Biological invasions are a population-level rather than a species-level phenomenon.

Biological invasions pose a rapidly expanding threat to the persistence, functioning and service provisioning of ecosystems globally, and to socio-economic interests. The stages of successful invasions are driven by the same mechanism that underlies adaptive changes across species in general-via natural selection on intraspecific variation in traits that influence survival and reproductive performance (i.e., fitness). Surprisingly, however, the rapid progress in the field of invasion science has resulted in a predominance of species-level approaches (such as deny lists), often irrespective of natural selection theory, local adaptation and other population-level processes that govern successful invasions. To address these issues, we analyse non-native species dynamics at the population level by employing a database of European freshwater macroinvertebrate time series, to investigate spreading speed, abundance dynamics and impact assessments among populations. Our findings reveal substantial variability in spreading speed and abundance trends within and between macroinvertebrate species across biogeographic regions, indicating that levels of invasiveness and impact differ markedly. Discrepancies and inconsistencies among species-level risk screenings and real population-level data were also identified, highlighting the inherent challenges in accurately assessing population-level effects through species-level assessments. In recognition of the importance of population-level assessments, we urge a shift in invasive species management frameworks, which should account for the dynamics of different populations and their environmental context. Adopting an adaptive, region-specific and population-focused approach is imperative, considering the diverse ecological contexts and varying degrees of susceptibility. Such an approach could improve and refine risk assessments while promoting mechanistic understandings of risks and impacts, thereby enabling the development of more effective conservation and management strategies.

Economic impact disharmony in global biological invasions.

A dominant syndrome of the Anthropocene is the rapid worldwide spread of invasive species with devastating environmental and socio-economic impacts. However, the dynamics underlying the impacts of biological invasions remain contested. A hypothesis posits that the richness of impactful invasive species increases proportionally with the richness of non-native species more generally. A competing hypothesis suggests that certain species features disproportionately enhance the chances of non-native species becoming impactful, causing invasive species to arise disproportionately relative to the numbers of non-native species. We test whether invasive species with reported monetary costs reflect global numbers of established non-native species among phyla, classes, and families. Our results reveal that numbers of invasive species with economic costs largely reflect non-native species richness among taxa (i.e., in 96 % of families). However, a few costly taxa were over- and under-represented, and their composition differed among environments and regions. Chordates, nematodes, and pathogenic groups tended to be the most over-represented phyla with reported monetary costs, with mammals, insects, fungi, roundworms, and medically-important microorganisms being over-represented classes. Numbers of costly invasive species increased significantly with non-native richness per taxon, while monetary cost magnitudes at the family level were also significantly related to costly invasive species richness. Costs were biased towards a few 'hyper-costly' taxa (such as termites, mosquitoes, cats, weevils, rodents, ants, and asters). Ordination analysis revealed significant dissimilarity between non-native and costly invasive taxon assemblages. These results highlight taxonomic groups which harbour disproportionately high numbers of costly invasive species and monetary cost magnitudes. Collectively, our findings support prevention of arrival and containment of spread of non-native species as a whole through effective strategies for mitigation of the rapidly amplifying impacts of invasive species. Yet, the hyper- costly taxa identified here should receive greater focus from managers to reduce impacts of current invasive species.

More losers than winners: investigating Anthropocene defaunation through the diversity of population trends.

The global-scale decline of animal biodiversity ('defaunation') represents one of the most alarming consequences of human impacts on the planet. The quantification of this extinction crisis has traditionally relied on the use of IUCN Red List conservation categories assigned to each assessed species. This approach reveals that a quarter of the world's animal species are currently threatened with extinction, and ~1% have been declared extinct. However, extinctions are preceded by progressive population declines through time that leave demographic 'footprints' that can alert us about the trajectories of species towards extinction. Therefore, an exclusive focus on IUCN conservation categories, without consideration of dynamic population trends, may underestimate the true extent of the processes of ongoing extinctions across nature. In fact, emerging evidence (e.g. the Living Planet Report), reveals a widespread tendency for sustained demographic declines (an average 69% decline in population abundances) of species globally. Yet, animal species are not only declining. Many species worldwide exhibit stable populations, while others are even thriving. Here, using population trend data for >71,000 animal species spanning all five groups of vertebrates (mammals, birds, reptiles, amphibians and fishes) and insects, we provide a comprehensive global-scale assessment of the diversity of population trends across species undergoing not only declines, but also population stability and increases. We show a widespread global erosion of species, with 48% undergoing declines, while 49% and 3% of species currently remain stable or are increasing, respectively. Geographically, we reveal an intriguing pattern similar to that of threatened species, whereby declines tend to concentrate around tropical regions, whereas stability and increases show a tendency to expand towards temperate climates. Importantly, we find that for species currently classed by the IUCN Red List as 'non-threatened', 33% are declining. Critically, in contrast with previous mass extinction events, our assessment shows that the Anthropocene extinction crisis is undergoing a rapid biodiversity imbalance, with levels of declines (a symptom of extinction) greatly exceeding levels of increases (a symptom of ecological expansion and potentially of evolution) for all groups. Our study contributes a further signal indicating that global biodiversity is entering a mass extinction, with ecosystem heterogeneity and functioning, biodiversity persistence, and human well-being under increasing threat.

Global Protected Areas as refuges for amphibians and reptiles under climate change.

Protected Areas (PAs) are the cornerstone of biodiversity conservation. Here, we collated distributional data for >14,000 (~70% of) species of amphibians and reptiles (herpetofauna) to perform a global assessment of the conservation effectiveness of PAs using species distribution models. Our analyses reveal that >91% of herpetofauna species are currently distributed in PAs, and that this proportion will remain unaltered under future climate change. Indeed, loss of species' distributional ranges will be lower inside PAs than outside them. Therefore, the proportion of effectively protected species is predicted to increase. However, over 7.8% of species currently occur outside PAs, and large spatial conservation gaps remain, mainly across tropical and subtropical moist broadleaf forests, and across non-high-income countries. We also predict that more than 300 amphibian and 500 reptile species may go extinct under climate change over the course of the ongoing century. Our study highlights the importance of PAs in providing herpetofauna with refuge from climate change, and suggests ways to optimize PAs to better conserve biodiversity worldwide.

The relative influence of sea surface temperature anomalies on the benthic composition of an Indo-Pacific and Caribbean coral reef over the last decade.

Rising ocean temperatures are the primary driver of coral reef declines throughout the tropics. Such declines include reductions in coral cover that facilitate the monopolization of the benthos by other taxa such as macroalgae, resulting in reduced habitat complexity and biodiversity. Long-term monitoring projects present rare opportunities to assess how sea surface temperature anomalies (SSTAs) influence changes in the benthic composition of coral reefs across distinct locations. Here, using extensively monitored coral reef sites from Honduras (in the Caribbean Sea), and from the Wakatobi National Park located in the center of the coral triangle of Indonesia, we assess the impact of global warming on coral reef benthic compositions over the period 2012-2019. Bayesian generalized linear mixed effect models revealed increases in the sponge, and hard coral coverage through time, while rubble coverage decreased at the Indonesia location. Conversely, the effect of SSTAs did not predict any changes in benthic coverage. At the Honduras location, algae and soft coral coverage increased through time, while hard coral and rock coverage were decreasing. The effects of SSTA at the Honduras location included increased rock coverage, but reduced sponge coverage, indicating disparate responses between both systems under SSTAs. However, redundancy analyses showed intralocation site variability explained the majority of variance in benthic composition over the course of the study period. Our findings show that SSTAs have differentially influenced the benthic composition between the Honduras and the Indonesian coral reefs surveyed in this study. However, the large intralocation variance that explains the benthic composition at both locations indicates that localized processes have a predominant role in explaining benthic composition over the last decade. The sustained monitoring effort is critical for understanding how these reefs will change in their composition as global temperatures continue to rise through the Anthropocene.

Evolutionary transitions in diet influence the exceptional diversification of a lizard adaptive radiation.

BACKGROUND: Diet is a key component of a species ecological niche and plays critical roles in guiding the trajectories of evolutionary change. Previous studies suggest that dietary evolution can influence the rates and patterns of species diversification, with omnivorous (animal and plant, 'generalist') diets slowing down diversification compared to more restricted ('specialist') herbivorous and carnivorous diets. This hypothesis, here termed the "dietary macroevolutionary sink" hypothesis (DMS), predicts that transitions to omnivorous diets occur at higher rates than into any specialist diet, and omnivores are expected to have the lowest diversification rates, causing an evolutionary sink into a single type of diet. However, evidence for the DMS hypothesis remains conflicting. Here, we present the first test of the DMS hypothesis in a lineage of ectothermic tetrapods-the prolific Liolaemidae lizard radiation from South America. RESULTS: Ancestral reconstructions suggest that the stem ancestor was probably insectivorous. The best supported trait model is a diet-dependent speciation rate, with independent extinction rates. Herbivory has the highest net diversification rate, omnivory ranks second, and insectivory has the lowest. The extinction rate is the same for all three diet types and is much lower than the speciation rates. The highest transition rate was from omnivory to insectivory, and the lowest transition rates were between insectivory and herbivory. CONCLUSIONS: Our findings challenge the core prediction of the DMS hypothesis that generalist diets represent an 'evolutionary sink'. Interestingly, liolaemid lizards have rapidly and successfully proliferated across some of the world's coldest climates (at high elevations and latitudes), where species have evolved mixed arthropod-plant (omnivore) or predominantly herbivore diets. This longstanding observation is consistent with the higher net diversification rates found in both herbivory and omnivory. Collectively, just like the evolution of viviparity has been regarded as a 'key adaptation' during the liolaemid radiation across cold climates, our findings suggest that transitions from insectivory to herbivory (bridged by omnivory) are likely to have played a role as an additional key adaptation underlying the exceptional diversification of these reptiles across extreme climates.

Marine protected areas do not buffer corals from bleaching under global warming.

BACKGROUND: The rising temperature of the oceans has been identified as the primary driver of mass coral reef declines via coral bleaching (expulsion of photosynthetic endosymbionts). Marine protected areas (MPAs) have been implemented throughout the oceans with the aim of mitigating the impact of local stressors, enhancing fish biomass, and sustaining biodiversity overall. In coral reef regions specifically, protection from local stressors and the enhanced ecosystem function contributed by MPAs are expected to increase coral resistance to global-scale stressors such as marine heatwaves. However, MPAs still suffer from limitations in design, or fail to be adequately enforced, potentially reducing their intended efficacy. Here, we address the hypothesis that the local-scale benefits resulting from MPAs moderate coral bleaching under global warming related stress. RESULTS: Bayesian analyses reveal that bleaching is expected to occur in both larger and older MPAs when corals are under thermal stress from marine heatwaves (quantified as Degree Heating Weeks, DHW), but this is partially moderated in comparison to the effects of DHW alone. Further analyses failed to identify differences in bleaching prevalence in MPAs relative to non-MPAs for coral reefs experiencing different levels of thermal stress. Finally, no difference in temperatures where bleaching occurs between MPA and non-MPA sites was found. CONCLUSIONS: Our findings suggest that bleaching is likely to occur under global warming regardless of protected status. Thus, while protected areas have key roles for maintaining ecosystem function and local livelihoods, combatting the source of global warming remains the best way to prevent the decline of coral reefs via coral bleaching.

Multiple forms of hotspots of tetrapod biodiversity and the challenges of open-access data scarcity.

The uneven spatial distribution of biodiversity is a defining feature of nature. In fact, the implementation of conservation actions both locally and globally has progressively been guided by the identification of biodiversity 'hotspots' (areas with exceptional biodiversity). However, different regions of the world differ drastically in the availability of fine-scale data on the diversity and distribution of species, thus limiting the potential to assess their local environmental priorities. Within South America-a megadiverse continent-Uruguay represents a peculiar area where multiple tropical and non-tropical eco-regions converge, creating highly heterogeneous ecosystems, but where the systematic quantification of biodiversity remains largely anecdotal. To investigate the constraints posed by the limited access to biodiversity data, we employ the most comprehensive database for tetrapod vertebrates in Uruguay (spanning 664 species) assembled to date, to identify hotspots of species-richness, endemism and threatened species for the first time. Our results reveal negligible spatial congruence among biodiversity hotspots, and that tetrapod sampling has historically concentrated in only a few areas. Collectively, our study provides a detailed account of the areas where urgent biodiversity monitoring efforts are needed to develop more accurate knowledge on biodiversity patterns, offering government and environmental bodies a critical scientific resource for future planning.

Biodiversidata: A novel dataset for the vascular plant species diversity in Uruguay.

BACKGROUND: South America hosts some of the world's most prominent biodiversity hotspots. Yet, Uruguay - a country where multiple major ecosystems converge - ranks amongst the countries with the lowest levels of available digital biodiversity data in the continent. Such prevalent data scarcity has significantly undermined our ability to progress towards evidence-based conservation actions - a critical limitation for a country with a strong focus on agricultural industries and only 1.3% of the land surface guarded by protected areas. Under today's rapid biodiversity loss and environmental changes, the need for open-access biodiversity data is more pressing than ever before. To address this national issue, Biodiversidata - Uruguay's first Consortium of Biodiversity Data - has recently emerged with the aim of assembling a constantly growing database for the biodiversity of this country. While the first phase of the project targeted vertebrate biodiversity, the second phase presented in this paper spans the biodiversity of plants. NEW INFORMATION: As part of the second phase of the Biodiversidata initiative, we present the first comprehensive open-access species-level database of the vascular plant diversity recorded in Uruguay to date (i.e. all species for which data are currently available and species presence has been confirmed). It contains 12,470 occurrence records from across 1,648 species and 160 families, which roughly represents 60% of the total recorded flora of Uruguay. The primary biodiversity data include extant native and introduced species from the lycophytes, ferns, gymnosperms and angiosperms groups. Records were collated from multiple sources, including data available in peer-reviewed scientific literature, institutional scientific collections and datasets contributed by members of the Biodiversidata initiative. The complete database can be accessed at the Zenodo repository: doi.org/10.5281/zenodo.3954406.

Rethinking the Effects of Body Size on the Study of Brain Size Evolution.

Body size correlates with most structural and functional components of an organism's phenotype - brain size being a prime example of allometric scaling with animal size. Therefore, comparative studies of brain evolution in vertebrates rely on controlling for the scaling effects of body size variation on brain size variation by calculating brain weight/body weight ratios. Differences in the brain size-body size relationship between taxa are usually interpreted as differences in selection acting on the brain or its components, while selection pressures acting on body size, which are among the most prevalent in nature, are rarely acknowledged, leading to conflicting and confusing conclusions. We address these problems by comparing brain-body relationships from across >1,000 species of birds and non-avian reptiles. Relative brain size in birds is often assumed to be 10 times larger than in reptiles of similar body size. We examine how differences in the specific gravity of body tissues and in body design (e.g., presence/absence of a tail or a dense shell) between these two groups can affect estimates of relative brain size. Using phylogenetic comparative analyses, we show that the gap in relative brain size between birds and reptiles has been grossly exaggerated. Our results highlight the need to take into account differences between taxa arising from selection pressures affecting body size and design, and call into question the widespread misconception that reptile brains are small and incapable of supporting sophisticated behavior and cognition.

Biodiversidata: An Open-Access Biodiversity Database for Uruguay.

BACKGROUND: The continental and marine territories of Uruguay are characterised by a rich convergence of multiple biogeographic ecoregions of the Neotropics, making this country a peculiar biodiversity spot. However, despite the biological significance of Uruguay for the South American subcontinent, the distribution of biodiversity patterns in this country remain poorly understood, given the severe gaps in available records of geographic species distributions. Currently, national biodiversity datasets are not openly available and, thus, a dominant proportion of the primary biodiversity data produced by researchers and institutions across Uruguay remains highly dispersed and difficult to access for the wider scientific and environmental community. In this paper, we aim to fill this gap by developing the first comprehensive, open-access database of biodiversity records for Uruguay (Biodiversidata), which is the result of a large-scale collaboration involving experts working across the entire range of taxonomic diversity found in the country. NEW INFORMATION: As part of the first phase of Biodiversidata, we here present a comprehensive database of tetrapod occurrence records native from Uruguay, with the latest taxonomic updates. The database provides primary biodiversity data on extant Amphibia, Reptilia, Aves and Mammalia species recorded within the country. The total number of records collated is 69,380, spanning 673 species and it is available at the Zenodo repository: https://doi.org/10.5281/zenodo.2650169. This is the largest and most geographically and taxonomically comprehensive database of Uruguayan tetrapod species available to date and it represents the first open repository for the country.

Alternative reproductive adaptations predict asymmetric responses to climate change in lizards.

Anthropogenic climate change ranks among the major global-scale threats to modern biodiversity. Extinction risks are known to increase via the interactions between rapid climatic alterations and environmentally-sensitive species traits that fail to adapt to those changes. Accumulating evidence reveals the influence of ecophysiological, ecological and phenological factors as drivers underlying demographic collapses that lead to population extinctions. However, the extent to which life-history traits influence population responses to climate change remains largely unexplored. The emerging 'cul-de-sac hypothesis' predicts that reptilian viviparity ('live-bearing' reproduction), a 'key innovation' facilitating historical invasions of cold climates, increases extinction risks under progressively warming climates compared to oviparous reproduction - as warming advances polewards/mountainwards, historically cold-climates shrink, leading viviparous species to face demographic collapses. We present the first large-scale test of this prediction based on multiple lizard radiations and on future projections of climate-based ecological niche models. Viviparous species were found to experience stronger elevational range shifts (and potentially increased extinctions) in coming decades, compared to oviparous lizards. Therefore, our analyses support the hypothesis's fundamental prediction that elevational shifts are more severe in viviparous species, and highlight the role that life-history adaptations play in the responses of biodiversity to ongoing climate change.

Live fast, diversify non-adaptively: evolutionary diversification of exceptionally short-lived annual killifishes.

BACKGROUND: Adaptive radiations are triggered by ecological opportunity - the access to novel niche domains with abundant available resources that facilitate the formation of new ecologically divergent species. Therefore, as new species saturate niche space, clades experience a diversity-dependent slowdown of diversification over time. At the other extreme of the radiation continuum, non-adaptively radiating lineages undergo diversification with minimal niche differentiation when 'spatial opportunity' (i.e. areas with suitable 'ancestral' ecological conditions) is available. Traditionally, most research has focused on adaptive radiations, while empirical studies on non-adaptive radiations remain lagging behind. A prolific clade of African fish with extremely short lifespan (Nothobranchius killifish), show the key evolutionary features of a candidate non-adaptive radiation - primarily allopatric species with minimal niche and phenotypic divergence. Here, we test the hypothesis that Nothobranchius killifish have non-adaptively diversified. We employ phylogenetic modelling to investigate the tempo and mode of macroevolutionary diversification of these organisms. RESULTS: Nothobranchius diversification has proceeded with minor niche differentiation and minimal morphological disparity among allopatric species. Additionally, we failed to identify evidence for a role of body size or biogeography in influencing diversification rates. Diversification has been homogeneous within this genus, with the only hotspot of species-richness not resulting from rapid diversification. However, species in sympatry show higher disparity, which may have been caused by character displacement among coexisting species. CONCLUSIONS: Nothobranchius killifish have proliferated following the tempo and mode of a non-adaptive radiation. Our study confirms that this exceptionally short-lived group have diversified with minimal divergent niche adaptation, while one group of coexisting species seems to have facilitated spatial overlap among these taxa via the evolution of ecological character displacement.

The Macroecology of Chemical Communication in Lizards: Do Climatic Factors Drive the Evolution of Signalling Glands?

Chemical communication plays a pivotal role in shaping sexual and ecological interactions among animals. In lizards, fundamental mechanisms of sexual selection such as female mate choice have rarely been shown to be influenced by quantitative phenotypic traits (e.g., ornaments), while chemical signals have been found to potentially influence multiple forms of sexual and social interactions, including mate choice and territoriality. Chemical signals in lizards are secreted by glands primarily located on the edge of the cloacae (precloacal glands, PG) and thighs (femoral glands), and whose interspecific and interclade number ranges from 0 to > 100. However, elucidating the factors underlying the evolution of such remarkable variation remains an elusive endeavour. Competing hypotheses suggest a dominant role for phylogenetic conservatism (i.e., species within clades share similar numbers of glands) or for natural selection (i.e., their adaptive diversification results in deviating numbers of glands from ancestors). Using the prolific Liolaemus lizard radiation from South America (where PG vary from 0 to 14), we present one of the largest-scale tests of both hypotheses to date. Based on climatic and phylogenetic modelling, we show a clear role for both phylogenetic inertia and adaptation underlying gland variation: (i) solar radiation, net primary productivity, topographic heterogeneity and precipitation range have a significant effect on PG variation, (ii) humid and cold environments tend to concentrate species with a higher number of glands, (iii) there is a strong phylogenetic signal that tends to conserve the number of PG within clades. Collectively, our study confirms that the inertia of niche conservatism can be broken down by the need of species facing different selection regimes to adjust their glands to suit the demands of their specific environments.

Macroevolutionary diversification with limited niche disparity in a species-rich lineage of cold-climate lizards.

BACKGROUND: Life diversifies via adaptive radiation when natural selection drives the evolution of ecologically distinct species mediated by their access to novel niche space, or via non-adaptive radiation when new species diversify while retaining ancestral niches. However, while cases of adaptive radiation are widely documented, examples of non-adaptively radiating lineages remain rarely observed. A prolific cold-climate lizard radiation from South America (Phymaturus), sister to a hyper-diverse adaptive radiation (Liolaemus), has extensively diversified phylogenetically and geographically, but with exceptionally minimal ecological and life-history diversification. This lineage, therefore, may offer unique opportunities to investigate the non-adaptive basis of diversification, and in combination with Liolaemus, to cover the whole spectrum of modes of diversification predicted by theory, from adaptive to non-adaptive. Using phylogenetic macroevolutionary modelling performed on a newly created 58-species molecular tree, we establish the tempo and mode of diversification in the Phymaturus radiation. RESULTS: Lineage accumulation in Phymaturus opposes a density-dependent (or 'niche-filling') process of diversification. Concurrently, we found that body size diversification is better described by an Ornstein-Uhlenbeck evolutionary model, suggesting stabilizing selection as the mechanism underlying niche conservatism (i.e., maintaining two fundamental size peaks), and which has predominantly evolved around two major adaptive peaks on a 'Simpsonian' adaptive landscape. CONCLUSIONS: Lineage diversification of the Phymaturus genus does not conform to an adaptive radiation, as it is characterised by a constant rate of species accumulation during the clade's history. Their strict habitat requirements (rocky outcrops), predominantly invariant herbivory, and especially the constant viviparous reproduction across species have likely limited their opportunities for adaptive diversifications throughout novel environments. This mode of diversification contrasts dramatically with its sister lineage Liolaemus, which geographically overlaps with Phymaturus, but exploits all possible microhabitats in these and other bioclimatic areas. Our study contributes importantly to consolidate these lizards (liolaemids) as promising model systems to investigate the entire spectrum of modes of species formations, from the adaptive to the non-adaptive extremes of the continuum.

The global distribution of tetrapods reveals a need for targeted reptile conservation.

The distributions of amphibians, birds and mammals have underpinned global and local conservation priorities, and have been fundamental to our understanding of the determinants of global biodiversity. In contrast, the global distributions of reptiles, representing a third of terrestrial vertebrate diversity, have been unavailable. This prevented the incorporation of reptiles into conservation planning and biased our understanding of the underlying processes governing global vertebrate biodiversity. Here, we present and analyse the global distribution of 10,064 reptile species (99% of extant terrestrial species). We show that richness patterns of the other three tetrapod classes are good spatial surrogates for species richness of all reptiles combined and of snakes, but characterize diversity patterns of lizards and turtles poorly. Hotspots of total and endemic lizard richness overlap very little with those of other taxa. Moreover, existing protected areas, sites of biodiversity significance and global conservation schemes represent birds and mammals better than reptiles. We show that additional conservation actions are needed to effectively protect reptiles, particularly lizards and turtles. Adding reptile knowledge to a global complementarity conservation priority scheme identifies many locations that consequently become important. Notably, investing resources in some of the world's arid, grassland and savannah habitats might be necessary to represent all terrestrial vertebrates efficiently.

Publisher Correction: The global distribution of tetrapods reveals a need for targeted reptile conservation.

In this Article originally published, owing to a technical error, the author 'Laurent Chirio' was mistakenly designated as a corresponding author in the HTML version, the PDF was correct. This error has now been corrected in the HTML version. Further, in Supplementary Table 3, the authors misspelt the surname of 'Danny Meirte'; this file has now been replaced.