Critically Endangered female angelsharks (Squatina squatina) are changing normal mating routines in warming oceans as they prioritise staying cool over visiting breeding grounds when things get too hot.
These changes are creating a potential mismatch in the mating behaviours between the sexes of angelshark that could have severe consequences for the future of the species, scientists say.
A team of marine scientists, co-led by researchers at Lancaster University and the Angel Shark Project: Canary Islands (a collaboration between Leibniz Institute for the Analysis of Biodiversity Change, the Universidad de Las Palmas de Gran Canaria and ZSL), used acoustic trackers to discover that prolonged warming of the seas around the Canary Islands is disrupting the reproductive behaviours of female angelsharks.
During a period of unusual and extreme high sea temperatures in 2022, the researchers found female angelsharks were largely absent from the species' traditional mating grounds within the La Graciosa Marine Reserve – which is located off the coast of Lanzarote and is the largest marine reserve in Spain.
That year, sea surface temperatures in the study area rose to more than 23.8°C and remained above 22.5°C for nearly three times longer than in previous years. Crucially, these very high temperatures persisted throughout the entire angelshark mating season, which traditionally starts late autumn, when seas should be cooler.
However, while the warmer seas appeared to deter the female angelsharks, males were not put off and returned to the sites in November as normal, in search of mating opportunities.
Dr David Jacoby, Lecturer in Zoology at Lancaster University and Principal Investigator of the study, said: "These more frequent and extreme heatwaves are potentially the wildfires of the ocean and are having untold effects on marine species.
"With angelsharks we observed important sex differences in behaviour, with the females being disproportionately influenced by sea temperature rises causing them to be absent from their traditional mating sites during this extended period of warming.
"The males were much more resilient to temperature rises and stuck to their regular patterns of arrival and departure, seemingly prioritising mating despite these temperature extremes."
The Canary Islands are at the southern extreme of angelshark distribution and the archipelago is a uniquely large stronghold for the species, which is listed as Critically Endangered by the International Union for Conservation of Nature (IUCN). Adults and juveniles are regularly sighted and are a flagship species for the local dive industry.
Between 2018 and 2023, the research team were able monitor the movement and distribution of over 100 individual angelsharks using acoustic tracking and link these data to environmental conditions.
Prior to 2022, both male and female angelsharks presence in the marine reserve consistently peaked in November and December each year.
However, in 2022 male angelshark numbers peaked as usual, but female numbers remained low all year round. The study showed that female angelshark presence is strongly linked to temperature, and that 22.5°C may be an approximate upper thermal limit for females.
During the five-year monitoring period the scientists observed a general upward trend in peak sea surface temperatures, and an increase in the number of days with temperatures above 22.5°C, from 30 days in 2019 to 85 days in 2022.
Crucially, sea surface temperatures in 2022 remained above 22.5°C into late November, only falling a month later than observed the previous year. Unusually high temperatures remained throughout the entire autumn and winter mating season.
The scientists believe that the reason female angelsharks are prioritising staying cool over mating is likely due to their biology. Female angelsharks have more energetically demanding lifestyles because of reproductive biology, and as a result are more sensitive to temperature as they need to regulate metabolic processes and energy expenditure.
Researchers are concerned that these disruptions to reproductive behaviours in angelsharks could have severe consequences for the future of the species.
"That fact that environmental extremes are driving differing male and female arrival times at coastal mating sites is of particular concern for this Critically Endangered species," said lead author of the study Dr Lucy Mead, a researcher at ZSL's Institute of Zoology and Lancaster University.
"Angelsharks – as with most other sharks – are ectothermic, which means their body temperature directly depends on surrounding water temperatures It seems that male angelsharks prioritise mating even when conditions are unfavourable, while females prioritise staying within their preferred temperature range.
"The Canary Islands are already at the warmer end of tolerable temperatures for angelsharks, and with significant warming projected here, our concern is that key areas may become inhospitable for females. These findings have important implications for how we conserve this highly threatened species in a warming world. Climate change impacts in the ocean tend to be 'out of sight, out of mind', but just as heatwaves and wildfires are becoming more frequent on land, so are extreme events in the oceans."
Eva Meyers, co-lead of the Angel Shark Project and researcher at the Leibniz Institute for the Analysis of Biodiversity Change (LIB), said: "These findings are a reminder of how climate extremes are already reshaping the behaviour of threatened marine species. This study highlights exactly why long-term monitoring of critical habitats in the Canary Islands must be a key pillar of any effective marine biodiversity recovery plan. The Canary Islands are one of the main strongholds for this species — safeguarding these waters is more urgent than ever."
Dr David Jiménez Alvarado, Co-Lead of the Angel Shark Project and postdoctoral researcher at the EcoAQUA Institute (University of Las Palmas de Gran Canaria), said: "It's important to understand how changes in the ocean's physicochemical conditions can affect the species that inhabit coastal ecosystems. These environmental shifts may alter the habitat use and behaviour of key predatory species that play a crucial role in maintaining trophic balance. Since many of these species are already globally threatened, studying how climate-related stressors impact their ecological function is essential for developing effective conservation and management strategies."
The research is outlined in the paper 'Rapid ocean warming drives sexually divergent habitat use in a threatened predatory marine ectotherm' which has been published in Global Change Biology.
The research has been supported by Shark Conservation Fund, Oceanário de Lisboa, Gobierno de Canarias, Loro Parque Fundación, Save Our Seas Foundation, Ocean Tracking Network, WWF Netherlands, Deutsche Elasmobranchier Gesellschaft, Queen Mary University of London, ZSL and the Natural Environment Research Council.
