Unveiling biogeographical patterns of the ichthyofauna in the Tuichi basin, a biodiversity hotspot in the Bolivian Amazon, using environmental DNA
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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
400 to 600 species inventoried, including species that are threatened or already extinct [72]. Moreover, this increase in endemicity with altitude would correspond to a diversification of the functional groups distributed in the basin headwaters, generating an increase in beta diver- sity [73]. Human threats and conservation. Many watersheds originating in the Andean valleys are under increasing anthropogenic pressure due to the construction of dams, gold mining [74] and pollution by wastewater from cities and industries (e.g. construction of sugar mills close to sites such as the Fuerte lake). In order to set up conservation strategies, the biodiversity of the aquatic fauna distributed in particular in the Andean foothills should be generalised and inves- tigated rapidly, as we have done for the Tuichi basin, using eDNA approaches. Owing to its location directly downstream of the capital city, La Paz, and its anthropogenic pressure (min- ing, pollution, landscape degradation, exploitation; [11]), but also to the presence of the Madidi NP and knowledge gaps [1], the Beni basin should be considered a priority area for carrying out further eDNA surveys. The results and methodology of the present study could serve as a reference point for future comparisons of river basins under different anthropogenic pressures with the lightly anthro- pized Andean basin of the Tuichi River. On a larger scale, anthropogenic effects in the Beni watershed, and in particular fishing pressures that remain poorly documented [75], should be
estimated and related to the specific assemblages and richness observed. An important anthro- pogenic threat is the introduction of species, such as Arapaima gigas, species CITES II on all its natural distribution range. Naturally absent from the upper Madeira, it has been introduced in the 70s from an aquaculture facility in Lake Sandoval on the Madre de Dios River, tributary of the Beni River [76, 77]. We have detected Arapaima in four lakes, Mentirosso, Tumichuca, PichiDuro and Colorado, but not higher upstream. The lake Colorado would therefore be at the front of colonisation of the species on the Beni River at the sampling period. The species Prochilodus argenteus, is normally endemic to the San Francisco basin [78]. A molecularly close species (COI gene), named Prochilodus aff. argenteus had been identified in the Beni River using metabarcoding of fish larvae [11]. More recently [1], reported its occurrence in the Coari River in the Brazilian Amazon. Now, using eDNA, we have again detected this species in the Beni watershed, which suggests a wider distribution range than currently described. How- ever, as this economically important species has already been introduced elsewhere in Brazil- ian rivers [25], an introduction in the Beni watershed is also likely. Another growing anthropogenic threat is the rapid expansion of hydroelectric dams in the Amazon basin [79– 83]. Three dams are currently planned in our study area (Fig 1), between the protected areas of the Madidi NP: one at the Bala strait in the middle of our study area, and two slightly upstream
of it at the Chepete and Beu straits [11]. Their construction would lead to > 50% losses of net- work connectivity in the Beni basin [79]. It would also result in profound alterations in the sedimentation patterns of the river (volume and flow of sediments), homogenizing down- stream habitats in the river and in the lakes [84]. Additionally, these dams would also result in the formation of extensive upstream reservoirs and the Bala dam would likely permanently flood a large portion of our study area. Other foreseeable impacts of these dams are similar to that observed on riverine fish communities elsewhere in the world and range from local extinction of species that cannot adapt to reservoirs and dam-tailwater conditions, to basin- wide extirpations of migratory species [85, 86]. The Amazon basin hosts a rich migratory fish fauna that accounts for the bulk of fisheries landing and dam construction is expected to severely impacts migratory species (review in Duponchelle et al., 2021 [87]). Several of these migratory species holding commercial and cultural importance were identified in our study area. A spawning area for several of these species, threatened by anthropogenic activities such as arid extraction or pollution, was recently identified in our study area [11]. The alteration of PLOS ONE Fish diversity and distribution in the Tuichi basin PLOS ONE | https://doi.org/10.1371/journal.pone.0262357 January 4, 2022 18 / 25
local environmental conditions by damming (sediment and flow patterns modifications, per- manent flooding of large area) will likely further compromise the usefulness of the identified spawning area. It will profoundly modify the structure of fish communities and the fisheries that depend on them, as observed in other dammed rivers of the Amazon basin (review in Duponchelle et al., 2021 [87]). Contributions and limitations of the eDNA approach in the biogeographic study of the region. The eDNA approach permitted a study of fish biodiversity in the Tuichi sub-basin and broader Beni basin within and immediately adjacent to the Madidi NP with a high species diversity thanks to a high taxonomic resolution, since 93.3% of the assigned OTUs (5,246) are at the spe- cies level. A majority of OTUs (8,205) although aligned with at least one sequence in the COI fish database could not be assigned taxonomically due to a too low percentage of identity with the reference (<97%). This is closely related to the fact that of 2,406 known Amazonian fish species [2], only a third (694) have a COI barcode available. The effectiveness of the method would therefore be considerably enhanced if the reference databases used for taxonomic attri- bution (Bold, GenBank) were improved over time, thereby improving our species identifica- tion capabilities. Markers other than COI have been used to record fish biodiversity, such as a 12S marker in French Guiana [26]. But the smaller size of the latter (65 bp versus 185–285 bp for the COI bar-
codes used here) and an even more limited database (181 available 12S barcode in Cilleros et al., 2018 [26]) than that of the COI, makes this marker less efficient than the COI, with more difficulty in assigning OTUs below family or gender level. The combination of several markers [88] and the availability of more exhaustive reference databases would allow a more accurate appreciation of species diversity. The eDNA approach, already widely used for species invento- ries, also seems to be a promising tool for localised studies to assess the impacts of anthropo- genic disturbance on biodiversity, such as dams, factories or mines, but also for carrying out a rapid census of biodiversity on more extensive regional scales. Ecological and conservation studies will require the complementarity of traditional sampling approaches to provide infor- mation on recruitment, age, size and precise abundance, as well as to identify the specimens needed to complete the DNA reference databases. Nevertheless, eDNA approaches to access large-scale species inventories in a rapid and non-destructive manner can complement these studies. Quantitative approaches based on eDNA sampling are being developed using qPCR or digital PCR techniques, in order to gain access to relative biomasses [89, 90]. Although many technical or biological biases still need to be overcome, access to biomass would provide infor- mation on the demographic patterns of species required to put in place conservation strategies essential for sustainable ecosystem management. Fishes are among the freshwater biota most
threatened by global changes [91, 92]. The evolution of fish biodiversity in the Tuichi study area could be monitored over several years in relation to climate change and dynamic anthro- pogenic threats in the region, and serve as a reference for the study of other river basins in the Amazon. Supporting information S1 Fig. Rarefaction curves at library and site level. (PDF) S2 Fig. Frequency spectrum of taxa. (PDF) S3 Fig. Taxonomic diversity at order level per site. (PDF) PLOS ONE Fish diversity and distribution in the Tuichi basin PLOS ONE | https://doi.org/10.1371/journal.pone.0262357 January 4, 2022 19 / 25
S4 Fig. NMDS ordination (site names plotted). (PDF) S5 Fig. NMDS ordination including all sites. Orders are split into different facets. (PDF) S6 Fig. Species dendrogram (binary Jaccard distance and Ward2 aggregation). (PDF) S1 Text. Scripts and command lines used for data analysis and plotting figures. (PDF) S2 Text. Assessment of the taxonomic resolution of markers used on Amazonian fish. (PDF) S1 Table. Informations on sites and points of collect (date, collected volume, depth, coor- dinates). (XLSX) S2 Table. COI fish database used (fasta file). (XLSX) S3 Table. Environmental variables (soils, altitude, coordinate, geology, richness, Jack2. . .). (XLSX) S4 Table. Sequencing results per library. (XLSX) S5 Table. Taxa abundance per library. (XLSX) S6 Table. Quality of assignation (%ID) and list of species assigned to affinis status. (XLSX) S7 Table. List of taxa present in each area of the Venn diagram constructed at the cluster level. (XLSX) Acknowledgments The authors acknowledge the IRD itrop HPC (South Green Platform) at IRD Montpellier for providing HPC resources that contributed to the research results reported within this paper (URL: https://bioinfo.ird.fr/- http://www.southgreen.fr). Author Contributions Conceptualization: Ce´dric Mariac, Fabrice Duponchelle, Jean-Franc¸ois Renno. Formal analysis: Ce´dric Mariac, Fabrice Duponchelle, Jean-Franc¸ois Renno. Methodology: Ce´dric Mariac, Guido Miranda, Camila Ramallo, Gabriel Tarifa, Jean-Franc¸ois Renno. Validation: Ce´dric Mariac. Writing – original draft: Ce´dric Mariac, Fabrice Duponchelle, Jean-Franc¸ois Renno.
PLOS ONE Fish diversity and distribution in the Tuichi basin PLOS ONE | https://doi.org/10.1371/journal.pone.0262357 January 4, 2022 20 / 25
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