Effects of mammal defaunation on natural ecosystem services and human well being throughout the entire Neotropical realm
Graphical abstract
Introduction
The Neotropical realm contains myriad endemic species and is the most biodiverse set of ecoregions on Earth. Yet this realm and its biogeographic provinces have been subjected to an unprecedented human-induced biodiversity crisis derived from multifaceted drivers of environmental degradation. The ongoing sixth mass extinction event has erased well over 300 mammal species, which required 3–5 million years of evolution (Davis et al., 2018). Mammal faunas represent the main elements of regional biotas that often succumb to nonrandom population depletion, leading to wholesale local extirpations, particularly in heavily settled parts of the tropics (Dirzo et al., 2014, Bogoni et al., 2018). As a result, the current extinction crisis has exponentially accelerated at local to continental scales compared to background extinction rates (Ceballos et al., 2017).
Several neotropical regions are overshadowed by an imminent mammal diversity collapse in moist humid forests, coastal zones and central plateaus, which have historically been rapidly replaced by anthropogenic habitats and experienced increasing overhunting pressure since the European colonization of the Americas (Dean, 1996). The concept of defaunation is a legacy of the “empty forest” term coined by Redford (1992) based on seminal studies (Terborgh, 1988, Peres, 1990). This community-level depletion phenomenon is defined primarily in terms of vertebrate species succumbing to demographic or functional extinctions, and downstream effects including the breakdown of key mammal-mediated ecological processes (Redford, 1992). Widespread evidence so far indicates either population depletion or full deletion of large-bodied species prior to replacements by small- to medium-sized species across the Neotropics. This process of density under-compensation increases the abundance of some species, which may partially balance the population decline, extirpation, or absence of potential competitors (Peres and Dolman, 2000), leading to cascading effects that proliferate throughout entire small vertebrate, invertebrate and plant communities (Dirzo et al., 2014).
Mammal population declines—which are often buffered by relatively intact areas—overlap the entire diversity gradient exhibited by the Neotropics. Based on a pool of ~ 1,550 species of mammals, this gradient of taxonomic diversity ranges from the lowest species richness in southwestern South America (<50 species) to the highest richness in northern South and Central America (>200 species) (Ojeda, 2013). Empirical studies have shown that mammalian functional diversity across the Neotropics follows a similar latitudinal pattern (e.g., Oliveira et al., 2016, González-Maya et al., 2017). Functional diversity is undoubtedly an important component of biodiversity because it represents the difference in functional traits between organisms (Tilman, 2001, Májeková et al., 2016), but measures of functional diversity depends on which life history traits are considered (Májeková et al., 2016). Based on morphological, ecological and behavioural criteria (Tilman, 2001), functional diversification resulted from stochastic and evolutionary events that have spawned “eco-spaces”, promoting both inter- and intra-ordinal diversification and impressive ecomorphological convergence (Meredith et al., 2011).
Hence, there is a close relationship between functional diversity and phylogeny, especially phylogenetic diversity (Flynn et al., 2011, Safi et al., 2011, Schweiger et al., 2018). The geography of mammal phylogenetic diversity throughout the Neotropics is also poorly understood. Despite several recent advances, the segmentation of well-known phylogenetic diversity patterns worldwide (e.g., Safi et al., 2011) lacks detail and depends on what phylogenetic data are available. Both phylogenetic and functional diversity embraces many biological aspects that are correlated with ecosystem functioning, due to the interrelated phylogenetic-functional differences among organisms (Tilman, 2001, Schweiger et al., 2018). Evolutionary history constrains species traits within clades (Safi et al. 2011), and these traits—beyond a proxy of species vulnerability to local and regional extinctions (Cardillo et al., 2005, Cardillo et al., 2008)—impacts their roles in ecosystem functioning. For example, phylogenetically-related ungulate megaherbivores share similar dietary and body size traits that influence many ecological processes, such as herbivory, seed dispersal, seed predation, and ecosystem landscaping (Lacher et al., 2019).
Ensuring well-functioning ecosystems is paramount to provide healthy flows of ecosystem services. Chronic human interferences in natural ecosystems are degrading their ability to provide ecosystem services (MEA (Millennium Ecosystem Assessment), 2003, MEA (Millennium Ecosystem Assessment), 2005, Díaz et al., 2013), which are defined as the benefits that people and their well-being obtain from natural ecosystems (MEA (Millennium Ecosystem Assessment), 2003, MEA (Millennium Ecosystem Assessment), 2005), usually free-of-charge. These include provision, regulation, cultural and support services that directly affect people under the operation of whole ecosystems (MEA (Millennium Ecosystem Assessment), 2003, MEA (Millennium Ecosystem Assessment), 2005). Provision services include food production, and availability of water, wood, and fiber. Regulatory regimes include climate buffering, disease regulation, biological and natural damage regulation, water purification, and pollination. Cultural services are linked to ecotourism, education, and cultural heritages and support related services such as soil formation, nutrient cycling and primary production (MEA (Millennium Ecosystem Assessment), 2003, MEA (Millennium Ecosystem Assessment), 2005).
The diversity of functional groups—of equivalent species sharing similar traits (Tilman, 2001)—is conceptually important in determining how ecosystem services are assessed (Hooper et al., 2005). Species traits reflect important ecological dimensions (Davidson et al., 2009), and are used to determine direct and indirect ecosystem services (Harrison et al., 2014). Defaunation therefore erodes not only several levels of diversity, but also exerts critical impact on ecosystem functioning and services. However, the extent, geographic distribution and magnitude of how defaunation may affect ecosystem services have not been quantified from local to biogeographic scales across an entire tropical realm.
Accelerated declines in population abundance and elevated extinction risk may degrade critical ecosystem processes mediated by mammals (see Lacher et al., 2019), further justifying more effective and comprehensive conservation action. We therefore seek to understand the effects of mammal defaunation on losses in functional diversity and ecosystem services across the entire Neotropical realm on the basis of thousands of putative baseline mammal assemblages. Based on the premise that cumulative local extinctions lead to a defaunation footprint of variable spatial scales and intensities across biogeographic gradients, we hypothesize that the worst-case scenarios of defaunation will deplete functional diversity and ecosystem services at magnitude similar to those of contemporary vertebrate population declines (i.e., >40% according to Ceballos et al., 2017). This may lead to an irreversible collapse in several mammal-mediated ecosystem processes that contribute to human well-being.
Section snippets
Meta-region of study: The Neotropical realm and its provinces
Several criteria have been used to define the biophysical boundaries of the tropics (Feeley and Stroud, 2018). The Neotropical realm includes all tropical terrestrial ecoregions of the Americas and the entire South American temperate zone, containing 46 biogeographic provinces (Udvardy, 1975). A strict classification of the Neotropical Ecozone ranges from central Mexico to southern Brazil, including Central America and the Caribbean (Schultz, 2005). Thus, our study region ranged from the
Overall trends in data compilation
We compiled data on 1,153 mammal species distributed across 2,427 assemblages encompassing ~ 20.4 million km2, which represented 165,633 presence records (or 5.92%) within a full matrix of 2,798,331 cells. Across the 49 Neotropical provinces, there were 49.5 (±56.8) assemblages per province, ranging from two (Bahama province: 5,443 km2) to 238 (Cerrado province: ~2M km2). This resulted in a ratio of 0.012 mammal assemblages per 100 km2 spaced apart by a mean distance of 3,182 km (±1,996 km;
Discussion
A paramount challenge in how conservation ecology can inform the emergent science of ecosystem services is to quantitatively understand the effects of biodiversity loss on human well-being. Recent empirical studies have shown the overwhelming simplification of mammal faunas worldwide, depleting perhaps the most charismatic biotic component of tropical environments, often undermining their ecosystem functions and services (e.g., Dirzo et al., 2014, Peres et al., 2016). Even accounting for the
Conclusions
In integrating our estimates with a wider body of empirical evidence, we can conclude that many ecosystem services are now threatened due to massive diversity loss. We emphasize that human well-being depends heavily on biodiversity conservation at varying spatiotemporal scales, and that the local effects of biodiversity loss are propagated at regional to continental scales. The central hypothesis we posed here has therefore been endorsed because the loss of large-bodied species, and/or
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
We sincerely thank all researchers who obtained and organized the datasets compiled in this study. We thank Adriano Chiarello, Arnauld Desbiez, Marcelo Magioli, Maurício Graipel, Rodrigo Massara, and Ronaldo Morato for their expert opinion about species-based ecosystem service attributions. We thanks two anonymous reviewers for important contribution on our manuscript.
Funding
JAB is supported by the São Paulo Research Foundation (FAPESP) postdoctoral fellowship grants 2018-05970-1 and 2019-11901-5. KMPMBF is funded by research grant (308632/2018-4) from the Conselho Nacional de Pesquisa e Desenvolvimento Científico e Tecnológico (CNPq).
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