https://onlinelibrary.wiley.com/doi/10.1111/brv.12974
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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.
I. INTRODUCTION
Animal populations and whole species are declining across the tree of life, making the Anthropocene defaunation crisis one of the most alarming syndromes of human impacts on environments globally (Ceballos, García & Ehrlich, 2010; Ceballos, Ehrlich & Dirzo, 2017; Dirzo et al., 2014; Pimm et al., 2014; Young et al., 2016). The widespread loss of biodiversity has reached unprecedented degrees of ecosystem degradation at rapid timescales (ongoing extinction rates are 1000–10,000 higher than ‘background’ extinction rates), leading to the growing consensus that life on Earth is entering its sixth mass extinction (Barnosky et al., 2011; Kolbert, 2014; Ceballos et al., 2015; McCallum, 2015; Cowie, Bouchet & Fontaine, 2022). However, compared with the previous five such events, this mass extinction is the first directly induced by a single species – humans.
The traditional approach employed to estimate levels of extinction risk across nature has focused on the International Union for Conservation of Nature (IUCN) Red List conservation categories that are assigned to each assessed species (IUCN, 2022b). These categories are based on the assessment of multiple species features (e.g. geographic range size, population size, and levels of fragmentation: IUCN, 2012) that combined suggest the most likely level of threat. At the time of assessment, species can be classed as ‘threatened’ with extinction [categories Vulnerable (VU), Endangered (EN), Critically Endangered (CR), Extinct in the Wild (EW)], ‘non-threatened’ [categories Least Concern (LC), Near Threatened (NT)], Data Deficient (DD) or unassessed (NA). While these categories capture the range of factors that underlie extinction risk across species with available data at a given time (Purvis et al., 2000; Fisher & Owens, 2004), the case of DD and NA groups is a cause for concern given that they lack conservation focus. Yet, high proportions of such species have been suggested to be threatened (Borgelt et al., 2022). Moreover, while conservation categories have been a pivotal instrument for developing conservation sciences and guiding priorities (Rodrigues et al., 2006; Hoffmann et al., 2008; Brooks et al., 2015; Chichorro, Juslén & Cardoso, 2019; Betts et al., 2020), actual allocation of conservation investment may be taxonomically and geographically biassed irrespective of extinction risk level (Rodrigues et al., 2006; Mammola et al., 2020; Adamo et al., 2022).
In recent years, the focus on conservation categories as proxies for extinction risk has been expanded with the incorporation of the assessment of changes in population sizes over time (‘population trends’ hereafter). The underlying rationale for the use of population trends is that processes of extinction are underpinned by the onset of demographic collapses that initiate progressive declines within a species, subsequently leading to extinction (Ceballos et al., 2010, 2017; Collen et al., 2011; Stein, 2020). Importantly, given that millions of populations have disappeared within the past 100 years alone (Dirzo et al., 2014; Ceballos et al., 2017; Ceballos, Ehrlich & Raven, 2020; Hallmann et al., 2017), declines in populations provide a more dynamic measure of endangerment through time, whereas conservation categories can be seen as ‘snapshots’ of species endangerment. Consequently, population trends may be used as a powerful additional proxy for extinction risk (Ceballos & Ehrlich, 2002; O’Grady et al., 2004; Ceballos et al., 2017; Pincheira-Donoso et al., 2023). Given the advantages of this approach, it has already been used to identify biological, ecological, climatic and threatening factors in common among declining species (e.g. Murray & Hose, 2005; Collen et al., 2011; Murray et al., 2011, 2014; González-Suárez, Lucas & Revilla, 2012). Likewise, large-scale analyses of population trends over time can be used to indicate from an alternative perspective the state of global biodiversity, such as the Living Planet Report’s average 69% decline in population abundance between 1970 and 2018 (WWF, 2022), and the ‘biological annihilation’ of global vertebrate populations (Ceballos et al., 2017). In fact, in the most comprehensive study based on species population trends to date, Ceballos et al. (2017) revealed that 32% (out of >27,000) of included land vertebrate species were declining. Importantly, these authors show two main signals of the severity of the defaunation crisis. Firstly, almost a third of species identified to be declining were classed as non-threatened by the IUCN. Secondly, while tropical species-rich regions host hotspots of declining species when measured as absolute numbers of species, these patterns shifted towards temperate regions when the figures of declining species were calculated as proportions. Collectively, their findings reveal that declines are ubiquitous across species and geographical regions, irrespective of endangerment levels or hotspot status.
An evident limitation of studies exclusively reporting patterns of species undergoing population declines is that the significant proportions of species that have remained stable over time, or which have even undergone increasing population sizes, are neglected. As such, criticism is growing towards large-scale aggregations of trends failing to identify not only ‘losers’ but also ‘winners’ [e.g. for the Living Planet Report (Dornelas et al., 2019; Leung et al., 2020)]. In addition, the reporting of widespread biodiversity loss and the public attention that these patterns can often gain have been criticised for their effects in the delivery of partial ‘big pictures’ (Leung et al., 2020). Thus, global-scale studies integrating the diversity of population trends to draw planetary patterns of declines, stability and increases across the tree of life remain a significant gap. Holistic consideration would provide a true representation of the state of current biodiversity – a means by which to inform both the scientific community and the broader public.
Here, we provide the first comprehensive global-scale overview of all four categories of population trends (decreasing, stable, and increasing, as well as species for which they remain unknown) for vertebrates and insects. Through both geographic and taxonomic space, the patterns of population trends across animal taxa are assessed comparatively to draw an integrative picture of how vertebrate and insect populations, and their proportions, are changing over time. Our overview expands the pioneering advances made in previous large-scale studies (e.g. Ceballos et al., 2017) by considering all population trends, utilising newly released and updated species data available from the IUCN Red List, and by incorporating additional taxonomic groups (fishes and insects). We advocate that quantification and forecasting of the spatial and phylogenetic distribution of extinction risk are underpinned by incorporating these different measures of demographic trends through time.
II. THE DEMOGRAPHIC TRAJECTORIES THAT LEAD SPECIES TO EXTINCTION
Extinctions are the outcome of progressive processes of population declines until a ‘tipping point’ where the degree of demographic collapse that prevents a species from recovering is reached (Cardillo et al., 2005; Sinervo et al., 2010; Collen et al., 2011; Hoffmann & Sgró, 2011; Chaparro-Pedraza, 2021; Pincheira-Donoso et al., 2021). The circumstances that trigger the onset of these processes of decline can be multiple, but they have in common an alteration in the interactions between environmental conditions and the traits that species have evolved to face those conditions (Ferriere, Dieckmann & Couvet, 2004; Hoglund, 2009; Hoffmann & Sgró, 2011; Pincheira-Donoso et al., 2021), i.e. when patterns of natural selection change at rates that exceed a species’ ability to respond or adapt to such changes (Parmesan, 2006; Brook, Sodhi & Bradshaw, 2008; Dirzo et al., 2014; Murray et al., 2014; Chaparro-Pedraza, 2021). Extinctions are, therefore, a demographically progressive process that can be anticipated based on the signatures that population trends leave in species through time (Collen et al., 2011; Chaparro-Pedraza, 2021), in contrast with conservation categories. Overall, using population trends to inspect the demographic progression of species towards extinction provides an ideal tool to reinforce predictions about the future status of species. Population increases may indicate recovery in species currently classed as threatened, whereas population decreases may signal progression towards future extinction risk in non-threatened species (Collen et al., 2011; Ceballos et al., 2017).
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