Coral Reefs

, Volume 35, Issue 4, pp 1297–1309 | Cite as

Sediments influence accumulation of two macroalgal species through novel but differing interactions with nutrients and herbivory

  • Rachel J. Clausing
  • Sarah Joy Bittick
  • Caitlin R. Fong
  • Peggy Fong
Report

Abstract

Despite increasing concern that sediment loads from disturbed watersheds facilitate algal dominance on tropical reefs, little is known of how sediments interact with two primary drivers of algal communities, nutrients and herbivory. We examined the effects of sediment loads on the thalli of two increasingly abundant genera of macroalgae, Galaxaura and Padina, in a bay subject to terrestrial sediment influx in Mo’orea, French Polynesia. Field experiments examining (1) overall effects of ambient sediments and (2) interacting effects of sediments (ambient/removal) and herbivores (caged/uncaged) demonstrated that sediments had strong but opposite effects on both species’ biomass accumulation. Sediment removal increased accumulation of Padina boryana Thivy 50% in the initial field experiment but had no effect in the second; rather, in a novel interaction, herbivores overcompensated for increases in tissue nutrient stores that occurred with sediments loads, likely by preferential consumption of nutrient-rich meristematic tissues. Despite negative effects of sediments on biomass, Padina maintained rapid growth across treatments in both experiments. In contrast, positive growth in Galaxaura divaricata Kjellman only occurred with ambient sediment loads. In mesocosm experiments testing interactions of added nutrients and sediments on growth, Galaxaura grew at equivalent rates with sediments (collected from thalli on the reef) as with additions of nitrate and phosphate, suggesting sediments provide a nutrient subsidy. For Padina, however, the only effect was a 50% reduction in growth with sediment. Overall, retention of thallus sediments creates a positive feedback that Galaxaura appears to require to sustain net growth, while Padina merely tolerates sediments. These results indicate that sediments can modify nutrient and herbivore control of algae in ways that differ among species, with the potential for strong and unexpected effects on the abundance and composition of tropical reef macroalgae.

Keywords

Sediments Macroalgae Selective herbivory Fringing reef Nutrients Tissue nutrients 

Notes

Acknowledgments

We thank the Department of Ecology and Evolutionary Biology at the University of California, Los Angeles, for financial support. Writing was completed with support by the National Science Foundation Graduate Research Fellowship Program. Rainfall and light data were provided by the Mo’orea Coral Reef Ecosystem LTER, funded by the US National Science Foundation (OCE-0417412). This is contribution #218 of the University of California Berkeley’s Gump South Pacific Research Station.

Supplementary material

338_2016_1477_MOESM1_ESM.docx (40 kb)
Supplementary material 1 (DOCX 40 kb)

References

  1. Adjeroud M, Salvat B (1996) Spatial patterns in biodiversity of a fringing reef community along Opunohu Bay, Mo’orea, French Polynesia. Bull Mar Sci 59:175–187Google Scholar
  2. Airoldi L (2003) The effects of sedimentation on rocky coast assemblages. Oceanogr Mar Biol Annu Rev 41:161–236Google Scholar
  3. Aisha KA, Shabana EF, El-Abyad MS, Kobbia IA, Schanz F (1995) Pulse feeding with nitrate and phosphate in relation to tissue composition and nutrient uptake by some macroalgae from the Red Sea at Ghardaqa (Egypt). J Basic Microbiol 35:135–145CrossRefGoogle Scholar
  4. Barsanti L, Gualtieri P (2014) Photosynthesis. In: Barsanti L, Gualtieri P. Algae: anatomy, biochemistry, and biotechnology. CRC Press, Boca Raton, pp 141–170Google Scholar
  5. Begin C, Wurzbacher J, Cote IM (2013) Variation in benthic communities of eastern Caribbean coral reefs in relation to surface sediment composition. Mar Biol 160:343–353CrossRefGoogle Scholar
  6. Bellwood DR, Fulton CJ (2008) Sediment-mediated suppression of herbivory on coral reefs: decreasing resilience to rising sea levels and climate change? Limnol Oceanogr 53:2695–2701CrossRefGoogle Scholar
  7. Bonaldo RM, Bellwood DR (2011) Spatial variation in the effects of grazing on epilithic algal turfs on the Great Barrier Reef, Australia. Coral Reefs 30:381–390CrossRefGoogle Scholar
  8. Boyer KE, Fong P, Armitage AR, Cohen RA (2004) Elevated nutrient content of tropical macroalgae increases rates of herbivory in coral, seagrass, and mangrove habitats. Coral Reefs 23:530–538Google Scholar
  9. Clausing RJ, Fong P (2016) Environmental variability drives rapid and dramatic changes in nutrient limitation of tropical macroalgae with different ecological strategies. Coral Reefs 35:669–680CrossRefGoogle Scholar
  10. Clausing R, Annunziata C, Baker G, Lee C, Bittick S, Fong P (2014) Effects of sediment depth on algal turf height are mediated by interactions with fish herbivory on a fringing reef. Mar Ecol Prog Ser 517:121–129CrossRefGoogle Scholar
  11. Connell S (2005) Assembly and maintenance of subtidal habitat heterogeneity: synergistic effects of light penetration and sedimentation. Mar Ecol Prog Ser 289:53–61CrossRefGoogle Scholar
  12. Cronin G, Hay ME (1996) Within-plant variation in seaweed palatability and chemical defenses: optimal defense theory versus the growth-differentiation balance hypothesis. Oecologia 105:361–368CrossRefGoogle Scholar
  13. De’ath G, Fabricius K (2010) Water quality as a regional driver of coral biodiversity and macroalgae on the Great Barrier Reef. Ecol Appl 20:840–850CrossRefPubMedGoogle Scholar
  14. Fabricius KE (2005) Effects of terrestrial runoff on the ecology of corals and coral reefs: review and synthesis. Mar Pollut Bull 50:125–146CrossRefPubMedGoogle Scholar
  15. Fong P, Paul VJ (2011) Coral reef algae. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition. Springer, Amsterdam, pp 241–272CrossRefGoogle Scholar
  16. Fong CR, Fong P (2014) Why species matter: an experimental assessment of assumptions and predictive ability of two functional-group models. Ecology 95:2055–2061CrossRefPubMedGoogle Scholar
  17. Fong P, Kamer K, Boyer KE, Boyle KA (2001) Nutrient content of macroalgae with differing morphologies may indicate sources of nutrients for tropical marine systems. Mar Ecol Prog Ser 220:137–152CrossRefGoogle Scholar
  18. Fong P, Boyer KE, Kamer K, Boyle KA (2003) Influence of initial tissue nutrient status of tropical marine algae on response to nitrogen and phosphorus additions. Mar Ecol Prog Ser 262:111–123CrossRefGoogle Scholar
  19. Fox RJ, Bellwood DR (2007) Quantifying herbivory across a coral reef depth gradient. Mar Ecol Prog Ser 339:49–59CrossRefGoogle Scholar
  20. Fung T, Seymour RM, Johnson CR (2011) Alternative stable states and phase shifts in coral reefs under anthropogenic stress. Ecology 92:967–982CrossRefPubMedGoogle Scholar
  21. Goatley CHR, Bellwood DR (2012) Sediment suppresses herbivory across a coral reef depth gradient. Biol Lett 8:1016–1018CrossRefPubMedPubMedCentralGoogle Scholar
  22. Goatley CHR, Bellwood DR (2013) Ecological consequences of sediment on high-energy coral reefs. PLoS One 8:e77737CrossRefPubMedPubMedCentralGoogle Scholar
  23. Goatley CHR, Bonaldo RM, Fox RJ, Bellwood DR (2016) Sediments and herbivory as sensitive indicators of coral reef degradation. Ecol Soc 21:29CrossRefGoogle Scholar
  24. Goecker ME, Heck KL, Valentine JF (2005) Effects of nitrogen concentrations in turtlegrass Thalassia testudinum on consumption by the bucktooth parrotfish Sparisoma radians. Mar Ecol Prog Ser 286:239–248CrossRefGoogle Scholar
  25. Gordon SE, Goatley CHR, Bellwood DR (2015) Low-quality sediments deter grazing by the parrotfish Scarus rivulatus on inner-shelf reefs. Coral Reefs 35:285–291CrossRefGoogle Scholar
  26. Gorgula SK, Connell SD (2004) Expansive covers of turf-forming algae on human-dominated coast: the relative effects of increasing nutrient and sediment loads. Mar Biol 145:613–619CrossRefGoogle Scholar
  27. Haas AF, Naumann MS, Struck U, Mayr C, El-Zibdah M, Wild C (2010) Organic matter release by coral reef-associated benthic algae in the Northern Red Sea. J Exp Mar Bio Eco. 389:53–60CrossRefGoogle Scholar
  28. Hay KB, Poore AGB, Lovelock CE (2011) The effects of nutrient availability on tolerance to herbivory in a brown seaweed. J Ecol 99:1540–1550CrossRefGoogle Scholar
  29. Hughes TP, Graham NAJ, Jackson JBC, Mumby PJ, Steneck RS (2010) Rising to the challenge of sustaining coral reef resilience. Trends Ecol Evol 25:633–642CrossRefPubMedGoogle Scholar
  30. 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 17:360–365CrossRefPubMedGoogle Scholar
  31. Kamer K, Fong P, Kennison RL, Schiff K (2004) The relative importance of sediment and water column supplies of nutrients to the growth and tissue nutrient content of the green macroalga Enteromorpha intestinalis along an estuarine resource gradient. Aquat Ecol 38:45–56CrossRefGoogle Scholar
  32. Kawamata S, Yoshimitsu S, Tanaka T, Igari T, Tokunaga S (2011) Importance of sedimentation for survival of canopy-forming fucoid algae in urchin barrens. J Sea Res 66:76–86CrossRefGoogle Scholar
  33. Kawamata S, Yoshimitsu S, Tokunaga S, Kubo S, Tanaka T (2012) Sediment tolerance of Sargassum algae inhabiting sediment-covered rocky reefs. Mar Biol 159:723–733CrossRefGoogle Scholar
  34. Larned ST (1998) Nitrogen-versus phosphorus-limited growth and sources of nutrients for coral reef macroalgae. Mar Biol 132:409–421CrossRefGoogle Scholar
  35. Larned ST, Stimson J (1996) Nitrogen-limited growth in the coral reef chlorophyte Dictyosphaeria cavernosa, and the effect of exposure to sediment-derived nitrogen on growth. Mar Ecol Prog Ser 145:95–108CrossRefGoogle Scholar
  36. Lee SC (2006) Habitat complexity and consumer-mediated positive feedbacks on a Caribbean coral reef. Oikos 112:442–447CrossRefGoogle Scholar
  37. Littler MM, Littler DS (1980) The evolution of thallus form and survival strategies in benthic marine macroalgae: field and laboratory tests of a functional form model. Am Nat 116:25–44CrossRefGoogle Scholar
  38. Littler MM, Littler DS, Brooks BL (2006) Harmful algae on tropical coral reefs: bottom-up eutrophication and top-down herbivory. Harmful Algae 5:565–585CrossRefGoogle Scholar
  39. Manly BFJ (1997) Randomization, bootstrap and Monte Carlo methods in biology. Chapman and Hall, Boca RatonGoogle Scholar
  40. Manly B, Francis RC (2002) Testing for mean and variance differences with samples from distributions that may be non-normal with unequal variances. J Stat Comput Simul 72:633–646CrossRefGoogle Scholar
  41. Mantyka C, Bellwood DR (2007) Macroalgal grazing selectivity among herbivorous coral reef fishes. Mar Ecol Prog Ser 352:177–185CrossRefGoogle Scholar
  42. McClanahan TR, Steneck RS, Pietri D, Cokos B, Jones S (2005) Interaction between inorganic nutrients and organic matter in controlling coral reef communities in Glovers Reef Belize. Mar Pollut Bull 50:566–575CrossRefPubMedGoogle Scholar
  43. McCook L (1996) Effects of herbivores and water quality on Sargassum distribution on the central Great Barrier Reef: cross-shelf transplants. Mar Ecol Prog Ser 139:179–192CrossRefGoogle Scholar
  44. McCook LJ (1999) Macroalgae, nutrients and phase shifts on coral reefs: scientific issues and management consequences for the Great Barrier Reef. Coral Reefs 18:357–367CrossRefGoogle Scholar
  45. McCulloch M, Fallon S, Wyndham T, Hendy E (2003) Coral record of increased sediment flux to the inner Great Barrier Reef since European settlement. Nature 42:727–730CrossRefGoogle Scholar
  46. Muthukrishnan R, Fong P (2014) Multiple anthropogenic stressors exert complex, interactive effects on a coral reef community. Coral Reefs 33:911–921CrossRefGoogle Scholar
  47. Nemeth R, Nowlis J (2001) Monitoring the effects of land development on the near-shore reef environment of St. Thomas. USVI. Bull Mar Sci 69:759–775Google Scholar
  48. Norström AV, Nyström M, Lokrantz J, Folke C (2009) Alternative states on coral reefs: beyond coral–macroalgal phase shifts. Mar Ecol Prog Ser 376:293–306CrossRefGoogle Scholar
  49. Nyström M, Folke C, Moberg F (2000) Coral reef disturbance and resilience in a human-dominated environment. Trends Ecol Evol 15:413–417CrossRefPubMedGoogle Scholar
  50. Onuf CP, Teal JM, Valiela I (1977) Interactions of nutrients, plant growth and herbivory in a mangrove ecosystem. Ecology 58:514–526CrossRefGoogle Scholar
  51. Paine RT, Tegner MJ, Johnson EA (1998) Compounded perturbations yield ecological surprises. Ecosystems 1:535–545CrossRefGoogle Scholar
  52. Poore AGB (1994) Selective herbivory by amphipods inhabiting the brown alga Zonaria angustata. Mar Ecol Prog Ser 107:113–124CrossRefGoogle Scholar
  53. Prouty NG, Field ME, Stock JD, Jupiter SD, McCulloch M (2010) Coral Ba/Ca records of sediment input to the fringing reef of the southshore of Moloka’i, Hawai’i over the last several decades. Mar Pollut Bull 60:1822–1835CrossRefPubMedGoogle Scholar
  54. R Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  55. Rasher DB, Engel S, Bonito V, Fraser GJ, Montoya JP, Hay ME (2012) Effects of herbivory, nutrients, and reef protection on algal proliferation and coral growth on a tropical reef. Oecologia 169:187–198CrossRefPubMedGoogle Scholar
  56. Richmond RH, Rongo T, Golbuu Y, Victor S, Idechong N, Davis G, Kostka W, Neth L, Hamnett M, Wolanski E (2007) Watersheds and coral reefs: conservation science, policy, and implementation. Bioscience 57:598–607CrossRefGoogle Scholar
  57. Schaffelke B (1999) Particulate organic matter as an alternative nutrient source for tropical Sargassum species (Fucales, Phaeophyceae). J Phycol 1157:1150–1157CrossRefGoogle Scholar
  58. Scheffer M, Carpenter SR (2003) Catastrophic regime shifts in ecosystems: linking theory to observation. Trends Ecol Evol 18:648–656CrossRefGoogle Scholar
  59. Stimson J, Larned S (2000) Nitrogen efflux from the sediments of a subtropical bay and the potential contribution to macroalgal nutrient requirements. J Exp Mar Bio Ecol 252:159–180CrossRefPubMedGoogle Scholar
  60. Suarez AV, Bolger DT, Case TJ (1998) Effects of fragmentation and invasion on native ant communities in coastal Southern California. Ecology 79:2041–2056CrossRefGoogle Scholar
  61. Thacker RW, Ginsburg DW, Paul VJ (2001) Effects of herbivore exclusion and nutrient enrichment on coral reef macroalgae and cyanobacteria. Coral Reefs 19:318–329CrossRefGoogle Scholar
  62. Umar MJ, McCook LJ, Price IR (1998) Effects of sediment deposition on the seaweed Sargassum on a fringing coral reef. Coral Reefs 17:169–177CrossRefGoogle Scholar
  63. Washburn L, Brooks A (2014) MCR LTER: Coral reef: Gump Station meteorological data, ongoing since 2006. Dataset knb-lter-mcr.9.41, Moorea Coral Reef Long Term. Ecological Research. doi: 10.6073/pasta/346b87a9afdf332faca4d480a0ddd76d Google Scholar
  64. Weber M, Lott C, Fabricius KE (2006) Sedimentation stress in a scleractinian coral exposed to terrestrial and marine sediments with contrasting physical, organic and geochemical properties. J Exp Mar Bio Ecol 336:18–32CrossRefGoogle Scholar
  65. Weber M, de Beer D, Lott C, Polerecky L, Kohls K, Abed RMM, Ferdelman TG, Fabricius KE (2012) Mechanisms of damage to corals exposed to sedimentation. Proc Natl Acad Sci U S A 109:E1558–E1567CrossRefPubMedPubMedCentralGoogle Scholar
  66. Williams SL, Ruckelshaus MH (1993) Effects of nitrogen availability and herbivory on eelgrass (Zostera marina) and epiphytes. Ecology 74:904–918CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Rachel J. Clausing
    • 1
  • Sarah Joy Bittick
    • 1
  • Caitlin R. Fong
    • 2
  • Peggy Fong
    • 1
  1. 1.Department of Ecology and Evolutionary BiologyUniversity of California, Los AngelesLos AngelesUSA
  2. 2.Department of Ecology, Evolution, and Marine BiologyUniversity of California Santa BarbaraSanta BarbaraUSA

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