Abstract

Arapaima, pirarucu or paiche (Arapaima gigas) is one of the largest freshwater fish in the world, and has a long history of commercial exploitation in the Amazon region. To estimate levels of genetic variability and historical and recent connectivity in Arapaima, we examined variation in eleven microsatellite DNA markers in individuals from 22 localities in Brazil, Colombia, and Peru. The results of analysis of molecular variance, Bayesian clustering and discriminant analysis of principal components showed that Arapaima in our samples represents two major populations, one in the Amazonas and one in the Araguaia-Tocantins River basins. The Amazonas population is further structured by isolation-by-distance with the hydrologically largely unconnected Amapá locality representing the eastern-most extreme of this continuum; gene flow predominates at distances of less than 1500 km with localities separated by over 2000 km dominated by genetic drift and effectively forming different populations. We saw no evidence of multiple species of Arapaima in the Amazonas basin, and analysis of pairwise genetic divergence (FST) with Mantel tests and correlograms indicated that this largest population exhibits a large-scale pattern of isolation-by-distance, with which results from MIGRATE-N agreed. The degree and significance of genetic divergence indicates that most sampled localities represent demographically independent sub-populations, although we did identify several recent migration events between both proximal and more distant localities. The levels of genetic diversity were heterogeneous across sites, including low genetic diversity, effective population sizes, and evidence of genetic bottlenecks in several places. On average the levels of gene diversity and rarefied allelic richness were higher for localities along the Amazonas mainstem than in the tributaries, despite these being the areas of highest fishing pressure, while the lowest values were found in tributary headwaters, where landscape modification is a significant threat. We recommend that managers consider the regional and local threats to these populations and tailor strategies accordingly, strategies which should ensure the ability of young A. gigas to disperse through floodplain corridors to maintain genetic diversity among otherwise sedentary adult sub-populations.

Highlights

  • The Amazon basin suffers from the myth of superabundance, wherein the natural resources present in this region, including its impressive diversity of fishes, are considered inexhaustible by any human demand [1, 2]

  • Expected heterozygosity (HE) varied from 0.26 in the specimens collected in the Araguaia-Tocantins drainage (APA Meandros do Araguaia) to 0.66 in the specimens collected near the main channel, at Mamiraua (S2 Fig)

  • We found that the greatest structure in our genetic data reflected geographic disjunction of A. gigas in the upper Araguaia-Tocantins —a basin that become effectively isolated from the Amazon basin at the Plio-Pleistocene boundary [63], while the remaining fishes from the Amazonas basin reflected a single, albeit

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Summary

Introduction

The Amazon basin suffers from the myth of superabundance, wherein the natural resources present in this region, including its impressive diversity of fishes, are considered inexhaustible by any human demand [1, 2] This myth derives in part from the huge scale of the Amazon, its high biodiversity, and its low relative human occupational density, since the perceived abundance of a region’s natural resources is directly related to the intensity of exploitation [2]. The iconic arapaima continues to be exploited, it is described on the IUCN Red List as Data Deficient (IUCN, 2017), meaning there is insufficient knowledge of its biology, ecology, and genetics to effectively manage its conservation Another prominent uncertainty surrounding the arapaima is the number of species present in this genus and their distribution. Stewart [9, 10] puts forth an argument that at least six species of Arapaima exist: 1) Arapaima gigas (Schinz, in Cuvier 1822) described from near [Vila] Santarem, Para State, Brazil, only known from the holotype (MNHN A.8837); 2) Arapaima mapae (Valenciennes, in Cuvier and Valenciennes, 1847) described from Lago do Amapaor Lago Grande in Região dos Lagos in Amapa State, Brazil, only known from the holotype (MNHN A.8836); 3) Arapaima arapaima (Valenciennes, in Cuvier and Valenciennes, 1847) described from Guyana (Essequibo basin), only known from the holotype (BMNH 2009.1.19.1) but the holotype is misplaced or lost; 4) Arapaima agassizii (Valenciennes, in Cuvier and Valenciennes, 1847) described from “Brazilian Amazon”, only known from an illustration of the holotype by Spix and Agassiz [11] and the holotype is lost; 5) Arapaima leposoma Steward 2013 described from one specimen collected from the Solimões River shortly upstream of the mouth of the Purus River, Amazonas State, Brazil, only known from the holotype (INPA 16847); and 6) Arapaima sp. incertae sedis, i.e. a species of uncertain taxonomic status, that apparently comprises all other Amazon basin Arapaima specimens deposited in scientific collections

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