Tropical herbivores provide resilience to a climate-mediated phase shift on temperate reefs

Ecology Letters

Volumn 18, Issue 7, 2015, Pages 714-723

  Bennett, Scott ^a   Wernberg, Thomas ^a   Harvey, Euan S ^b   Santana Garcon, Julia ^a   Saunders, Benjamin J ^b  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b CURTIN UNIVERSITY   (Australia)

Author keywords

Climate change; Coral reef; Fishes; Kelp; Regime shift; Tropicalisation

Indexed keywords

ABUNDANCE; BIOMASS; CORAL REEF; DISTURBANCE; ECOSYSTEM RESILIENCE; FEEDING BEHAVIOR; FISH; GLOBAL WARMING; HERBIVORE; INTERSPECIFIC INTERACTION; SEAWEED; SPECIES DIVERSITY; TEMPERATE ENVIRONMENT; TROPICAL ENVIRONMENT;

ANTHOZOA; PISCES;

ANIMAL; AUSTRALIA; CLIMATE CHANGE; CORAL REEF; FISH; HERBIVORY; KELP; TROPIC CLIMATE;

ANIMALS; AUSTRALIA; CLIMATE CHANGE; CORAL REEFS; FISHES; HERBIVORY; KELP; TROPICAL CLIMATE;

EID: 84931578759     PISSN: 1461023X     EISSN: 14610248     Source Type: Journal    
DOI: 10.1111/ele.12450     Document Type: Article

References (58)

1. Bellwood, D.R. & Choat, J.H. (1990). A functional analysis of grazing in parrotfishes (family Scaridae): the ecological implications. Environ. Biol. Fishes, 28, 189-214.
2. Bellwood, D.R. & Fulton, C.J. (2008). Sediment-mediated suppression of herbivory on coral reefs: decreasing resilience to rising sea levels and climate change? Limnol. Oceanogr., 53, 2695-2701.
3. Bellwood, D., Hughes, T., Folke, C. & Nyström, M. (2004). Confronting the coral reef crisis. Nature, 429, 827-833.
4. Bellwood, D.R., Hughes, T.P. & Hoey, A.S. (2006). Sleeping functional group drives coral-reef recovery. Curr. Biol., 16, 2434-2439.
5. Bennett, S. & Bellwood, D.R. (2011). Latitudinal variation in macroalgal consumption by fishes on the Great Barrier Reef. Mar. Ecol. Prog. Ser., 426, U241-U269.
6. Bertness, M.D., Brisson, C.P., Coverdale, T.C., Bevil, M.C., Crotty, S.M. & Suglia, E.R. (2014). Experimental predator removal causes rapid salt marsh die-off. Ecol. Lett. 17, 830-835.
7. de Bettignies, T., Wernberg, T., Lavery, P.S., Vanderklift, M.A. & Mohring, M.B. (2013). Contrasting mechanisms of dislodgement and erosion contribute to production of kelp detritus. Limnol. Oceanogr., 58, 1680-1688.
8. Bonaldo, R.M. & Bellwood, D.R. (2008). Size-dependent variation in the functional role of the parrotfish Scarus rivulatus on the Great Barrier Reef, Australia. Mar. Ecol. Prog. Ser., 360, 237-244.
9. Burkepile, D.E. & Hay, M.E. (2008). Herbivore species richness and feeding complementarity affect community structure and function on a coral reef. Proc. Natl. Acad. Sci. USA, 105, 16201-16206.
10. Burkepile, D.E. & Hay, M.E. (2011). Feeding complementarity versus redundancy among herbivorous fishes on a Caribbean reef. Coral Reefs, 30, 351-362.
11. Cai, W., Wang, G., Santoso, A., McPhaden, M.J., Wu, L., Jin, F.-F. et al. (2015). Increased frequency of extreme La Nina events under greenhouse warming. Nat. Clim. Chang., 5, 132-137.
12. Cappo, M., Harvey, E., Malcolm, H. & Speare, P. (2003). Potential of video techniques to monitor diversity, abundance and size of fish in studies of marine protected areas. In: Aquatic Protected Areas-What Works Best and How Do We Know: World Congress on Protected Areas. Cairns, Australia, August 2002 (ed. Beumer, J.P., Grant, A. & Smith, D.C.) Australian Society for fish biology, pp. 455-464.
13. Chong-Seng, K., Nash, K., Bellwood, D. & Graham, N. (2014). Macroalgal herbivory on recovering versus degrading coral reefs. Coral Reefs, 33, 409-419.
14. Coleman, M.A., Roughan, M., Macdonald, H.S., Connell, S.D., Gillanders, B.M., Kelaher, B.P. et al. (2011). Variation in the strength of continental boundary currents determines continent-wide connectivity in kelp. J. Ecol., 99, 1026-1032.
15. Connell, S.D., Russell, B.D. & Irving, A.D. (2011). Can strong consumer and producer effects be reconciled to better forecast 'catastrophic'phase-shifts in marine ecosystems? J. Exp. Mar. Biol. Ecol., 400, 296-301.
16. Connell, S., Foster, M. & Airoldi, L. (2014). What are algal turfs? Towards a better description of turfs. Mar. Ecol. Prog. Ser., 495, 299-307.
17. Flukes, E., Johnson, C. & Ling, S. (2012). Forming sea urchin barrens from the inside out: an alternative pattern of overgrazing. Mar. Ecol. Prog. Ser., 464, 179-194.
18. Fox, R. & Bellwood, D. (2008a). Remote video bioassays reveal the potential feeding impact of the rabbitfish Siganus canaliculatus (f: Siganidae) on an inner-shelf reef of the Great Barrier Reef. Coral Reefs, 27, 605-615.
19. Fox, R.J. & Bellwood, D.R. (2008b). Direct versus indirect methods of quantifying herbivore grazing impact on a coral reef. Mar. Biol., 154, 325-334.
20. Froese, R. & Pauly, D. (2014). FishBase. World Wide Web electronic publication. Available at: http://www.fishbase.org, version (04/2014). Last accessed 5 October 2014.
21. Graham, N.A., Bellwood, D.R., Cinner, J.E., Hughes, T.P., Norström, A.V. & Nyström, M. (2013). Managing resilience to reverse phase shifts in coral reefs. Frontiers in Ecology and the Environment, 11, 541-548.
22. Harvey, E.S. & Shortis, M.R. (1998). Calibration stability of an underwater stereo-video system: implications for measurement accuracy and precision. Mar. Technol. Soc. J., 32, 3-17.
23. Hoey, A. & Bellwood, D. (2008). Cross-shelf variation in the role of parrotfishes on the Great Barrier Reef. Coral Reefs, 27, 37-47.
24. Hoey, A.S. & Bellwood, D.R. (2009). Limited functional redundancy in a high diversity system: single species dominates key ecological process on coral reefs. Ecosystems, 12, 1316-1328.
25. Hoey, A. & Bellwood, D. (2010). Cross-shelf variation in browsing intensity on the Great Barrier Reef. Coral Reefs, 29, 499-508.
26. Hoey, A.S. & Bellwood, D.R. (2011). Suppression of herbivory by macroalgal density: a critical feedback on coral reefs? Ecol. Lett., 14, 267-273.
27. Kortsch, S., Primicerio, R., Beuchel, F., Renaud, P.E., Rodrigues, J., Lonne, O.J. et al. (2012). Climate-driven regime shifts in Arctic marine benthos. Proc. Natl. Acad. Sci. USA, 109, 14052-14057.
28. Krause-Jensen, D., Marba, N., Olesen, B., Sejr, M.K., Christensen, P.B., Rodrigues, J. et al. (2012). Seasonal sea ice cover as principal driver of spatial and temporal variation in depth extension and annual production of kelp in Greenland. Glob. Change Biol., 18, 2981-2994.
29. Kulbicki, M., Guillemot, N. & Amand, M. (2005). A general approach to length-weight relationships for New Caledonian lagoon fishes. Cybium, 29, 235-252.
30. Last, P.R., White, W.T., Gledhill, D.C., Hobday, A.J., Brown, R., Edgar, G.J. et al. (2011). Long-term shifts in abundance and distribution of a temperate fish fauna: a response to climate change and fishing practices. Glob. Ecol. Biogeogr., 20, 58-72.
31. Ling, S., Johnson, C., Frusher, S. & Ridgway, K. (2009a). Overfishing reduces resilience of kelp beds to climate-driven catastrophic phase shift. Proc. Natl Acad. Sci., 106, 22341-22345.
32. Ling, S., Johnson, C., Ridgway, K., Hobday, A. & Haddon, M. (2009b). Climate-driven range extension of a sea urchin: inferring future trends by analysis of recent population dynamics. Glob. Change Biol., 15, 719-731.
33. Longo, G. & Floeter, S. (2012). Comparison of remote video and diver's direct observations to quantify reef fishes feeding on benthos in coral and rocky reefs. J. Fish Biol., 81, 1773-1780.
34. Michael, P.J., Hyndes, G.A., Vanderklift, M.A. & Vergés, A. (2013). Identity and behaviour of herbivorous fish influence large-scale spatial patterns of macroalgal herbivory in a coral reef. Mar. Ecol. Prog. Ser., 482, 227-240.
35. Mumby, P.J., Dahlgren, C.P., Harborne, A.R., Kappel, C.V., Micheli, F., Brumbaugh, D.R. et al. (2006). Fishing, trophic cascades, and the process of grazing on coral reefs. Science, 311, 98-101.
36. Pace, M.L., Cole, J.J., Carpenter, S.R. & Kitchell, J.F. (1999). Trophic cascades revealed in diverse ecosystems. Trends Ecol. Evol., 14, 483-488.
37. Pages, J.F., Farina, S., Gera, A., Arthur, R., Romero, J. & Alcoverro, T. (2012). Indirect interactions in seagrasses: fish herbivores increase predation risk to sea urchins by modifying plant traits. Funct. Ecol., 26, 1015-1023.
38. Pearce, A.F. & Feng, M. (2013). The rise and fall of the "marine heat wave" off Western Australia during the summer of 2010/2011. J. Mar. Syst., 111, 139-156.
39. Poloczanska, E.S., Brown, C.J., Sydeman, W.J., Kiessling, W., Schoeman, D.S., Moore, P.J. et al. (2013). Global imprint of climate change on marine life. Nat. Clim. Chang., 3, 919-925.
40. Poore, A.G., Campbell, A.H., Coleman, R.A., Edgar, G.J., Jormalainen, V., Reynolds, P.L. et al. (2012). Global patterns in the impact of marine herbivores on benthic primary producers. Ecol. Lett., 15, 912-922.
41. Rasher, D.B., Hoey, A.S. & Hay, M.E. (2013). Consumer diversity interacts with prey defenses to drive ecosystem function. Ecology, 94, 1347-1358.
42. Robson, S., Shortis, M. & Woodhouse, N. (2006). Vision Measurement System (VMS). Geometric Software, Coburg, Australia.
43. Saunders, B.J., Harvey, E.S. & Kendrick, G.A. (2014). Factors influencing distribution and habitat associations in an endemic group of temperate Western Australian reef fishes over a latitudinal gradient. Mar. Ecol. Prog. Ser., 517, 193-208.
44. Schmitz, O.J., Hambäck, P.A. & Beckerman, A.P. (2000). Trophic cascades in terrestrial systems: a review of the effects of carnivore removals on plants. Am. Nat., 155, 141-153.
45. Smale, D.A. & Wernberg, T. (2013). Extreme climatic event drives range contraction of a habitat-forming species. Proc. Biol. Sci., 280, 20122829.
46. Taylor, D.I. & Schiel, D.R. (2010). Algal populations controlled by fish herbivory across a wave exposure gradient on southern temperate shores. Ecology, 91, 201-211.
47. Taylor, R.B. & Willis, T.J. (1998). Relationships amongst length, weight and growth of north-eastern New Zealand reef fishes. Mar. Freshw. Res., 49, 255-260.
48. Tummers, B. (2006). DataThief III. Available at http://datathief.org/
49. Vergés, A., Steinberg, P.D., Hay, M.E., Poore, A.G., Campbell, A.H., Ballesteros, E. et al. (2014a). The tropicalization of temperate marine ecosystems: climate-mediated changes in herbivory and community phase shifts. Proc. Biol. Sci., 281, 20140846.
50. Vergés, A., Tomas, F., Cebrian, E., Ballesteros, E., Kizilkaya, Z., Dendrinos, P. et al. (2014b). Tropical rabbitfish and the deforestation of a warming temperate sea. J. Ecol. 102, 1518-1527.
51. Waite, A., Thompson, P., Pesant, S., Feng, M., Beckley, L., Domingues, C. et al. (2007). The Leeuwin Current and its eddies: an introductory overview. Deep Sea Res. Part II, 54, 789-796.
52. Wardle, D.A., Bardgett, R.D., Callaway, R.M. & Van der Putten, W.H. (2011). Terrestrial ecosystem responses to species gains and losses. Science, 332, 1273-1277.
53. Watson, D.L., Harvey, E.S., Anderson, M.J. & Kendrick, G.A. (2005). A comparison of temperate reef fish assemblages recorded by three underwater stereo-video techniques. Mar. Biol., 148, 415-425.
54. Welsh, J. & Bellwood, D. (2014). Herbivorous fishes, ecosystem function and mobile links on coral reefs. Coral Reefs, 33, 303-311.
55. Wernberg, T., Coleman, M., Fairhead, A., Miller, S. & Thomsen, M. (2003). Morphology of Ecklonia radiata (Phaeophyta: Laminarales) along its geographic distribution in south-western Australia and Australasia. Mar. Biol., 143, 47-55.
56. Wernberg, T., Thomsen, M.S., Tuya, F., Kendrick, G.A., Staehr, P.A. & Toohey, B.D. (2010). Decreasing resilience of kelp beds along a latitudinal temperature gradient: potential implications for a warmer future. Ecol. Lett., 13, 685-694.
57. Wernberg, T., Smale, D.A., Tuya, F., Thomsen, M.S., Langlois, T.J., de Bettignies, T. et al. (2013). An extreme climatic event alters marine ecosystem structure in a global biodiversity hotspot. Nat. Clim. Chang., 3, 78-82.
58. Zarnetske, P.L., Skelly, D.K. & Urban, M.C. (2012). Biotic multipliers of climate change. Science, 336, 1516-1518.