Dispersal limitation induces long-term biomass collapse in overhunted Amazonian forests

Abstract

Tropical forests are the global cornerstone of biological diversity, and store 55% of the forest carbon stock globally, yet sustained provisioning of these forest ecosystem services may be threatened by hunting-induced extinctions of plant-animal mutualisms that maintain long-term forest dynamics. Large-bodied Atelinae primates and tapirs in particular offer nonredundant seed-dispersal services for many large-seeded Neotropical tree species, which on average have higher wood density than smaller-seeded and wind-dispersed trees. We used field data and models to project the spatial impact of hunting on large primates by ∼ 1 million rural households throughout the Brazilian Amazon. We then used a unique baseline dataset on 2,345 1-ha tree plots arrayed across the Brazilian Amazon to model changes in aboveground forest biomass under different scenarios of hunting-induced large-bodied frugivore extirpation. We project that defaunation of the most harvest-sensitive species will lead to losses in aboveground biomass of between 2.5-5.8% on average, with some losses as high as 26.5-37.8%. These findings highlight an urgent need to manage the sustainability of game hunting in both protected and unprotected tropical forests, and place full biodiversity integrity, including populations of large frugivorous vertebrates, firmly in the agenda of reducing emissions from deforestation and forest degradation (REDD+) programs.

Keywords: ecosystem services; forest carbon; hunting; large frugivores; tropical forest.

Fig. 1.

Relationships between primate body mass and population biomass density at 166 Amazonian forest sites surveyed to date, showing the local extirpation or population collapse of large-bodied atelines in heavily hunted sites. All forest sites were hunted to varying degrees but were otherwise structurally undisturbed at the time of line-transect surveys. Data are presented for four major classes of HP (none, light, moderate, and heavy) (SI Results). Black lines represent smoothers within 95% CI regions.

Fig. 2.

Maps of the (A) spatial distribution of all georeferenced rural households across the phytogeographic boundaries of Brazilian Amazonia; (B) population depletion envelopes for a game species that is highly sensitive to hunting (spider monkey, Ateles spp.) based on a biodemographic model that considers both the behavior of central-place hunters and the population dynamics of prey species; and (C) the overall distribution of depletion envelopes excluding all deforested areas as of 2013 (shown in orange). Small Inset square shows depletion envelopes in greater detail. The combined areas across the Brazilian Amazon (D) encompass radially asymmetric annuli around each household in which spider monkeys have been driven to extinction or depleted to small populations <50% of carrying capacity, K (dark to light red annuli) or 50–90% of K (light to dark blue annuli). Green vertical bar represents the total area remaining inaccessible to central-place game hunters.

Fig. 3.

Examples of whole fresh fruits and seeds within a typical tree family (Sapotaceae) within the morphological guild of undispersed tree species (A–F). These bear one to a few large, gut-dispersed seeds within hard-husked indehiscent exocarps and are most likely to succumb to seedling recruitment bottlenecks resulting from local extinctions of large-bodied prehensile-tailed ateline primates. (G) Coefficient estimates (±95% CI) showing the magnitude and direction of effect sizes of different forest site and biophysical predictors of the aggregate plot-scale basal area of undispersed tree taxa across the entire Brazilian Amazon. For a description of predictor variables, see SI Results.

Fig. 4.

Schematic representation of (A) a nonhunted, faunally intact forest and an (B) overhunted, half-empty forest in lowland Amazonia, showing the degree to which large arboreal and terrestrial forest frugivores are either extirpated or severely decline in abundance; and (C) abundance-based lottery transition models considering 129,720 canopy trees contained within 2,345 (1-ha) plots in which undispersed species at time t₀ are replaced by any other dispersed species (green tree) at time t₁ with a probability that is proportional to their cooccurring abundances at t₀ within each plot. A total of 1,000 simulation runs for both random and nonrandom replacements (from t₀ to t₁) were performed for each plot, with a total number of 48,237 stem substitutions per run.

Fig. 5.

(A) Inverse distance-weighting interpolation of forest AGB estimates based on (B) 2,345 1-ha forest plots arrayed across all nine states within the phytogeographic boundaries of Brazilian Amazonia, which were surveyed by the RADAMBRASIL forest inventory program in the 1970s to early 1980s. These estimates are highly variable but follow a (C) log-normal distribution with a mean (±SD) value of 128.6 ± 57.5 Mg/ha^‒1, ranging from 26.1 to 684.4 Mg/ha^‒1.

Fig. 6.

Distribution of simulated changes in plot-scale AGB estimates under two mutualism extirpation scenarios considering two functional groups of large-bodied seed dispersal vectors that are highly sensitive to HP throughout Amazonian forests: (A) large atelinae primates (Lagothrix spp. and Ateles spp.), and (B) both large ateline primates and the largest neotropical forest ungulate, lowland tapir (Tapirus terrestris). The resulting Δ_AGB values are predominantly negative under both scenarios (orange bars to the left of dashed vertical dashed lines), with 77% and 88% of all 2,345 plots losing biomass under dispersal-limitation scenario I (A) and scenario II (B), respectively.

Fig. 7.

Geographic trends in either positive or negative simulated changes in ABG (∆_agb) interpolated across the entire Brazilian Amazon from time t₀ to t₁ considering two conservative faunal extinction scenarios, in which (A) only large ateline primates (i.e., Ateles and Lagothrix) are extirpated (scenario I); and (B) both ateline genera and lowland tapir are extirpated (scenario II). The full spectrum of committed losses or gains in AGB (%) is color-coded from red to blue. Small Inset maps show the total number of 1-ha RADAMBRASIL plots that either lost (white dots) or gained (black dots) biomass across floristic transitions (see SI Results and Fig. 5).