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 winddispersed 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. T ropical forests worldwide store >460 billion tons of carbonover half of the total atmospheric storage (1)-and tropical forest conversion and degradation account for as much as 20% of global anthropogenic greenhouse gas emissions (2). Tropical forests are also the most species-rich ecosystems on Earth, yet the role of species interactions in stabilizing tropical forest dynamics and maintaining the flow of natural ecosystem services, including long-term forest carbon pools, remains poorly understood. Over 80-96% of all woody plant species in tropical forests produce vertebrate-dispersed fleshy fruits (3, 4), yet many large-bodied frugivore populations in tropical forest regions have already been severely overhunted (5), resulting in functionally "empty" or "half-empty" forests with subsequent disruptions in seed dispersal mutualisms (6). Indeed, the total forest area degraded by unsustainable hunting in the largest remaining tropical forest regions may exceed the combined extent of deforestation, selective logging, and wildfires (7,8). Even formally decreed forest reserves in remote areas have succumbed to population declines and local extinctions of large vertebrates (9, 10), yet the consequences of this pervasive defaunation process to the persistence of tropical forest ecosystem services remains poorly explored.Overhunting can amplify dispersal limitation in many largeseeded plant species relying primarily or exclusively on harvestsensitive large-bodied frugivores. The causal mechanisms through which hunting leads to altered phytodemographics-recruitment bottlenecks resulting from replacement of seedlings f...

The value of trophic interactions for ecosystem function: dung beetle communities influence seed burial and seedling recruitment in tropical forests

“…Conceptual frameworks predict that large-seeded species are mostly at risk from the negative impacts of defaunation owing to the extirpation of their large-bodied primary dispersers [23,24]. Here, we demonstrate that large seeds may also be differentially vulnerable to the loss of their secondary dispersers through anthropogenic driven reductions in large-bodied dung beetles [33,48].…”

“…We therefore have a poor understanding of direct effects of diversity within higher trophic levels or the indirect, cascading effects of biodiversity loss across tropic levels (but see [14]). There is mounting evidence that changes in forest vertebrate communities can lead to direct top-down consequences for plant demography, community composition and diversity [15][16][17][18][19][20][21][22], with knock-on effects for forest services and resilience [23,24]. However, because the indirect, multitrophic consequences of changing mammal communities are rarely experimentally tested, we have limited understanding of the ecosystem-wide consequences of anthropogenic impacts on tropical forests.…”

Rivers shape population genetic structure in Mauritia flexuosa (Arecaceae)

“…Furthermore, as humans increasingly hunted large vertebrates in forests typically far from the water (Peres, Emilio, Schietti, Desmoulière, & Levi, 2016), animal‐dependent seed dispersal of M. flexuosa decreased in those areas, resulting in lower gene flow, all the while maintained closer to rivers. Although these observations remain to be tested explicitly, our patterns of high diversity are also consistent with the hypothesis that large population sizes of this species have been maintained by continuous activities of human cultivation, likely for thousands of years (Levis et al., 2017).…”

Abundance and composition of the medium to large-sized mammals in a private area of a REDD+ project in Acre, Brazil

“…In addition, hunting activity in the Amazon has shown to be an important cause in the loss of species during the "Anthropocene age" (Peres 2000a, Dirzo et al 2014, Peres et al 2016, capable of altering different ecosystem services, such as seed dispersal, and also causing changes in the structure of the plant community (Peres 2000b, Stoner et al 2007, Terborgh et al 2008, Dirzo et al 2014, Culot et al 2017. The disappearance of mammals in forest ecosystems can have a direct effect on the structure of the plant community and the food chain (Stoner et al 2007, Dirzo et al 2014.…”

“…The main change is the increase in the abundance of plant species that have no dispersion associated with vertebrates, to the detriment of other species with large seeds that are dispersed by large vertebrates (Terborgh et al 2008, Culot et al 2017. Such a change in plant community caused by defaunation is detrimental to the carbon market, since large biomass trees can have their recruitment reduced by the absence of their dispersers, reducing the carbon stock of the areas (Bello et al 2015, Peres et al 2016 Acre is considered of extreme importance for the conservation of mammals. The State has approximately 86% of its territory covered by forests and is situated in one of the areas with the most endemic plants of the Amazon (Maury 2002, INPE 2016.…”