Oecologia

, Volume 181, Issue 1, pp 13–24 | Cite as

Distribution, behavior, and condition of herbivorous fishes on coral reefs track algal resources

Highlighted Student Research

Abstract

Herbivore distribution can impact community structure and ecosystem function. On coral reefs, herbivores are thought to play an important role in promoting coral dominance, but how they are distributed relative to algae is not well known. Here, we evaluated whether the distribution, behavior, and condition of herbivorous fishes correlated with algal resource availability at six sites in the back reef environment of Moorea, French Polynesia. Specifically, we tested the hypotheses that increased algal turf availability would coincide with (1) increased biomass, (2) altered foraging behavior, and (3) increased energy reserves of herbivorous fishes. Fish biomass and algal cover were visually estimated along underwater transects; behavior of herbivorous fishes was quantified by observations of focal individuals; fish were collected to assess their condition; and algal turf production rates were measured on standardized tiles. The best predictor of herbivorous fish biomass was algal turf production, with fish biomass increasing with algal production. Biomass of herbivorous fishes was also negatively related to sea urchin density, suggesting competition for limited resources. Regression models including both algal turf production and urchin density explained 94 % of the variation in herbivorous fish biomass among sites spread over ~20 km. Behavioral observations of the parrotfish Chlorurus sordidus revealed that foraging area increased as algal turf cover decreased. Additionally, energy reserves increased with algal turf production, but declined with herbivorous fish density, implying that algal turf is a limited resource for this species. Our findings support the hypothesis that herbivorous fishes can spatially track algal resources on coral reefs.

Keywords

Foraging Ideal free distribution Resilience Herbivory Algal turf 

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:e23717. doi:10.1371/journal.pone.0023717 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Adler PB, Raff DA, Lauenroth WK (2001) The effect of grazing on the spatial heterogeneity of vegetation. Oecologia 128:465–479CrossRefGoogle Scholar
  3. Avgar T, Kuefler D, Fryxell M (2011) Linking rates of diffusion and consumption in relation to resources. Am Nat 178:182–190CrossRefPubMedGoogle Scholar
  4. Bellwood DR, Choat JH (1990) A functional analysis of grazing in parrotfishes (family Scaridae): the ecological implications. In: Bruton MN (ed) Alternative life-history styles of fishes. Springer, Netherlands, pp 189–214CrossRefGoogle Scholar
  5. Bellwood DR, Hughes TP, Folke C, Nyström M (2004) Confronting the coral reef crisis. Nature 429:827–833CrossRefPubMedGoogle Scholar
  6. Birrell CL, McCook LJ, Willis B, Diaz-Pulido GA (2008) Effects of benthic algae on the replenishment of corals and the implications for the resilience of coral reefs. Oceanogr Mar Biol 46:25–63Google Scholar
  7. Brooks A (2013) MCR LTER: Coral reef: long-term population and community dynamics: fishes.  http://metacat.lternet.edu/knb/metacat/knb-lter-mcr.6.48/lter. Accessed 01 Jan 2013
  8. Brown JS, Kotler BP (2004) Hazardous duty pay and foraging cost of predation. Ecol Lett 7:999–1014CrossRefGoogle Scholar
  9. Burkepile DE, Hay ME (2008) Herbivore species richness and feeding complementarity affect community structure and function on a coral reef. Proc Natl Acad Sci 105:16201–16206. doi:10.1073/pnas.0801946105 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Burkepile DE, Burns CE, Tambling CJ, Amendola E, Buis GM, Govender N, Nelson V, Thompson DI, Zinn AD, Smith MD (2013) Habitat selection by large herbivores in a southern African savanna: the relative roles of bottom-up and top-down forces. Ecosphere 11:139CrossRefGoogle Scholar
  11. Carpenter RC (1986) Partitioning herbivory and its effects on coral reef algal communities. Ecol Monogr 56:345–363CrossRefGoogle Scholar
  12. Carpenter RC (1990) Mass mortality of Diadema antillarum. Mar Biol 104:79–86CrossRefGoogle Scholar
  13. Carpenter RC (2013) MCR LTER: Coral reef: long-term population and community dynamics: other benthic invertebrates. http://metacat.lternet.edu/knb/metacat/knb-lter-mcr.8.26/lter. Accessed 01 Jan 2013
  14. Carpenter SR, Kitchell JF, Hodgson JR, Cochran PA, Elser JJ, Lodge MM, Kretchmer D, He X, Von Ende CN (1987) Regulation of lake primary productivity by food web structure. Ecology 68:1863–1876CrossRefGoogle Scholar
  15. Carpenter RC, Hackney JM, Adey WH (1991) Measurements of primary productivity and nitrogenase activity of coral reef algae in a chamber incorporating oscillatory flow. Limnol Oceanogr 36:40–49CrossRefGoogle Scholar
  16. Caughley G, Lawton JH (1981) Plant-herbivore systems. In: Caughley G, Lawton JH (eds) Theoretical ecology. Blackwell, Oxford, pp 132–166Google Scholar
  17. Charnov EL (1976) Optimal foraging: the marginal value theorem. Theor Pop Biol 9:129–136CrossRefGoogle Scholar
  18. Choat JH, Clements KD, Robbins WD (2002) The trophic status of herbivorous fishes on coral reefs—I: dietary analyses. Mar Biol 140:613–623CrossRefGoogle Scholar
  19. Done TJ (1992) Phase shifts in coral reef communities and their ecological significance. Hydrobiologia 247:121–132CrossRefGoogle Scholar
  20. Duffy JE (2002) Biodiversity and ecosystem function: the consumer connection. Oikos 99:201–219CrossRefGoogle Scholar
  21. Dulvy NK, Polunin NVC, Mill AC, Graham NAJ (2004) Size structural change in lightly exploited coral reef fish communities: evidence for weak ecological release. Can J Fish Aquat Sci 61:466–475CrossRefGoogle Scholar
  22. Ellison GN, Gotelli NJ (2004) A primer of ecological statistics. Sinauer, SunderlandGoogle Scholar
  23. Estes JA, Tinker MT, Williams TM, Doak DF (1998) Killer whale predation on sea otters linking oceanic and nearshore ecosystems. Science 282:473–476CrossRefPubMedGoogle Scholar
  24. Estes JA, Terborgh J, Brashares JS, Power ME, Berger J, Bond WJ, Carpenter SR, Essington TE, Holt RD, Jackson JBC, Marquis RJ, Oksanen L, Oksanen T, Paine RT, Pikitch EK, Ripple WJ, Sandin SA, Scheffer M, Schoener TW, Shurin JB, Sinclair ARE, Soulé ME, Virtanen R, Wardle DA (2011) Trophic downgrading of planet earth. Science 333:301–306CrossRefPubMedGoogle Scholar
  25. Fretwell SD (1972) Populations in a seasonal environment. Princeton University Press, PrincetonGoogle Scholar
  26. Fretwell SD, Lucas HL (1970) On territorial behaviour and other factors influencing habitat distribution in birds. I. Theoretical development. Acta Biotheor 19:16–36CrossRefGoogle Scholar
  27. Fryxell JM (1991) Forage quality and aggregation by large herbivores. Am Nat 138:478–498CrossRefGoogle Scholar
  28. Fryxell JM, Wilmshurst JF, Sinclair ARE (2004) Predictive models of movement by Serengeti grazers. Ecology 85:2429–2435CrossRefGoogle Scholar
  29. Gilmour JP, Smith LD, Heyward AJ, Baird AH, Pratchett MS (2013) Recovery of an isolated coral reef system following severe disturbance. Science 6128:69–71CrossRefGoogle Scholar
  30. Graham NAJ, Nash KL (2013) The importance of structural complexity in coral reef ecosystems. Coral Reefs 32:315–326. doi:10.1007/s00338-012-0984-y CrossRefGoogle Scholar
  31. Han X (2012) MCR LTER: Coral reef: diadema predation and recruitment in Moorea, French Polynesia. Retrieved January 01, 2013.  knb-lter-mcr.2003.2. http://metacat.lternet.edu/knb/metacat/knb-lter-mcr.2003.2/lter. Accessed 01 Jan 2013
  32. Hart AM, Klumpp DW, Russ GR (1996a) Response of herbivorous fishes to crown-of-thorns starfish Acanthaster planci outbreaks. I. Substratum analysis and feeding ecology of Acanthurus nigrofuscus and Scarus frenatus. Mar Ecol Prog Ser 132:11–19CrossRefGoogle Scholar
  33. Hart AM, Klumpp DW, Russ GR (1996b) Response of herbivorous fishes to crown-of-thorns starfish Acanthaster planci outbreaks. II. Density and biomass of selected species of herbivorous fish and fish-habitat correlations. Mar Ecol Prog Ser 132:21–30CrossRefGoogle Scholar
  34. Hay ME (1981) The functional morphology of turf-forming seaweeds: persistence in stressful marine habitats. Ecology 62:739–750CrossRefGoogle Scholar
  35. Hay ME (1984) Patterns of fish and urchin grazing on Caribbean coral reefs: are previous results typical? Ecology 65:446–454. doi:10.2307/1941407 CrossRefGoogle Scholar
  36. Hay ME, Taylor PR (1985) Competition between herbivorous fishes and urchins on Caribbean reefs. Oecologia 65:591–598CrossRefGoogle Scholar
  37. Hebblewhite M, Merrill EH (2009) Trade-offs between predation risk and forage differ between migrant strategies in a migratory ungulate. Ecology 90:3445–3454. doi:10.1890/08-2090.1 CrossRefPubMedGoogle Scholar
  38. Hench JL, Leichter JJ, Monismith SG (2008) Episodic circulation and exchange in a wave-driven coral reef and lagoon system. Limnol Oceanogr 53:2681–2694CrossRefGoogle Scholar
  39. Hixon MA, Brostoff WN (1983) Damselfish as keystone species in reverse: intermediate disturbance and diversity of reef algae. Science 220:511–513CrossRefPubMedGoogle Scholar
  40. Hixon MA, Brostoff WN (1996) Succession and herbivory: effects of differential fish grazing on Hawaiian coral-reef algae. Ecol Monogr 66:67–90CrossRefGoogle Scholar
  41. Hughes TP (1994) Catastrophes, phase shifts, and large-scale degradation of a Caribbean coral reef. Science 265:1547–1551CrossRefPubMedGoogle Scholar
  42. Hunte W, Wittenberg M (1992) Effects of eutrophication and sedimentation on juvenile corals. II. Settlement. Mar Biol 114:625–631CrossRefGoogle Scholar
  43. Huntly NJ (1991) Herbivores and the dynamics of communities and ecosystems. Annu Rev Ecol Syst 22:477–503CrossRefGoogle Scholar
  44. Jarman PJ (1974) The social organization of antelope in relation to their ecology. Behaviour 48:215–266CrossRefGoogle Scholar
  45. Jennings S, Polunin NVC (1997) Impacts of predator depletion by fishing on the biomass and diversity of non-target reef fish communities. Coral Reefs 16:71–82CrossRefGoogle Scholar
  46. Jones GP, Andrew NL (1990) Herbivory and patch dynamics on rocky reefs in temperate Australasia, the role of fish and sea urchins. Aust J Ecol 15:505–520CrossRefGoogle Scholar
  47. Jouffray JB, Nyström M, Norström AV, Williams ID, Wedding LM, Kittinger JN, Williams GJ (2015) Identifying multiple coral reef regimes and their drivers across the Hawaiian archipelago. Phil Trans R Soc B Biol Sci 370:20130268CrossRefGoogle Scholar
  48. Klaassen RHG, Nolet BA, Bankert D (2006) Movement of foraging tundra swans explained by spatial pattern in cryptic food densities. Ecology 87:2244–2254CrossRefPubMedGoogle Scholar
  49. Klumpp DW, McKinnon AD (1989) Temporal and spatial patterns in primary production of a coral reef epilithic algal community. J Exp Mar Biol and Ecol 131:1–22CrossRefGoogle Scholar
  50. Kohler KE, Gill SM (2006) Coral Point Count with Excel extensions (CPCe): a Visual Basic program for the determination of coral and substrate coverage using random point count methodology. Comput Geosci 32(9):1259–1269. doi:10.1016/j.cageo.2005.11.009 CrossRefGoogle Scholar
  51. Kulbicki N, Guillemot N, Amand M (2005) A general approach to length–weight relationships for New Caledonian Lagoon fishes. Cybium 29:235–252Google Scholar
  52. Lewis SM (1986) The role of herbivorous fishes in the organization of a Caribbean reef community. Ecol Monogr 56:183–200CrossRefGoogle Scholar
  53. McClanahan TR (1997) Primary succession of coral-reef algae: differing patterns on fished versus unfished reefs. J Exp Mar Biol Ecol 218:77–102CrossRefGoogle Scholar
  54. McClanahan TR, Shafir SH (1990) Causes and consequences of sea urchin abundance and diversity in Kenyan coral. Oecologia 83:362–370CrossRefGoogle Scholar
  55. McClanahan TR, Kamukuru AT, Muthiga NA, Gilagabher Yebio M, Obura D (1996) Effect of sea urchin reductions on algae, coral, and fish populations. Conserv Biol 10:136–154CrossRefGoogle Scholar
  56. McNaughton SJ (1985) Ecology of a grazing ecosystem: the Serengeti. Ecol Monogr 53:291–320CrossRefGoogle Scholar
  57. McNaughton SJ (1990) Mineral nutrition and seasonal movements of African migratory ungulates. Nature 345:613–615CrossRefGoogle Scholar
  58. McNaughton SJ, Banyikwa FF, McNaughton MM (1997) Promotion of the cycling of diet-enhancing nutrients by African grazers. Science 278:1798–1800CrossRefPubMedGoogle Scholar
  59. Montgomery WL, Myrberg AA, Fishelson L (1989) Feeding ecology of surgeonfishes (Acanthuridae) in the northern Red Sea, with particular reference to Acanthurus nigrofuscus (Forsskal). J Exp Mar Biol Ecol 132:179–207CrossRefGoogle Scholar
  60. Morrison D (1988) Comparing fish and urchin grazing in shallow and deeper coral reef algal communities. Ecology 69:1367–1382CrossRefGoogle Scholar
  61. Morse DE, Hooker N, Morse ANC, Jensen RA (1988) Control of larval metamorphosis and recruitment in sympatric agariciid corals. J Exp Mar Biol Ecol 116:193–217CrossRefGoogle Scholar
  62. Mumby PJ, Steneck RS (2008) Coral reef management and conservation in light of rapidly evolving ecological paradigms. Trends Ecol Evol 23:555–563CrossRefPubMedGoogle Scholar
  63. Nyström M, Folke C, Moberg F (2000) Coral reef disturbance and resilience in a human-dominated environment. Trends Ecol Evol 15:413–417CrossRefPubMedGoogle Scholar
  64. Ogutu JO, Piepho HP, Reid RS, Rainy ME, Kruska RL, Worden S, Nyabenge M, Hobbs NT (2010) Large herbivore responses to water and settlements in savannas. Ecol Monogr 80:241–266CrossRefGoogle Scholar
  65. Paddack MJ, Cowen RK, Sponaugle S (2006) Grazing pressure of herbivorous coral reef fishes on low coral-cover reefs. Coral Reefs 25:461–472. doi:10.1007/s00338-006-0112-y CrossRefGoogle Scholar
  66. Polunin NVC, Klumpp DW (1992) Algal food supply and grazer demand in a very productive coral-reef zone. J Exp Mar Biol Ecol 164:1–15CrossRefGoogle Scholar
  67. Pratchett MS, Munday MS, Wilson SK, Graham NAJ, Cinner JE, Bellwood DR, Jones GP, Polunin NVC, McClanahan TR (2008) Effects of climate-induced coral bleaching on coral-reef fishes. Ecological and economic consequences. Oceanogr Mar Biol Annu Rev 46:251–296CrossRefGoogle Scholar
  68. Price N (2010) Habitat selection, facilitation, and biotic settlement cues affect distribution and performance of coral recruits in French Polynesia. Oecologia 163:747–758CrossRefPubMedPubMedCentralGoogle Scholar
  69. Prins HHT, Vanderjeugd HP (1993) Herbivore population crashes and woodland structure in east Africa. J Ecol 81:305–314CrossRefGoogle Scholar
  70. Pyke GH, Pulliam HR, Charnov EL (1977) Optimal foraging: a selective review of theory and tests. Quart Rev Biol 52:137–154CrossRefGoogle Scholar
  71. Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  72. Rasher DB, Hoey AS, Hay ME (2013) Consumer diversity interacts with prey defenses to drive ecosystem function. Ecology 94:1347–1358CrossRefPubMedPubMedCentralGoogle Scholar
  73. Robertson DR, Gaines DS (1986) Interference competition structures habitat use in a local assemblage of coral reef surgeonfishes. Ecology 67(1372):1383Google Scholar
  74. Robertson DR, Polunin NVC (1981) Coexistence: symbiotic sharing of feeding territories and algal food by some coral reef fishes from the Western Indian Ocean. Mar Biol 62(185):195Google Scholar
  75. Russ GR (2003) Grazer biomass correlates more strongly with production than with biomass of algal turfs on a coral reef. Coral Reefs 22:63–67. doi:10.1007/s00338-003-0286-5 Google Scholar
  76. Sammarco PW, Carleton JH (1981) Damselfish territoriality and coral community structure: reduced grazing, coral recruitment, and effects on coral spat. In: Proceedings of the 4th International Coral Reef Symposium, vol 2. pp 524–535Google Scholar
  77. Sandin SA, Smith JE, DeMartini EE, Dinsdale EA, Donner SD, Friedlander AM, Sala E (2008) Baselines and degradation of coral reefs in the northern Line Islands. PLoS One 3:e1548CrossRefPubMedPubMedCentralGoogle Scholar
  78. Scheffer M, Carpenter S, Foley JA, Folke C, Walker B (2001) Catastrophic shifts in ecosystems. Nature 413:591–596CrossRefPubMedGoogle Scholar
  79. Schmitz OJ, Hambäck PA, Beckerman AP (2000) Trophic cascades in terrestrial systems: a review of the effects of carnivore removals on plants. Am Nat 155:141–153CrossRefPubMedGoogle Scholar
  80. Schoener TW (1971) Theory of feeding strategies. Ann Rev Ecol Syst 2:369–404CrossRefGoogle Scholar
  81. Solomon ME (1949) The natural control of animal populations. J Anim Ecol 18:1–35CrossRefGoogle Scholar
  82. Steneck RS (1988) Herbivory on coral reefs: a synthesis. In: Choat JH et al (eds) Proc 6th Int Coral Reef Symp, vol 1. Townsville, Australia, pp 37–49Google Scholar
  83. Stockwell B, Jadloc CRL, Abesamis RA, Alcala AC, Russ GR (2009) Trophic and benthic responses to no-take marine reserve protection in the Philippines. Mar Ecol Prog Ser 389:1–15CrossRefGoogle Scholar
  84. Sutherland WJ (1983) Aggregation and the “ideal free” distribution. J Anim Ecol 52:821–828CrossRefGoogle Scholar
  85. Sutherland WJ, Parker GA (1992) The relationship between continuous input and interference models of ideal free distributions with unequal competitors. Anim Behav 44:345–355CrossRefGoogle Scholar
  86. Tregenza T (1995) Building on the ideal free distribution. Adv Ecol Res 26:253–307CrossRefGoogle Scholar
  87. Vermeij MJA, van Moorselaar I, Engelhard S, Hornlein C, Vonk SM, Visser PM (2010) The effects of nutrient enrichment and herbivore abundance on the ability of turf algae to overgrow coral in the Caribbean. PLoS One 5:e14312. doi:10.1371/journal.pone.0014312 CrossRefPubMedPubMedCentralGoogle Scholar
  88. Welsh JQ, Bellwood DR (2012) How far do schools of roving herbivores rove? A case study using Scarus rivulatus. Coral Reefs 31:9911003. doi:10.1007/s00338-012-0922-z Google Scholar
  89. Williams ID, Polunin NVC (2001) Large-scale associations between macroalgal cover and grazer biomass on mid-depth reefs in the Caribbean. Coral Reefs 19:358–366. doi:10.1007/s003380000121 CrossRefGoogle Scholar
  90. 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

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.Department of BiologyCalifornia State University, NorthridgeNorthridgeUSA

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