpy eagle (Harpia harpyja) getting here at a nest with a brown capuchin monkey (photo: Jiang Chunsheng).
Harpy eagles exert solid top-down manage on their food populations28,40. The literary works widely explains sloths together the key prey taxon, complied with by mid-sized primates26. Huge reptiles (notably eco-friendly iguanas, Iguana iguana) and large birds (such as guans and also curassows; Cracidae) room less important prey varieties for harpy eagles26. Terrestrial ungulates such as brocket-deer (Mazama spp.) and also peccaries (Tayassuidae) are even less constant in your diet25. Studying just how landscape degradation affects the feeding ecology of harpy eagles can shed light on just how they readjust their diet v habitat loss. While dietary profiles are the main element studied in harpy eagle ecology, v over 1000 food records obtainable in the literature25, over there is no details on the effects of landscape-scale main habitat switch on the feeding ecology that harpy eagles. Yet ecological limitations such as habitat loss and also prey scarcity are an essential to knowledge their extirpation thresholds in human-modified landscapes.
To recognize the results of forest loss on harpy eagle feeding ecology, our intends here to be fourfold. Firstly, us examined the effects of harpy eagle sexual dimorphism on their feeding ecology. We predicted the larger-bodied females would prey on larger-bodied and also less varied prey species than smaller sized males. Secondly, we tested the effects of landscape destruction on predation rates of non-forest and also disturbance-tolerant prey species. Us predicted the pairs nesting in extremely deforested sites would prey on these species, and sustain a more diverse diet. Thirdly, us investigated the effects of landscape degradation on numerical and biomass rates of prey delivery to eaglets. We predicted that eaglets would challenge lower prey distribution rates at much longer intervals in degraded landscapes, resulting in lower food biomass acquisition. Lastly, we scaled increase our approximates of the deforestation yongin threshold the harpy eagles and associated prey scarcity to a much bigger human-modified an ar of the Amazon.
By exploring the above, us were able to estimate the after-effects of comprehensive tropical deforestation on the persistence of breeding pairs that harpy eagles. Finding and capturing sufficient prey is the crucial issue because that the persistence of together an apex predator. Therefore, their population viability in human-modified landscapes depends on their yongin threshold to food stress, i m sorry is presently unknown.
We recognised a complete of 306 food items from harpy eagle nests, 253 the which from camera-traps and also 53 native bone material. From a total of 279 food deliveries tape-recorded by camera-traps, 253 (89.7%) were figured out to the level of varieties or genus throughout 16 different harpy eagle nests. Us complemented camera-trapping data with evaluation of bones detritus built up both within and also underneath nests. We found bones that 76 different individual prey, of which 53 (69.7%) could be identified. We videotaped 92 and 75 prey deliveries to colonies by female and also male eagles, respectively (♀♀ 34.5 vs. ♂♂ 27.2%). Second 74 (26.9%) prey items it was observed on nests could no be unambiguously connected to delivery by an adult eagle. These added prey the unknown beginning either result from the eaglet searching its very own prey, or camera trap failing to record the adult’s arrival. Because that the staying 34 prey deliveries (12.3%), we could not identify the sex the the adult because its talons were not visible in the camera trap images. All food deliveries, merged with bone identification analysis, surrendered 306 food items representing 37 vertebrate varieties (Table 1). This were conquered by arboreal mammals, with three top-ranking varieties representing 49.7% of all deliveries and also 50.0% that the all at once prey biomass: two-toed sloths (Choloepus didactylus, 23.9%), brown capuchin monkeys (Sapajus apella, 18.3%) and also grey woolly chimpanzees (Lagothrix cana, 7.5%).
Table 1 types composition of harpy eagle food items taped in this research from both skeleton material and camera-trapping data.
Females and also males preyed top top proportionally similar arboreal prey (♀♀ 75.8 vs. ♂♂ 70.6%), whose difference is not statistically far-ranging (null model, P = 0.756). The same used to both scansorial (♀♀ 17.5 vs. ♂♂ 16.0%, null model, P = 0.611) and terrestrial prey (♀♀ 4.4 vs. ♂♂ 6.6%, null version P = 0.283). Females preyed primarily on adult prey, while the smaller males desired juveniles and also subadults (Fig. 2), which caused a far-ranging difference in food body mass in between the sexes. Male food averaged 0.74 ± 0.69 kg (geometric mean ± SD), if female prey was 57.3% heavier, averaging 1.29 ± 0.88 kg (null model, P 3). The biggest individual prey carried to a colony by any type of female was a ~ 4.7-kg, lower body section of an adult spider monkey, when for any type of male, this to be a ~ 3.2 kg reduced body quarters of a howler monkey. One adult whose sex might not be established simultaneously carried into a nest the lower body of a common opossum (Didelphis spp.) and the reduced body of a juvenile spider monkey (totalling ~ 3.6 kg). Levin’s niche width evaluation yielded similar values for the sexes: 7.20 because that females and 7.42 for males (n = 84 ♀♀, 69 ♂♂). Adhering to bootstrapping based upon a null model, however, the niche width fell to 2.40 for females and also 4.62 because that males, i m sorry was considerably different (P S1).
Prey age classes consumed by either male and female harpy eagles. The 10 most essential prey varieties (representing > 80% of the total) space ordered peak to bottom by adult body mass. Prey age course (stacked horizontal bars) are shown according to the legend. Male harpy eagles are less likely to go after adult prey, an especially in large-bodied prey species.
Prey body mass brought into swarms by either masculine (n = 75) or female (n = 92) harpy eagles. Male food averaged 0.74 kg, if female prey was 57.3% heavier, averaging 1.29 kg (hatched lines). The largest individual prey items carried into a colony were a ~ 4.7 kg lower body the a spider monkey eliminated by a female, and a ~ 3.2 kg lower body the a howler monkey eliminated by a male.
Nest density and buffer definition
Using the maximum packed colony density method, the mean distance come the nearest adjoining harpy eagle nest within a colony cluster to be 2.99 km (Cluster A, n = 6, SD = 1.52) and also 5.90 km (Cluster B, n = 5, SD = 0.89). A total of 124 km2 the the 195 km2 previously forested area roughly Cluster A still retained forest cover, while forest cover spanned 254 km2 that the 633 km2 roughly Cluster B. These data analyzed into a colony density of 1.97–4.84 nests/100 km2 of forest habitat, or 0.79–3.07 nests/100 km2 if we also include deforested locations (Fig. 4). We for this reason used both the 3-km and also 6-km radii as buffers for landscape analyses. A rough approximation between these (4 km, or 50 km2) was used as the reproduction territory size (consistent with the literature41), and also therefore supplied as the hexagonal cell size for the regional-scale analysis of habitat loss.
Examples of the spatial circulation of energetic breeding nests. Colony density to be calculated by the maximum Packed colony Density (MPND) method. Distances to the nearest neighbouring swarm were 2.99 km to 5.90 km depending on the nest cluster identity, i m sorry we supplied to calculation the 3-km and 6-km see buffers. The 2 southernmost nests in swarm A room the people excluded for sitting in riparian woodlands (QGIS V.3.16; https://www.qgis.org).
Prey file responses come deforestation
Contrary come our expectations, the level that deforestation did not significantly change the prey varieties composition because that harpy eagles (Fig. 5), nor did distance to livestock pastures (range: 0–6300 m, X̅ = 1159 ± 1703 m, n = 14 nests) or lot of woodland cover within a 3-km radius (range: 14–100%, X̅ = 69 ± 28%; NMDS, 999 permutations, stress = 0.1335, P = 0.332 for forest loss and also 0.079 for street to pasture, n = 14 nests). Eagles continued to record sloths and primates together their key prey, even in swarms sited in severely deforested areas. The level of forest loss did not influence Levin’s niche breadth index nor prey types richness (GLM, residual deviance: 152.59 top top 10 DF, P = 0.23, n = 12 nests), showing that harpy eagles relied mainly on large arboreal prey and also barely switched to open-country terrestrial vertebrates even in highly-deforested landscapes (Fig. 6).
Species composition of food items yielded to active harpy eagle nests. Key prey species are ordered in terms of all at once abundance. Each shaft represents a nest, notified by the landscape context from the shortest to the greatest amount of forest loss within a 3-km buffer area about each nest site. The harpy eagle food base is composed of arboreal forest vertebrate types even when colonies are located in very deforested landscapes.
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Effects of woodland loss (3-km buffer) top top the predation ecology of harpy eagles. Eagles nesting in highly deforested landscapes displayed levels of prey diversity and dietary niche breadth that were similar to those in much more relatively intact landscapes, through sloths and primates as the key prey.
Effects of deforestation on food delivery and biomass
Data indigenous 16 nest-phases (12 nests) and 189 prey delivery events proved that habitat lose induced far-reaching food stress and anxiety on nesting harpy eagles (Fig. 7). For these analyses, us excluded the two nests that were located in otherwise deforested riparian forest remnants, which space clear outliers due to the fact that they experienced abnormally high food biomass delivery rates, which was equivalent to reproduction territories in completely forested landscapes. Prey delivery intervals to be on mean 4.20 ± 1.97 days (n = 16 nest-phases). Prey biomass shipment rates averaged 0.37 ± 0.27 kg/day (range: 0.10–0.65 kg/day, n = 16 nest-phases). Details on food body parts lugged to the colonies are presented in Table 2. The nesting phase had a an unfavorable effect ~ above prey distribution rates, with much longer time intervals tape-recorded for older eaglets. Woodland habitat loss resulted in an increase in the number of days between consecutive prey deliveries considering both the 3-km (GLMM, F2,11 = 102.06, P F2,11 = 795.01, P F2,11 = 35.74, P F2,11 = 780.82, P F2,11 = 34.80, P F2,11 = 27.29, P Figure 7
Full dimension table