Chemistry of the consumption and excretion of the bumphead parrotfish (Bolbometopon muricatum), a coral reef mega-consumer

Abstract

Bolbometopon muricatum are ecologically unique mega-consumers in coral reef ecosystems. They primarily divide their dietary intake between living scleractinian corals and coral rock, a substrate richly colonized by non-coral biota. Here we examine how the chemical, structural, and energetic content of these two main classes of forage material may influence B. muricatum feeding behavior and selectivity. We then also examine nutrient content, pH, and alkalinity of the carbonate-rich feces of B. muricatum as a step toward understanding how B. muricatum defecation could affect reef nutrient dynamics and localized seawater chemistry. Our results suggest that by most measures, coral rock constitutes a richer food source than living corals, exhibiting higher levels of eight biologically relevant elements, and containing approximately three times greater caloric value than living corals. Additionally, the two forage types also presented distinct mineralogy, with the coral rock resembling a Mg-enriched carbonate phase in contrast to the primarily aragonitic live corals. Despite the fact that individual B. muricatum excrete tons of macerated coral annually, the low measured concentrations of N and P in feces suggest that this excretion may have relatively minor effects of reef macronutrient budgets. We also observed negligible local-scale impacts of B. muricatum feces on seawater pH and alkalinity. The approaches applied here integrate perspectives from marine biogeochemistry, materials science, and ecology. Collectively, these results provide preliminary insight into how reef chemistry could shape foraging of this dominant and vulnerable coral reef consumer and how it, in turn, might affect the chemistry of these reefs.

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References

  1. Addadi L, Raz S, Weiner S (2003) Taking advantage of disorder: Amorphous calcium carbonate and its roles in biomineralization. Adv Mater 15:959–970

    CAS  Article  Google Scholar 

  2. Allgeier JE, Valdivia A, Cox C, & Layman CA (2016). Fishing down nutrients on coral reefs. Nat Comm 7:12461; https://doi.org/10.1038/ncomms12461

  3. Asner GP (2009) Tropical forest carbon assessment: integrating satellite and airborne mapping approaches. Env Res Lett 4(3):034009

    Article  CAS  Google Scholar 

  4. Bailey, TG, & Robertson, DR (1982). Organic and caloric levels of fish feces relative to its consumption by coprophagous reef fishes. Marine Biology, 69(1), 45–50

  5. Bedke DK, Vanderwaal CD (2011) Chlorosulfolipids: Structure, synthesis, and biological relevance. Nat Prod Rep 28:15–25

    CAS  PubMed  Article  Google Scholar 

  6. Bellwood DR (1995) Carbonate transport and within-reef patterns of bioerosion and sediment release by parrotfishes (family Scaridae) on the Great Barrier Reef. Mar Ecol Prog Ser 117:127–136

    Article  Google Scholar 

  7. Bellwood DR, Choat JH (1990) A functional analysis of grazing in parrotfishes (family Scaridae): the ecological implications. Env Biol Fishes 28(1–4):189–214

    Article  Google Scholar 

  8. Bellwood DR, Hoey AS, Choat JH (2003) Limited functional redundancy in high diversity systems: resilience and ecosystem function on coral reefs. Ecol Lett 6(4):281–285

  9. Bonaldo RM, Hoey AS, & Bellwood DR (2014). The ecosystem roles of parrotfishes on tropical reefs. Oceanography and Marine Biology: An Annual Review, 52, 81–132

  10. Bray RN, Miller AC, Geesey GG (1981) The fish connection: a trophic link between planktonic and rocky reef communities? Science 214:204–205

    CAS  PubMed  Article  Google Scholar 

  11. Burkepile DE, Allgeier JE, Shantz AA, Pritchard CE, Lemoine NP, Bhatti LH, Layman CA (2013). Nutrient supply from fishes facilitates macroalgae and suppresses corals in a Caribbean coral reef ecosystem. Sci Rep 3: 1493

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  12. Cabrita MT, Vale C, Rauter AP (2010) Halogenated compounds from marine algae. Mar Drugs 8(8):2301–2317

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  13. Campion-Alsumard T, Golubic S, Hutchings P (1995) Microbial endoliths in skeletons of live and dead corals: Porites lobata (Moorea, French Polynesia). Mar Ecol Prog Ser 117:149–157

    Article  Google Scholar 

  14. Choat JH, Clements KD, Robbins WD (2002) The trophic status of herbivorous fishes on coral reefs. 1. Dietary analyses. Mar Biol 140:613–623

    CAS  Article  Google Scholar 

  15. Choat JH, Davies C, Ackerman J, Mapstone B (2006) Age structure and growth in a large teleost, Cheilinus undulatus, with a review of size distribution in labrid fishes. Mar Ecol Prog Ser 318:237–246

    Article  Google Scholar 

  16. 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. Biol J Linnean Soc 120(4):729–751

    Google Scholar 

  17. Comeros-Raynal MT, Choat JH, Polidoro BA, Clements KD, Abesemis R, Craig MT, Lazuardi ME, McIlwain J, Muljadi A, Myers RF, Nanola CL, Pardede S, Rocha LA, Russell B, Sanciangco JC, Stockwell B, Harwell H, Carpenter KE (2012) The likelihood of extinction of iconic and dominant herbivores and detritivores of coral reefs: The Parrotfishes and Surgeonfishes. PLoS ONE 7:1–13

    Article  CAS  Google Scholar 

  18. Das B, Mittal PK, Kamat SY (1981) Bromine and iodine content in sponges and algae of the Andaman Sea. Indian J Mar Sci 10:301–302

    Google Scholar 

  19. Davis SN, Whittemore DO, Fabryka-Martin J (1998) Use of chloride/bromide ratios in studies of potable waters. Groundwater 36(2):338–350

    CAS  Article  Google Scholar 

  20. de Vrind-de Jong EW, & de Vrind, JP (1997). Algal deposition of carbonates and silicates. Reviews in Mineralogy and Geochemistry, 35(1), 267–307

    Google Scholar 

  21. Dickson AG (1981) An exact definition of total alkalinity and a procedure for the estimation of alkalinity and total inorganic carbon from titration data. Deep Sea Part A – Oceanographic Res Papers 28:609–623

    CAS  Article  Google Scholar 

  22. Dickson AG, Sabine CL, Christian JR (2007) Guide to Best Practices for Ocean CO2 Measurements PICES Special Publication 3, 191 pp

  23. Donaldson, TJ, & Dulvy, NK (2004). Threatened fishes of the world: Bolbometopon muricatum (Valenciennes 1840)(Scaridae). Environmental Biology of Fishes, 70(4), 373-373

  24. Dulvy NK, Polunin NV (2004) Using informal knowledge to infer human-induced rarity of a conspicuous reef fish. Anim Conserv 7(4):365–374

    Article  Google Scholar 

  25. Estes JA, Heithaus M, McCauley DJ, Rasher DB, Worm B (2016). Megafaunal Impacts on Structure and Function of Ocean Ecosystems. Annu Rev Environ Res 41:83–116

    Article  Google Scholar 

  26. Geesey GG, Alexander GV, Bray RN, Miller AC (1984) Fish fecal pellets are a source of minerals for inshore reef communities. Mar Ecol Prog Ser 15(1):19–25

    Article  Google Scholar 

  27. Gerking SD (1994) Feeding Ecology of Fish. Academic Press, San Diego

    Google Scholar 

  28. Goffredo S, Caroselli E, Mezzo F, Laiolo L, Vergni P, Pasquini L, Levy O, Zaccanti F, Tribollet A, Dubinsky Z, Falini G (2012) The puzzling presence of calcite in skeletons of modern solitary corals from the Mediterranean Sea. Geochimica et Cosmochimica Acta 15(85):187–199

    Article  CAS  Google Scholar 

  29. Glynn P, Krupp D (1986) Feeding biology of a Hawaiian sea star corallivore, Culcita novaeguineae Muller & Troschel. J Exp Mar Biol Ecol 96:75–96

    Article  Google Scholar 

  30. Haramaty L (1991) Reproduction effort in the nudibranch Phestilla sihogae: Calorimetric analysis of food and eggs. Pac Sci 45(3):257–262

    Google Scholar 

  31. Hay ME, Fenical W, Gustafson K (1987) Chemical defense against diverse coral reef herbivores. Ecol 68(6):1581–1591

    CAS  Article  Google Scholar 

  32. Hay ME, Kappel QE, Fenical W (1994) Synergisms in plant defenses against herbivores: interactions of chemistry, calcification, and plant quality. Ecol 75(6):1714–1726

    Article  Google Scholar 

  33. Heyland A, Moroz LL (2005) Cross-kingdom hormonal signaling: an insight from thyroid hormone functions in marine larvae. J Exp Biol 208:4355–4361

    CAS  PubMed  Article  Google Scholar 

  34. Hoey AS, Bellwood DR (2008) Cross-shelf variation in the role of parrotfishes on the Great Barrier Reef. Coral Reefs, 27(1):37–47

    Article  Google Scholar 

  35. Hourigan TF (1987) The behavioral ecology of three species of butterflyfishes (family Chaetodontidae). PhD Dissertation, University of Hawai’I, Manoa

  36. Hughes RN (1980). Optimal foraging theory in the marine context. Oceanogr Mar Biol Annu Rev, 18, 423–481

    Google Scholar 

  37. ICDD (2015) PDF-4+ 2015 (Database), edited by Dr. Soorya Kabekkodu, International Centre for Diffraction Data, Newtown Square, PA, USA

  38. Johansson O, Wedborg M (1982) On the evaluation of potentiometric titrations of seawater with hydrochloric acid. Ocean Acta 5(2):209–218

    CAS  Google Scholar 

  39. Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Oikos 69:373–386

    Article  Google Scholar 

  40. Lobel PS (1981) Trophic biology of herbivorous reef fishes: alimentary pH and digestive capabilities. J Fish Biol 19(4):365–397

    Article  Google Scholar 

  41. Luzinova Y, Dobbs GT, Lapham L, Chanton JP, Mizaikoff B (2011) Detection of cold seep derived authigenic carbonates with infrared spectroscopy. Mar Chem 125:8–18

    CAS  Article  Google Scholar 

  42. McCauley DJ, Keesing F, Young TP, Allan BF, Pringle RM (2006) Indirect effects of large herbivores on snakes in an African savanna. Ecol 87(10):2657–2663

    Article  Google Scholar 

  43. McCauley DJ, Micheli F, Young HS, Tittensor DP, Brumbaugh DR, Madin EM, 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(12):2739–2750

    PubMed  PubMed Central  Article  Google Scholar 

  44. McCauley DJ, Young HS, Dunbar RB, Estes JA, Semmens B X, Micheli F (2012). Assessing the effects of large mobile predators on ecosystem connectivity. Ecol Appl 22(6):1711–1717

    PubMed  Article  Google Scholar 

  45. McCauley DJ, Young HS, Guevara R, Williams GJ, Power EA, Dunbar RB, Bird DW, Durham WH, Micheli F (2014) Positive and negative effects of a threatened parrotfish on reef ecosystems. Cons Biol 28(5):1312–1321

    Article  Google Scholar 

  46. Meyer JL, Schultz ET (1985) Migrating haemulid fishes as a source of nutrients and organic matter on coral reefs. Limn Ocean 30(1):146–156

    Article  Google Scholar 

  47. Michel FM, Macdonald J, Feng J, Phillips BL, Ehm L, Tarabrella C, Parise JB, Reeder RJ (2008) Structural characteristics of synthetic amorphous calcium carbonate. Chem Mater 20:4720–4728

    CAS  Article  Google Scholar 

  48. Millero FJ, Zhang J-Z, Lee K, and Campbell DM, Titration alkalinity of seawater, Mar Chem, 44, pp. 153–165 (1993)

    CAS  Article  Google Scholar 

  49. Ohde S, & van Woesik R (1999) Carbon dioxide flux and metabolic processes of a coral reef, Okinawa. Bulletin of Marine Science, 65(2): 559–576

    Google Scholar 

  50. Owen-Smith RN (1988) Megaherbivores: The influence of very large body size on ecology. Cambridge University Press, Cambridge UK

    Google Scholar 

  51. Perry CT, Kench PS, O’Leary MJ, Morgan KM, Januchowski-Hartley F (2015) Linking reef ecology to island building: Parrotfish identified as major producers of island-building sediment in the Maldives. Geology 43(6):503–506

    Article  Google Scholar 

  52. Pinnegar JK, Polunin NVC (2006) Planktivorous damselfish support significant nitrogen and phosphorus fluxes to Mediterranean reefs. Mar Biol 148(5):1089–1099

    Article  Google Scholar 

  53. Pinnegar JK, Polunion NVC, Videler JJ, de Wiljes JJ (2007) Daily carbon, nitrogen and phosphorus budgets for the Mediterranean planktivorous damselfish Chromis chromis. J Exp Mar Biol Ecol 352:378–391

    CAS  Article  Google Scholar 

  54. Pringle RM, Young TP, Rubenstein DI, McCauley DJ (2007) Herbivore-initiated interaction cascades and their modulation by productivity in an African savanna. Proc Nat Acad Sci 104(1):193–197

    CAS  PubMed  Article  Google Scholar 

  55. Pytkowicz RM (1967) Carbonate cycle and the buffer mechanism of recent oceans. Geochim Cosmochim Acta 31(1):63–73

    CAS  Article  Google Scholar 

  56. Raab TK, Vogel JP (2004) Ecological and agricultural applications of synchrotron IR microscopy. Infr Phys Tech 45:393–402

    CAS  Article  Google Scholar 

  57. R Core Team (2012) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

  58. Radha AV, Forbes TZ, Killian CE, Gilbert PUPA, Navrotsky A (2010) Transformation and crystallization energetics of synthetic and biogenic amorphous caclcium carbonate. Proc Nat Acad Sci 107:16438–16443

    CAS  PubMed  Article  Google Scholar 

  59. Roman J, Estes JA, Morissette L, Smith C, Costa D, McCarthy J, Nation JB, Nicol S, Pershing A, Smetacek V (2014) Whales as marine ecosystem engineers. Front Ecol Environ 12(7):377–385

    Article  Google Scholar 

  60. Rotjan RD, Lewis SM (2005) Selective predation by parrotfishes on the reef coral Porites astreoides. Mar Ecol Prog Ser 305:193–201

    CAS  Article  Google Scholar 

  61. Rotjan RD, Lewis SM (2006) Parrotfish abundance and selective corallivory on a Belizean coral reef. J Exp Mar Biol Ecol 335:292–301

    Article  Google Scholar 

  62. Schneider K, Silverman J, Woolsey W, Eriksson H, Byrne M, Caldeira K (2011) Potential influence of sea cucumbers on coral reef CaCO3 budget: A case study at One Tree Reef. J Geophys Res 116:G04032

    Article  CAS  Google Scholar 

  63. Schoener TW (1971) Theory of feeding strategies. Annu Rev Ecol Syst 2:369–404

    Article  Google Scholar 

  64. Smriga S, Sandin SA, Azam F (2010). Abundance, diversity, and activity of microbial assemblages associated with coral reef fish guts and feces. FEMS Microbiology Ecol 73(1):31–42

    CAS  Google Scholar 

  65. Stevenson C, Katz LS, Micheli F, Block B, Heiman KW, Perle C, Weng K, Dunbar R, Witting J (2007) High apex predator biomass on remote Pacific islands. Coral Reefs 26(1):47–51

    Article  Google Scholar 

  66. Targett TE, Targett NM (1990) Energetics of food selection by the herbivorous. Mar Ecol Prog Ser 66:13–21

    Article  Google Scholar 

  67. Targett NM, Targett TE, Vrolijk NH, Ogden JC (1986) Effect of macrophyte secondary metabolites on feeding preferences of the herbivorous parrotfish Sparisoma radians. Mar Biol 92(1):141–148

    CAS  Article  Google Scholar 

  68. Tribollet, A (2008) The boring microflora in modern coral reef ecosystems: a review of its roles. Current developments in bioerosion, (pp. 67–94). Springer, Berlin, Heidelberg

  69. Tricas TC (1989) Prey selection by coral-feeding butterflyfishes: strategies to maximize the profit. The butterflyfishes: success on the coral reef, (pp. 171–186). Springer Netherlands

  70. Unson MD, Holland ND, Faulkner DJ (1994) A brominated secondary metabolite synthesized by the cyanobacterial symbiont of a marine sponge and accumulation of the crystalline metabolite in the sponge tissue. Mar Biol 119(1):1–11

    CAS  Article  Google Scholar 

  71. Urmos J, Sharma SK, Mackenzie FT (1991) Characterization of some biogenic carbonates with Raman spectroscopy. Am Mineral 76:641–646

    CAS  Google Scholar 

  72. Wang RZ, Addadi L, Weiner S (1997) Design strategies of sea urchin teeth: structure, composition and micromechanical relations to function. Phil Trans Royal Soc B: Biol Sci 352:469–480

    CAS  Article  Google Scholar 

  73. Wilson RW, Millero FJ, Taylor JR, Walsh PJ, Christensen V, Jennings S, Grosell M (2009) Contribution of fish to the marine inorganic carbon cycle. Science 323:359–362

    CAS  PubMed  Article  Google Scholar 

  74. Winchester JW, Duce RA (1967) The global distribution of iodine, bromine, and chlorine in marine aerosols. Naturwissen 54:110–113

    CAS  Article  Google Scholar 

  75. Woosley RJ, Millero FJ, Grosell M (2012) The solubility of fish-produced high magnesian calcite in seawater. J Geophys Res 117:C04018

    Article  CAS  Google Scholar 

  76. Young HS, McCauley DJ, Dunbar RB, Dirzo R (2010) Plants cause ecosystem nutrient depletion via the interruption of bird-derived spatial subsidies. Proc Nat Acad Sci 107(5):2072–2077

    CAS  PubMed  Article  Google Scholar 

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Acknowledgements

For research permission and invaluable research support we thank the US Fish and Wildlife Service, the staff of the Nature Conservancy, and the Palmyra Atoll Research Consortium. Funding was provided by the National Science Foundation, the Woods Institute for the Environment, the Sloan Foundation, the Benioff Ocean Initiative, and the Stanford University Vice Provost for Undergraduate Education student grant program. TKR and GG would like to thank Drs. Jeff Tok of Stanford’s Soft Materials Facility (Department of Material Science) for untrammeled access to the DSC, Hans Bechtel of the Advanced Light Source (LBNL) for access to the Raman microscope, and Dr. Juan Lezama Pacheco for discretionary time at BL 11-2. Use of the Stanford Synchrotron Radiation Lightsource, SLAC National Accelerator Laboratory, is supported by the U.S. Department of Energy, Office of Science, Office of Basic Energy Sciences under Contract No. DE-AC02-76SF00515.

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Goldberg, E.G., Raab, T.K., Desalles, P. et al. Chemistry of the consumption and excretion of the bumphead parrotfish (Bolbometopon muricatum), a coral reef mega-consumer. Coral Reefs 38, 347–357 (2019). https://doi.org/10.1007/s00338-019-01781-0

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Keywords

  • Parrotfish
  • Coral
  • Reef
  • Nutrients
  • Calorimetry
  • Carbonates
  • Bolbometopon
  • pH