An ocean habitat trap? Impacts of global oxygen-minimum zone expansions on threatened apex predator ecology

Lead Research Organisation: Marine Biological Association
Department Name: Marine Biology

Abstract

Permanent oxygen minimum zones (OMZs) that extend to over 10 million km3 of ocean (ca. 8% of ocean volume) are expanding geographically and vertically due to climate-driven reductions in dissolved oxygen (DO). Potential impacts on marine animal distributions and abundance may be particularly significant for high-oxygen-demand apex predators, such as oceanic pelagic sharks, by reducing habitat volumes through OMZ shoaling and concentrating them further in surface waters where they become more vulnerable to fisheries. But predictions of how exploited oceanic fish actually respond to OMZ expansions are not based on mechanistic understandings, principally because direct measurements of oxygen tolerances during normal behaviour have not been determined for large predatory fish in the open ocean. The proposed research will bring about a step change in our understanding of OMZ impacts on oceanic ecology by applying our existing expertise in animal movement studies and by deploying new telemetry technologies for measuring oxygen environments actually encountered by free-living oceanic sharks moving above/within OMZs. This will enable major unknowns to be addressed concerning how oceanic sharks respond physiologically and behaviourally to OMZs, how oceanic shark habitats change with predicted OMZ expansion, and whether this will increase shark vulnerability to fishing gear. The project will achieve its objectives through linked field and modelling studies on two Red-Listed species, the warm-bodied (endothermic) shortfin mako, Isurus oxyrinchus, and the ectothermic blue shark, Prionace glauca, that are the two pelagic shark species most frequently caught in high seas fisheries. By focusing in depth on key processes underlying shark responses to DO in situ, our new modelling approaches will establish effects of future warming and OMZ shoaling on fish niches and determine how these shift distributions and alter capture risk by fisheries. The project represents a discipline-spanning approach linking physiology to ecology and oceanography, with wide-ranging outcomes for understanding global biotic responses to warming and ocean deoxygenation with direct relevance to sustainable fisheries and species conservation.

Planned Impact

There are two main potential science outcomes of the proposed research that may lead to significant impacts. Firstly, vertical space-use of oceanic blue and shortfin mako sharks may be shifted to shallower depths by the expanding eastern tropical Atlantic OMZ and sharks may remain that region for long periods of time due to greater foraging opportunities (as prey are similarly habitat compressed). As a result, the vulnerability of oceanic sharks to capture by fisheries may be much greater in the OMZ than in normoxic waters elsewhere in the Atlantic. This would identify the need to consider OMZs as areas requiring consideration of special management measures with respect to oceanic sharks and perhaps other pelagics (e.g. tunas, swordfish). OMZs may be particularly important areas that support large catches of sharks but that have gone undetected as major sources because of poor reporting of catches and the lack of regulation. Therefore, the proposed research may be of great interest to the International Commission for the Conservation of Atlantic Tunas (ICCAT) for informing plans to develop sustainable exploitation of oceanic sharks in the Atlantic. Similarly, the International Union for the Conservation of Nature (IUCN) World Commission on Protected Areas (WCPA) are interested in the project results because they address an emerging interest in assessing the status and global impacts of ocean deoxygenation. Furthermore IUCN WCPA are interested in exploring the potential of OMZs as a network of high seas Marine Protected Areas (MPA).
In the proposed research we plan to engage directly with ICCAT regarding shark catch limits in OMZs and with the IUCN WCPA on upper-trophic level impacts of ocean deoxygenation and to explore a potential role of OMZs as high seas MPAs. We plan to present the results of the proposed research formally to ICCAT as part of the annual intersessional meetings of the shark species group in addition to the species data preparatory meetings and stock assessment sessions (which the P.I. and Project Partner have attended as part of the EU delegation). A potential outcome will be bringing new data and understanding on shark movements, electronic tag recapture rates to estimate potential fishing mortality between different ocean areas, and the effects of environmental changes on risk of shark capture from fisheries, into the shark stock assessment process to inform recommendations for management. The proposed project may contribute results that identify OMZs as areas at particular risk from overfishing.
Engagement with the IUCN will be in collaboration with our Project Partner Prof Dan Laffoley who is the Marine Vice-Chair of the IUCN WCPA. We will work with Prof Laffoley in two linked areas. First, the WCPA are to produce an authoritative report on the impacts of ocean deoxygenation that will be launched at a future meeting of the World Conservation Congress. The proposed research will form the key source of new information detailing how IUCN Red-Listed oceanic sharks will respond to the combined effects of ocean deoxygenation, warming and fishing exploitation. Secondly, as part of the collaborative reporting of the effects of deoxygenation on sharks, we will explore with IUCN the potential for identifying OMZs as candidate high seas MPAs in the event that they are identified as key shark habitats that appear to be undergoing overfishing. We aim to feed project results into focused meetings with IUCN to determine whether there is scope and opportunity for proposing OMZs as MPAs as part of their Global Plan of Action.

Publications

10 25 50
 
Description Climate-driven expansions of ocean hypoxic zones are predicted to concentrate pelagic fish in surface layers, but how expanding hypoxia and high-seas fisheries will interact to affect threatened pelagic sharks has not been studied. In this research we have analysed the movements and behaviour of satellite-tracked blue sharks - the most fished pelagic shark - and longline fishing vessels above the eastern tropical Atlantic oxygen minimum zone (OMZ). The results show sharks are shifted into surface layers by low dissolved oxygen at depth, while higher fishing intensity occurs above the OMZ compared to oxygenated adjacent waters. We developed a models to determine the environmental drivers of vertical habitat use of sharks and to predict distribution shifts above future OMZ areas using Earth System Model (ESM) Coupled Model Intercomparison Project Phase 6 (CMIP6) future environmental conditions. In addition, we modelled OMZ expansion effects on the risk of shark capture by surface longlines. The models predicts that shark maximum dive depth above the OMZ will be reduced on average by 122 m over the next three decades, consistent with hypoxia-based habitat compression. We estimate this will double the encounter rate of sharks with longline hook depths, suggesting sharks above expanding OMZs may become more susceptible to fisheries capture. Stricter fisheries controls in OMZ areas may be needed to counteract deoxygenation effects on shark catches as oceans continue warming.
Exploitation Route There are two main ways the science results may lead to significant impacts. The demonstration that the vertical space-use of pelagic sharks is shifted to shallower depths above the eastern tropical Atlantic OMZ leading to habitat compression of sharks and estimated increases in susceptibility to capture by fisheries, shows sharks will be at greater risk of exposure to fisheries capture above the eastern tropical Atlantic OMZ than in normoxic waters elsewhere in the Atlantic. These results will be of interest to fisheries management bodies tasked with the management of sharks in International Waters of the Atlantic, such as the International Commission for the Conservation of Atlantic Tunas (ICCAT). This is because shark habitat compression above OMZs with progressing ocean deoxygenation will likely alter catch rates and the distribution of longline fisheries, which predicts regional declines in abundance without mitigating management measures. This may require ICCAT to consider management measures in the light of climate change effects, something which has yet to be incorporated into any shark management measure anywhere in the world. Furthermore, global conservation bodies with an interest in climate change effects on apex predators and in high seas Marine Protected Areas, such as the IUCN World Commission on Protected Areas (WCPA), will be interested in the results to inform proposals for protected large-scale areas of the ocean as MPAs for sharks and associated biodiversity.
Sectors Environment,Government, Democracy and Justice

URL http://www.globalsharkmovement.org
 
Description The research has contributed to a major IUCN (International Union for the Conservation of Nature) report entitled "Ocean Deoxygenation - Everyone's Problem: Causes, Impacts, Consequences and Solutions", edicted by D. Laffoley and J. Baxter, which is due for publication in 2019. Our research contributed the entire chapter on the effects of ocean deoxygenation on sharks, skates and rays. It is anticipated that this IUCN report will be a landmark publication to galvanise interest, support and international action on the issue of ocean deoxygenation.
First Year Of Impact 2019
Sector Environment
Impact Types Economic,Policy & public services

 
Title Global Shark Movement and Environment Database 
Description The Global Shark Movement Project Database holds satellite tracking locations and associated data of over 2,000 pelagic sharks (23 species) with environmental data (17 variables) extracted for each shark daily location. It holds approximately 300,000 track days of shark movements. The shark movement tracking data were contributed by 40 research groups in over 100 institutes in 26 countries. The GMSP Database is managed by the P.I. 
Type Of Material Database/Collection of data 
Year Produced 2019 
Provided To Others? No  
Impact The GSMP Database is being used widely across the 40 research teams to address key questions in shark ecology, conservation and interactions with fisheries. Research publications are currently in review and preparation. It seems likely that the first paper will be published in time to have an impact at the CITES (Convention on International Trade in Endangered Species) Conference of Parties in May 2019. 
URL https://www.globalsharkmovement.org/
 
Title Animal-attached electronic tag for recording dissolved oxygen, depth, temperature and animal heading and body movements 
Description The new tag developed in collaboration with this project provides unparalleled detail of fish movements, behaviour and environment in hypoxic ocean regions. The tag contains tri-axial accelerometer, pressure, water temperature, optical dissolved oxygen and heading sensors. The optical DO sensor maintains calibration for long periods of time (months). The printed circuit boards (PCBs) contain a low-power accelerometer, magnetometer, depth and temperature sensors enabling fine-scale 3D movements of tagged animals to be recorded; the tag is recovered after it releases from a predator and can be re-used. Given the large amounts of data typically produced by accelerometers, the sampling rate is configurable and varies between 1 and 50 Hz, with a mini-storage device (microSD card) incorporated to enable environmental data to be collected at very high temporal resolution (1s) allowing 3D movements to be linked with oxygen gradients during dives ('casts'). Furthermore, the tag can record subtle body movements associated with tail beat frequency, power-glide cycles, and overall dynamic body acceleration (ODBA) that can be used as a proxy for energy expenditure in the wild (field metabolic rate; see next section). A timed-release device releases the tag from the fish and a GPS unit allows tag recovery when it floats to the surface. The tag will enable short, 1-3 d data-rich deployments on free-ranging sharks and tunas that potentially dive to 1,700m. A second version incorporating a video camera (DVL2000M; Little Leonardo, Tokyo) has been built that records prey concentrations encountered at different depth and DO environments (down to 2000 m and incorporating red LED lights for recording in the dark). 
Type Of Technology New/Improved Technique/Technology 
Year Produced 2019 
Impact The tag has been tested in the lab and in large aquaria, and has been trialled on ocean sunfish at sea where it collected data on dissolved oxygen, depth and temperature along the swimming paths of fish for 4 days. The tags will be deployed on large pelagic sharks to gain novel insights into behaviour in environments undergoing deoxygenation. 
 
Title Source code for global analysis of pelagic shark spatial density and fishing effort 
Description The source code can be used to undertake analyses and to prepare figures, in addition to the derived data underlying global maps of shark relative spatial density, longline-fishing effort and shark-longline-fishing overlap and fisheries exposure index (FEI) and plots of spatial overlap and FEI. Freely available on GitHub (https://github.com/GlobalSharkMovement/GlobalSpatialRisk). 
Type Of Technology Software 
Year Produced 2019 
Impact The code was used to undertake analyses contributing to the 2019 paper in NATURE by Queiroz et al., Sims which received worldwide media coverage. 
URL https://www.nature.com/articles/s41586-019-1444-4