Abalones at risk: A global Red List assessment of Haliotis in a changing climate

Introduction Extinction risk for species in marine environments was once considered nearly impossible owing to their perceived abundance and the belief that marine species had unlimited fecundity [1], but today it has become reality [2]. Marine molluscs such as the eelgrass limpet (Lottia alveus), horned snail (Neoplanorbis carinatus), Chinese periwinkle (Littoraria flammea) and rocky shore limpet (Lottia edmitchelli) have all become extinct [3, 4], with white abalone (H. sorenseni) now also on the verge of extinction [5]. Given the combined impacts of human exploitation and a changing climate, the risk of marine extinctions is now universally accepted within policy arenas with overexploitation as the principal driver [2]. As human populations increase, overfishing, both legal and illegal, is affecting the abundance and productivity of marine taxa [6–8]. Deficiency of data, that would otherwise flag population change, can result in overfishing even of common species [9] and rare species frequently lack data on abundance [10]. For example, the giant clam (Tridacna gigas) has been fished out of extensive areas it once inhabited including within Fiji, Guam and New Caledonia and is listed Vulnerable on the IUCN Red List [11]. Similarly, queen conch (Lobatus gigas) has been overfished in many parts of the Caribbean [12]. Overfishing of California’s once abalone-rich nearshore waters has resulted in the serial depletion of abalone stocks in a gradient from the most popular to the least popular species, and nearest to furthest from port [13].

Effects of overfishing are exacerbated by a variety of human-mediated environmental stressors most notably elevated levels of CO2. Increases in CO2 resulting from the combustion of fossil fuels, both intensifies ocean warming and leads to ocean acidification, where excess CO2 combines with seawater and if unchecked can impede calcification in molluscs and other marine invertebrates [14]. Changes in climate are leading to rising sea levels, with warming oceans intensifying the incidence and severity of hurricanes, inundating low-lying coastal zones, and displacing human populations [15]. Climate-driven marine heatwaves (MHWs) together with pollution and other stressors are causing catastrophic declines in abundance of marine taxa, accelerating the loss of biodiversity and changes to marine food-webs [16, 17]. Further declines in foundation species can lead to transitions to alternate states that are far less species rich. In coral reef systems, declines in corals due to a combination of overfishing, pollu- tion and disease have precipitated the transition from coral dominated systems to macroalgal systems with the concurrent loss of biodiversity [18]. Similarly, MHWs have triggered the loss of kelp forests, transitioning to sea urchin barrens—large areas with high sea urchin popula- tions, no macroalgae and little or no abalones [19–21]. In Australia, warming waters have led to the expansion of the sea urchin Centrostephanus rodgersii into waters that were previously too cold for these warm water echinoderms [22, 23]. Disease outbreaks, thought to be exacer-

bated by warming, are also a major cause of decline in marine populations and biodiversity [24, 25]. Black abalone (H. cracherodii) populations, once abundant in the intertidal habitats in southern California, have been decimated by overfishing and disease throughout the Channel Islands [26] with black abalone now listed under the US Endangered Species Act. Clearly there are tipping points [27] beyond which many marine ecosystems collapse [28]. Approximately 46 000 marine mollusc species have been recorded with possibly a further 150 000 waiting to be identified and described, many from the deep seas [29]. Despite their importance to biodiversity, the marine food web and as a fishery resource, their conservation status is barely known. Mollusca is the phylum most impacted by extinction with more than 300 species listed by IUCN Red List as having become extinct and although marine species may be less prone to extinction than terrestrial or freshwater species, the true number may be considerably more than this [30]. However, despite their ubiquity, the IUCN Red List of Threatened Species, the world’s leading database on species’ extinction risk, includes just 1886 PLOS ONE Abalones at risk: A global Red List assessment of Haliotis PLOS ONE | https://doi.org/10.1371/journal.pone.0309384 December 23, 2024 2 / 25 Competing interests: The authors have declared that no competing interests exist.