Skip to main content

Impacts of parrotfish predation on a major reef-building coral: quantifying healing rates and thresholds of coral recovery

Abstract

Parrotfishes are important Caribbean herbivores that are believed to indirectly benefit corals by grazing algae; yet, some species also feed on live coral, which may have direct negative impacts on coral growth and survivorship. Caribbean parrotfishes prey upon multiple coral species but have particularly high rates of predation on Orbicella annularis, a major framework building coral and an endangered species. While some researchers have suggested that parrotfishes may have significant long-term impacts on heavily targeted species such as O. annularis, the patterns of coral recovery from parrotfish predation scars remain poorly understood. To address this knowledge gap, we tracked the fate of parrotfish bite scars on O. annularis colonies across two Caribbean islands for up to 2 months. We evaluated differences in coral healing between islands in response to a number of variables including the initial scar surface area, scar abundance per coral colony, colony surface area, and water depth. We used these data to develop a predictive model of O. annularis tissue loss from recent parrotfish bite scars. We then applied this model to surveys of the distribution of bite scars at a point in time to estimate long-term tissue loss of O. annularis colonies from a standing stock of bite scars. Our findings suggest that the initial scar surface area is one of the most important predictors of coral tissue loss. The data also indicate that there are thresholds in patterns of coral tissue regeneration: we observed that small scars (≤ 1.25 cm2) often fully heal, while larger scars (≥ 8.2 cm2) had minimal tissue regeneration. The vast majority of observed scars (~ 87%) were 1.25 cm2 or less, and our model predicted that O. annularis colonies would regenerate nearly all the corresponding scar area. In contrast, while scars greater than or equal to 8.2 cm2 were infrequent (~ 6% of all observed scars), our model predicted that these larger scars would account for over 96% of the total tissue loss for grazed colonies. Overall, our results suggest that the immediate negative impacts of parrotfish predation on coral tissue loss appear to be driven primarily by a few exceptionally large bite scars. While further work is needed to understand the long-term impacts of corallivory and quantify the net impacts of parrotfish herbivory and corallivory on Caribbean coral reefs, this study is an important step in addressing factors that impact the recovery of a heavily targeted and ecologically important Caribbean coral from parrotfish predation.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Data Availability Statement

Data are available from the NOAA National Centers for Environmental Information (NCEI Accession 0213589) at https://accession.nodc.noaa.gov/0213589.

References

  1. Adam TC, Duran A, Fuchs C, Roycroft MV, Rojas MC, Ruttenberg BI, Burkepile DE (2018) Comparative analysis of foraging behavior and bite mechanics reveals complex functional diversity among Caribbean parrotfishes. Mar Ecol Prog Ser 597:207–220

    Google Scholar 

  2. Adam TC, Kelley M, Ruttenberg BI, Burkepile DE (2015) Resource partitioning along multiple niche axes drives functional diversity in parrotfishes on Caribbean coral reefs. Oecologia 179:1173–1185

    PubMed  Google Scholar 

  3. Aronson R, Bruckner A, Moore J, Precht B, Weil E (2008) IUCN red list of endangered species: Montastraea annularis. IUCN Red List

  4. Bak RPM, Steward-Van Es Y (1980) Regeneration of superficial damage in the Scleractinian corals Agaricia Agaricites F. Purpurea and Porites Astreoides. Bull Mar Sci 30:883–887

    Google Scholar 

  5. Barott KL, Williams GJ, Vermeij MJA, Harris J, Smith JE, Rohwer FL, Sandin SA (2012) Natural history of coral—algae competition across a gradient of human activity in the Line Islands. Mar Ecol Prog Ser 460:1–12

    Google Scholar 

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

    Google Scholar 

  7. Bonaldo RM, Bellwood DR (2011) Parrotfish predation on massive Porites on the Great Barrier Reef. Coral Reefs 30:259–269

    Google Scholar 

  8. Bonaldo RM, Krajewski PJ, Bellwood DR (2011) Relative impact of parrotfish grazing scars on massive Porites corals at Lizard Island, Great Barrier Reef. Mar Ecol Prog Ser 423:223–233

    Google Scholar 

  9. Brandt ME, Zurcher N, Acosta A, Ault JS, Bohnsack JA, Feeley MW, Harper DE, Hunt JH, Kellison GT, McClellan DB, Patterson ME, Smith SG (2009) A cooperative multi-agency reef fish monitoring protocol for the Florida Keys coral reef ecosystem. Natural Resource Report NPS/SFCN/NRR—2009/150. National Park Service, Fort Collins, Colorado

  10. Bruckner AW, Bruckner RJ, Sollins P (2000) Parrotfish predation on live coral: “spot biting” and “focused biting”. Coral Reefs 19:50

    Google Scholar 

  11. Burkepile DE (2012) Context-dependent corallivory by parrotfishes in a Caribbean reef ecosystem. Coral Reefs 31:111–120

    Google Scholar 

  12. Burkepile DE, Adam TC, Roycroft M, Ladd MC, Munsterman KS, Ruttenberg BI (2019) Species-specific patterns in corallivory and spongivory among Caribbean parrotfishes. Coral Reefs 38:417–423

    Google Scholar 

  13. 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 105:16201–16206

    CAS  PubMed  Google Scholar 

  14. Bythell JC, Gladfelter EH, Bythell M (1993) Chronic and catastrophic natural mortality of three common Caribbean reef corals. Coral Reefs 12:143–152

    Google Scholar 

  15. Carpenter KE, Abrar M, Aeby G, Aronson RB, Banks S, Bruckner A, Chiriboga A, Cortés J, Delbeek JC, DeVantier L, Edgar GJ, Edwards AJ, Fenner D, Guzmán HM, Hoeksema BW, Hodgson G, Johan O, Licuanan WY, Livingstone SR, Lovell ER, Moore JA, Obura DO, Ochavillo D, Polidoro BA, Precht WF, Quibilan MC, Reboton C, Richards ZT, Rogers AD, Sanciangco J, Sheppard A, Sheppard C, Smith J, Stuart S, Turak E, Veron JEN, Wallace C, Weil E, Wood E (2008) One-third of reef-building corals face elevated extinction risk from climate change and local impacts. Science 321:560–563

    CAS  PubMed  Google Scholar 

  16. Carpenter RC (1990) Mass mortality of Diadema antillarum II Effects on population densities and grazing intensity of parrotfishes and surgeonfishes. Mar Biol 86:79–86

    Google Scholar 

  17. 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 Linn Soc

  18. Cramer KL, O’Dea A, Clark TR, Zhao J, Norris RD (2017) Prehistorical and historical declines in Caribbean coral reef accretion rates driven by loss of parrotfish. Nat Commun 8:14160

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Cróquer A, Villamizar E, Noriega N (2002) Environmental factors affecting tissue regeneration of the reef-building coral Montastraea annularis (Faviidae) at Los Roques National Park, Venezuela. Rev Biol Trop 50:1055–1065

    PubMed  Google Scholar 

  20. D’Angelo C, Wiedenmann J (2014) Impacts of nutrient enrichment on coral reefs: new perspectives and implications for coastal management and reef survival. Curr Opin Environ Sustain 7:82–93

    Google Scholar 

  21. De’ath G, Fabricius KE, Sweatman H, Puotinen M (2012) The 27-year decline of coral cover on the Great Barrier Reef and its causes. Proc Natl Acad Sci 109:17995–17999

    PubMed  Google Scholar 

  22. Diaz-Pulido G, McCook LJ, Dove S, Berkelmans R, Roff G, Kline DI, Weeks S, Evans RD, Williamson DH, Hoegh-Guldberg O (2009) Doom and boom on a resilient reef: climate change, algal overgrowth and coral recovery. PLoS ONE 4:e5239

    PubMed  PubMed Central  Google Scholar 

  23. DPNR (2005) U.S. Virgin Islands marine resources and fisheries strategic and comprehensive conservation plan. Division of Fish and Wildlife, Department of Planning and Natural Resources, St. Croix, USVI

  24. Edmunds PJ, Elahi R (2007) The demographics of a 15-year decline in cover of the Caribbean reef coral Montastraea annularis. Ecol Monogr 77:3–18

    Google Scholar 

  25. Executive Council of the Bonaire Island Territory (2010) Island Resolution Nature Management Bonaire. Section III—Protection of Animal and Plant Species

  26. Ezzat L, Lamy T, Maher RL, Munsterman KS, Landfield KM, Schmeltzer ER, Clements CS, Vega Thurber RL, Burkepile DE (2020) Parrotfish predation drives distinct microbial communities in reef-building corals. Anim Microbiome 2:5

    Google Scholar 

  27. Frydl P (1979) The effect of parrotfish (Scaridae) on coral in Barbados. W. I. Int Rev Gesamten Hydrobiol Hydrogr 64:737–748

    Google Scholar 

  28. Garzon-Ferreira J, Reyes-Nivia M (2001) Incidencia de la depredacion por peces en corales petreos de cuatro atolones del archipeielago de san andres y providencia (Caribe Colombiano). Bol Invest Mar Cost 30:133–150

    Google Scholar 

  29. Hoegh-Guldberg O, Poloczanska ES, Skirving W, Dove S (2017) Coral reef ecosystems under climate change and ocean acidification. Front Mar Sci 4:1–20

    Google Scholar 

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

    Google Scholar 

  31. Hrong-Tai Fai A, Cornelius PL (1996) Approximate F-tests of multiple degree of freedom hypotheses in generalized least squares analyses of unbalanced split-plot experiments. J Stat Comput Simul 54:363–378

    Google Scholar 

  32. Hughes TP, Barnes ML, Bellwood DR, Cinner JE, Cumming GS, Jackson JBC, Kleypas J, Van De Leemput IA, Lough JM, Morrison TH, Palumbi SR, Van Nes EH, Scheffer M (2017) Coral reefs in the Anthropocene. Nature 546:82–90

    CAS  PubMed  Google Scholar 

  33. 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 17:360–365

    CAS  PubMed  Google Scholar 

  34. Hughes TP, Tanner JE (2000) Recruitment failure, life histories, and long-term decline of Caribbean corals. Ecology 81:2250–2263

    Google Scholar 

  35. Jackson JBC, Donovan MK, Cramer KL, Lam V, Lam W (2014) Status and trends of Caribbean coral reefs: 1970–2012. Global Coral Reef Monitoring Network, IUCN, Gland

    Google Scholar 

  36. Jayewardene D, Donahue MJ, Birkeland C (2009) Effects of frequent fish predation on corals in Hawaii. Coral Reefs 28:499–506

    Google Scholar 

  37. Kuznetsova A, Brockhoff PB, Christensen RHB (2017) lmerTest package: tests in linear mixed effects models. J Stat Softw 82:1–26

    Google Scholar 

  38. Lenth R (2020) emmeans: Estimated Marginal Means, aka Least-Squares Means. R package version 1.4.8. https://CRAN.R-project.org/package=emmeans

  39. Lessios HA (1988) Mass mortality of Diadema antillarum in the Caribbean: What have we learned? Annu Rev Ecol Syst 19:371–393

    Google Scholar 

  40. Lirman D (2000) Lesion regeneration in the branching coral Acropora palmata: effects of colonization, colony size, lesion size, and lesion shape. Mar Ecol Prog Ser 197:209–215

    Google Scholar 

  41. Lirman D (2001) Competition between macroalgae and corals: effects of herbivore exclusion and increased algal biomass on coral survivorship and growth. Coral Reefs 19:392–399

    Google Scholar 

  42. Littler M, Taylor P, Littler D (1989) Complex interactions in the control of coral zonation on a Caribbean reef flat. Oecologia 80:331–340

    CAS  PubMed  Google Scholar 

  43. Meesters EH, Noordeloos M, Bak RPM (1994) Damage and regeneration: links to growth in the reef-building coral Montastrea annularis. Mar Ecol Prog Ser 112:119–128

    Google Scholar 

  44. Meesters EH, Pauchli W, Bak RPM (1997) Predicting regeneration of physical damage on a reef-building coral by regeneration capacity and lesion shape. Mar Ecol Prog Ser 146:91–99

    Google Scholar 

  45. Miller MW, Hay ME (1998) Effects of fish predation and seaweed competition on the survival and growth of corals. Oecologia 113:231–238

    PubMed  Google Scholar 

  46. Mumby PJ (2006) The impact of exploiting grazers (Scaridae) on the dynamics of Caribbean coral reefs. Ecol Appl 16:747–769

    PubMed  Google Scholar 

  47. Mumby PJ (2009) Herbivory versus corallivory: Are parrotfish good or bad for Caribbean coral reefs? Coral Reefs 28:683–690

    Google Scholar 

  48. Nakagawa S, Schielzeth H (2012) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142

    Google Scholar 

  49. Naumann MS, Niggl W, Laforsch C, Glaser C, Wild C (2009) Coral surface area quantification—evaluation of established techniques by comparison with computer tomography. Coral Reefs 28:109–117

    Google Scholar 

  50. Nicholson GM, Clements KD (2020) Resolving resource partitioning in parrotfishes (Scarini) using microhistology of feeding substrata. Coral Reefs

  51. NOAA, NMFS (2012) Analyses of commercial parrotfish landings in the U.S. Caribbean. Natl Ocean Atmospheric Assoc Tech Rep SERO LAPP 2:1–22

    Google Scholar 

  52. NOAA, Nmfs, Dept. of Commerce (2014) Endangered and threatened wildlife and plants: final listing determinations on proposal to list 66 reef-building coral species and to reclassify Elkhorn and Staghorn Corals. National Oceanic and Atmospheric Administration, Silver Spring

    Google Scholar 

  53. R Core Team (2019) R: A language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria. https://www.R-project.org/

  54. Rice MM, Ezzat L, Burkepile DE (2019) Corallivory in the Anthropocene: interactive effects of anthropogenic stressors and corallivory on coral reefs. Front Mar Sci 5:525

    Google Scholar 

  55. Roff G, Ledlie MH, Ortiz JC, Mumby PJ (2011) Spatial patterns of parrotfish corallivory in the Caribbean: the importance of coral taxa, density and size. PLOS ONE 6:e29133

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Rotjan RD, Dimond JL (2010) Discriminating causes from consequences of persistent parrotfish corallivory. J Exp Mar Biol Ecol 390:188–195

    Google Scholar 

  57. Rotjan RD, Dimond JL, Thornhill DJ, Leichter JJ, Helmuth B, Kemp DW, Lewis SM (2006) Chronic parrotfish grazing impedes coral recovery after bleaching. Coral Reefs 25:361–368

    Google Scholar 

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

    Google Scholar 

  59. Rotjan RD, Lewis SM (2008) Impact of coral predators on tropical reefs. Mar Ecol Prog Ser 367:73–91

    Google Scholar 

  60. Rotjan RD, Lewis SM (2009) Predators selectively graze reproductive structures in a clonal marine organism. Mar Biol 156:569–577

    Google Scholar 

  61. RStudio Team (2019) RStudio: integrated development for R. RStudio: Integrated Development for R. RStudio Inc., Boston, MA. http://www.rstudio.com/

  62. Sánchez JA, Gil MF, Chasqui LH, Alvarado EM (2004) Grazing dynamics on a Caribbean reef-building coral. Coral Reefs 23:578–583

    Google Scholar 

  63. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675

    CAS  PubMed  PubMed Central  Google Scholar 

  64. Schwarz G (1978) Estimating the dimension of a model. Ann Stat 6:461–464

    Google Scholar 

  65. Smith JE, Hunter CL, Smith CM (2010) The effects of top-down versus bottom-up control on benthic coral reef community structure. Oecologia 163:497–507

    PubMed  Google Scholar 

  66. Smith SG, Ault JS, Bohnsack JA, Harper DE, Luo J, McClellan DB (2011) Multispecies survey design for assessing reef-fish stocks, spatially explicit management performance, and ecosystem condition. Fish Res 109:25–41

    Google Scholar 

  67. Steneck RS, Arnold SN, Mumby PJ (2014) Experiment mimics fishing on parrotfish: insights on coral reef recovery and alternative attractors. Mar Ecol Prog Ser 506:115–127

    Google Scholar 

  68. Steneck RS, Mumby PJ, Macdonald C, Rasher DB, Stoyle G (2018) Attenuating effects of ecosystem management on coral reefs. Sci Adv 4:1–12

    Google Scholar 

  69. Van Veghel M, Bak R (1993) Reproductive characteristics of the polymorphic Caribbean reef building coral Montastrea annularis. III. Reproduction in damaged and regenerating colonies. Mar Ecol Prog Ser 109:229–234

    Google Scholar 

  70. van de Water JAJM, Ainsworth TD, Leggat W, Bourne DG, Willis BL, van Oppen MJH (2015) The coral immune response facilitates protection against microbes during tissue regeneration. Mol Ecol 24:3390–3404

    PubMed  Google Scholar 

  71. Welsh JQ, Bonaldo RM, Bellwood DR (2015) Clustered parrotfish feeding scars trigger partial coral mortality of massive Porites colonies on the inshore Great Barrier Reef. Coral Reefs 34:81–86

    Google Scholar 

  72. Wickham H, Averick M, Bryan J, Chang W, McGowan L, François R, Grolemund G, Hayes A, Henry L, Hester J, Kuhn M, Pedersen T, Miller E, Bache S, Müller K, Ooms J, Robinson D, Seidel D, Spinu V, Takahashi K, Vaughan D, Wilke C, Woo K, Yutani H (2019) Welcome to the Tidyverse. J Open Source Softw 4:1686

    Google Scholar 

  73. Wong TT (2015) Performance evaluation of classification algorithms by k-fold and leave-one-out cross validation. Pattern Recognit 48:2839–2846

    Google Scholar 

  74. Zuur AF, Ieno EN, Walker N, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York

    Google Scholar 

Download references

Acknowledgements

We thank E. Barton, M. Goodman, M. Lippert, L. Palma, M. Roycroft, P. Vanderbloomer, A. Wolman, and J. Zaring for assistance with field work. We thank C. Francis for data analysis advice and the two anonymous reviewers for comments that improved this manuscript. We are grateful to the St. Croix National Park Service and STINAPA Bonaire National Parks Foundation for logistical support and to Dive Friends Bonaire for their donation of dive tanks for this study. We thank the Balaba and Everlove families for in-kind donations to support travel and accommodations for this study. This research was funded by the NOAA Coral Reef Conservation Program (Grant No. NA16NOS4820050), California State University Council on Ocean Affairs, Science & Technology (CSU COAST), Dr. Earl H. Myers & Ethel M. Myers Oceanographic & Marine Biology Trust, Harvard Travellers Club Permanent Fund, American Museum of Natural History Lerner-Gray Fund for Marine Research, and California Polytechnic State University Frost Fund.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Hannah S. Rempel.

Ethics declarations

Conflict of interest statement

On behalf of all authors, the corresponding author states that there is no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Topic Editor Andrew Hoey

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 32 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Rempel, H.S., Bodwin, K.N. & Ruttenberg, B.I. Impacts of parrotfish predation on a major reef-building coral: quantifying healing rates and thresholds of coral recovery. Coral Reefs 39, 1441–1452 (2020). https://doi.org/10.1007/s00338-020-01977-9

Download citation

Keywords

  • Corallivory
  • Tissue regeneration
  • Coral healing
  • Parrotfish
  • Caribbean
  • Orbicella annularis