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Climate change-driven cooling can kill marine megafauna at their distributional limits

Abstract

The impacts on marine species from secular warming and heatwaves are well demonstrated; however, the impacts of extreme cold events are poorly understood. Here we link the death of organisms from 81 species to an intense cold upwelling event in the Agulhas Current, and show trends of increasing frequency and intensification of upwelling in the Agulhas Current and East Australian Current. Using electronic tagging, we illustrate the potential impacts of upwelling events on the movement behaviour of bull sharks Carcharhinus leucas, including alterations of migratory patterns and maintenance of shallower dive profiles when transiting through upwelling cells. Increasing upwelling could result in ‘bait and switch’ situations, where climate change expands subtropical species’ distribution, while simultaneously exposing climate migrants to an increased risk of cold-mortality events at poleward distributional limits. This shows the potential impacts of increased cold events, an understudied aspect of climate change research, and highlights the complexities of climate change effects on marine ecosystems.

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Fig. 1: Anatomy of a killer cold event.
Fig. 2: Marine taxa killed during the killer upwelling event in March 2021.
Fig. 3: Trends in upwelling intensity and frequency along the South African coast.
Fig. 4: Trends in upwelling intensity and frequency along the Australian east coast.
Fig. 5: Seasonal movements of bull sharks in southern Africa and eastern Australia based on acoustic detections.
Fig. 6: Timeline of combined daily acoustic detections and PSAT-tag geolocations of sharks from southern Africa.
Fig. 7: Extracting data with which to explore trends in upwelling.

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Data availability

Both the OSTIA and the CCI satellite SST product were accessed at https://marine.copernicus.eu/. The AVHRR Night satellite SST product was accessed at https://coastwatch.pfeg.noaa.gov/erddap/griddap/erdPH53sstnmday_Lon0360.html, while the AVHRR Day satellite SST product was accessed at https://coastwatch.pfeg.noaa.gov/erddap/griddap/erdPH53sstdmday_Lon0360.html. The level-3 Aqua MODIS satellite SST product was accessed at https://coastwatch.pfeg.noaa.gov/erddap/griddap/erdMH1sstd1dayR20190SQ.html. NetCDF-files used to map the progression of the lethal upwelling event were downloaded from the OceanColor webserver (https://oceancolor.gsfc.nasa.gov/l3/). Long-term wind data for South Africa can be requested from the South African Weather Service at https://www.weathersa.co.za/. Wind data for key dates in the paper are supplied in Supplementary Information. Data associated with bull sharks tagged in Sydney Harbour (temperature, depth, acoustic detections) are publicly available from the animal tracking facility at IMOS https://animaltracking.aodn.org.au/ (see Supplementary Information for tagging dates of sharks). Acoustic tracking data for bull sharks tagged in Southern Africa are available from the South African Acoustic Tracking Array Platform, https://www.saiab.ac.za/atap.htm. Mooring temperature data for Sydney are publicly available at the Australian Ocean Data Network at https://portal.aodn.org.au/ (mooring code SYD100). In situ temperature data collected by a logger at Port Alfred are supplied in Supplementary Information. PSAT temperature and depth data for bull sharks tagged in southern Africa (n = 15) are available at https://doi.org/10.5061/dryad.xd2547dn1 together with an example file for the OSTIA satellite SST product and example code66.

Code availability

Example code for modelling of upwelling variables over time can be accessed at https://doi.org/10.5061/dryad.xd2547dn1 (ref. 66). No public code was used. All code was produced in the statistical software R (https://www.R-project.org/)64. The main packages used were heatwaveR60 and Dharma, which is available at http://florianhartig.github.io/DHARMa/.

References

  1. Brierley, A. S. & Kingsford, M. J. Impacts of climate change on marine organisms and ecosystems. Curr. Biol. 19, R602–R614 (2009).

    Article  CAS  Google Scholar 

  2. Poloczanska, E. S. et al. Responses of marine organisms to climate change across oceans.Front. Mar. Sci. 62, 3 (2016).

    Google Scholar 

  3. Cooley, S. et al. in Climate Change 2022: Impacts, Adaptation and Vulnerability (eds Pörtner, H.-O. et al.) 37–118 (IPCC, Cambridge Univ. Press, 2022).

  4. Vergés, A. et al. The tropicalization of temperate marine ecosystems: climate-mediated changes in herbivory and community phase shifts. Proc. R. Soc. B 281, 20140846 (2014).

    Article  Google Scholar 

  5. Smale, D. A. et al. Marine heatwaves threaten global biodiversity and the provision of ecosystem services. Nat. Clim. Change 9, 306–312 (2019).

    Article  Google Scholar 

  6. Frölicher, T. L. & Laufkötter, C. Emerging risks from marine heat waves. Nat. Commun. https://doi.org/10.1038/s41467-018-03163-6 (2018).

  7. Webb, T. J., Lines, A. & Howarth, L. M. Occupancy‐derived thermal affinities reflect known physiological thermal limits of marine species. Ecol. Evol. 10, 7050–7061 (2020).

    Article  Google Scholar 

  8. Bakun, A. Global climate change and intensification of coastal ocean upwelling. Science 247, 198–201 (1990).

    Article  CAS  Google Scholar 

  9. Bakun, A. et al. Anticipated effects of climate change on coastal upwelling ecosystems. Curr. Clim. Change Rep. 1, 85–93 (2015).

    Article  Google Scholar 

  10. James, N. C. et al. Effects of climate change on South African estuaries and associated fish species. Clim. Res. 57, 233–248 (2013).

    Article  Google Scholar 

  11. Poloczanska, E. S., Limpus, C. J. & Hays, G. C. Vulnerability of marine turtles to climate change. Adv. Mar. Biol. 56, 151–211 (2009).

    Article  Google Scholar 

  12. Griffin, L. P. et al. Warming seas increase cold-stunning events for Kemp’s ridley sea turtles in the northwest Atlantic. PLoS ONE 14, e0211503 (2019).

    Article  CAS  Google Scholar 

  13. Hanekom, N., Hutchings, L., Joubert, P. & Van Der Byl, P. Sea temperature variations in the Tsitsikamma Coastal National Park, South Africa, with notes on the effect of cold conditions on some fish populations. South Afr. J. Mar. Sci. 8, 145–153 (1989).

    Article  Google Scholar 

  14. Lutjeharms, J. Three decades of research on the greater Agulhas Current. Ocean Sci. 3, 129–147 (2007).

    Article  Google Scholar 

  15. Goschen, W., Bornman, T., Deyzel, S. & Schumann, E. Coastal upwelling on the far eastern Agulhas Bank associated with large meanders in the Agulhas Current. Cont. Shelf Res. 101, 34–46 (2015).

    Article  Google Scholar 

  16. Schumann, E. H. Wind-driven mixed layer and coastal upwelling processes off the south coast of South Africa. J. Mar. Res. 57, 671–691 (1999).

    Article  Google Scholar 

  17. Harrison, T. D. & Whitfield, A. K. Estuarine typology and the structuring of fish communities in South Africa. Environ. Biol. Fishes 75, 269–293 (2006).

    Article  Google Scholar 

  18. Lutjeharms, J., Cooper, J. & Roberts, M. Upwelling at the inshore edge of the Agulhas Current. Cont. Shelf Res. 20, 737–761 (2000).

    Article  Google Scholar 

  19. Reid, C. H. et al. An updated review of cold shock and cold stress in fish. J. Fish Biol. 100, 1102–1137 (2022).

    Article  Google Scholar 

  20. Hobday, A. J. et al. A hierarchical approach to defining marine heatwaves. Prog. Oceanogr. 141, 227–238 (2016).

    Article  Google Scholar 

  21. Murie, K. A. & Bourdeau, P. E. Energetic context determines the effects of multiple upwelling-associated stressors on sea urchin performance. Sci. Rep. 11, 141 (2021).

    Article  Google Scholar 

  22. Matich, P. & Heithaus, M. R. Effects of an extreme temperature event on the behavior and age structure of an estuarine top predator, Carcharhinus leucas. Mar. Ecol. Prog. Ser. 447, 165–178 (2012).

    Article  Google Scholar 

  23. Carlisle, A. B. et al. Reconstructing habitat use by juvenile salmon sharks links upwelling to strandings in the California Current. Mar. Ecol. Prog. Ser. 525, 217–228 (2015).

    Article  Google Scholar 

  24. Rohner, C. et al. Trends in sightings and environmental influences on a coastal aggregation of manta rays and whale sharks. Mar. Ecol. Prog. Ser. 482, 153–168 (2013).

    Article  Google Scholar 

  25. Farmer, N. A. et al. The distribution of manta rays in the western North Atlantic Ocean off the eastern United States. Sci. Rep. 12, 482 (2022).

    Article  Google Scholar 

  26. Lubitz, N. et al. Context drives movement patterns in a mobile marine predator. Mov. Ecol. 11, 28 (2023).

    Article  Google Scholar 

  27. García-Reyes, M. et al. Under pressure: climate change, upwelling, and eastern boundary upwelling ecosystems. Front. Mar. Sci. 2, 109 (2015).

    Article  Google Scholar 

  28. Wang, D., Gouhier, T. C., Menge, B. A. & Ganguly, A. R. Intensification and spatial homogenization of coastal upwelling under climate change. Nature 518, 390–394 (2015).

    Article  CAS  Google Scholar 

  29. Roughan, M. & Middleton, J. H. A comparison of observed upwelling mechanisms off the east coast of Australia. Cont. Shelf Res. 22, 2551–2572 (2002).

    Article  Google Scholar 

  30. Leber, G. M., Beal, L. M. & Elipot, S. Wind and current forcing combine to drive strong upwelling in the Agulhas Current. J. Phys. Oceanogr. 47, 123–134 (2017).

    Article  Google Scholar 

  31. Suthers, I. M. et al. The Strengthening East Australian Current, Its Eddies and Biological Effects: An Introduction and Overview 538–546 (Elsevier, 2011).

  32. Beal, L. M. & Elipot, S. Broadening not strengthening of the Agulhas Current since the early 1990s. Nature 540, 570–573 (2016).

    Article  CAS  Google Scholar 

  33. Huang, Z. & Wang, X. H. Mapping the spatial and temporal variability of the upwelling systems of the Australian south-eastern coast using 14-year of MODIS data. Remote Sens. Environ. 227, 90–109 (2019).

    Article  Google Scholar 

  34. Schilling, H. T., Hinchliffe, C., Gillson, J. P., Miskiewicz, A. G. & Suthers, I. M. Coastal winds and larval fish abundance indicate a recruitment mechanism for southeast Australian estuarine fisheries. Fish. Oceanogr. 31, 40–55 (2022).

    Article  Google Scholar 

  35. Meneghesso, C. et al. Remotely-sensed L4 SST underestimates the thermal fingerprint of coastal upwelling. Remote Sens. Environ. 237, 111588 (2020).

    Article  Google Scholar 

  36. Duncan, M., James, N., Bates, A., Goschen, W. & Potts, W. Localised intermittent upwelling intensity has increased along South Africa’s south coast due to El Niño–Southern Oscillation phase state. Afr. J. Mar. Sci. 41, 325–330 (2019).

    Article  Google Scholar 

  37. Heupel, M. R. & Simpfendorfer, C. A. Movement and distribution of young bull sharks Carcharhinus leucas in a variable estuarine environment. Aquat. Biol. 1, 277–289 (2008).

    Article  Google Scholar 

  38. Smoothey, A. F. et al. Patterns of occurrence of sharks in Sydney Harbour, a large urbanised estuary. PLoS ONE 11, e0146911 (2016).

    Article  Google Scholar 

  39. Curtis, T. H., Adams, D. H. & Burgess, G. H. Seasonal distribution and habitat associations of bull sharks in the Indian River Lagoon, Florida: a 30-year synthesis. Trans. Am. Fish. Soc. 140, 1213–1226 (2011).

    Article  Google Scholar 

  40. Cliff, G. & Dudley, S. Sharks caught in the protective gill nets off Natal, South Africa. 4. The bull shark Carcharhinus leucas Valenciennes. South Afr. J. Mar. Sci. 10, 253–270 (1991).

    Article  Google Scholar 

  41. Smoothey, A. F., Lee, K. A. & Peddemors, V. M. Long-term patterns of abundance, residency and movements of bull sharks (Carcharhinus leucas) in Sydney Harbour, Australia. Sci. Rep. 9, 10 (2019).

    Article  Google Scholar 

  42. Spurgeon, E., Anderson, J. M., Liu, Y., Barajas, V. L. & Lowe, C. G. Quantifying thermal cues that initiate mass emigrations in juvenile white sharks. Sci. Rep. 12, 19874 (2022).

    Article  Google Scholar 

  43. Marchesiello, P., Gibbs, M. T. & Middleton, J. H. Simulations of coastal upwelling on the Sydney continental shelf. Mar. Freshw. Res. 51, 577–588 (2000).

    Article  Google Scholar 

  44. Harrison, T. & Whitfield, A. Temperature and salinity as primary determinants influencing the biogeography of fishes in South African estuaries. Estuar. Coast. Shelf Sci. 66, 335–345 (2006).

    Article  Google Scholar 

  45. Armstrong, A. J. et al. The geographic distribution of reef and oceanic manta rays (Mobula alfredi and Mobula birostris) in Australian coastal waters. J. Fish. Biol. 96, 835–840 (2020).

    Article  Google Scholar 

  46. Goschen, W. & Schumann, E. Upwelling and the occurrence of cold water around Cape Recife, Algoa Bay, South Africa. South Afr. J. Mar. Sci. 16, 57–67 (1995).

    Article  Google Scholar 

  47. Roy, C., Van der Lingen, C., Coetzee, J. & Lutjeharms, J. Abrupt environmental shift associated with changes in the distribution of Cape anchovy Engraulis encrasicolus spawners in the southern Benguela. Afr. J. Mar. Sci. 29, 309–319 (2007).

    Article  Google Scholar 

  48. Bolton, J., Anderson, R., Smit, A. & Rothman, M. South African kelp moving eastwards: the discovery of Ecklonia maxima (Osbeck) Papenfuss at De Hoop Nature Reserve on the south coast of South Africa. Afr. J. Mar. Sci. 34, 147–151 (2012).

    Article  Google Scholar 

  49. Muñiz, C., McQuaid, C. D. & Weidberg, N. Seasonality of primary productivity affects coastal species more than its magnitude. Sci. Total Environ. 757, 143740 (2021).

    Article  Google Scholar 

  50. Nelson, G. & Hutchings, L. The Benguela upwelling area. Prog. Oceanogr. 12, 333–356 (1983).

    Article  Google Scholar 

  51. Hutchings, L. et al. The Benguela Current: an ecosystem of four components. Prog. Oceanogr. 83, 15–32 (2009).

    Article  Google Scholar 

  52. Last, P. et al. Rays of the World (CSIRO, 2016).

  53. Compagno, L., Dando, M. & Fowler, S. A Field Guide to the Sharks of the World (Collins, 2005).

  54. Niella, Y., Smoothey, A. F., Peddemors, V. & Harcourt, R. Predicting changes in distribution of a large coastal shark in the face of the strengthening East Australian Current. Mar. Ecol. Prog. Ser. 642, 163–177 (2020).

    Article  Google Scholar 

  55. Griffiths, C. L., Robinson, T. B., Lange, L. & Mead, A. Marine biodiversity in South Africa: an evaluation of current states of knowledge. PLoS ONE 5, e12008 (2010).

    Article  Google Scholar 

  56. Archer, M. R., Roughan, M., Keating, S. R. & Schaeffer, A. On the variability of the East Australian Current: jet structure, meandering, and influence on shelf circulation. J. Geophys. Res. Oceans 122, 8464–8481 (2017).

    Article  Google Scholar 

  57. Abrahams, A., Schlegel, R. W. & Smit, A. J. A novel approach to quantify metrics of upwelling intensity, frequency, and duration. PLoS ONE 16, e0254026 (2021).

    Article  CAS  Google Scholar 

  58. Good, S. et al. The current configuration of the OSTIA system for operational production of foundation sea surface temperature and ice concentration analyses. Remote Sens. 12, 720 (2020).

    Article  Google Scholar 

  59. Yang, C. et al. Sea surface temperature intercomparison in the framework of the Copernicus Climate Change Service (C3S). J. Clim. 34, 5257–5283 (2021).

    Article  Google Scholar 

  60. Schlegel, R. W. & Smit, A. J. heatwaveR: a central algorithm for the detection of heatwaves and cold-spells. J. Open Source Softw. 3, 821 (2018).

    Article  Google Scholar 

  61. Schlegel, R. W., Oliver, E. C., Hobday, A. J. & Smit, A. J. Detecting marine heatwaves with sub-optimal data. Front. Mar. Sci. 6, 737 (2019).

    Article  Google Scholar 

  62. Daly, R., Smale, M. J., Cowley, P. D. & Froneman, P. W. Residency patterns and migration dynamics of adult bull sharks (Carcharhinus leucas) on the east coast of southern Africa. PLoS ONE 9, e109357 (2014).

    Article  Google Scholar 

  63. Brunnschweiler, J. M. Sharksucker–shark interaction in two carcharhinid species. Mar. Ecol. 27, 89–94 (2006).

    Article  Google Scholar 

  64. R Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2021); https://www.R-project.org/

  65. Stuart-Smith, R. D., Edgar, G. J., Barrett, N. S., Kininmonth, S. J. & Bates, A. E. Thermal biases and vulnerability to warming in the world’s marine fauna. Nature 528, 88–92 (2015).

    Article  CAS  Google Scholar 

  66. Lubitz, N. Climate-change-driven cooling can kill marine megafauna at their distributional limits. Dryad https://doi.org/10.5061/dryad.xd2547dn1 (2024).

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Acknowledgements

We thank the Acoustic Tracking Array Platform (ATAP) hosted by the National Research Foundation - South African Institute for Aquatic Biodiversity, the Ocean Tracking Network, the Department of Science and Innovation−Shallow Marine and Coastal Research Infrastructure programme, and the NRF-South African Environmental Observation Network Elwandle Node for providing acoustic telemetry hardware and in situ ocean temperature recorders that facilitated data collection for this study. We thank the Save Our Seas Foundation and the African Coelacanth Ecosystem Programme for funding running expenses for the ATAP. Additional temperature logger (UTR) data were used from the ‘SASMIA UTR Southcoast network’ (South African Squid Management Industrial Association). We thank the iSimangaliso Marine Protected Area and iSimangaliso Wetland Park management and Ezemvelo KZN Wildlife, together with the Maputo National Park and Park Warden, M. Gonçalves, for their ongoing support of this research. The Australian New South Wales component of this work was completed under NSW DPI Research Permit Section 37 (Ref. PO1/0059A-2.0) and Animal Care and Ethics permit 07/08. Additional data were sourced from Australia’s Integrated Marine Observing System (IMOS) Animal Tracking Database (https://animaltracking.aodn.org.au). IMOS is enabled by the National Collaborative Research Infrastructure Strategy (NCRIS). This project would not have been possible without the dedicated support of NSW DPI shark research team, contracted SMART drumline fishers and countless volunteers. This research was funded by the NSW Government through the NSW Department of Primary Industries Bull shark tagging research programme and NSW Shark Management Program. M.J.R. is the UK-SA Bilateral Research Chair in Ocean Science and Marine Food Security, a partnership between Nelson Mandela University and the National Oceanography Centre, University of Southampton.

Author information

Authors and Affiliations

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Contributions

N.L. conceived the study, analysed most of the data and drafted the paper. All authors contributed significantly to the writing and editing of this paper. R.D. collected data, conceived the study and helped draft the paper. A.F.S. and P.V. collected data and helped conceive the study. P.V. and M.J.R. analysed some data and helped conceive the study. D.S.S. helped conceive the study and helped in drafting the manuscript. M. Sheaves provided supervision and guidance in writing the paper. P.D.C., L.D., F.G.F., M. Soria, V.M.P., J.D.F., P.A.B. and G.B. collected data. A.B. provided supervision, helped conceive the study and helped edit the paper.

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Correspondence to Nicolas Lubitz.

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Nature Climate Change thanks Juerg Brunnschweiler, Nuno Queiroz and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Extended data

Extended Data Fig. 1 Sharks stay near the surface and experience colder temperatures in upwelling zones.

a) The percentage of time at temperature and depth bins based on PSAT-tag recordings for sharks tagged in the Breede River, South Africa: when in the Breede River, the upwelling zone, and past the upwelling zone, in the subtropic/tropics. b) Percentage of time at temperature and depth bins recorded by acoustic transmitters during detections for sharks tagged in Sydney Harbour, Australia: when inside Sydney Harbour (green), outside in the vicinity of Sydney Harbour, the upwelling zone, and past the upwelling zone, in the subtropic/tropics.

Extended Data Fig. 2 Bull shark detections when sharks are seasonally present at their seasonal distributional limits.

Percentages are given for detections inside and outside Sydney Harbour for sharks tagged in Sydney Harbour and for inside and outside the Breede River Estuary for sharks tagged in the Breede River Estuary.

Extended Data Table 1 Marine megafauna deaths along south-eastern South Africa due to intense upwelling

Supplementary information

Supplementary Information

Supplementary Figs. 1–22 and Tables 1–15.

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Lubitz, N., Daly, R., Smoothey, A.F. et al. Climate change-driven cooling can kill marine megafauna at their distributional limits. Nat. Clim. Chang. (2024). https://doi.org/10.1038/s41558-024-01966-8

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