Benthic ecosystems and environmental change
Marine ecosystems are highly valuable to human societies, through the provision of ecological goods and services. They are, however, changing rapidly in the face of multiple concurrent stressors, such as seawater warming, ocean acidification, nutrient and pollution input, over-fishing and the spread of non-native species. Understanding how life in the sea is responding to global change is critical if we are to effectively manage and plan for further change and, ultimately, conserve precious living marine resources for future generations.
We are a young but steadily growing research group based at the Marine Biological Association of the United Kingdom. We use a combination of traditional ecological techniques and innovative experimental approaches (lab and field) to better understand how life in the sea is changing, and to predict how it is likely to change in the future.
We try to do two things. First, we collaborate. We are ‘bucket and spade’ ecologists but we collaborate with microbiologists, virologists, physiologists, oceanographers and climate scientists. We also collaborate with like-minded researchers across Europe, Australia and elsewhere. We collaborate because complex systems and problems require complex approaches to better understand them. Second, we observe. Our team and our wider network of collaborators have spent countless days working in shallow-water marine ecosystems in recent years. We do this because appreciating spatial and temporal variability in ecological pattern and process is the first step to understanding human impacts on natural systems.
Benthic ecosystems and environmental change
Kelp forest ecology
Kelp forests dominate shallow rocky habitats across much of the world’s temperate coastline. As foundation species, kelps support high levels of primary productivity, magnified secondary productivity, and provide habitat for highly diverse associated assemblages.
Kelp forests also serve as habitat and nursery grounds for socioeconomically important species of fish, crustaceans and molluscs. However, the structure and extent of kelp forests is affected by environmental change factors, including ocean warming, extreme climatic events and the spread on non-native species.
A key research focus is to address pressing knowledge gaps in our fundamental understanding of the ecological structure and functioning of these critical marine habitats, in order to better predict how kelp populations and communities will respond to current and future environmental changes.
Ecosystem responses to ocean warming and marine heatwaves
The global ocean has warmed significantly in recent decades. As a result, the geographical ranges of many marine species have shifted, generally polewards, with unexpected consequences for the structure and functioning of marine ecosystems.
Understanding how gradual warming trends and extreme climatic events affect marine biodiversity is a major focus of the research group. To achieve this, we are examining the physical drivers of ocean warming and quantifying regional and global patterns in warming trends and the occurrence of marine heatwaves.
We are also assessing the impacts of warming trends and events on marine populations, communities and ecosystems. This research will improve the wider understanding and appreciation of the effects of ocean warming on marine biodiversity.
Impacts of non-native species
The spread of non-native species in marine environments poses a major threat to biodiversity and ecosystem structure and function, and costs the global economy billions of pounds each year. Some marine organisms, including some seaweeds and sea squirts, which can be translocated on ship’s hulls or in ballast water, are potent global invaders that impact aquaculture, biofouling and local biodiversity.
Understanding how the ecological performance of native versus non-native species will be influenced by environmental change is critically important. We are using novel experimental techniques to examine how warming influences both native and non-native species (e.g. ascidians, bryozoans, seaweeds) attached to submerged hard surfaces (e.g. rocky reefs, pylons, jetties).
Furthermore, we are examining how non-native species, such as the Japanese Kelp Undaria pinnatifida (‘Wakame’), may spread from artificial habitats (e.g. ports and marinas) into natural habitats (e.g. rocky reefs and invade native assemblages. The impacts of Wakame invasions on native plants and animals are poorly understood, especially in Europe, and we aim to better understand its impacts in southern England through field and laboratory experiments.
Extreme Climatic Events in Marine Ecosystems
This multi-faceted project focusses on how short-term extreme climatic events, such as marine heatwaves and anomalous storm and freshening events, impact coastal marine ecosystems. The research will examine (1) trends in the frequency and magnitude of these events; (2) the impacts of...
How will ocean warming and changes in storminess and turbidity affect the structure, productivity and resilience of UK kelp forests?
This large-scale field-based project will examine the structure and functioning of UK kelp forests along existing natural gradients in temperature, wave exposure and turbidity. The project employs scientific diving as a tool to access highly productive and diverse kelp forests on shallow...
The influence of multiple global change stressors on marine communities: a novel field approach
Understanding the global impacts and implications of range-shifting species in marine systems
This large, multi-national project aims to better understand the wider implications of species' range shifts in marine ecosystems. Many marine species have shifted their geographical distributions, predominantly poleward, in response to recent oceanic warming. The wider impacts of the...
Peer-reviewed journal articles
71. Pessarrodona, A., Foggo, A., Smale, D. A (2018) Can ecosystem functioning be maintained despite climate-driven shifts in species composition? Insights from novel marine forests. Journal of Ecology (in press)
70. Hereward, H., Foggo, A., Hinckley, S., Greenwood, J. Smale, D. A. (2018) Seasonal variability in the population structure of a habitat-forming kelp and a conspicuous gastropod grazer: Do blue-rayed limpets (Patella pellucida) exert top-down pressure on Laminaria digitata populations? Journal of Experimental Marine Biology and Ecology 506: 171-181
69. Epstein, G. Hawkins, S. J., Smale, D. A. (2018) Removal treatments alter the recruitment dynamics of a global marine invader - Implications for management feasibility. Marine Environmental Research Online early
68. Teagle, H. Moore, P. J., Jenkins, H., Smale, D. A. (2018) Spatial variability in the diversity and structure of faunal assemblages associated with kelp holdfasts (Laminaria hyperborea) in the northeast Atlantic. PLoS ONE 13 (7) e0200411
67. Brewin, R. J. W., Smale, D. A., Moore, P. J., Dall’Olmo, G., Miller, P. I., Taylor, B. H., Smyth, T. J., Fishwick, J. R., Yang, M. (2018) Evaluating operational AVHRR Sea Surface Temperature data at the coastline using benthic temperature loggers. Remote Sensing 10 (6): 1-23
66. Pessarrodona, A., Moore, P. J., Sayer, M., Smale, D. A. (2018) Carbon assimilation and transfer through kelp forests in the NE Atlantic is diminished under a warmer ocean climate. Global Change Biology (online early)
65. Hobday, A. J., Oliver, E. C. J., Sen Gupta, A., Benthuysen, J. A., Burrows, M. T. Donat, M. G., Holbrook, N., Moore, P. J., Thomsen, M. S., Wernberg, T., Smale, D. A. (2018) Categorizing and naming marine heatwaves. Oceanography (online early)
64. Teagle, H. & Smale, D. A. (2018) Climate-driven substitution of habitat-forming species leads to reduced biodiversity within a temperate marine community. Diversity and Distributions (online early)
63. Oliver E., Donat M.G., Burrows M.T., Moore P.J., Smale D.A., Alexander L.V., Benthuysen J.A., Feng M., Sen Gupta A., Hobday A.J., et al. (2018) Ocean warming brings longer and more frequent marine heatwaves. Nature Communications 9:1324.
62. Smale, D. A., Moore, P. J., Queirós, A. M., Higgs, N. D., Burrows, M. T. (2018) Appreciating interconnectivity between habitats is key to Blue Carbon management. Frontiers in Ecology and the Environment 16 (2): 71-73
61. Epstein, G. & Smale, D. A. (2017) Environmental and ecological factors influencing the spillover of the non-native kelp, Undaria pinnatifida, from marinas into natural rocky reef communities. Biological Invasions 20 (4): 1049-1072
60. King, N., McKeown, N. J., Smale, D. A., Moore, P. J. (2017) The importance of phenotypic plasticity and local adaptation in driving intraspecific variability in thermal niches of marine macrophytes. Ecography (online early)
59. King, N., Wilcockson, D., Smale, D. A., Webster, R., Hoelters, L., Moore, P. J. (2017) Cumulative stress restricts niche filling potential of habitat-forming kelps in a future climate. Functional Ecology 32 (2): 288-299
58. Epstein, G. & Smale, D. A. (2017) Undaria pinnatifida: a case study to highlight challenges in marine invasion ecology and management. Ecology and Evolution 7: 8624–8642
57. Smale, D. A., Taylor, J. D., Coombs, S. H., Moore, G., Cunliffe, M. (2017) Community responses to seawater warming are conserved across diverse biological groupings and taxonomic resolutions. Proceedings of the Royal Society B: Biological Sciences 284: 20170534.
56. De Leij, R., Epstein, G., Brown, M., Smale, D. A. (2017) The influence of native macroalgal canopies on the distribution and abundance of the non-native kelp Undaria pinnatifida in natural reef habitats. Marine Biology 164: 156-163
55. Simpson, T. J. S., Smale, D. A., Justin I. McDonald, J. I., Wernberg, T. (2017) Large scale variability in the structure of sessile invertebrate assemblages in artificial habitats reveals the importance of local-scale processes. Journal of Experimental Marine Biology and Ecology 494:10-19
54. Smale, D. A., Wernberg, T., Vanderklift, M. (2017) Regional-scale variability in the response of benthic macroinvertebrate assemblages to a marine heatwave. Marine Ecology Progress Series 568: 17-30
53. Joint, I. & Smale, D. A. (2017) Marine heatwaves and optimal temperatures for microbial assemblage activity. FEMS Microbiology Ecology 93 (2): fiw243
52. Hargrave, M., Foggo, A., Pessarrodona, A., Smale, D. A. (2017) The effects of warming on the ecophysiology of two co-existing kelp species with contrasting distributions. Oecologia 183: 531-543
51. Smale, D. A. & Moore, P. J. (2017) Variability in kelp forest structure along a latitudinal gradient in ocean temperature. Journal of Experimental Marine Biology and Ecology 486: 255–264 Abstract
50. Wernberg, T.,Bennett, S., Babcock, R.C.,de Bettignies, T., Cure, K., Depczynski, M., Dufois, F., Fromont, J., Fulton, C.J., Hovey, R.K., Harvey, E.S., Holmes, T.H., Kendrick, G.A., Radford, B., Santana-Garcon, J., Saunders, B.J., Smale, D. A., Thomsen, M.S., Tuckett, C.A., Tuya, F., Vanderklift, M.A., Wilson, S.K. (2016) Climate driven regime shift of a temperate marine ecosystem. Science 353 (6295) 169-172 Abstract
49. Teagle, H., Hawkins, S. J., Moore, P. J., Smale, D. A. (2016) The role of kelp species as biogenic habitat formers in coastal marine ecosystems. Journal of Experimental Marine Biology and Ecologyaccepted
48. Hobday, A. J., Alexander, L. V., Perkins, S. E., Smale, D. A., Straub, S. C., Oliver, E. C., Benthuysen, J., Burrows, M. T., Donat, M. G., Feng, M., Holbrook, N. J., Moore, P. J., Scannell, H. A., Sen Gupta, A., Wernberg, T. (2016) A hierarchical approach to defining marine heatwaves. Progress in Oceanography 141: 227-238 Abstract
47. Smale, D. A., Michael T. Burrows, Ally J. Evans, Nathan King, Martin D. J. Sayer, Anna L. E. Yunnie, Pippa J. Moore (2016) Linking environmental variables with regional-scale variability in ecological structure and carbon storage function of kelp forests in the United Kingdom. Marine Ecology Progress Series 542:79-95 Abstract
46. Arnold, M., Teagle, H., Brown, M., Smale, D. A. (2016) The structure of biogenic habitat and epibiotic assemblages associated with the global invasive kelp Undaria pinnatifida in comparison to native macroalgae. Biological Invasions 18: 661-676 Abstract
45. Smale, D. A. and Vance, T. (2015) Climate-driven shifts in species’ distributions may exacerbate the impacts of storm disturbances on northeast Atlantic kelp forests. Marine and Freshwater Research 67:65-74 Abstract
44. Sunday J.M., Pecl G.T., Frusher S., Hobday A.J., Hill N.A., Holbrook N.J., Edgar G.J., Stuart-Smith R.D., Barrett N.S., Wernberg T., Watson R.A., Smale, D. A., Fulton E.A., Slawinski D., Feng M., Radford B.T. and Bates A.E. (2015) Species traits and climate velocity explain geographic range shifts in an ocean warming hotspot. Ecology Letters 18: 944-953 Abstract
43. Smale, D. A., Vance, T., Yunnie, A. L. E., Widdicombe, S. (2015). Disentangling the impacts of heat wave magnitude, duration and timing on the structure and diversity of sessile marine assemblages. PeerJ, 3 e863 Article
42. Marzinelli E.M., Williams S.B., Babcock R.C., Barrett N.S., Johnson C.R., Jordan A., Kendrick G.A., Pizarro O.R., Smale, D. A. and Steinberg P.D. (2015) Large-scale geographic variation in distribution and abundance of Australian deep-water kelp forests. PLoS ONE, 10, e0118390 Article
41. Bates, A. E., Bird, T. J., Stuart-Smith, R. D., Wernberg, T., Sunday, J. M., Barrett, N. S., Edgar, G. J., Frusher, S., Hobday, A. J., Pecl, G. T., Smale, D. A., McCarthy, M. (2015) Distinguishing geographical range shifts from artefacts of detectability and sampling effort. Diversity and Distributions. Early view Abstract
40. Smale, D. A., Wernberg, T., Yunnie, A. & Vance, T., (2014) The rise of Laminaria ochroleuca in the Western English Channel (UK) and comparisons with its competitor and assemblage dominant Laminaria hyperborea. Marine Ecology. Early view Abstract
39. Verges, A., Steinberg, P. D., Hay, M. E., Poore, A. G. B., Campbell, A. H., Ballesteros, E., Heck Jr., K. L., Booth, D. J., Coleman, M. A., Feary, D. A., Figueira, W., Langlois, T., Marzinelli, E. M., Mizerek, T., Mumby, P. J., Nakamura, Y., Roughan, M., van Sebille, E., Sen Gupta, A., Smale, D. A., Tomas, F., Wernberg, T., & Wilson, S. (2014) The tropicalisation of temperate marine ecosystems: climate-mediated changes in herbivory and community phase shifts. Proceedings of the Royal Society B. 281: 20140846 Abstract
38. Brodie J., Williamson C.J., Smale D.A., Kamenos N.A., Mieszkowska N., Santos R., Cunliffe M., Steinke M., Yesson C., Anderson K.M., Asnaghi V., Brownlee C., Burdett H.L., Burrows M.T., Collins S., Donohue P.J.C., Harvey B., Foggo A., Noisette F., Nunes J., Ragazzola F., Raven J.A., Schmidt D.N., Suggett D., Teichberg M. & Hall-Spencer J.M. (2014). The future of the northeast Atlantic benthic flora in a high CO2 world. Ecology and Evolution, 4: 2787-2798 Full text
37. Bates, A. E., Pecl, G. T., Frusher S., Hobday, A. J., Wernberg, T. Smale, D. A., Sunday, J. M., Hill, N., Dulvy, N. K., Colwell, R. K., Holbrook, N., Fulton, E. A., Dirk Slawinski, D., Feng, M., Edgar, G. J., Radford, B. T., Thompson, P. A., Watson, R. A. (2014) Defining and observing climate-mediated range shifts in marine systems. Global Environmental Change, 26: 27-38 Abstract
36. Foster, S., Smale, D. A., How, J. de Lestang, S., Brearley, A., Kendrick, G. A. (2014) Regional-scale patterns of mobile invertebrate assemblage structure on artificial habitats off Western Australia. Journal of Experimental Marine Biology and Ecology 453: 43-53 Abstract
35. Smale D. A. and Wernberg T. (2014) Population structure of the purple sea urchin Heliocidaris erythrogramma along a latitudinal gradient in southwest Australia. Journal of the Marine Biological Association of the United Kingdom, 94: 1033-1040 Abstract
34. Azzarello, J., Smale, D. A., Langlois, T., Hansson, E. (2014) Linking habitat characteristics to abundance patterns of canopy-forming macroalgae and sea urchins in southwest Australia. Marine Biology Research, 10: 682-693 Abstract
33. Smale, D. A., Burrows, M., Moore, P., O’Connor, N. and Hawkins, S. (2013) Threats and knowledge gaps for ecosystem services provided by kelp forests: a northeast Atlantic perspective. Ecology and Evolution, 3: 4016–4038 Abstract Text
32. Smale, D. A. (2013) Multi-scale patterns of spatial variability in sessile assemblage structure do not alter predictably with development time. Marine Ecology Progress Series, 482: 29-41 Abstract
31. Smale, D. A. & Wernberg, T. (2013) Extreme climatic event drives range contraction of a habitat-forming species. Proceedings of the Royal Society B, 280: 20122829 Abstract
30. Wernberg, T., Smale, D. A., Tuya, F. et al (2013) An extreme climatic event alters marine ecosystem structure in a global biodiversity hotspot. Nature Climate Change, 3: 78-82 Abstract
29. Smale, D. A. (2012) Spatial variability in sessile assemblage development in subtidal habitats off southwest Australia (southeast Indian Ocean). Journal of Experimental Marine Biology and Ecology, 438: 76-83 Abstract
28. Smale, D.A., Kendrick, G.A., Harvey, E.S. et al (2012) Regional-scale benthic monitoring for Ecosystem-Based Fisheries Management (EBFM) using an Autonomous Underwater Vehicle (AUV). ICES Journal of Marine Science, 69: 1108-1118 Abstract
26. Smale, D.A. and Wernberg, T (2012) Short-term in situ warming influences early development of sessile assemblages. Marine Ecology Progress Series 453: 129-136 Abstract
25. Wernberg, T., Smale, D. A. and Thomsen, M. (2012) A decade of climate change experiments on marine organisms: procedures, patterns and problems. Global Change Biology 18: 1491–1498 Abstract
24. Smale, D. A and Childs, S. (2012) The occurrence of a widespread marine invader, Didemnum perlucidum (Tunicata, Ascidiacea) in Western Australia. Biological Invasions 14: 1325-1330 Abstract
23. Smale, D.A. and Wernberg, T (2012) Ecological observations associated with an anomalous warming event at the Houtman Abrolhos Islands, Western Australia. Coral Reefs 31: 441 Abstract
22. Jamieson, R.E., Rogers, A.D., Billett, D.S.M., Smale, D.A. and Pearce, D.A. (2012) Patterns of marine bacterioplankton biodiversity in the surface waters of the Scotia Arc, Southern Ocean. FEMS Microbiology Ecology 80:452-468 Abstract
21. Smale D. A., Barnes, D. K. A., Barnes R. S. K., Smith D. J., Suggett, D. J. (2012) Spatial variability in the structure of intertidal crab and gastropod assemblages within the Seychelles Archipelago (Indian Ocean). Journal of Sea Research 69: 8-15 Abstract
20. Smale, D. A., Wernberg, T., Vance, T. (2011) Community development on temperate subtidal reefs: the influences of wave energy and the stochastic recruitment of a dominant kelp. Marine Biology. 158:1757–1766 Abstract
19. Smale, D. A., Wernberg, T., Peck, L. S. and Barnes, D. K. A. (2011) Turning on the heat: ecological response to simulated warming in the sea. PLoS One 6: e16050 1-4 Full text
18. Smale, D. A., Kendrick, G. A., and Wernberg, T. (2011) Subtidal macroalgal richness, diversity and turnover, at multiple spatial scales, along the southwestern Australian coastline. Estuarine, Coastal and Shelf Science 91: 224-231 Abstract
17. Wernberg, T., Russell, B. D., Moore, P. J., Ling, S. D., Smale, D. A., Campbell, A., Coleman, M., Steinberg, P. D., Kendrick, G. A., Connell, S. D. (2011) Impacts of climate change in a global hotspot for temperate marine biodiversity and ocean warming. Journal of Experimental Marine Biology and Ecology400: 7-16 Abstract
16. Smale, D. A., Langlois, T., Kendrick, G. A., Meeuwig, J. Harvey, E. S. (2011) From fronds to fish: the use of indicators for ecological monitoring in marine benthic ecosystems, with case studies from temperate Western Australia. Reviews in Fish Biology and Fisheries 21: 311-337 Abstract
15. Smale, D. A. (2010) Monitoring marine macroalgae: the influence of spatial scale on the usefulness of biodiversity surrogates. Diversity and Distributions 16: 985-995 Abstract
14. Smale, D. A., Kendrick, G. A., and Wernberg, T. (2010) Assemblage turnover and taxonomic sufficiency of subtidal macroalgae at multiple spatial scales. Journal of Experimental Marine Biology and Ecology 384: 76-86 Abstract
13. Smale, D. A., Kendrick, G. A., Waddington, K. I. Van Niel, K. P., Meeuwig, J. J. and Harvey, E. S. (2010) Benthic assemblage composition on subtidal reefs along a latitudinal gradient in Western Australia.Estuarine, Coastal and Shelf Science 86: 83-92 Abstract
12. Smale D. A. and Wernberg T. (2009) Satellite-derived SST data as a proxy for water temperature in nearshore benthic ecology. Marine Ecology- Progress Series 387: 27-37 Abstract
11. Smale, D. A., Brown, K. M., Barnes, D. K. A., Fraser, K. P. P., Clarke, A. (2008) Ice scour disturbance in Antarctic shallow waters. Science 321: 371 Abstract
10. Smale, D. A. (2008) Ecological traits of benthic assemblages in shallow Antarctic waters: does ice scour disturbance select for small, mobile, scavengers with high dispersal potential? Polar Biology 31: 1225-123 Abstract
9. Smale, D. A. and Barnes, D. K. A. (2008) Likely responses of the Antarctic benthos to climate related changes in physical disturbance during the 21st Century, based primarily on evidence from the West Antarctic Peninsula region. Ecography 31: 289-305 Abstract
8. Smale, D.A., Barnes, D.K.A., Fraser, K.P.P. and Peck, L.S. (2008) Benthic community response to iceberg scouring at an intensely disturbed shallow water site at Adelaide Island, Antarctica. Marine Ecology- Progress Series 355: 85-94 Abstract
7. Smale, D. A. (2008) Spatial variability in the distribution of dominant shallow-water benthos at Adelaide Island, Antarctica. Journal of Experimental Marine Biology and Ecology 347: 140-148 Abstract
6. Smale, D.A. (2008) Continuous benthic community change along a depth gradient in Antarctic shallows: evidence of patchiness but not zonation. Polar Biology 31: 189-198 Abstract
5. Barnes, D.K.A., Linse, K. Enderlein P. Smale, D. A. Fraser, K.P.P. and Brown, M. P. (2008) Marine richness and gradients at Deception Island, Antarctica. Antarctic Science 20: 271-280 Abstract
3. Smale, D.A., Barnes, D.K.A. and Fraser, K.P.P. (2007). The influence of depth, site exposure and season on the intensity of iceberg scouring in nearshore Antarctic waters. Polar Biology 30: 769-779 Abstract
2. Smale, D.A, Barnes, D.K.A., Fraser, K.P.P, Mann, P.J. and Brown M.P. (2007) Scavenging in Antarctica: intense variation between sites and seasons in shallow benthic necrophagy. Journal of Experimental Marine Biology and Ecology 349: 405-417 Abstract
1. Smale, D.A., Barnes, D.K.A. and Fraser, K.P.P. (2007) The influence of ice scour on benthic communities at three contrasting sites at Adelaide Island, Antarctica. Austral Ecology 32: 878-888 Abstract
Contributions to compiled volumes
- Wernberg, T., Campbell, A., Coleman, M.A., Connell, S.D., Kendrick, G.A., Moore, P.J., Russell, B.D.,Smale, D.A. & Steinberg, P.D. (2009). Macroalgae and Temperate Rocky Reefs. In: A Marine Climate Change Impacts and Adaptation Report Card for Australia 2009. Eds. Poloczanska, E.S., Hobday, A.J. & Richardson, A.J. NCCARF publication 05/09, ISBN 978-1-921609-03-9.
- Wernberg, T. Smale, D.A., Verges, A., Campbell, A. H. Russell, B. D., Coleman, M. A., Ling, S. D., Steinberg, P. D., Johnson, C. R., Kendrick, G. A. & Connell, S. D. (2012) Macroalgae and Temperate Rocky Reefs. In: A Marine Climate Change Impacts and Adaptation Report Card for Australia 2012. Eds. Poloczanska, E.S., Hobday, A.J. & Richardson. ISBN: 978-0-643-10928-5
- Barnes, D., Bergstrom, D. Bindschadler, R. and 36 others including Smale, D. A. (2009) The Next 100 Years. In Turner, J., Bindschadler, R., Convey, P., Di Prisco, G., Fahrbach, E., Gutt, J., Hodgson, D., Mayewski, P. and Summerhayes, C. (Eds.) Antarctic climate change and the environment (pp. 299-389). Scientific Committee on Antarctic Research, Cambridge UK.