Advertisement

Coral Reefs

, Volume 37, Issue 4, pp 1075–1084 | Cite as

Holdfasts of Sargassum swartzii are resistant to herbivory and resilient to damage

  • Zoe LofflerEmail author
  • Alexia Graba-Landry
  • Joel T. Kidgell
  • Eva C. McClure
  • Morgan S. Pratchett
  • Andrew S. Hoey
Report

Abstract

The importance of herbivory in both preventing and reversing shifts to macroalgae dominance on coral reefs has been extensively investigated. However, most studies examining the capacity for herbivores to consume fleshy macroalgae (e.g., Sargassum) have investigated removal of the ‘leafy’ biomass without considering the susceptibility of other components of the macroalga, in particular the holdfast, to herbivory. Here, we investigate the susceptibility of Sargassum components (blades, stipes and holdfasts) to herbivory and investigate the capacity for Sargassum to regrow following damage to the holdfast. We placed entire thalli of Sargassum swartzii on the reef crest at Lizard Island, northern Great Barrier Reef, for 24 d, and used photographs and video recordings to quantify rates of removal over this period. The blades of the S. swartzii were rapidly removed (100% in 2 d), whereas the stipes were less susceptible to herbivores, with 72% of experimental thalli having partial stipes remaining after 24 d. Only one holdfast (out of 54) was removed during the experiment, while all of the remaining holdfasts were largely undamaged. When S. swartzii holdfasts were experimentally damaged, we found no detectable effect on thallus height or holdfast size among regrown thalli after 1 y. There was, however, a 50% reduction in survival for S. swartzii individuals when 75% of the holdfast was removed. This study shows that holdfasts of S. swartzii are extremely resistant to herbivory, and that incidental bites on S. swartzii holdfasts are unlikely to affect their growth or survival unless three-quarters of the holdfast is removed. The capacity of Sargassum to regenerate from damaged holdfasts, coupled with the low rate of herbivory on holdfasts, suggests that sustained browsing (preventing regrowth of the stipe and blades) may be more important in reversing macroalgae dominance than physical removal of holdfasts by herbivorous fishes.

Keywords

Herbivory Sargassum Holdfasts Regime shift Coral reef Resilience Nitrogen 

Notes

Acknowledgements

We would like to thank G. Torras Jorda for field assistance and the staff at Lizard Island Research Station for invaluable field support. Financial support was provided by The Ian Potter Doctoral Fellowship at Lizard Island (ZL) and the Australian Research Council (ASH DE130100688).

Compliance with ethical standards

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

Supplementary material

338_2018_1745_MOESM1_ESM.docx (913 kb)
Supplementary material 1 (DOCX 912 kb)

References

  1. Adam TC, Schmitt RJ, Holbrook SJ, Brooks AJ, Edmunds PJ, Carpenter RC, Bernardi G (2011) Herbivory, Connectivity, and Ecosystem Resilience: Response of a Coral Reef to a Large-Scale Perturbation. Plos One 6:e23717CrossRefGoogle Scholar
  2. Ang PO Jr (1985) Regeneration Studies of Sargassum siliquoswn J. ag. and S. paniculatum J. Ag. (Phaeophyta, Sargassaceae). Botanica marina 28:231–236CrossRefGoogle Scholar
  3. Battista W, Kelly RP, Erickson A, Fujita R (2016) A comprehensive method for assessing marine resource governance: case study in Kāne’ohe Bay, Hawai’i. Coastal Management 44:295–332CrossRefGoogle Scholar
  4. Bellwood DR, Hughes TP, Folke C, Nystrom M (2004) Confronting the coral reef crisis. Nature 429:827–833CrossRefGoogle Scholar
  5. Bellwood DR, Hughes TP, Hoey AS (2006) Sleeping functional group drives coral-reef recovery. Current Biology 16:2434–2439CrossRefGoogle Scholar
  6. Bennett S, Bellwood D (2011) Latitudinal variation in macroalgal consumption by fishes on the Great Barrier Reef. Marine Ecology Progress Series 426:241–252CrossRefGoogle Scholar
  7. Choat JH, Robbins WD, Clements KD (2004) The trophic status of herbivorous fishes on coral reefs. Marine Biology 145:445–454CrossRefGoogle Scholar
  8. Chong-Seng KM, Nash KL, Bellwood DR, Graham NAJ (2014) Macroalgal herbivory on recovering versus degrading coral reefs. Coral Reefs 33:409–419CrossRefGoogle Scholar
  9. Clements KD, Choat JH (1995) Fermentation in Tropical Marine Herbivorous Fishes. Physiol Zool 68:355–378CrossRefGoogle Scholar
  10. Clements KD, German DP, Piché J, Tribollet A, Choat JH (2016) Integrating ecological roles and trophic diversification on coral reefs: multiple lines of evidence identify parrotfishes as microphages. Biological Journal of the Linnean Society 120:729–751Google Scholar
  11. Conklin EJ, Smith JE (2005) Abundance and spread of the invasive red algae, Kappaphycus spp., in Kane’ohe Bay, Hawai’i and an experimental assessment of management options. Biological Invasions 7:1029–1039CrossRefGoogle Scholar
  12. De’ath G, Fabricius KE, Sweatman H, Puotinen M (2012) The 27–year decline of coral cover on the Great Barrier Reef and its causes. Proceedings of the National Academy of Sciences USA 109:17995–17999CrossRefGoogle Scholar
  13. Dell CLA, Longo GO, Hay ME (2016) Positive Feedbacks Enhance Macroalgal Resilience on Degraded Coral Reefs. PloS one 11:e0155049CrossRefGoogle Scholar
  14. Diaz-Pulido G, McCook LJ (2002) The fate of bleached corals: Patterns and dynamics of algal recruitment. Marine Ecology Progress Series 232:115–128CrossRefGoogle Scholar
  15. Diaz-Pulido G, McCook LJ (2003) Relative roles of herbivory and nutrients in the recruitment of coral-reef seaweeds. Ecology 84:2026–2033CrossRefGoogle Scholar
  16. Fishelson L, Delarea Y (2014) Comparison of the oral cavity architecture in surgeonfishes (Acanthuridae, Teleostei), with emphasis on the taste buds and jaw “retention plates”. Environmental biology of fishes 97:173–185CrossRefGoogle Scholar
  17. Gevaert F, Davoult D, Creach A, Kling R, Janquin MA, Seuront L, Lemoine Y (2001) Carbon and nitrogen content of Laminaria saccharina in the eastern English Channel: biometrics and seasonal variations. J Mar Biol Assoc UK 81:727–734CrossRefGoogle Scholar
  18. Gilmour JP, Smith LD, Heyward AJ, Baird AH, Pratchett MS (2013) Recovery of an isolated coral reef system following severe disturbance. Science 340:69–71CrossRefGoogle Scholar
  19. Gomez IM, Westermeier RC (1991) Frond regrowth from basal disc in Iridaea laminarioides (Rhodophyta, Gigartinales) at Mehuín, southern Chile. Marine Ecology Progress Series 73:83–91CrossRefGoogle Scholar
  20. Goreau TJ, Smith JE, Conklin EJ, Smith CM, Hunter CL (2008) Fighting algae in Kaneohe Bay. Science 319:157–158CrossRefGoogle Scholar
  21. Gorham J, Lewey SA (1984) Seasonal changes in the chemical composition of Sargassum muticum. Marine biology 80:103–107CrossRefGoogle Scholar
  22. Graham NAJ, Bellwood DR, Cinner JE, Hughes TP, Norström AV, Nyström M (2013) Managing resilience to reverse phase shifts in coral reefs. Frontiers in Ecology and the Environment 11:541–548CrossRefGoogle Scholar
  23. Harborne AR, Rogers A, Bozec Y-M, Mumby PJ (2017) Multiple Stressors and the Functioning of Coral Reefs. Annu Rev Mar Sci 9:445–468CrossRefGoogle Scholar
  24. Hay ME (1981) Herbivory, Algal Distribution, and the Maintenance of Between-Habitat Diversity on a Tropical Fringing Reef. The American Naturalist 118:520–540CrossRefGoogle Scholar
  25. Heron SF, Maynard JA, Van Hooidonk R, Eakin CM (2016) Warming trends and bleaching stress of the world’s coral reefs 1985–2012. Sci Rep-Uk 6:38402CrossRefGoogle Scholar
  26. Hoey AS, Bellwood DR (2009) Limited functional redundancy in a high diversity system: single species dominates key ecological process on coral reefs. Ecosystems 12:1316–1328CrossRefGoogle Scholar
  27. Hoey AS, Bellwood DR (2010a) Cross-shelf variation in browsing intensity on the Great Barrier Reef. Coral Reefs 29:499–508CrossRefGoogle Scholar
  28. Hoey AS, Bellwood DR (2010b) Damselfish territories as a refuge for macroalgae on coral reefs. Coral Reefs 29:107–118CrossRefGoogle Scholar
  29. Hoey AS, Bellwood DR (2011) Suppression of herbivory by macroalgal density: a critical feedback on coral reefs? Ecology Letters 14:267–273CrossRefGoogle Scholar
  30. Hughes TP, Tanner JE (2000) Recruitment failure, life histories, and long-term decline of Caribbean corals. Ecology 81:2250–2263CrossRefGoogle Scholar
  31. Hughes TP, Rodrigues MJ, Bellwood DR, Ceccarelli D, Hoegh-Guldberg O, McCook L, Moltschaniwskyj N, Pratchett MS, Steneck RS, Willis B (2007) Phase shifts, herbivory, and the resilience of coral reefs to climate change. Curr Biol 17:360–365CrossRefGoogle Scholar
  32. Hughes TP, Kerry JT, Álvarez-Noriega M, Álvarez-Romero JG, Anderson KD, Baird AH, Babcock RC, Beger M, Bellwood DR, Berkelmans R, Bridge TC, Butler IR, Byrne M, Cantin NE, Comeau S, Connolly SR, Cumming GS, Dalton SJ, Diaz-Pulido G, Eakin CM, Figueira WF, Gilmour JP, Harrison HB, Heron SF, Hoey AS, Hobbs J-PA, Hoogenboom MO, Kennedy EV, C-y Kuo, Lough JM, Lowe RJ, Liu G, McCulloch MT, Malcolm HA, McWilliam MJ, Pandolfi JM, Pears RJ, Pratchett MS, Schoepf V, Simpson T, Skirving WJ, Sommer B, Torda G, Wachenfeld DR, Willis BL, Wilson SK (2017) Global warming and recurrent mass bleaching of corals. Nature 543:373–377CrossRefGoogle Scholar
  33. Konow N, Bellwood DR, Wainwright PC, Kerr AM (2008) Evolution of novel jaw joints promote trophic diversity in coral reef fishes. Biological Journal of the Linnean Society 93:545–555CrossRefGoogle Scholar
  34. Lefèvre CD, Bellwood DR (2010) Seasonality and dynamics in coral reef macroalgae: variation in condition and susceptibility to herbivory. Marine biology 157:955–965CrossRefGoogle Scholar
  35. Loffler Z, Hoey AS (2018) Canopy-forming macroalgal beds (Sargassum) on coral reefs are resilient to physical disturbance. J Ecol 106:1156–1164CrossRefGoogle Scholar
  36. McCook LJ, Chapman ARO (1992) Vegetative regeneration of Fucus rockweed canopy as a mechanism of secondary succession on an exposed rocky shore. Botanica marina 35:35–46CrossRefGoogle Scholar
  37. Michael PJ, Hyndes GA, Vanderklift MA, 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 482:227–240CrossRefGoogle Scholar
  38. Mumby PJ (2006) The impact of exploiting grazers (Scaridae) on the dynamics of Caribbean coral reefs. Ecological Applications 16:747–769CrossRefGoogle Scholar
  39. Mumby PJ, Steneck RS (2008) Coral reef management and conservation in light of rapidly evolving ecological paradigms. Trends Ecol Evol 23:555–563CrossRefGoogle Scholar
  40. Mumby PJ, Hastings A, Edwards HJ (2007) Thresholds and the resilience of Caribbean coral reefs. Nature 450:98–101CrossRefGoogle Scholar
  41. Norstrom AV, Nystrom M, Lokrantz J, Folke C (2009) Alternative states on coral reefs: beyond coral-macroalgal phase shifts. Marine Ecology Progress Series 376:295–306CrossRefGoogle Scholar
  42. O’Brien JM, Scheibling RE (2016) Nipped in the bud: mesograzer feeding preference contributes to kelp decline. Ecology 97:1873–1886CrossRefGoogle Scholar
  43. Poore AG, Gutow L, Pantoja JF, Tala F, Madariaga DJ, Thiel M (2014) Major consequences of minor damage: impacts of small grazers on fast-growing kelps. Oecologia 174:789–801CrossRefGoogle Scholar
  44. Purcell SW, Bellwood DR (1993) A functional analysis of food procurement in two surgeonfish species, Acanthurus nigrofuscus and Ctenochaetus striatus (Acanthuridae). Environmental Biology of Fishes 37:139–159CrossRefGoogle Scholar
  45. Rasher DB, Hoey AS, Hay ME (2013) Consumer diversity interacts with prey defenses to drive ecosystem function. Ecology 94:1347–1358CrossRefGoogle Scholar
  46. Scheffer M, Carpenter S, Foley JA, Folke C, Walker B (2001) Catastrophic shifts in ecosystems. Nature 413:591–596CrossRefGoogle Scholar
  47. Steinberg P, Edyvane K, De Nys R, Birdsey R, Van Altena I (1991) Lack of avoidance of phenolic-rich brown algae by tropical herbivorous fishes. Mar Biol 109:335–343CrossRefGoogle Scholar
  48. Streit RP, Hoey AS, Bellwood DR (2015) Feeding characteristics reveal functional distinctions among browsing herbivorous fishes on coral reefs. Coral Reefs 34:1037–1047CrossRefGoogle Scholar
  49. Taylor RB, Sotka E, Hay ME (2002) Tissue-specific induction of herbivore resistance: seaweed response to amphipod grazing. Oecologia 132:68–76CrossRefGoogle Scholar
  50. Tebbett SB, Goatley CHR, Bellwood DR (2017) Clarifying functional roles: algal removal by the surgeonfishes Ctenochaetus striatus and Acanthurus nigrofuscus. Coral Reefs 36:803–813CrossRefGoogle Scholar
  51. van de Leemput IA, Hughes TP, van Nes EH, Scheffer M (2016) Multiple feedbacks and the prevalence of alternate stable states on coral reefs. Coral Reefs 35:857–865CrossRefGoogle Scholar
  52. Venera-Ponton DE, Diaz-Pulido G, McCook LJ, Rangel-Campo A (2011) Macroalgae reduce growth of juvenile corals but protect them from parrotfish damage. Marine Ecology Progress Series 421:109–115CrossRefGoogle Scholar
  53. Vuki VC, Price IR (1994) Seasonal changes in the Sargassum populations on a fringing coral reef, Magnetic Island, Great Barrier Reef region, Australia. Aquat Bot 48:153–166CrossRefGoogle Scholar
  54. Webster FJ, Babcock RC, Van Keulen M, Loneragan NR (2015) Macroalgae inhibits larval settlement and increases recruit mortality at Ningaloo Reef. Western Australia. PLoS One 10:e0124162CrossRefGoogle Scholar
  55. Westermeier R, Murúa P, Patiño DJ, Muñoz L, Ruiz A, Atero C, Müller DG (2013) Utilization of holdfast fragments for vegetative propagation of Macrocystis integrifolia in Atacama, Northern Chile. Journal of Applied Phycology 25:639–642CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.ARC Centre of Excellence for Coral Reef StudiesJames Cook UniversityTownsvilleAustralia
  2. 2.MACRO: The Centre for Macroalgal Resources and BiotechnologyJames Cook UniversityTownsvilleAustralia
  3. 3.College of Science and EngineeringJames Cook UniversityTownsvilleAustralia

Personalised recommendations