Diversity across organisational scale emerges through dispersal ability and speciation dynamics in tropical fish.

BACKGROUND: Biodiversity exists at different levels of organisation: e.g. genetic, individual, population, species, and community. These levels of organisation all exist within the same system, with diversity patterns emerging across organisational scales through several key processes. Despite this inherent interconnectivity, observational studies reveal that diversity patterns across levels are not consistent and the underlying mechanisms for variable continuity in diversity across levels remain elusive. To investigate these mechanisms, we apply a spatially explicit simulation model to simulate the global diversification of tropical reef fishes at both the population and species levels through emergent population-level processes. RESULTS: We find significant relationships between the population and species levels of diversity which vary depending on both the measure of diversity and the spatial partitioning considered. In turn, these population-species relationships are driven by modelled biological trait parameters, especially the divergence threshold at which populations speciate. CONCLUSIONS: To explain variation in multi-level diversity patterns, we propose a simple, yet novel, population-to-species diversity partitioning mechanism through speciation which disrupts continuous diversity patterns across organisational levels. We expect that in real-world systems this mechanism is driven by the molecular dynamics that determine genetic incompatibility, and therefore reproductive isolation between individuals. We put forward a framework in which the mechanisms underlying patterns of diversity across organisational levels are universal, and through this show how variable patterns of diversity can emerge through organisational scale.

Catchment-based sampling of river eDNA integrates terrestrial and aquatic biodiversity of alpine landscapes.

Monitoring of terrestrial and aquatic species assemblages at large spatial scales based on environmental DNA (eDNA) has the potential to enable evidence-based environmental policymaking. The spatial coverage of eDNA-based studies varies substantially, and the ability of eDNA metabarcoding to capture regional biodiversity remains to be assessed; thus, questions about best practices in the sampling design of entire landscapes remain open. We tested the extent to which eDNA sampling can capture the diversity of a region with highly heterogeneous habitat patches across a wide elevation gradient for five days through multiple hydrological catchments of the Swiss Alps. Using peristaltic pumps, we filtered 60 L of water at five sites per catchment for a total volume of 1800 L. Using an eDNA metabarcoding approach focusing on vertebrates and plants, we detected 86 vertebrate taxa spanning 41 families and 263 plant taxa spanning 79 families across ten catchments. For mammals, fishes, amphibians and plants, the detected taxa covered some of the most common species in the region according to long-term records while including a few more rare taxa. We found marked turnover among samples from distinct elevational classes indicating that the biological signal in alpine rivers remains relatively localised and is not aggregated downstream. Accordingly, species compositions differed between catchments and correlated with catchment-level forest and grassland cover. Biomonitoring schemes based on capturing eDNA across rivers within biologically integrated catchments may pave the way toward a spatially comprehensive estimation of biodiversity.

Long-term changes in temperate marine fish assemblages are driven by a small subset of species.

The species composition of plant and animal assemblages across the globe has changed substantially over the past century. How do the dynamics of individual species cause this change? We classified species into seven unique categories of temporal dynamics based on the ordered sequence of presences and absences that each species contributes to an assemblage time series. We applied this framework to 14,434 species trajectories comprising 280 assemblages of temperate marine fishes surveyed annually for 20 or more years. Although 90% of the assemblages diverged in species composition from the baseline year, this compositional change was largely driven by only 8% of the species' trajectories. Quantifying the reorganization of assemblages based on species shared temporal dynamics should facilitate the task of monitoring and restoring biodiversity. We suggest ways in which our framework could provide informative measures of compositional change, as well as leverage future research on pattern and process in ecological systems.

The shape of abundance distributions across temperature gradients in reef fishes.

Improving predictions of ecological responses to climate change requires understanding how local abundance relates to temperature gradients, yet many factors influence local abundance in wild populations. We evaluated the shape of thermal-abundance distributions using 98 422 abundance estimates of 702 reef fish species worldwide. We found that curved ceilings in local abundance related to sea temperatures for most species, where local abundance declined from realised thermal 'optima' towards warmer and cooler environments. Although generally supporting the abundant-centre hypothesis, many species also displayed asymmetrical thermal-abundance distributions. For many tropical species, abundances did not decline at warm distribution edges due to an unavailability of warmer environments at the equator. Habitat transitions from coral to macroalgal dominance in subtropical zones also influenced abundance distribution shapes. By quantifying the factors constraining species' abundance, we provide an important empirical basis for improving predictions of community re-structuring in a warmer world.

Temperature-Driven Biodiversity Change: Disentangling Space and Time.

Temperature regimes have multiple spatial and temporal dimensions that have different impacts on biodiversity. Signatures of warming across these dimensions may contribute uniquely to the large-scale species redistributions and abundance changes that underpin community dynamics. A comprehensive review of the literature reveals that 86% of studies were focused on community responses to temperature aggregated over spatial or temporal dimensions (e.g., mean, median, or extremes). Therefore, the effects of temperature variation in space and time on biodiversity remain generally unquantified. In the present article, we argue that this focus on aggregated temperature measures may limit advancing our understanding of how communities are being altered by climate change. In light of this, we map the cause-and-effect pathways between the different dimensions of temperature change and communities in space and time. A broadened focus, shifted toward a multidimensional perspective of temperature, will allow better interpretation and prediction of biodiversity change and more robust management and conservation strategies.

Deconstructing the geography of human impacts on species' natural distribution.

It remains unknown how species' populations across their geographic range are constrained by multiple coincident natural and anthropogenic environmental gradients. Conservation actions are likely undermined without this knowledge because the relative importance of the multiple anthropogenic threats is not set within the context of the natural determinants of species' distributions. We introduce the concept of a species 'shadow distribution' to address this knowledge gap, using explainable artificial intelligence to deconstruct the environmental building blocks of current species distributions. We assess shadow distributions for multiple threatened freshwater fishes in Switzerland which indicated how and where species respond negatively to threats - with negative threat impacts covering 88% of locations inside species' environmental niches leading to a 25% reduction in environmental suitability. Our findings highlight that conservation of species' geographic distributions is likely insufficient when biodiversity mapping is based on species distribution models, or threat mapping, without also quantifying species' expected or shadow distributions. Overall, we show how priority actions for nature's recovery can be identified and contextualised within the multiple natural constraints on biodiversity to better meet national and international biodiversity targets.

Neglecting biodiversity baselines in longitudinal river connectivity restoration impacts priority setting.

River habitats are fragmented by barriers which impede the movement and dispersal of aquatic organisms. Restoring habitat connectivity is a primary objective of nature conservation plans with multiple efforts to strategically restore connectivity at local, regional, and global scales. However, current approaches to prioritize connectivity restoration do not typically consider how barriers spatially fragment species' populations. Additionally, we lack knowledge on biodiversity baselines to predict which species would find suitable habitat after restoring connectivity. In this paper, we asked how neglecting these biodiversity baselines in river barrier removals impacts priority setting for conservation planning. We applied a novel modelling approach combining predictions of species distributions with network connectivity models to prioritize conservation actions in rivers of the Rhine-Aare system in Switzerland. Our results show that the high number and density of barriers has reduced structural and functional connectivity across representative catchments within the system. We show that fragmentation decreases habitat suitability for species and that using expected distributions as biodiversity baselines significantly affects priority settings for connectivity restorations compared to species-agnostic metrics based on river length. This indicates that priorities for barrier removals are ranked higher within the expected distributions of species to maximize functional connectivity while barriers in unsuitable regions are given lower importance scores. Our work highlights that the joint consideration of existing barriers and species past and current distributions are critical for restoration plans to ensure the recovery and persistence of riverine fish diversity.

Environmental DNA recovers fish composition turnover of the coral reefs of West Indian Ocean islands.

Islands have been used as model systems to study ecological and evolutionary processes, and they provide an ideal set-up for validating new biodiversity monitoring methods. The application of environmental DNA metabarcoding for monitoring marine biodiversity requires an understanding of the spatial scale of the eDNA signal, which is best tested in island systems. Here, we investigated the variation in Actinopterygii and Elasmobranchii species composition recovered from eDNA metabarcoding along a gradient of distance-to-reef in four of the five French Scattered Islands in the Western Indian Ocean. We collected surface water samples at an increasing distance from reefs (0 m, 250 m, 500 m, 750 m). We used a metabarcoding protocol based on the 'teleo' primers to target marine reef fishes and classified taxa according to their habitat types (benthic or pelagic). We investigated the effect of distance-to-reef on ß diversity variation using generalised linear mixed models and estimated species-specific distance-to-reef effects using a model-based approach for community data. Environmental DNA metabarcoding analyses recovered distinct fish species compositions across the four inventoried islands and variations along the distance-to-reef gradient. The analysis of ß-diversity variation showed significant taxa turnover between the eDNA samples on and away from the reefs. In agreement with a spatially localised signal from eDNA, benthic species were distributed closer to the reef than pelagic ones. Our findings demonstrate that the combination of eDNA inventories and spatial modelling can provide insights into species habitat preferences related to distance-to-reef gradients at a small scale. As such, eDNA can not only recover large compositional differences among islands but also help understand habitat selection and distribution of marine species at a finer spatial scale.

A functional vulnerability framework for biodiversity conservation.

Setting appropriate conservation strategies in a multi-threat world is a challenging goal, especially because of natural complexity and budget limitations that prevent effective management of all ecosystems. Safeguarding the most threatened ecosystems requires accurate and integrative quantification of their vulnerability and their functioning, particularly the potential loss of species trait diversity which imperils their functioning. However, the magnitude of threats and associated biological responses both have high uncertainties. Additionally, a major difficulty is the recurrent lack of reference conditions for a fair and operational measurement of vulnerability. Here, we present a functional vulnerability framework that incorporates uncertainty and reference conditions into a generalizable tool. Through in silico simulations of disturbances, our framework allows us to quantify the vulnerability of communities to a wide range of threats. We demonstrate the relevance and operationality of our framework, and its global, scalable and quantitative comparability, through three case studies on marine fishes and mammals. We show that functional vulnerability has marked geographic and temporal patterns. We underline contrasting contributions of species richness and functional redundancy to the level of vulnerability among case studies, indicating that our integrative assessment can also identify the drivers of vulnerability in a world where uncertainty is omnipresent.

Fish heating tolerance scales similarly across individual physiology and populations.

Extrapolating patterns from individuals to populations informs climate vulnerability models, yet biological responses to warming are uncertain at both levels. Here we contrast data on the heating tolerances of fishes from laboratory experiments with abundance patterns of wild populations. We find that heating tolerances in terms of individual physiologies in the lab and abundance in the wild decline with increasing temperature at the same rate. However, at a given acclimation temperature or optimum temperature, tropical individuals and populations have broader heating tolerances than temperate ones. These congruent relationships implicate a tight coupling between physiological and demographic processes underpinning macroecological patterns, and identify vulnerability in both temperate and tropical species.

Species richness and identity both determine the biomass of global reef fish communities.

Changing biodiversity alters ecosystem functioning in nature, but the degree to which this relationship depends on the taxonomic identities rather than the number of species remains untested at broad scales. Here, we partition the effects of declining species richness and changing community composition on fish community biomass across >3000 coral and rocky reef sites globally. We find that high biodiversity is 5.7x more important in maximizing biomass than the remaining influence of other ecological and environmental factors. Differences in fish community biomass across space are equally driven by both reductions in the total number of species and the disproportionate loss of larger-than-average species, which is exacerbated at sites impacted by humans. Our results confirm that sustaining biomass and associated ecosystem functions requires protecting diversity, most importantly of multiple large-bodied species in areas subject to strong human influences.

How many replicates to accurately estimate fish biodiversity using environmental DNA on coral reefs?

Quantifying fish species diversity in rich tropical marine environments remains challenging. Environmental DNA (eDNA) metabarcoding is a promising tool to face this challenge through the filtering, amplification, and sequencing of DNA traces from water samples. However, because eDNA concentration is low in marine environments, the reliability of eDNA to detect species diversity can be limited. Using an eDNA metabarcoding approach to identify fish Molecular Taxonomic Units (MOTUs) with a single 12S marker, we aimed to assess how the number of sampling replicates and filtered water volume affect biodiversity estimates. We used a paired sampling design of 30 L per replicate on 68 reef transects from 8 sites in 3 tropical regions. We quantified local and regional sampling variability by comparing MOTU richness, compositional turnover, and compositional nestedness. We found strong turnover of MOTUs between replicated pairs of samples undertaken in the same location, time, and conditions. Paired samples contained non-overlapping assemblages rather than subsets of one another. As a result, non-saturated localized diversity accumulation curves suggest that even 6 replicates (180 L) in the same location can underestimate local diversity (for an area <1 km). However, sampling regional diversity using ~25 replicates in variable locations (often covering 10 s of km) often saturated biodiversity accumulation curves. Our results demonstrate variability of diversity estimates possibly arising from heterogeneous distribution of eDNA in seawater, highly skewed frequencies of eDNA traces per MOTU, in addition to variability in eDNA processing. This high compositional variability has consequences for using eDNA to monitor temporal and spatial biodiversity changes in local assemblages. Avoiding false-negative detections in future biomonitoring efforts requires increasing replicates or sampled water volume to better inform management of marine biodiversity using eDNA.

Temperature-related biodiversity change across temperate marine and terrestrial systems.

Climate change is reshaping global biodiversity as species respond to changing temperatures. However, the net effects of climate-driven species redistribution on local assemblage diversity remain unknown. Here, we relate trends in species richness and abundance from 21,500 terrestrial and marine assemblage time series across temperate regions (23.5-60.0° latitude) to changes in air or sea surface temperature. We find a strong coupling between biodiversity and temperature changes in the marine realm, where species richness mostly increases with warming. However, biodiversity responses are conditional on the baseline climate, such that in initially warmer locations richness increase is more pronounced while abundance declines with warming. In contrast, we do not detect systematic temperature-related richness or abundance trends on land, despite a greater magnitude of warming. As the world is committed to further warming, substantial challenges remain in maintaining local biodiversity amongst the non-uniform inflow and outflow of 'climate migrants'. Temperature-driven community restructuring is especially evident in the ocean, whereas climatic debt may be accumulating on land.

The geography of biodiversity change in marine and terrestrial assemblages.

Human activities are fundamentally altering biodiversity. Projections of declines at the global scale are contrasted by highly variable trends at local scales, suggesting that biodiversity change may be spatially structured. Here, we examined spatial variation in species richness and composition change using more than 50,000 biodiversity time series from 239 studies and found clear geographic variation in biodiversity change. Rapid compositional change is prevalent, with marine biomes exceeding and terrestrial biomes trailing the overall trend. Assemblage richness is not changing on average, although locations exhibiting increasing and decreasing trends of up to about 20% per year were found in some marine studies. At local scales, widespread compositional reorganization is most often decoupled from richness change, and biodiversity change is strongest and most variable in the oceans.