Coral Reefs

, Volume 33, Issue 4, pp 1145–1151

Vermetid gastropods reduce foraging by herbivorous fishes on algae on coral reefs

Report

Abstract

Vermetid gastropods have the potential to reduce foraging by herbivorous fishes on algae on coral reefs because they produce mucous nets that cover the surfaces of coral skeletons, potentially inhibiting foraging by fishes. We assessed this possibility using both observational and experimental approaches in Moorea, French Polynesia. Foraging rates of herbivorous fishes (total number of bites by all species per minute) were recorded in plots that varied naturally in the cover of vermetid mucous nets. This study, done at six sites, revealed that foraging on algal turf declined with increasing cover of vermetid mucous nets, ranging from ~2 to 22 bites m−2 min−1 at 0 % coverage to 0–5 bites m−2 min−1 at 100 % coverage. The magnitude of this effect of vermetid nets varied among microhabitats (high, mid, and low bommies) and sites, presumably due to variation in the intensity of herbivory. Experimental removal of vermetid mucous nets from plots more than doubled the foraging intensity on turf algae relative to when vermetid nets were present at high (≥70 %) cover. Our results indicate that algal turf on coral reefs may benefit from associational refuge from grazing provided by vermetid gastropods, which might in turn harm corals via increased competition with algal turf.

Keywords

Vermetid Microhabitat Herbivorous Foraging Algae Grazing 

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(8):e23717PubMedCentralPubMedCrossRefGoogle Scholar
  2. Bellwood DR (1995) Direct estimate of bioerosion by two parrotfish species, Chlorurus gibbus and C. sordidus, on the Great Barrier Reef, Australia. Mar Biol 121:419–429CrossRefGoogle Scholar
  3. Bellwood D, Choat J (1990) A functional analysis of grazing in parrotfishes (family Scaridae): the ecological implications. Environ Biol Fishes 28:189–214CrossRefGoogle Scholar
  4. Bellwood DR, Hughes TP, Folke C, Nyström M (2004) Confronting the coral reef crisis. Nature 429:827–833PubMedCrossRefGoogle Scholar
  5. Birrell CL, McCook LJ, Willis BL, 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 Annu Rev 46:25–64Google Scholar
  6. Bonaldo RM, Krajewski JP, Sazima C, Sazima I (2006) Foraging activity and resource use by three parrotfish species at Fernando de Noronha Archipelago, tropical West Atlantic. Mar Biol 149:423–433CrossRefGoogle Scholar
  7. Burkepile DE, Hay ME (2006) Herbivore vs. nutrient control of marine primary producers: context-dependent effects. Ecology 87:3128–3139PubMedCrossRefGoogle Scholar
  8. Burkepile DE, Hay ME (2008) Herbivore species richness and feeding complementarity affect community structure and function on a coral reef. Proc Natl Acad Sci USA 105:16201–16206PubMedCentralPubMedCrossRefGoogle Scholar
  9. Cebrian J (1999) Patterns in the fate of production in plant communities. Am Nat 154:449–468PubMedCrossRefGoogle Scholar
  10. 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
  11. 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
  12. Diaz-Pulido G, McCook LJ (2002) The fate of bleached corals: patterns and dynamics of algal recruitment. Mar Ecol Prog Ser 232:115–128CrossRefGoogle Scholar
  13. Done TJ (1992) Phase shifts in coral reef communities and their ecological significance. Hydrobiologia 247:121–132CrossRefGoogle Scholar
  14. Ellison GN, Gotelli NJ (2004) A primer of ecological statistics. Sinauer, Sunderland, Massachusetts, USAGoogle Scholar
  15. Graham JE, Wilcox LW, Graham LE (2009) Algae, second edition, 2nd edn. Benjamin-Cummings, San Francisco, USAGoogle Scholar
  16. Hackney JM, Carpenter RC, Adey WH (1989) Characteristic adaptations to grazing among algal turfs on a Caribbean coral reef. Phycologia 28:109–119CrossRefGoogle Scholar
  17. Hadfield M, Kay EA, Gillette MU, Lloyd MC (1972) The Vermetidae (Mollusca: Gastropoda) of the Hawaiian Islands. Mar Biol 12:81–98Google Scholar
  18. Hatcher BG (1988) Coral reef primary productivity: a beggars banquet. Trends Ecol Evol 3:106–111PubMedCrossRefGoogle Scholar
  19. Hay ME (1981) The functional morphology of turf-forming seaweeds: persistence in stressful marine habitats. Ecology 62:739–750CrossRefGoogle Scholar
  20. Hay ME (1986) Associational plant defenses and the maintenance of species diversity: turning competitors into accomplices. Am Nat 128:617–641CrossRefGoogle Scholar
  21. Hay ME (1991) Fish-seaweed interactions on coral reefs: effects of herbivorous fishes and adaptations of their prey. In: Sale PF (ed) The ecology of fishes on coral reefs. Academic Press, San Diego, CA, pp 96–119CrossRefGoogle Scholar
  22. Hay ME, Steinberg PD (1992) The chemical ecology of plant-herbivore interactions in marine versus terrestrial communities. In: Rosenthal GA, Berenbaum MR (eds) Herbivores: Their interactions with secondary metabolites, evolutionary and ecological processes. Academic Press, San Diego, California, pp 111–145Google Scholar
  23. Heck KL, Valentine JF (2007) The primacy of top-down effects in shallow benthic ecosystems. Estuaries Coasts 30:371–381CrossRefGoogle Scholar
  24. Hixon MA, Brostoff WN (1996) Succession and herbivory: effects of differential fish grazing on Hawaiian coral-reef algae. Ecol Monogr 66:67–90CrossRefGoogle Scholar
  25. Hoey AS, Bellwood DR (2011) Suppression of herbivory by macroalgal density: a critical feedback on coral reefs? Ecol Lett 14:267–273PubMedCrossRefGoogle Scholar
  26. Holling CS (1973) Resilience and stability of ecological systems. Annu Rev Ecol Syst 4:1–23CrossRefGoogle Scholar
  27. Horn MH (1989) Biology of marine herbivorous fishes. Oceanogr Mar Biol 27:167–272Google Scholar
  28. Hughes RN, Lewis AH (1974) On the spatial distribution, feeding and reproduction of the vermetid gastropod Dendropoma maximum. J Zool 172:531–547CrossRefGoogle Scholar
  29. Hughes TP (1994) Catastrophes, phase shifts, and large-scale degradation of a Caribbean coral reef. Science 265:1547–1551PubMedCrossRefGoogle 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 17:360–365PubMedCrossRefGoogle Scholar
  31. Jompa J, McCook LJ (2002) The effects of nutrients and herbivory on competition between a hard coral (Porites cylindrica) and a brown alga (Lobophora variegata). Limnol Oceanogr 47:527–534CrossRefGoogle Scholar
  32. Kappner I, Al-Moghrabi SM, Richter C (2000) Mucus-net feeding by the vermetid gastropod Dendropoma maxima in coral reefs. Mar Ecol Prog Ser 204:309–313CrossRefGoogle Scholar
  33. Klumpp DW, McKinnon AD (1992) Community structure, biomass and productivity of epilithic algal communities on the Great Barrier Reef: dynamics at different spatial scales. Mar Ecol Prog Ser 86:77–89CrossRefGoogle Scholar
  34. Larkum A, Koch E, Kühl M (2003) Diffusive boundary layers and photosynthesis of the epilithic algal community of coral reefs. Mar Biol 142:1073–1082Google Scholar
  35. Lenihan HS, Holbrook SJ, Schmitt RJ, Brooks AJ (2011) Influence of corallivory, competition, and habitat structure on coral community shifts. Ecology 92:1959–1971PubMedCrossRefGoogle Scholar
  36. Luckhurst BE, Luckhurst K (1978) Analysis of influence of substrate variables on coral-reef fish communities. Mar Biol 49:317–323CrossRefGoogle Scholar
  37. 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
  38. 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
  39. McManus JW, Polsenberg JF (2004) Coral–algal phase shifts on coral reefs: ecological and environmental aspects. Prog Oceanogr 60:263–279CrossRefGoogle Scholar
  40. Mumby PJ, Hastings A, Edwards HJ (2007) Thresholds and the resilience of Caribbean coral reefs. Nature 450:98–101PubMedCrossRefGoogle Scholar
  41. Nyström M, Folke C, Moberg F (2000) Coral reef disturbance and resilience in a human-dominated environment. Trends Ecol Evol 15:413–417PubMedCrossRefGoogle Scholar
  42. 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 169:187–198PubMedCentralPubMedCrossRefGoogle Scholar
  43. Shima JS, Osenberg CW, Stier AC (2010) The vermetid gastropod Dendropoma maximum reduces coral growth and survival. Biol Lett 6:815–818PubMedCentralPubMedCrossRefGoogle Scholar
  44. Shima JS, Phillips NE, Osenberg CW (2013) Consistent deleterious effects of vermetid gastropods on coral performance. J Exp Mar Biol Ecol 439:1–6CrossRefGoogle Scholar
  45. Silenzi S, Antonioli F, Chemello R (2004) A new marker for sea surface temperature trend during the last centuries in temperate areas: vermetid reef. Glob Planet Change 40:105–114CrossRefGoogle Scholar
  46. Smally TL (1984) Possible effects of intraspecific competition on the population structure of a solitary vermetid mollusc. Mar Ecol Prog Ser 14:139–144CrossRefGoogle Scholar
  47. Stier AC, McKeon CS, Osenberg CW, Shima JS (2010) Guard crabs alleviate deleterious effects of vermetid snails on a branching coral. Coral Reefs 29:1019–1022CrossRefGoogle Scholar
  48. Tootell JS (2013) Processes affecting the grazing, distribution, behavior, and condition of herbivorous fishes on coral reefs. MS Thesis, California State University, Northridge, p 36 http://hdl.handle.net/10211.2/3635
  49. 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:e14312PubMedCentralPubMedCrossRefGoogle Scholar
  50. Vroom PS, Braun CL (2010) Benthic composition of a healthy subtropical reef: baseline species-level cover, with an emphasis on algae, in Northwestern Hawaiian Islands. PLoS One 5:e9733PubMedCentralPubMedCrossRefGoogle Scholar
  51. Wilson SK, Bellwood DR, Choat JH, Furnas MJ (2003) Detritus in the epilithic algal matrix and its use by coral reef fishes. Oceanogr and Mar Biol 41:279–309Google Scholar
  52. Zemke-White LW, Choat J, Clements K (2002) A re-evaluation of the diel feeding hypothesis for marine herbivorous fishes. Mar Biol 141:571–579CrossRefGoogle Scholar
  53. Zvuloni A, Armoza-Zvuloni R, Loya Y (2008) Structural deformation of branching corals associated with the vermetid gastropod Dendropoma maxima. Mar Ecol Prog Ser 363:103–108CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  1. 1.Department of BiologyCalifornia State University, NorthridgeNorthridgeUSA

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