Deforestation strengthens environmental filtering and competitive exclusion in Neotropical streams and rivers.

Understanding how anthropization impacts the assembly of species onto communities is pivotal to go beyond the observation of biodiversity changes and reveal how disturbances affect the environmental and biotic processes shaping biodiversity. Here, we propose a simple framework to measure the assembly processes underpinning functional convergence/divergence patterns. We applied this framework to northern Amazonian fish communities inventoried using environmental DNA in 35 stream sites and 64 river sites. We found that the harsh and unstable environmental conditions characterizing streams conveyed communities towards functional convergence, by filtering traits related to food acquisition and, to a lower extent, dispersal. Such environmental filtering also strengthened competition by excluding species having less competitive food acquisition traits. Instead, random species assembly was more marked in river communities, which may be explained by the downstream position of rivers facilitating the dispersion of species. Although fish assembly rules differed between streams and river fish communities, anthropogenic disturbances reduced functional divergence in both ecosystems, with a reinforcement of both environmental filtering and weaker competitor exclusion. This may explain the substantial biodiversity alterations observed under slight deforestation levels in Neotropical freshwater ecosystems and underlines their vulnerability to anthropic disturbances that not only affect species persistence but also modify community assembly rules.

Environmental DNA reveals a mismatch between diversity facets of Amazonian fishes in response to contrasting geographical, environmental and anthropogenic effects.

Freshwater ecosystems are among the most endangered ecosystem in the world. Understanding how human activities affect these ecosystems requires disentangling and quantifying the contribution of the factors driving community assembly. While it has been largely studied in temperate freshwaters, tropical ecosystems remain challenging to study due to the high species richness and the lack of knowledge on species distribution. Here, the use of eDNA-based fish inventories combined to a community-level modelling approach allowed depicting of assembly rules and quantifying the relative contribution of geographic, environmental and anthropic factors to fish assembly. We then used the model predictions to map spatial biodiversity and assess the representativity of sites surveyed in French Guiana within the EU Water Framework Directive (WFD) and highlighted areas that should host unique freshwater fish assemblages. We demonstrated a mismatch between the taxonomic and functional diversity. Taxonomic assemblages between but also within basins were mainly the results of dispersal limitation resulting from basin isolation and natural river barriers. Contrastingly, functional assemblages were ruled by environmental and anthropic factors. The regional mapping of fish diversity indicated that the sites surveyed within the EU WFD had a better representativity of the regional functional diversity than taxonomic diversity. Importantly, we also showed that the assemblages expected to be the most altered by anthropic factors were the most poorly represented in terms of functional diversity in the surveyed sites. The predictions of unique functional and taxonomic assemblages could, therefore, guide the establishment of new survey sites to increase fish diversity representativity and improve this monitoring program.

Boosting freshwater fish conservation with high-resolution distribution mapping across a large territory.

The lack of high-resolution distribution maps for freshwater species across large extents fundamentally challenges biodiversity conservation worldwide. We devised a simple framework to delineate the distributions of freshwater fishes in a high-resolution drainage map based on stacked species distribution models and expert information. We applied this framework to the entire Chinese freshwater fish fauna (>1600 species) to examine high-resolution biodiversity patterns and reveal potential conflicts between freshwater biodiversity and anthropogenic disturbances. The correlations between spatial patterns of biodiversity facets (species richness, endemicity, and phylogenetic diversity) were all significant (r = 0.43-0.98, p < 0.001). Areas with high values of different biodiversity facets overlapped with anthropogenic disturbances. Existing protected areas (PAs), covering 22% of China's territory, protected 25-29% of fish habitats, 16-23% of species, and 30-31% of priority conservation areas. Moreover, 6-21% of the species were completely unprotected. These results suggest the need for extending the network of PAs to ensure the conservation of China's freshwater fishes and the goods and services they provide. Specifically, middle to low reaches of large rivers and their associated lakes from northeast to southwest China hosted the most diverse species assemblages and thus should be the target of future expansions of the network of PAs. More generally, our framework, which can be used to draw high-resolution freshwater biodiversity maps combining species occurrence data and expert knowledge on species distribution, provides an efficient way to design PAs regardless of the ecosystem, taxonomic group, or region considered.

Potenciación de la conservación de peces de agua dulce con mapeos de distribución de alta resolución a lo largo de un territorio extenso Resumen La falta de mapas de distribución en alta resolución para las especies de agua dulce en grandes extensiones es un reto importante para la conservación mundial de la biodiversidad. Diseñamos un marco simple para delinear la distribución de los peces de agua dulce en un mapa de drenaje en alta resolución basado en los modelos apilados de la distribución de las especies y la información de expertos. Aplicamos este marco a toda la ictiofauna de agua dulce en China (>1600 especies) para analizar los patrones en alta resolución de la biodiversidad y revelar los conflictos potenciales entre la biodiversidad de agua dulce y las perturbaciones antropogénicas. Todas las correlaciones entre los patrones espaciales de las facetas de la biodiversidad (riqueza de especies, endemismo y diversidad filogenética) fueron importantes (r = 0.43-0.98, p < 0.001). Las áreas con valores altos de diferentes facetas de la biodiversidad se traslaparon con las perturbaciones antropogénicas. Las áreas protegidas existentes que actualmente cubren el 22% del territorio de China, protegen 25-2% del hábitat de los peces, 16-23% de las especies y 30-31% de las áreas de conservación prioritarias. Además, 6-21% de las especies se encontraban totalmente desprotegidas. Estos resultados sugieren que se necesita extender la red de áreas protegidas para asegurar la conservación de los peces de agua dulce de China y los bienes y servicios que proporcionan. En concreto, los niveles medio a bajo de los grandes ríos y sus lagos asociados del noreste al suroeste de China albergaron los ensambles de especies más diversos y por lo tanto deberían ser el objetivo de las futuras expansiones de la red de áreas protegidas. De forma más generalizada, nuestro marco, el cual puede usarse para trazar mapas en alta resolución de la biodiversidad de agua dulce al combinar los datos de presencia de las especies y el conocimiento de los expertos sobre su distribución, proporciona un método eficiente para diseñar las áreas protegidas sin importar el ecosistema, región o grupo taxonómico considerado.

Drainage network position and historical connectivity explain global patterns in freshwater fishes' range size.

Identifying the drivers and processes that determine globally the geographic range size of species is crucial to understanding the geographic distribution of biodiversity and further predicting the response of species to current global changes. However, these drivers and processes are still poorly understood, and no ecological explanation has emerged yet as preponderant in explaining the extent of species' geographical range. Here, we identify the main drivers of the geographic range size variation in freshwater fishes at global and biogeographic scales and determine how these drivers affect range size both directly and indirectly. We tested the main hypotheses already proposed to explain range size variation, using geographic ranges of 8,147 strictly freshwater fish species (i.e., 63% of all known species). We found that, contrary to terrestrial organisms, for which climate and topography seem preponderant in determining species' range size, the geographic range sizes of freshwater fishes are mostly explained by the species' position within the river network, and by the historical connection among river basins during Quaternary low-sea-level periods. Large-ranged fish species inhabit preferentially lowland areas of river basins, where hydrological connectivity is the highest, and also are found in river basins that were historically connected. The disproportionately high explanatory power of these two drivers suggests that connectivity is the key component of riverine fish geographic range sizes, independent of any other potential driver, and indicates that the accelerated rates in river fragmentation might strongly affect fish species distribution and freshwater biodiversity.

The combined effects of climate change and river fragmentation on the distribution of Andean Amazon fishes.

Upstream range shifts of freshwater fishes have been documented in recent years due to ongoing climate change. River fragmentation by dams, presenting physical barriers, can limit the climatically induced spatial redistribution of fishes. Andean freshwater ecosystems in the Neotropical region are expected to be highly affected by these future disturbances. However, proper evaluations are still missing. Combining species distribution models and functional traits of Andean Amazon fishes, coupled with dam locations and climatic projections (2070s), we (a) evaluated the potential impacts of future climate on species ranges, (b) investigated the combined impact of river fragmentation and climate change and (c) tested the relationships between these impacts and species functional traits. Results show that climate change will induce range contraction for most of the Andean Amazon fish species, particularly those inhabiting highlands. Dams are not predicted to greatly limit future range shifts for most species (i.e., the Barrier effect). However, some of these barriers should prevent upstream shifts for a considerable number of species, reducing future potential diversity in some basins. River fragmentation is predicted to act jointly with climate change in promoting a considerable decrease in the probability of species to persist in the long-term because of splitting species ranges in smaller fragments (i.e., the Isolation effect). Benthic and fast-flowing water adapted species with hydrodynamic bodies are significantly associated with severe range contractions from climate change.

Non-native species led to marked shifts in functional diversity of the world freshwater fish faunas.

Global spread of non-native species profoundly changed the world biodiversity patterns, but how it translates into functional changes remains unanswered at the world scale. We here show that while in two centuries the number of fish species per river increased on average by 15% in 1569 basins worldwide, the diversity of their functional attributes (i.e. functional richness) increased on average by 150%. The inflation of functional richness was paired with changes in the functional structure of assemblages, with shifts of species position toward the border of the functional space of assemblages (i.e. increased functional divergence). Non-native species moreover caused shifts in functional identity toward higher body sized and less elongated species for most of assemblages throughout the world. Although varying between rivers and biogeographic realms, such changes in the different facets of functional diversity might still increase in the future through increasing species invasion and may further modify ecosystem functioning.

A global database of nitrogen and phosphorus excretion rates of aquatic animals.

Animals can be important in modulating ecosystem-level nutrient cycling, although their importance varies greatly among species and ecosystems. Nutrient cycling rates of individual animals represent valuable data for testing the predictions of important frameworks such as the Metabolic Theory of Ecology (MTE) and ecological stoichiometry (ES). They also represent an important set of functional traits that may reflect both environmental and phylogenetic influences. Over the past two decades, studies of animal-mediated nutrient cycling have increased dramatically, especially in aquatic ecosystems. Here we present a global compilation of aquatic animal nutrient excretion rates. The dataset includes 10,534 observations from freshwater and marine animals of N and/or P excretion rates. These observations represent 491 species, including most aquatic phyla. Coverage varies greatly among phyla and other taxonomic levels. The dataset includes information on animal body size, ambient temperature, taxonomic affiliations, and animal body N:P. This data set was used to test predictions of MTE and ES, as described in Vanni and McIntyre (2016; Ecology DOI: 10.1002/ecy.1582).

Global imprint of historical connectivity on freshwater fish biodiversity.

The relative importance of contemporary and historical processes is central for understanding biodiversity patterns. While several studies show that past conditions can partly explain the current biodiversity patterns, the role of history remains elusive. We reconstructed palaeo-drainage basins under lower sea level conditions (Last Glacial Maximum) to test whether the historical connectivity between basins left an imprint on the global patterns of freshwater fish biodiversity. After controlling for contemporary and past environmental conditions, we found that palaeo-connected basins displayed greater species richness but lower levels of endemism and beta diversity than did palaeo-disconnected basins. Palaeo-connected basins exhibited shallower distance decay of compositional similarity, suggesting that palaeo-river connections favoured the exchange of fish species. Finally, we found that a longer period of palaeo-connection resulted in lower levels of beta diversity. These findings reveal the first unambiguous results of the role played by history in explaining the global contemporary patterns of biodiversity.

Homogenization patterns of the world's freshwater fish faunas.

The world is currently undergoing an unprecedented decline in biodiversity, which is mainly attributable to human activities. For instance, nonnative species introduction, combined with the extirpation of native species, affects biodiversity patterns, notably by increasing the similarity among species assemblages. This biodiversity change, called taxonomic homogenization, has rarely been assessed at the world scale. Here, we fill this gap by assessing the current homogenization status of one of the most diverse vertebrate groups (i.e., freshwater fishes) at global and regional scales. We demonstrate that current homogenization of the freshwater fish faunas is still low at the world scale (0.5%) but reaches substantial levels (up to 10%) in some highly invaded river basins from the Nearctic and Palearctic realms. In these realms experiencing high changes, nonnative species introductions rather than native species extirpations drive taxonomic homogenization. Our results suggest that the "Homogocene era" is not yet the case for freshwater fish fauna at the worldwide scale. However, the distressingly high level of homogenization noted for some biogeographical realms stresses the need for further understanding of the ecological consequences of homogenization processes.

Global diversity patterns and cross-taxa convergence in freshwater systems.

Whereas global patterns and predictors of species diversity are well known for numerous terrestrial taxa, our understanding of freshwater diversity patterns and their predictors is much more limited. Here, we examine spatial concordance in global diversity patterns for five freshwater taxa (i.e. aquatic mammals, aquatic birds, fishes, crayfish and aquatic amphibians) and investigate the environmental factors driving these patterns at the river drainage basin grain. We find that species richness and endemism patterns are significantly correlated among taxa. We also show that cross-taxon congruence patterns are often induced by common responses of taxa to their contemporary and historical environments (i.e. convergent patterns). Apart from some taxa distinctiveness (i.e. fishes), the 'climate/productivity' hypothesis is found to explain the greatest variance in species richness and endemism patterns, followed by factors related to the 'history/dispersion' and 'area/environmental heterogeneity' hypotheses. As aquatic amphibians display the highest levels of congruency with other taxa, this taxon appears to be a good 'surrogate' candidate for developing global freshwater conservation planning at the river drainage basin grain.

Species invasiveness and community invasibility of North American freshwater fish fauna revealed via trait-based analysis.

While biological invasions are recognized as a major threat to global biodiversity, determining non-native species' abilities to establish in new areas (species invasiveness) and the vulnerability of those areas to invasions (community invasibility) is challenging. Here, we use trait-based analysis to profile invasive species and quantify the community invasibility for >1,800 North American freshwater fish communities. We show that, in addition to effects attributed to propagule pressure caused by human intervention, species with higher fecundity, longer lifespan and larger size tend to be more invasive. Community invasibility peaks when the functional distance among native species was high, leaving unoccupied functional space for the establishment of potential invaders. Our findings illustrate how the functional traits of non-native species determining their invasiveness, and the functional characteristics of the invaded community determining its invasibility, may be identified. Considering those two determinants together will enable better predictions of invasions.

Characterizing the spatial signal of environmental DNA in river systems using a community ecology approach.

Environmental DNA (eDNA) is gaining a growing popularity among scientists but its applicability to biodiversity research and management remains limited in river systems by the lack of knowledge about the spatial extent of the downstream transport of eDNA. Here, we assessed the ability of eDNA inventories to retrieve spatial patterns of fish assemblages along two large and species-rich Neotropical rivers. We first examined overall community variation with distance through the distance decay of similarity and compared this pattern to capture-based samples. We then considered previous knowledge on individual species distributions, and compared it to the eDNA inventories for a set of 53 species. eDNA collected from 28 sites in the Maroni and 25 sites in the Oyapock rivers permitted to retrieve a decline of species similarity with increasing distance between sites. The distance decay of similarity derived from eDNA was similar and even more pronounced than that obtained with capture-based methods (gill-nets). In addition, the species upstream-downstream distribution range derived from eDNA matched to the known distribution of most species. Our results demonstrate that environmental DNA does not represent an integrative measure of biodiversity across the whole upstream river basin but provides a relevant picture of local fish assemblages. Importantly, the spatial signal gathered from eDNA was therefore comparable to that gathered with local capture-based methods, which describes fish fauna over a few hundred metres.

Low level of anthropization linked to harsh vertebrate biodiversity declines in Amazonia.

Assessing the impact of human activity on ecosystems often links local biodiversity to disturbances measured within the same locality. However, remote disturbances may also affect local biodiversity. Here, we used environmental DNA metabarcoding to evaluate the relationships between vertebrate biodiversity (fish and mammals) and disturbance intensity in two Amazonian rivers. Measurements of anthropic disturbance -here forest cover losses- were made from the immediate vicinity of the biodiversity sampling sites to up to 90 km upstream. The findings suggest that anthropization had a spatially extended impact on biodiversity. Forest cover losses of <11% in areas up to 30 km upstream from the biodiversity sampling sites were linked to reductions of >22% in taxonomic and functional richness of both terrestrial and aquatic fauna. This underscores the vulnerability of Amazonian biodiversity even to low anthropization levels. The similar responses of aquatic and terrestrial fauna to remote disturbances indicate the need for cross-ecosystem conservation plans that consider the spatially extended effects of anthropization.

Applying convolutional neural networks to speed up environmental DNA annotation in a highly diverse ecosystem.

High-throughput DNA sequencing is becoming an increasingly important tool to monitor and better understand biodiversity responses to environmental changes in a standardized and reproducible way. Environmental DNA (eDNA) from organisms can be captured in ecosystem samples and sequenced using metabarcoding, but processing large volumes of eDNA data and annotating sequences to recognized taxa remains computationally expensive. Speed and accuracy are two major bottlenecks in this critical step. Here, we evaluated the ability of convolutional neural networks (CNNs) to process short eDNA sequences and associate them with taxonomic labels. Using a unique eDNA data set collected in highly diverse Tropical South America, we compared the speed and accuracy of CNNs with that of a well-known bioinformatic pipeline (OBITools) in processing a small region (60 bp) of the 12S ribosomal DNA targeting freshwater fishes. We found that the taxonomic labels from the CNNs were comparable to those from OBITools, with high correlation levels for the composition of the regional fish fauna. The CNNs enabled the processing of raw fastq files at a rate of approximately 1 million sequences per minute, which was about 150 times faster than with OBITools. Given the good performance of CNNs in the highly diverse ecosystem considered here, the development of more elaborate CNNs promises fast deployment for future biodiversity inventories using eDNA.

Partitioning global patterns of freshwater fish beta diversity reveals contrasting signatures of past climate changes.

Here, we employ an additive partitioning framework to disentangle the contribution of spatial turnover and nestedness to beta diversity patterns in the global freshwater fish fauna. We find that spatial turnover and nestedness differ geographically in their contribution to freshwater fish beta diversity, a pattern that results from contrasting influences of Quaternary climate changes. Differences in fish faunas characterized by nestedness are greater in drainage basins that experienced larger amplitudes of Quaternary climate oscillations. Conversely, higher levels of spatial turnover are found in historically unglaciated drainage basins with high topographic relief, these having experienced greater Quaternary climate stability. Such an historical climate signature is not clearly detected when considering the overall level of beta diversity. Quantifying the relative roles of historical and ecological factors in explaining present-day patterns of beta diversity hence requires considering the different processes generating these patterns and not solely the overall level of beta diversity.

Fish invasions in the world's river systems: when natural processes are blurred by human activities.

Because species invasions are a principal driver of the human-induced biodiversity crisis, the identification of the major determinants of global invasions is a prerequisite for adopting sound conservation policies. Three major hypotheses, which are not necessarily mutually exclusive, have been proposed to explain the establishment of non-native species: the "human activity" hypothesis, which argues that human activities facilitate the establishment of non-native species by disturbing natural landscapes and by increasing propagule pressure; the "biotic resistance" hypothesis, predicting that species-rich communities will readily impede the establishment of non-native species; and the "biotic acceptance" hypothesis, predicting that environmentally suitable habitats for native species are also suitable for non-native species. We tested these hypotheses and report here a global map of fish invasions (i.e., the number of non-native fish species established per river basin) using an original worldwide dataset of freshwater fish occurrences, environmental variables, and human activity indicators for 1,055 river basins covering more than 80% of Earth's surface. First, we identified six major invasion hotspots where non-native species represent more than a quarter of the total number of species. According to the World Conservation Union, these areas are also characterised by the highest proportion of threatened fish species. Second, we show that the human activity indicators account for most of the global variation in non-native species richness, which is highly consistent with the "human activity" hypothesis. In contrast, our results do not provide support for either the "biotic acceptance" or the "biotic resistance" hypothesis. We show that the biogeography of fish invasions matches the geography of human impact at the global scale, which means that natural processes are blurred by human activities in driving fish invasions in the world's river systems. In view of our findings, we fear massive invasions in developing countries with a growing economy as already experienced in developed countries. Anticipating such potential biodiversity threats should therefore be a priority.

Extinction of threatened vertebrates will lead to idiosyncratic changes in functional diversity across the world.

Although species with larger body size and slow pace of life have a higher risk of extinction at a global scale, it is unclear whether this global trend will be consistent across biogeographic realms. Here we measure the functional diversity of terrestrial and freshwater vertebrates in the six terrestrial biogeographic realms and predict their future changes through scenarios mimicking a gradient of extinction risk of threatened species. We show vastly different effects of extinctions on functional diversity between taxonomic groups and realms, ranging from almost no decline to deep functional losses. The Indo-Malay and Palearctic realms are particularly inclined to experience a drastic loss of functional diversity reaching 29 and 31%, respectively. Birds, mammals, and reptiles regionally display a consistent functional diversity loss, while the projected losses of amphibians and freshwater fishes differ across realms. More efficient global conservation policies should consider marked regional losses of functional diversity across the world.

Human impacts on global freshwater fish biodiversity.

Freshwater fish represent one-fourth of the world's vertebrates and provide irreplaceable goods and services but are increasingly affected by human activities. A new index, Cumulative Change in Biodiversity Facets, revealed marked changes in biodiversity in >50% of the world's rivers covering >40% of the world's continental surface and >37% of the world's river length, whereas <14% of the world's surface and river length remain least impacted. Present-day rivers are more similar to each other and have more fish species with more diverse morphologies and longer evolutionary legacies. In temperate rivers, where the impact has been greatest, biodiversity changes were primarily due to river fragmentation and introduction of non-native species.

Amazonian mammal monitoring using aquatic environmental DNA.

Environmental DNA (eDNA) metabarcoding has emerged as one of the most efficient methods to assess aquatic species presence. While the method can in theory be used to investigate nonaquatic fauna, its development for inventorying semi-aquatic and terrestrial fauna is still at an early stage. Here we investigated the potential of aquatic eDNA metabarcoding for inventorying mammals in Neotropical environments, be they aquatic, semi-aquatic or terrestrial. We collected aquatic eDNA in 96 sites distributed along three Guianese watersheds and compared our inventories to expected species distributions and field observations derived from line transects located throughout French Guiana. Species occurrences and emblematic mammalian fauna richness patterns were consistent with the expected distribution of fauna and our results revealed that aquatic eDNA metabarcoding brings additional data to line transect samples for diurnal nonaquatic (terrestrial and arboreal) species. Aquatic eDNA also provided data on species not detectable in line transect surveys such as semi-aquatic, aquatic and nocturnal terrestrial and arboreal species. Although the application of eDNA to inventory mammals still needs some developments to optimize sampling efficiency, it can now be used as a complement to traditional surveys.

Erosion of global functional diversity across the tree of life.

Although one-quarter of plant and vertebrate species are threatened with extinction, little is known about the potential effect of extinctions on the global diversity of ecological strategies. Using trait and phylogenetic information for more than 75,000 species of vascular plants, mammals, birds, reptiles, amphibians, and freshwater fish, we characterized the global functional spectra of each of these groups. Mapping extinction risk within these spectra showed that larger species with slower pace of life are universally threatened. Simulated extinction scenarios exposed extensive internal reorganizations in the global functional spectra, which were larger than expected by chance for all groups, and particularly severe for mammals and amphibians. Considering the disproportionate importance of the largest species for ecological processes, our results emphasize the importance of actions to prevent the extinction of the megabiota.