Unveiling biogeographical patterns of the ichthyofauna in the Tuichi basin, a biodiversity hotspot in the Bolivian Amazon, using environmental DNA

Biogeographic structure. The fish species composition revealed among the sites of this study through environmental DNA provides a sufficiently localised signature for a biogeographic pattern to emerge. The sampling sites were close to the confluences of the Quiquibey, Quende- que and Hondo rank 2 rivers and the rank 3 tributaries of the Tuichi, allowing the identifica- tion of the fauna located at only few km upstream of the sampling points. In oxbow lakes and tectonic lakes, the absence of inflows from streams allows the identification of the local ich- thyofauna present at the sampled site. Four biogeographic entities are highlighted according to the specific composition of their ichthyofauna in relation to the structure of the hydrographic network (rank 1–2, rank 3, Alto-Tuichi) with an even stronger distinction of the ichthyofauna between rivers or lakes biotopes constituting the fourth entity. The ability of eDNA to more accurately report on the structuring of species than more traditional inventories (net, electric fishing, rotenone) is recognized [26, 66]. The entire ecosystem is better apprehended with a sharp reduction in the biases inherent to sampling a complexity of habitats in which rare and cryptic species would be much more difficult to access and register by traditional means. Simi- lar richness coverage between the 4 biogeographic entities (from 70 to 80%) reflecting similar sampling efforts allows comparing their ichthyodiversity with limited bias. The distribution patterns of the ichthyofauna according to the ranks of the tributaries and

therefore according to their sizes, have been demonstrated many times in all latitudes (review in Hugueny, Oberdorff, & Tedescco, 2010 [67]). In the Beni basin, the patterns of differentia- tion between lake and river ichthyofauna are particularly contrasting with all the lakes from upstream to downstream of the Beni clustered in the same biogeographic entity. Furthermore, two sub-units can be distinguished among lakes: the lakes of the Rio Beni plain and those located in the upstream portion of the basin in the Madidi reserve (lakes Ruta, Santa Rosa and Chalala´n). For Santa Rosa and Chalala´n lakes, which are tectonic and older, species diversity is lower than in the oxbow lakes, however, for the latter neither their age of appearance, nor their surface area is correlated with their species richness. We also note that lake Ruta, although young (2005) and small (4 ha), has the same number of species as the older (<1950) and much larger (180 times) lake Mentiroso located in the Madre de Dios plain (Fig 3). In contrast with the Ruta lake, Mentirosso is under strong human pressure (fishing, mining activities). The distribution of fish populations’ biogeographic entities in the Tuichi basin is strongly correlated with hydro-ecoregions patterns [31] that include several local environmental vari- ables, sometimes correlated with each other, highlighting the relationship between fish distri- bution and waters quality in the Amazon [68]. The physico-chemical parameters involved in water quality have not been directly measured in this study, but are nevertheless integrated in

the four main categories of variables considered. The biogeography of the lake ichthyofauna is correlated to altitude, itself correlated to the longitude and the nature of soils. The composition of the ichthyofauna of the different rivers is correlated with the same environmental parame- ters as lakes, to which is added geology, itself in relation to altitude. Usually, the nature of the substrate on which the continental waters flow (river and lake) partly explains the distribution of the Amazonian ichthyofauna [69], since the variation of the soils and subsoils drives the var- iation of the physicochemical parameters of the water, the living environment of the fish, as well as the type of riparian vegetation, which is itself a food resource and nursery for numerous fish species [70]. In the present study the observed species richness drops considerably with altitude in lotic biotopes, with less than a dozen species detected only above 700 m elevation. The decline in species richness with increasing altitude is described as being related to decreased temperature, an increase in dissolved oxygen and pH, also accompanied by a turnover of species, as observed in the Colombian Andes [71]. However, this drop in diversity is also accompanied by an increase in the proportion of endemic species in the Andean foothills: around 40% of the PLOS ONE Fish diversity and distribution in the Tuichi basin PLOS ONE | https://doi.org/10.1371/journal.pone.0262357 January 4, 2022 17 / 25