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

Tasman Sea east of Port Macquarie, NSW. The island is small, just 10 km in length. Because of this species’ rarity, highly restricted range and exposure to MHWs, it has been assessed as CR. In New Zealand, there are three abalone species, known as pãua, two of which are exploited, and although the smaller H. australis (LC) was once fished on a commercial basis, the fishery is now closed and it is only taken by recreational fishers for which there are enforced daily bag limits and size restrictions. H. iris (LC), known as blackfoot pãua, is the only active commercial abalone fishery in New Zealand in which it is fished for food, used in jewellery and raised in hatcheries for pearls. It is also subject to strict fishery controls, where the total allowable com- mercial catch (TACC) is based on population trend models largely influenced by catch per unit effort (CPUE), with all recent data suggesting that the stock has been improving since the mid-2000s [89]. Since 2010, the use of dive loggers has been steadily increasing, enabling fine- scale monitoring which should allow complex metrics such as spatial CPUE. All other species in this sector are LC. Eastern Pacific. This sector includes all abalone species occurring along the western sea- board of the USA, Canada and Mexico together with the only two species found at islands off Central and South America. There are nine species (Table 7). Of the two Eastern Pacific species that occur outside North America, H. dalli (DD) is a small, rare, deep-water species from the Gala´pagos Islands and also Gorgona Island off the

Pacific coast of Colombia, with a separate subspecies occurring off Cocos Island, Costa Rica. Fig 7. H rubiginosa (CR). Occurs in Lord Howe Island, NSW. The only critically endangered unexploited species. Reprinted under a CC BY license with permission from Buzz Owen, original copyright. https://doi.org/10.1371/journal.pone.0309384.g007 Table 7. Abalone species of Eastern Pacific. Species Size C Distribution Cat mm Eastern Pacific H. corrugata 245 C Pt Conception, California to Baja California Sur, Mexico incl Guadalupe Is. CR H. cracherodii 216 C Point Arena, California to Bahia Tortugas, Baja California Sur and Guadalupe Is CR H. fulgens 255 C Point Conception, California to central Baja California Sur and Guadalupe Is. CR H. kamtschatkana 187 C Sitka, Alaska south to central Baja California EN H. rufescens 313 C Central Oregon to central Baja California, Mexico CR H. sorenseni 226 C Point Conception, California to Central Baja California, Mexico and Guadalupe CR H. walallensis 179 C Oregon to central Baja California, Mexico and San Benito Is. CR H. dalli 47 Galapagos Is., Gorgona Is. (Colombia), Cocos Island (Costa Rica) DD H. drogini 65 Cocos Island, Costa Rica VU ‘C’ denotes commercially fished. https://doi.org/10.1371/journal.pone.0309384.t007 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 16 / 25

There are few data on its ecology. H. drogini (VU), endemic to Cocos Island, although also suffering a paucity of data owing to its highly restricted range, is vulnerable to catastrophic events such as MHWs. Of the remaining Eastern Pacific abalone, all but one are listed as CR, including the white abalone (H. sorenseni) (CR) which is on the U.S. Endangered Spe- cies List and on the verge of extinction in the wild [5]. This species now has a well-estab- lished recovery programme including a captive breeding component which has been in the making for nearly 20 years when the first wild white abalone were captured for conservation aquaculture. Today, thousands of juveniles have been produced and a robust partnership has been developed with federal, state, universities and private partners [65], leading to an annual restocking programme begun in 2019, but with abundant predators in the region and a loss of kelp through MHWs, reseeding has been challenging and remnant populations continue to decline. Black abalone (H. cracherodii) (CR) was also overfished and then suf- fered mass mortalities owing to Withering Syndrome, a disease triggered when abalone test- ing positive to the causative bacteria are exposed to warm water events. Today, there are some hopeful signs of recruitment in some areas being reported, but other areas, including Mud Creek in central California, have been hit by landslides occurring when heavy winter rains fall in fire-scarred areas of the central California coastline. Pink abalone (H. corrugata)

(CR) continues to be at low densities in California [90] compared to the 1970s when it was a dominant species in the fisheries. Subsequent to the southern California fisheries closure in 1997 there has been persistent recruitment failure resulting from the Allee Effect. Green abalone (H. fulgens) (CR) is still uncommon in most locations after more than 24 years of fishery closure, but is making a comeback in very few locations in southern California such as Santa Catalina Island [91] although their spatially restricted rebound is a concern for their vulnerability. Flat abalone (H. walallensis) (CR) is also close to extinction in the wild. In the past, this species was always low in abundance with a very narrow distribution [10]. Today it has disappeared from the Monterey area and recent surveys (2022) in northern California, a former stronghold of the species, resulted in no flat abalone sightings (Rogers- Bennett pers. observ.). Northern or pinto abalone (H. kamtschatkana) (EN) in contrast has a wide geographical distribution and, in some regions, such as British Columbia, are numer- ous with signs of recruitment with juveniles greater than 20 mm [92]. This species has two morphologies with H. kamtschatkana kamtschatkana or pinto abalone (aka northern aba- lone) in the north and H. kamtschatkana assimilis or threaded abalone in the south of its range. In southern regions, it is less abundant, and populations continue to decline. In Washington State, there is an active restoration programme and juveniles produced in

hatcheries are stocked in the wild, where they are showing good signs of growth and sur- vival, particularly at some restoration sites [93]. Red abalone (H. rufescens) (CR) (Fig 8), once the foundation of the commercial abalone fishery, was extirpated in central California owing to a combination of fishing and sea otter predation but remained for a time abundant in southern California until their decline due to overfishing, forcing the closure of all aba- lone fisheries in the south in 1997 [13]. There had been a robust free diving (only) recrea- tional fishery in northern California worth an estimated $44 M with more than 31 000 participants per year [94]. The fishery had many sustainability management measures in place including size limits, seasonal closures, daily and annual bag limits as well as gear restrictions including no SCUBA. From 2014–2016 a massive MHW decimated the bull kelp (Nereocystis luetkeana) forests and sea urchin populations increased, dominating the system leading to mass abalone mortalities. Rapid declines by more than 80% of the red aba- lone [21, 52] led to the closure of this, the last open abalone fishery in the United States in 2018 (with the exception of small-scale subsistence fisheries for pinto abalone in SE Alaska). 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 17 / 25

Discussion Our analysis clearly shows that abalone species exposed to fishing have a reduced resilience and a significantly greater chance of extinction compared to those that are unexploited. The few unexploited species assessed as threatened are generally characterised by occurring within a highly restricted range where MHWs and loss of habitat could drive an extinction event. Although overfishing for abalones can be observed through an historical lens, the impact is felt to this day in fisheries around the world where widespread stock declines have left remaining populations more vulnerable to a suite of stressors [53]. Most fisheries nowadays are subject to management controls ranging from total closure to enforcement of quotas, mandatory data loggers and the banning of SCUBA. Management measures that restrict catch provide greater protection of minimum abalone densities necessary for successful fertilization. These include bag and size limits, permanent MPAs to protect identifiable populations, and prohibition of SCUBA for deep stock conservation, rather than seasonal closures which simply shift catch effort to later seasons. Monitoring stocks using fishery independent surveys provides baselines estimates for comparisons following major environmental events [95]. Ideally, this should include kelp and algal cover, as well as competitors such as sea urchins, and also predators that can, when out of balance, severely impact abalones. Pre-impact data can also inform managers of the causes of any subsequent population declines, including identification of harmful algal

blooms [96] that also devastate farmed abalones [97]. Although wild abalone fisheries have declined in most regions globally, with estimated 1970s landings of 20 000 tonnes reduced to 4500 tonnes by 2020/21 [54], the commercial loss has been more than replaced by an upscaling in aquaculture, where total global production in 2010 of 65 344 tonnes had, by 2020/21, reached 243 506 tonnes. Aquaculture production is dominated by China with 89% of the total, followed by Korea with 8%, South Africa at 1% and ten other countries each below one percent [54]. Regrettably, this explosive development has not seemingly reduced the pressure on wild populations which continue to be fished, often to unsustainable levels. Nevertheless, aquaculture offers a bonus in sourcing seed for augmenting depleted wild fisheries, enabling ocean ranching and encouraging population recovery [98], although reintroduction programmes demand complex and costly stock management and record-keeping to safeguard the genetic diversity of wild populations. Heasman et al. (2007) suggest a minimum number of parents at 30 to 40 of each sex, with a large number of mating pairs over each successive generation to avoid inbreeding problems [98]. Fig 8. H. rufescens (CR). At 313 mm, the world’s largest abalone Reprinted under a CC BY license with permission from Buzz Owen, original copyright. https://doi.org/10.1371/journal.pone.0309384.g008 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 18 / 25

While this partnership between aquaculture and wild fisheries can appear promising, espe- cially in the face of climate driven stressors, greater support and funding by foundations and governments is still needed. Despite this exponential increase in abalone aquaculture, the decline in wild populations persists while success to reverse it can only be described as modest with current levels of support. Even with sustainable fisheries, failures in policing and enforce- ment can rapidly reverse gains where there is aggressive and widespread poaching, especially from organised criminal gangs. It may be the case that effective visible protection of large wild abalone assemblages will be more successful and less costly than relying on restocking with aquaculture produced abalones [99]. Recent work has demonstrated the importance of sus- tainable fishing, conservative fishing quotas and periodic fishery closures. While protecting larger females within MPAs that can serve as climate refugia, bolstering resilience to climate stressors will require close collaboration between fishers, fishery managers and scientists [100]. Elevated sea-surface temperatures are giving rise to a multiplicity of immediate threats through loss of algae and habitat, expansion of pathogens and transition of marine ecosystems. Acidification of the oceans, resulting from the current levels of absorption of CO2 from the atmosphere, will have a deleterious effect not only on the development of larval shells but also on the crustose coralline algae (CCA) on which larval settlement depends [14, 101, 102]. How-

ever, it should be noted that while CCA may have reduced growth and survival during acidifi- cation, it has been recorded that elevated pCO2 in upwelling acclimated waters maintained settlement cues for H. rufescens after prolonged acidification exposure [103]. Furthermore, low oxygen conditions in a warming ocean will also impact growth and survival of abalones [104]. Evidence shows that over future decades, abalones, in common with most, if not all calcareous marine taxa, will become increasingly vulnerable to such changes in ocean chemistry. In addi- tion to the impact on calcification, fertilisation, embryonic larval development and settlement may all be compromised [105] allowing for less surplus productivity for fisheries. We know the environment for abalones will in future be warmer and less oxygenated as MHWs are predicted to increase in frequency, intensity and duration [106]. Anomalous heat- ing at the ocean surface is driven by changing climate and further influenced by El Niño- Southern Oscillation (ENSO). ENSO events result in the episodic warming and cooling of the tropical Pacific, and although this effect is centred on the eastern Pacific, its influence can be observed across the whole of the Pacific, Atlantic and Indian Oceans [107]. During the austral summer of 2010/11 an extreme MHW affecting 2000 km of Western Australia coastline resulted in 99% mortality of Roe’s abalone (H. roei) [108]. Such MHWs not only cause mortal- ity of sedentary taxa such as abalones, but the algae on which they survive. Bull kelp (Nereocyc-

tis luetkeana), the principal diet of the red abalone (H. rufescens), is usually common off the northern California coast but declined by more than 90% following the 2014–2015 MHW [109]. This decline in kelp was aggravated by an explosion in population of the purple sea urchin (Strongylocentrotus purpuratus) along with the extirpation from sea star wasting syn- drome of the sunflower star (Pycnopodia helianthoides) [110], an important urchin predator in kelp forest ecosystems [21]. This resulted in 80% mortality of abalones in Northern California and the closure in 2018 of the valuable, popular and culturally important recreational red aba- lone fishery. Similarly, low oxygen events are impacting abalones in Baja California, Mexico [111]. Unless the combustion of fossil fuels that is driving temperature and acidification is arrested, the long-term future of abalones together with all other marine molluscs remains uncertain. We will need to use all the tools at our disposal including restoration aquaculture, reductions in fishing pressure, MPAs [112], favourable microclimates [113] and genetically more resilient families [114] to support abalones given that we know how vulnerable these molluscs are to climate stressors. They are truly oceanic “canaries in the coalmine”. 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 19 / 25

Acknowledgments We would like to thank (in alphabetical order), Rodrigo Beas-Luna, Amanda Bird, Philippe Bouchet, Peter Britz, Emmanuel Capinpin, Jr., Cynthia Catton, Rowan Chick, Michel Claere- boudt, Julia Coates, Fabio Crocetta, Lafargo de la Cruz, Rowena De Shields, Alexis Estrada, Hywel Evans, Daniel Geiger, Scott Groth, Katherine Heldt, David Herbert, Sylvain Huchette, Tomohiko Kawamura, Setsuo Kiyomoto, Joanne Klemke, Kylie Kuwada, Lynn Lee, Stephen Mayfield, Aoife Molloy, Hugh Morrison, Reyn Naylor, Toshihiro Onitsuka, Aaron Pan, Ed Petuch, Guido Poppe, Lachlan Strain, Sheila Tagaro, Hideki Takami, Susan Wang and Caitlin Woods for volunteering their time and expertise to assist in this global assessment and review our findings; Daniel Geiger and Buzz Owen for use of images and maps for the Red List; Simon Stuart of Synchronicity Earth for helping to launch the project; Mary Seddon of the IUCN Mollusc Specialist Group for reviewing our assessments, and Caroline Pollock of the IUCN Red List Unit for bringing the assessments to publication. This publication is a contri- bution of University of York, Bodega Marine Lab UC Davis & Coastal Marine Science Insti- tute, and Old Dominion University. Author Contributions Conceptualization: Howard Peters. Data curation: Howard Peters, Laura Rogers-Bennett. Formal analysis: Howard Peters, Gina M. Ralph. Investigation: Howard Peters, Laura Rogers-Bennett. Methodology: Howard Peters. Project administration: Howard Peters. Resources: Howard Peters, Gina M. Ralph, Laura Rogers-Bennett. Supervision: Howard Peters.

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