Advertisement

Coral Reefs

, Volume 34, Issue 4, pp 1023–1035 | Cite as

Small herbivores suppress algal accumulation on Agatti atoll, Indian Ocean

  • Nicole H. CernohorskyEmail author
  • Timothy R. McClanahan
  • Idrees Babu
  • Michal Horsák
Report

Abstract

Despite large herbivorous fish being generally accepted as the main group responsible for preventing algal accumulation on coral reefs, few studies have experimentally examined the relative importance of herbivore size on algal communities. This study used exclusion cages with two different mesh sizes (1 × 1 cm and 6 × 6 cm) to investigate the impact of different-sized herbivores on algal accumulation rates on the shallow (<2 m) back-reef of Agatti atoll, Lakshadweep. The fine-mesh cages excluded all visible herbivores, which had rapid and lasting effects on the benthic communities, and, after 127 d of deployment, there was a visible and significant increase in algae (mainly macroalgae) with algal volume being 13 times greater than in adjacent open areas. The coarse-mesh cages excluded larger fishes (>8 cm body depth) while allowing smaller fishes to access the plots. In contrast to the conclusions of most previous studies, the exclusion of large herbivores had no significant effect on the accumulation of benthic algae and the amount of algae present within the coarse-mesh cages was relatively consistent throughout the experimental period (around 50 % coverage and 1–2 mm height). The difference in algal accumulation between the fine-mesh and coarse-mesh cages appears to be related to the actions of small individuals from 12 herbivorous fish species (0.17 ind. m−2 and 7.7 g m−2) that were able to enter through the coarse mesh. Although restricted to a single habitat, these results suggest that when present in sufficient densities and diversity, small herbivorous fishes can prevent the accumulation of algal biomass on coral reefs.

Keywords

Ecological redundancy Diet specialization Macroalgae Phase shifts Size-dependent processes 

Notes

Acknowledgments

This work was supported by the Czech Science Foundation 526/09/H025. Necessary permissions to reside and carry out research on the islands of Lakshadweep were provided by the Bombay Natural History Society and the Department of Environment and Forests, Lakshadweep. Thanks to M. K. M. Hussain, M. Noushad, Salahudheen V. K., Sakeer Hussain, P. Sahib, and K. Sahib for valuable assistance in the field.

Supplementary material

338_2015_1331_MOESM1_ESM.docx (19 kb)
Supplementary material 1 (DOCX 19 kb)

References

  1. Anthony KRN, Maynard JA, Guillermodiaz-Pulido G, Mumby PJ, Marshal PA, Long C, Hoegh-Guldberg O (2011) Ocean acidification and warming will lower coral reef resilience. Glob Chang Biol 17:1798–1808PubMedCentralCrossRefGoogle Scholar
  2. Arthur R, Done TJ, Marsh H, Harriott V (2006) Local processes strongly influence post-bleaching benthic recovery in the Lakshadweep Islands. Coral Reefs 25:427–440CrossRefGoogle Scholar
  3. Ateweberhan M, McClanahan TR, Graham NAJ, Sheppard C (2011) Episodic heterogeneous decline and recovery of coral cover in the Western Indian Ocean. Coral Reefs 30:739–752CrossRefGoogle Scholar
  4. Bellwood DR (1988) Ontogenetic changes in diet of early post-settlement Scarus species (Pisces: Scaridae). J Fish Biol 33:213–219CrossRefGoogle Scholar
  5. Bellwood DR, Hoey AS, Choat JH (2003) Limited functional redundancy in high diversity systems: resilience and ecosystem function on coral reefs. Ecol Lett 6:281–285CrossRefGoogle Scholar
  6. Bellwood DR, Hughes TP, Hoey AS (2006) Sleeping functional group drives coral-reef recovery. Curr Biol 16:2434–2439CrossRefPubMedGoogle Scholar
  7. Bellwood DR, Hoey AS, Hughes TP (2012) Human activity selectively impacts the ecosystem roles of parrotfishes on coral reefs. Proc R Soc Lond B Biol Sci 279:1621–1629CrossRefGoogle Scholar
  8. Bellwood DR, Hughes TP, Folke C, Nyström M (2004) Confronting the coral reef crisis. Nature 429:827–833CrossRefPubMedGoogle Scholar
  9. Bonaldo RM, Bellwood DR (2008) Size-dependent variation in the functional role of the parrotfish Scarus rivulatus on the Great Barrier Reef, Australia. Mar Ecol Prog Ser 360:237–244CrossRefGoogle Scholar
  10. Bonaldo RM, Bellwood DR (2011) Parrotfish predation on massive Porites on the Great Barrier Reef. Coral Reefs 30:259–269CrossRefGoogle Scholar
  11. Bonaldo RM, Hoey AS, Bellwood DR (2014) The ecosystem roles of parrotfishes on tropical reefs. Oceanogr Mar Biol Annu Rev 52:81–132Google Scholar
  12. Brown MB, Forsythe AB (1974) The small sample behavior of some statistics which test the equality of several means. Technometrics 16:129–132CrossRefGoogle Scholar
  13. Bruggemann JH, Van Kessel AM, Van Rooij JM, Breeman AM (1996) Bioerosion and sediment ingestion by the Caribbean parrotfish Scarus vetula and Sparisoma viride: implications of fish size, feeding mode and habitat use. Mar Ecol Prog Ser 134:59–71CrossRefGoogle Scholar
  14. Bruggemann JH, Begeman J, Bosma EM, Verburg P, Breeman AM (1994) Foraging by the stoplight parrotfish Sparisoma viride. II. Intake and assimilation of food, protein, and energy. Mar Ecol Prog Ser 106:57–71CrossRefGoogle Scholar
  15. Bruno JF, Selig ER (2007) Regional decline of coral cover in the Indo-Pacific: timing, extent, and subregional comparisons. PLoS One 2:e711PubMedCentralCrossRefPubMedGoogle Scholar
  16. Campbell AC, Dart JK, Head SM, Ormond RF (1973) The feeding activity of Echinostrephus molaris (de Blainville) in the central Red Sea. Mar Behav Physiol 2:155–169CrossRefGoogle Scholar
  17. Carpenter RC (1981) Grazing by Diadema antillarum (Philippi) and its effects on the benthic algal community. J Mar Res 39:749–765Google Scholar
  18. Cheal AJ, MacNeil MA, Cripps E, Emslie MJ, Jonker M, Schaffelke B, Sweatman H (2010) Coral–macroalgal phase shifts or reef resilience: links with diversity and functional roles of herbivorous fishes on the Great Barrier Reef. Coral Reefs 29:1005–1015CrossRefGoogle Scholar
  19. Chong-Seng KM, Nash KL, Bellwood DR, Graham NAJ (2014) Macroalgal herbivory on recovering versus degrading coral reefs. Coral Reefs 33:409–419CrossRefGoogle Scholar
  20. Cvitanovic C, Bellwood DR (2009) Local variation in herbivore feeding activity on an inshore reef of the Great Barrier Reef. Coral Reefs 28:127–133CrossRefGoogle Scholar
  21. Dudgeon SR, Aronson RB, Bruno JF, Precht WF (2010) Phase shifts and stable states on coral reefs. Mar Ecol Prog Ser 413:201–216CrossRefGoogle Scholar
  22. Edwards CB, Friedlander AM, Green AG, Hardt MJ, Sala E, Sweatman HP, Williams ID, Zgliczynski B, Sandin SA, Smith JE (2014) Global assessment of the status of coral reef herbivorous fishes: evidence for fishing effects. Proc R Soc Lond B Biol Sci 281:20131835CrossRefGoogle Scholar
  23. Fox RJ, Bellwood DR (2008) 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 27:605–615CrossRefGoogle Scholar
  24. Fox RJ, Bellwood DR (2014) Herbivores in a small world: network theory highlights vulnerability in the function of herbivory on coral reefs. Funct Ecol 28:642–651CrossRefGoogle Scholar
  25. Games PA, Howell JF (1976) Pair wise multiple comparisons procedures with unequal n’s and/or variances: a Monte Carlo study. J Educ Behav Stat 1:113–125CrossRefGoogle Scholar
  26. Gomes I, Erzini K, McClanahan TR (2014) Trap modification opens new gates to achieve sustainable coral reef fisheries. Aquat Conserv 24:680–695CrossRefGoogle Scholar
  27. Graham NA, Wilson SK, Jennings S, Polunin NV, Bijoux JP, Robinson J (2006) Dynamic fragility of oceanic coral reef ecosystems. Proc Natl Acad Sci USA 103:8425–8429PubMedCentralCrossRefPubMedGoogle Scholar
  28. Graham NA, Bellwood DR, Cinner JE, Hughes TP, Norström AV, Nyström M (2013) Managing resilience to reverse phase shifts in coral reefs. Front Ecol Environ 11:541–548CrossRefGoogle Scholar
  29. Green AL, Bellwood DR, Choat H (2009) Monitoring functional groups of herbivorous reef fishes as indicators of coral reef resilience—A practical guide for coral reef managers in the Asia Pacific region. Switzerland, IUCN working group on Climate Change and Coral Reefs, Gland, p 70Google Scholar
  30. Hamilton SL, Smith JE, Price NN, Sandin SA (2014) Quantifying patterns of fish herbivory on Palmyra Atoll (USA), an uninhabited predator-dominated central Pacific coral reef. Mar Ecol Prog Ser 501:141–155CrossRefGoogle Scholar
  31. Hay ME (1984) Patterns of fish and urchin grazing on Caribbean coral reefs: are previous results typical? Ecology 65:446–454CrossRefGoogle Scholar
  32. Hixon MA, Brostoff WN (1996) Succession and herbivory: effects of differential fish grazing on Hawaiian coral-reef algae. Ecol Monogr 66:67–90CrossRefGoogle Scholar
  33. Hoey AS, Bellwood DR (2008) Cross-shelf variation in the role of parrotfishes on the Great Barrier Reef. Coral Reefs 27:37–47CrossRefGoogle Scholar
  34. 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
  35. Hoey AS, Bellwood DR (2010) Among habitat variation in herbivory on Sargassum spp. On a mid-shelf reef in the northern Great Barrier Reef. Mar Biol 157:189–200CrossRefGoogle Scholar
  36. Hoey AS, Brandl SJ, Bellwood DR (2013) Diet and cross-shelf distribution of rabbitfishes (f. Siganidae) on the northern Great Barrier Reef: implications for ecosystem function. Coral Reefs 32:973–984CrossRefGoogle Scholar
  37. Hughes TP (1994) Catastrophes, phase shifts, and large-scale degradation of a Caribbean coral reef. Science 265:1547–1551CrossRefPubMedGoogle Scholar
  38. Hughes TP, Graham NA, Jackson JB, Mumby PJ, Steneck RS (2010) Rising to the challenge of sustaining coral reef resilience. Trends Ecol Evol 25:633–642CrossRefPubMedGoogle Scholar
  39. Hughes TP, Rodrigues MJ, Bellwood DR, Ceccarelli D, Hoegh-Guldberg O, McCook L, Willis B (2007) Phase shifts, herbivory, and the resilience of coral reefs to climate change. Curr Biol 17:360–365CrossRefPubMedGoogle Scholar
  40. Humphries AT, McClanahan TR, McQuaid CD (2014) Differential impacts of coral reef herbivores on algal succession in Kenya. Mar Ecol Prog Ser 504:119–132CrossRefGoogle Scholar
  41. Jayewardene D (2009) A factorial experiment quantifying the influence of parrotfish density and size on algal reduction on Hawaiian coral reefs. J Exp Mar Bio Ecol 375:64–69CrossRefGoogle Scholar
  42. Johansson CL, van de Leemput IA, Depczynski M, Hoey AS, Bellwood DR (2013) Key herbivores reveal limited functional redundancy on inshore coral reefs. Coral Reefs 32:963–972CrossRefGoogle Scholar
  43. Kulbicki M, Guillemot N, Amand M (2005) A general approach to length–weight relationships for New Caledonian lagoon fishes. Cybium 29:235–252Google Scholar
  44. Ledlie MH, Graham NAJ, Bythell JC, Wilson SK, Jennings S, Polunin NVC, Hardcastle J (2007) Phase shifts and the role of herbivory in the resilience of coral reefs. Coral Reefs 26:641–653CrossRefGoogle Scholar
  45. Lewis SM (1986) The role of herbivorous fishes in the organization of a Caribbean reef community. Ecol Monogr 56:183–200CrossRefGoogle Scholar
  46. Lokrantz J, Nystrom M, Thyresson M, Johansson CL (2008) The non-linear relationship between body size and function in parrotfishes. Coral Reefs 27:967–974CrossRefGoogle Scholar
  47. McCauley DJ, Micheli F, Young HS, Tittensor DP, Brumbaugh DR, Madin EMP, Holmes KE, Smith JE, Lotze HK, DeSalles PA, Arnold SN, Worm B (2010) Acute effects of removing large fish from a near-pristine coral reef. Mar Biol 157:2739–2750PubMedCentralCrossRefPubMedGoogle Scholar
  48. McClanahan TR (2008) Response of the coral reef benthos and herbivory to fishery closure management and the 1998 ENSO disturbance. Oecologia 155:169–177CrossRefPubMedGoogle Scholar
  49. McClanahan TR (2014) Recovery of functional groups and trophic relationships in tropical fisheries closures. Mar Ecol Prog Ser 497:13–23CrossRefGoogle Scholar
  50. McClanahan TR, Shafir SH (1990) Causes and consequences of sea urchin abundance and diversity in Kenyan coral reef lagoons. Oecologia 83:362–370CrossRefGoogle Scholar
  51. McClanahan TR, Kurtis JD (1991) Population regulation of the rock-boring sea urchin Echinometra mathaei (de Blainville). J Exp Mar Bio Ecol 147:121–146CrossRefGoogle Scholar
  52. McClanahan TR, Nugues M, Mwachireya S (1994) Fish and sea urchin herbivory and competition in Kenyan coral reef lagoons: the role of reef management. J Exp Mar Bio Ecol 184:237–254CrossRefGoogle Scholar
  53. McClanahan TR, Sala E, Stickels PA, Cokos BA, Baker AC, Starger CJ, Jones SH (2003) Interaction between nutrients and herbivory in controlling algal communities and coral condition on Glover’s Reef, Belize. Mar Ecol Prog Ser 261:135–147CrossRefGoogle Scholar
  54. McClanahan TR, Graham NAJ, MacNeil MA, Muthiga NA, Cinner JE, Bruggemann JH, Wilson SK (2011) Critical thresholds and tangible targets for ecosystem-based management of coral reef fisheries. Proc Natl Acad Sci USA 108:17230–17233PubMedCentralCrossRefPubMedGoogle Scholar
  55. McCook LJ (1996) Effects of herbivores and water quality on Sargassum distribution on the central Great Barrier Reef: crossshelf transplants. Mar Ecol Prog Ser 139:179–192CrossRefGoogle Scholar
  56. Mörk E, Sjöö GL, Kautsky N, McClanahan TR (2009) Top–down and bottom–up regulation of macroalgal community structure on a Kenyan reef. Estuar Coast Shelf Sci 84:331–336CrossRefGoogle Scholar
  57. Mumby PJ, Steneck RS, Hastings A (2013) Evidence for and against the existence of alternate attractors on coral reefs. Oikos 122:481–491CrossRefGoogle Scholar
  58. Nash KL, Graham NA, Januchowski-Hartley FA, Bellwood DR (2012) Influence of habitat condition and competition on foraging behaviour of parrotfishes. Mar Ecol Prog Ser 457:113–124CrossRefGoogle Scholar
  59. Norström AV, Nyström M, Lokrantz J, Folke C (2009) Alternative states on coral reefs: beyond coral-macroalgal phase shifts. Mar Ecol Prog Ser 376:295–306CrossRefGoogle Scholar
  60. O’Leary JK, Potts D, Schoenrock KM, McClanahan TR (2013) Fish and sea urchin grazing opens settlement space equally but urchins reduce survival of coral recruits. Mar Ecol Prog Ser 493:165–177CrossRefGoogle Scholar
  61. R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
  62. Rasher DB, Hay ME (2010) Chemically rich seaweeds poison corals when not controlled by herbivores. Proc Natl Acad Sci USA 107:9683–9688PubMedCentralCrossRefPubMedGoogle Scholar
  63. Rasher DB, Hoey AS, Hay ME (2013) Consumer diversity interacts with prey defenses to drive ecosystem function. Ecology 94:1347–1358PubMedCentralCrossRefPubMedGoogle Scholar
  64. Robertson DR, Gaines D (1986) Interference competition structures habitat use in a local assemblage of coral reef surgeonfishes. Ecology 67:1372–1383CrossRefGoogle Scholar
  65. Robertson DR, Polunin NV, Leighton K (1979) The behavioral ecology of three Indian Ocean surgeonfishes (Acanthurus lineatus, A. leucosternon and Zebrasoma scopas): their feeding strategies, and social and mating systems. Environ Biol Fishes 4:125–170CrossRefGoogle Scholar
  66. Robichaud D, Hunte W, Chapman MR (2000) Factors affecting the catchability of reef fishes in Antillean fish traps. Bull Mar Sci 67:831–844Google Scholar
  67. Russ GR (1987) Is rate of removal of algae by grazers reduced inside territories of tropical damselfishes? J Exp Mar Biol Ecol 110:1–17CrossRefGoogle Scholar
  68. Scheffer M, Carpenter S, Foley JA, Folke C, Walker B (2001) Catastrophic shifts in ecosystems. Nature 413:591–596CrossRefPubMedGoogle Scholar
  69. Sheppard CR (2003) Predicted recurrences of mass coral mortality in the Indian Ocean. Nature 425:294–297CrossRefPubMedGoogle Scholar
  70. Smith J, Smith C, Hunter C (2001) An experimental analysis of the effects of herbivory and nutrient enrichment on benthic community dynamics on a Hawaiian reef. Coral Reefs 19:332–342CrossRefGoogle Scholar
  71. Steele JH (1998) Regime shifts in marine ecosystems. Ecol Appl 8:S33–S36CrossRefGoogle Scholar
  72. Steneck RS (2001) Functional groups. In: Levin S (ed) Encyclopedia of biodiversity, vol 3. Academic Press, Princeton, pp 121–139CrossRefGoogle Scholar
  73. Steneck RS, Dethier MN (1994) A functional approach to the structure of algal dominated communities. Oikos 69:476–498CrossRefGoogle Scholar
  74. Steneck RS, Arnold SN, Mumby PJ (2014) Experiment mimics fishing on parrotfish: insights on coral reef recovery and alternative attractors. Mar Ecol Prog Ser 506:115–127CrossRefGoogle Scholar
  75. Thibaut LM, Connolly SR, Sweatman HPA (2012) Diversity and stability of herbivorous fishes on coral reefs. Ecology 93:891–901CrossRefPubMedGoogle Scholar
  76. Trapon ML, Pratchett MS, Hoey AS, Baird AH (2013) Influence of fish grazing and sedimentation on the early post-settlement survival of the tabular coral Acropora cytherea. Coral Reefs 32:1051–1059CrossRefGoogle Scholar
  77. Vanderklift MA, Lavery PS, Waddington KI (2009) Intensity of herbivory on kelp by fish and sea urchins differs from inshore and offshore reefs. Mar Ecol Prog Ser 376:203–211CrossRefGoogle Scholar
  78. Williams ID, Polunin NV, Hendrick VJ (2001) Limits to grazing by herbivorous fishes and the impact of low coral cover on macroalgal abundance on a coral reef in Belize. Mar Ecol Prog Ser 222:187–196CrossRefGoogle Scholar
  79. Wilson SK, Bellwood DR, Choat JH, Furnas MJ (2003) Detritus in the epilithic algal matrix and its use by coral reef fishes. Oceanogr Mar Biol Annu Rev 41:279–309Google Scholar
  80. Zychaluk K, Bruno JF, Clancy D, McClanahan TR, Spencer M (2012) Data-driven models of regional coral-reef dynamics. Ecol Lett 15:151–158CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.Department of Botany and Zoology, Faculty of ScienceMasaryk UniversityBrnoCzech Republic
  2. 2.Marine ProgramsWildlife Conservation SocietyBronxUSA
  3. 3.Department of Science and TechnologyCoral Reef ResearchUT of LakshadweepIndia

Personalised recommendations