Elsevier

Biological Conservation

Volume 242, February 2020, 108417
Biological Conservation

Large-scale assessment of genetic diversity and population connectivity of Amazonian jaguars (Panthera onca) provides a baseline for their conservation and monitoring in fragmented landscapes

https://doi.org/10.1016/j.biocon.2020.108417Get rights and content

Abstract

Jaguar population genetics has so far not been investigated on a broad scale in the Amazon rainforest, which constitutes the largest remaining block of continuous habitat for the species. Given its size, it serves not only as a stronghold but also as a reference for jaguar conservation genetics, against which fragmented landscapes can be compared. We assessed genetic diversity and population structure of Amazonian jaguars using 11 microsatellite loci and performed comparative analyses incorporating available data from two other South American biomes (Pantanal and Atlantic Forest) in which the species has faced different amounts of habitat loss and fragmentation. Using the largest genetic data set assembled to date for jaguars (n = 190), we observed that all diversity indices were consistently higher for the Amazonian population, with no genetic subdivision detected in that region, indicating large-scale connectivity across >3000 km. In contrast, we corroborate the inference of anthropic-driven genetic structure and bottlenecks for two Atlantic Forest populations. Our results indicate that the Amazon is a critically important stronghold for jaguars, comprising a highly diverse, panmictic population that allows a glimpse into the patterns of genetic connectivity that characterized this species prior to human intervention. In contrast, the Atlantic Forest populations jointly still retain considerable levels of genetic diversity, but this is currently partitioned among isolated fragments that are increasingly subjected to heavy anthropic disturbance. These results have important implications for jaguar conservation planning, highlighting the critical condition of Atlantic Forest populations and providing a genetic baseline to which they can be compared.

Introduction

Tropical ecosystems harbour a large proportion of global biological diversity, reaching >50% of the world's terrestrial biodiversity (Gardner et al., 2010). Increasing human activities on those regions are exerting pressure on the biota, reducing local abundance and causing defaunation, driving thousands of species to extinction even before they are discovered (Dirzo et al., 2014). Habitat loss and fragmentation are two of the main threats to species survival, especially for large carnivores (Costa et al., 2005; Crooks, 2002), such as the jaguar (Panthera onca). This felid is the top predator of the Neotropics, and given its keystone role, constitutes an umbrella and flagship species for biodiversity conservation (Thornton et al., 2016). Globally, it is considered ‘Near Threatened’ by the IUCN (Caso et al., 2008), but it is categorized as Endangered or Vulnerable in most national red lists across its distribution (e.g. Aprile et al., 2012; ESA, 1973; Rodríguez-Mahecha et al., 2006; SEMARNAT, 2010).

In Brazil, jaguars currently occur in five out of six major biomes, and their populations are subjected to different threats on a regional basis, making them more vulnerable in some areas than others (Nijhawan, 2012; Sollmann et al., 2008). It is ‘Critically Endangered’ in the Atlantic Forest due to a drastic population reduction during the last three decades (Beisiegel et al., 2012), as this biome is severely imperilled by habitat loss and fragmentation (Tabarelli et al., 2005). In contrast, the Amazon and the Pantanal, given their extent, habitat suitability and comparatively lower levels of fragmentation, are regarded as the two main strongholds for the jaguar, both nationally and globally, although its status is ‘Vulnerable’ in both of these biomes (Cavalcanti et al., 2012; de Oliveira et al., 2012).

The Brazilian portion of the Amazon covers nearly 3.5 million km2, and it is assumed that jaguars occupy most of this area (de Oliveira et al., 2012). For this reason, this biome is regarded as the most important block of continuous habitat for jaguars, harbouring one of the largest populations of the species, with good perspectives for long-term persistence. Nevertheless, jaguars in this biome are threatened by illegal hunting, and the so-called “arc of deforestation” is advancing on the eastern and southern portions of the region, already representing a loss of 18% of the originally forested area (de Oliveira et al., 2012). Likewise, the Pantanal is one of the largest wetlands in the world, encompassing 140,000 km2 (85% of which remain conserved), with jaguars occupying between 88,000 and 125,000 km2 (Cavalcanti et al., 2012). In the Pantanal, retaliatory hunting of jaguars that prey on cattle is the main threat to the species' survival. Interestingly, ecotourism focused on jaguars in this region is currently fifty times more profitable than cattle ranching (Tortato et al., 2017), which has helped to alleviate the hunting pressure. In sharp contrast, the Atlantic Forest is a biodiversity hotspot with a high degree of endemism (Myers et al., 2000), whose primary cover has been decimated in the last four decades, declining from 1.3 million to 150,000 km2 (Ribeiro et al., 2009). Currently, jaguars occupy <50% of this area, persisting in small, isolated fragments in which jaguars also suffer from prey depletion and illegal hunting (Beisiegel et al., 2012; Paviolo et al., 2016).

As a large mammalian carnivore, jaguars have high mobility and, as a result, could potentially attain high levels of dispersal and gene flow across the landscape (Row et al., 2012; Tammeleht et al., 2010). However, relatively few molecular studies with jaguars have been published to date. Jaguars have shown moderate to high levels of genetic diversity (Eizirik et al., 2001; Roques et al., 2016; Ruiz-Garcia et al., 2006; Wultsch et al., 2016a), without evidence of strong population structure across their range, possibly due to a recent population expansion and high connectivity on broad spatial scales. Major geographical barriers such as the Amazon River and perhaps the Darien strait were suggested as having restricted historical gene flow among four incompletely isolated phylogeographic groups: southern South America, northern South America, Central America and Mexico-Guatemala (Eizirik et al., 2001). However, the authors of that study stressed the need for further sampling that could reveal a finer pattern of subdivision or isolation by distance on a regional level.

In-depth analyses of regional jaguar populations in Brazil initially revealed that a recently fragmented area of the inner Atlantic Forest showed evidence of drift-induced population differentiation and loss of allelic richness, driven by anthropogenic habitat loss and isolation (Haag et al., 2010). The problem is so severe that one of the sampled populations (“Porto Primavera”) was extirpated due to the flooding of a hydroelectric dam before that study was published. Valdez et al. (2015) further analysed these subpopulations in conjunction with jaguars sampled at four sites within the southern Pantanal and found that the latter region forms a single genetic cluster with higher genetic diversity than each of the Atlantic forest demes. Subsequently, Srbek-Araujo et al. (2018) analysed an isolated population from the coastal Atlantic Forest and demonstrated that it also bears signs of anthropogenic loss of diversity, at a rate that may be even higher than that of the inland fragments.

Any genetic study is sensitive to the geographic scale considered in the analysis, potential gaps in sampling, and numbers of markers and their information content (Radespiel and Bruford, 2014). Furthermore, ancient demographic processes left genetic imprints in edge-populations (vs. core-populations) that are analogous to signals detected in shrinking populations subject to contemporaneous anthropic-driven drift (Slatkin and Excoffier, 2012), potentially hindering the disentanglement of the underlying process. For instance, jaguars have shown a marked population structure altogether but a weak signal of isolation by distance across Central America, which increased when Mexican (edge-) populations were included in the analysis (Wultsch et al., 2016a, Wultsch et al., 2016b). Similarly, comparing 11 microsatellite loci typed in jaguars from Brazil and Mexico, Roques et al. (2016) found a marked genetic structure, with samples from Brazil forming three genetic clusters, corresponding to the Amazon/Cerrado, the Pantanal, and the Caatinga. Genetic differentiation was not only related to geographic distance, but also to the intensity of drift, as the isolated population from the Caatinga showed low allelic richness and reduced gene flow relative to the other areas within Brazil. This is a likely consequence of a recent (within the last 20 to 30 years) demographic reduction, which may reflect the Caatinga region contemporary habitat deterioration. Jaguars sampled in the Amazon rainforest showed high levels of genetic diversity and panmixia across considerable distances, while the genetic diversity was lower towards the limits of the species' range (Mexico, Caatinga and Pantanal). However, Roques et al. (2016) did not survey the Amazon as a whole, as their geographic sampling of this vast region was restricted to a north-south transect covering only the central portion of the biome, leaving large sampling gaps in the eastern and western Amazon. In addition, that study did not include comparisons with Atlantic Forest populations, which have been found to be severely impacted by recent fragmentation (Haag et al., 2010; Srbek-Araujo et al., 2018).

In this context, the aim of this study was to survey the jaguar's genetic variability and population structure across the Amazon, and to perform comparative analyses of this data set jointly with those reported previously for Atlantic Forest (Haag et al., 2010; Srbek-Araujo et al., 2018) and southern Pantanal (Valdez et al., 2015) populations. In particular, we aimed to employ standardized molecular markers to assess the hypothesis that jaguars in the large, continuous Amazon rainforest show greater levels of genetic diversity and population size and connectivity than in the highly fragmented Atlantic Forest. We included the Pantanal biome as a control for high-quality habitat availability, as this later region currently harbours roughly the same extension as the sum of Atlantic Forest remnant fragments. This result would further corroborate our previous inference that the population structure observed in the Atlantic Forest is anthropogenic (Haag et al., 2010; Srbek-Araujo et al., 2018), and stress the importance of generating baseline data for jaguar genetics and ecology in a habitat that still retains large-scale continuity.

The specific aims of this study were as follows:

  • 1.

    To contribute data on jaguar population structure and genetic diversity in the Amazon region, which currently represents its main stronghold for global conservation, but is still understudied due to its vastness and inaccessibility.

  • 2.

    To compare these results with those previously published for two different biomes, the Pantanal and the Atlantic Forest, which are subjected to different intensities of anthropogenic disturbance.

  • 3.

    To summarize the amounts of genetic diversity and population structure in these populations, characterizing their spatial distribution within and among biomes.

  • 4.

    To provide baseline data for assessment of jaguar vulnerability to genetic erosion in its core range, as well as in other areas, which should be relevant in the context of current and projected scenarios of habitat degradation.

Section snippets

Sampling protocol

We obtained samples of biological material from 73 Amazonian jaguars, including blood samples from animals captured for field ecology studies or kept in captivity, and pelt/hair samples from material confiscated by local environmental authorities or collected during wildlife surveys within indigenous and other riverine human communities (Supporting information Table S1). Field-captured animals were covered by capture permit 11095-8, issued by SISBIO/ICMBio, Brazil. The overall Amazonian sample

Dataset features

For the joint data set, using the 0.69 threshold of genotyped loci, we discarded three individuals that did not meet this criterion. After checking for exact duplicate genotypes, one additional individual was removed from the Amazon dataset (likely deriving from tube mislabelling during sample collection or processing), as well as another one showing an excess of homozygous genotypes. Two out the 13 loci showed >20% of missing genotypes: F124 (n = 48; 24.7% missing) and FCA741 (n = 41.5; 21.4%

General patterns

Genetic diversity studies constitute a pillar in the field of conservation biology, although their practical application has often not been fully achieved so far (de la Torre et al., 2018; Hoban et al., 2013; Rivers et al., 2014). As a contribution to fill this gap, we analysed the most broadly distributed set of genetic samples for Amazonian jaguars surveyed to date, and directly compared it with two other biomes, potentially serving as a baseline for the assessment of jaguar population

Data accessibility statement

Part of the data used in this paper has been published previously (Haag et al., 2010; Valdez et al., 2015; Srbek-Araujo et al., 2018). Two of these previous data sets have been deposited in the Dryad digital repository (https://doi.org/10.5061/dryad.1884/1; https://doi.org/10.5061/dryad.371c6). The third previous data set (Srbek-Araujo et al., 2018) and the novel data reported here have been deposited in the Mendeley Data Repository (DOI: doi:10.17632/gdf5fj7f2s.1; DOI: 10.17632/nwdm9f9rrj.2).

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

GL, LH and EE acknowledge CNPq/Brazil for financial support. This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nivel Superior – Brasil (CAPES) – Finance Code 001. We thank Centro de Instrução de Guerra na Selva (CIGS) and IBAMA-Manaus for providing access to biological material from the animals present in these institutions. We also thank Benoit de Thoisy, Gervásio S. Carvalho, Tania Sanaiotti, Gislene Vilara, Maria da Conceição Santos, Julia Verba, Waleska

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