Skip to main content

Advertisement

SpringerLink
Log in

Empirical relationships among resilience indicators on Micronesian reefs

  • Report
  • Published:
Coral Reefs Aims and scope Submit manuscript

Abstract

A process-orientated understanding of ecosystems usually starts with an exploratory analysis of empirical relationships among potential drivers and state variables. While relationships among herbivory, algal cover, and coral recruitment, have been explored in the Caribbean, the nature of such relationships in the Pacific appears to be variable or unclear. Here, we examine potential drivers structuring the benthos and herbivorous fish assemblages of outer-shelf reefs in Micronesia (Palau, Guam and Pohnpei). Surveys were stratified by wave exposure and protection from fishing. High biomass of most herbivores was favoured by high wave exposure. High abundance of large-bodied scarids was associated with low turf abundance, high coral cover, and marine reserves. The remaining herbivores were more abundant in reefs with low coral cover, possibly because space and hence food limitation occur in high-coral-cover reefs. Rugosity had no detectable effect on herbivorous fish abundance once differences in exposure and coral cover were accounted for. At identical depths, high wave exposure was associated with greater volumes (cover × canopy height) of macroalgae and algal turfs, which most likely resulted from high primary productivity driven by flow. In exposed areas, macroalgal cover declined as the acanthurid biomass increased. The volume of algal turfs was negatively associated with coral cover and herbivore biomass. In turn, high coral cover and herbivore biomass are likely to intensify grazing. The density of juvenile corals was variable where macroalgal cover was low but was confined to lower densities where macroalgal cover was high. High coral cover and density of juvenile corals were favoured in sheltered habitats. While a weak positive relationship was found between scarid biomass and juvenile coral density, we hypothesise that high scarid densities may hinder juvenile density through increased corallivory. New hypotheses emerged that will help clarify the role of acanthurids, wave exposure, and corallivory in driving the recovery of Pacific coral communities.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

References

  • Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA+ for PRIMER: Guide to software and statistical methods. PRIMER-E, Plymouth, UK

    Google Scholar 

  • Arnold SN, Steneck RS, Mumby PJ (2010) Running the gauntlet: inhibitory effects of algal turfs on the process of coral recruitment. Mar Ecol Prog Ser 414:91–105

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Bellwood DR, Fulton CJ (2008) Sediment-mediated suppression of herbivory on coral reefs: decreasing resilience to rising sea levels and climate change? Limnol Oceanogr 53:2695–2701

    Article  Google Scholar 

  • Bellwood DR, Hughes TP, Folke C, Nystrom M (2004) Confronting the coral reef crisis. Nature 429:827–833

    Article  PubMed  CAS  Google Scholar 

  • Birrell CL, McCook LJ, Willis BL (2005) Effects of algal turfs and sediment on coral settlement. Mar Pollut Bull 51:408–414

    Article  PubMed  CAS  Google Scholar 

  • Carpenter RC, Williams SL (2007) Mass transfer limitation of photosynthesis of coral reef algal turfs. Mar Biol 151:435–450

    Article  Google Scholar 

  • Choat JH (1991) The biology of herbivorous fishes on coral reefs. In: Sale PF (ed) The ecology of fishes on coral reefs. Academic Press, San Diego, pp 120–155

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Choat JH, Robbins WD, Clements KD (2004) The trophic status of herbivorous fishes on coral reefs - II. food processing modes and trophodynamics. Mar Biol 145:445–454

    Article  Google Scholar 

  • Clarke A, Johnston NM (1999) Scaling of metabolic rate with body mass and temperature in teleost fish. J Anim Ecol 68:893–905

    Article  Google Scholar 

  • Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143

    Article  Google Scholar 

  • Connell JH (1997) Disturbance and recovery of coral assemblages. Coral Reefs 16:S101–S113

    Article  Google Scholar 

  • Crawley MJ (2007) The R Book. John Wiley & Sons Ltd, Chichester

    Book  Google Scholar 

  • Crowder LB, Cooper WE (1982) Habitat structural complexity and the interaction between bluegills and their prey. Ecology 63:1802–1813

    Article  Google Scholar 

  • Done TJ, Dayton PK, Dayton AE, Steger R (1991) Regional and local variability in recovery of shallow coral communities: Moorea, French Polynesia and central Great Barrier Reef. Coral Reefs 9:183–192

    Article  Google Scholar 

  • Edmunds PJ, Carpenter RC (2001) Recovery of Diadema antillarum reduces macroalgal cover and increases abundance of juvenile corals on a Caribbean reef. Proc Natl Acad Sci USA 98:5067–5071

    Article  PubMed  CAS  Google Scholar 

  • Fitzpatrick SM, Donaldson TJ (2007) Anthropogenic impacts to coral reefs in Palau, western Micronesia during the Late Holocene. Coral Reefs 26:915–930

    Article  Google Scholar 

  • Friedlander AM, Brown E, Monaco ME (2007) Defining reef fish habitat utilization patterns in Hawaii: comparisons between marine protected areas and areas open to fishing. Mar Ecol Prog Ser 351:221–233

    Article  Google Scholar 

  • Friedlander AM, Brown E, Jokiel PL, Smith WR, Rodgers KS (2003) Effects of habitat, wave exposure, and marine protected area status on coral reef fish assemblages in the Hawaiian archipelago. Coral Reefs 22:291–305

    Article  Google Scholar 

  • Goatley CHR, Bellwood DR (2010) Biologically mediated sediment fluxes on coral reefs: sediment removal and off-reef transportation by the surgeonfish Ctenochaetus striatus. Mar Ecol Prog Ser 415:237–245

    Article  Google Scholar 

  • Golbuu Y, Bauman A, Kuartei J, Victor S (2005) The state of coral reef ecosystems of Palau. In: Waddell J (ed) The state of coral reef ecosystems of the United States and Pacific freely associated states: 2005 NOAA Technical Memorandum NOS NCCOS 11. NOAA/NCCOS, Silver Spring, MD, pp 488–507

    Google Scholar 

  • Gombos M, Gutierrez J, Brown V (2007) Guam coral reef MPA summary. Report on the status of marine protected areas in coral reef ecosystems of the United States 1: Marine protected areas managed by US states, territories, and commonwealths: 2007. NOAA Technical Memorandum CRCP 2. NOAA Coral Reef Conservation Program, Silver Spring, MD. p129 + Appendices

  • Hensley RA, Sherwood TS (1993) An overview of Guam's inshore fisheries. Mar Fish Rev 55:129–138

    Google Scholar 

  • Holmes TH, McCormick MI (2010) Size-selectivity of predatory reef fish on juvenile prey. Mar Ecol Prog Ser 399:273–283

    Article  Google Scholar 

  • Houk P, Rhodes K, Cuetos-Bueno J, Lindfield S, Fread V, McIlwain JL (2012) Commercial coral-reef fisheries across Micronesia: A need for improving management. Coral Reefs 31:455–459

    Article  Google Scholar 

  • Hughes TP (1985) Life histories and population dynamics of early successional corals. Proc 5th Int Coral Reef Congr 4:101–106

  • Hughes TP (1994) Catastrophes, phase shifts, and large-scale degradation of a Caribbean coral reef. Science 265:1547–1551

    Article  PubMed  CAS  Google Scholar 

  • Hughes TP, Bellwood DR, Folke C, Steneck RS, Wilson J (2005) New paradigms for supporting the resilience of marine ecosystems. Trends Ecol Evol 20:380–386

    Article  PubMed  Google Scholar 

  • Hughes TP, Baird AH, Dinsdale EA, Moltschaniwskyj NA, Pratchett MS, Tanner JE, Willis BL (1999) Patterns of recruitment and abundance of corals along the Great Barrier Reef. Nature 397:59–63

    Article  CAS  Google Scholar 

  • Hughes TP, Rodrigues MJ, Bellwood DR, Ceccarelli D, Hoegh-Guldberg O, McCook L, Moltschaniwskyj N, Pratchett MS, Steneck RS, Willis BL (2007) Phase shifts, herbivory, and the resilience of coral reefs to climate change. Curr Biol 17:360–365

    Article  PubMed  CAS  Google Scholar 

  • Hutchings PA (1986) Biological destruction of coral reefs. Coral Reefs 4:239–252

    Article  Google Scholar 

  • Idjadi JA, Lee SC, Bruno JF, Precht WF, Allen-Requa L, Edmunds PJ (2006) Rapid phase-shift reversal on a Jamaican coral reef. Coral Reefs 25:209–211

    Article  Google Scholar 

  • Kitalong A, Dalzell P (1994) A preliminary assessment of the status of inshore coral reef fish stocks in Palau. Inshore Fisheries Research Project technical document no 6. Noumea, New Caledonia South Pacific Commission

  • Lang JC (1973) Interspecific aggression by scleractinian corals. 2. Why the race is not only to the swift. Bull Mar Sci 23:260–279

    Google Scholar 

  • Logan M (2010) Biostatistical design and analysis using R. John Wiley & Sons Chichester

  • Mapstone BD, Andrew NL, Chancerelle Y, Salvat B (2007) Mediating effects of sea urchins on interactions among corals, algae and herbivorous fish in the Moorea lagoon, French Polynesia. Mar Ecol Prog Ser 332:143–153

    Article  Google Scholar 

  • Marshell A, Mumby PJ (2012) Revisiting the functional roles of the surgeonfish Acanthurus nigrofuscus and Ctenochaetus striatus. Coral Reefs [DOI: 10.1007/s00338-012-0931-y]

  • McClanahan TR, Muthiga N (2001) The ecology of Echinometra. In: Lawrence JM (ed) Edible sea urchins: biology and ecology. Elsevier Science, New York, pp 225–243

    Chapter  Google Scholar 

  • Mumby PJ, Wabnitz CCC (2002) Spatial patterns of aggression, territory size, and harem size in five sympatric Caribbean parrotfish species. Environ Biol Fishes 63:265–279

    Article  Google Scholar 

  • Mumby PJ, Steneck RS (2008) Coral reef management and conservation in light of rapidly-evolving ecological paradigms. Trends Ecol Evol 23:555–563

    Article  PubMed  Google Scholar 

  • Mumby PJ, Harborne AR (2010) Marine reserves enhance the recovery of corals on Caribbean reefs. PLoS One 5:e8657

    Article  PubMed  Google Scholar 

  • Mumby PJ, Hastings A, Edwards HJ (2007a) Thresholds and the resilience of Caribbean coral reefs. Nature 450:98–101

    Article  PubMed  CAS  Google Scholar 

  • Mumby PJ, Harborne AR, Hedley JD, Zychaluk K, Blackwell PG (2006) Revisiting the catastrophic die-off of the urchin Diadema antillarum on Caribbean coral reefs: Fresh insights on resilience from a simulation model. Ecol Model 196:131–148

    Article  Google Scholar 

  • Mumby PJ, Harborne AR, Williams J, Kappel CV, Brumbaugh DR, Micheli F, Holmes KE, Dahlgren CP, Paris CP, Blackwell PG (2007b) Trophic cascade facilitates coral recruitment in a marine reserve. Proc Natl Acad Sci USA 104:8362–8367

    Article  PubMed  CAS  Google Scholar 

  • Munday PL, Jones GP (1998) The ecological implications of small body size among coral-reef fishes. Oceanogr Mar Biol Annu Rev 36:373–411

    Google Scholar 

  • Nelson WG, Bonsdorff E (1990) Fish predation and habitat complexity: are complexity thresholds real? J Exp Mar Biol Ecol 141:183–194

    Article  Google Scholar 

  • Ogden JC (1987) Comparison of the tropical western Atlantic (Caribbean) and the Indo-Pacific: herbivore–plant interactions. UNESCO Rep Mar Sci 46:167–169

    Google Scholar 

  • Penin L, Michonneau F, Baird AH, Connolly SR, Pratchett MS, Kayal M, Adjeroud M (2010) Early post-settlement mortality and the structure of coral assemblages. Mar Ecol Prog Ser 408:55–64

    Article  Google Scholar 

  • Peyrot-Clausade M, Chabanet P, Conand C, Fontaine MF, Letourneur Y, Harmelin-Vivien M (2000) Sea urchin and fish bioerosion on La Réunion and Moorea Reefs. Bull Mar Sci 66:477–485

    Google Scholar 

  • Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-plus. Springer-Verlag New York

  • Polunin NVC, Harmelin-Vivien M, Galzin R (1995) Contrasts in algal food processing among five herbivorous coral reef fishes. J Fish Biol 47:455–465

    Article  Google Scholar 

  • Purcell SW, Bellwood DR (1993) A functional analysis of food procurement in 2 surgeonfish species, Acanthurus nigrofuscus and Ctenochaetus striatus (Acanthuridae). Environ Biol Fishes 37:139–159

    Article  Google Scholar 

  • Renken H, Mumby PJ, Matsikis I, Edwards HJ (2010) Effects of physical environmental conditions on the patch dynamics of Dictyota pulchella and Lobophora variegata on Caribbean coral reefs. Mar Ecol Prog Ser 403:63–74

    Article  Google Scholar 

  • Rhodes KL, Tupper MH (2007) A preliminary market-based analysis of the Pohnpei, Micronesia, grouper (Serranidae: Epinephelinae) fishery reveals unsustainable fishing practices. Coral Reefs 26:335–344

    Article  Google Scholar 

  • Roff G, Mumby PJ (2012) Global disparity in the resilience of coral reefs. Trends Ecol Evol 27(7):404–413

    Article  PubMed  Google Scholar 

  • Rogers CS, Fitz HC, Gilnack M, Beets J, Hardin J (1984) Scleractinian coral recruitment patterns at Salt River Submarine Canyon, St. Croix, U.S. Virgin Islands. Coral Reefs 3:69–76

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Sammarco PW (1980) Diadema and its relationship to coral spat mortality: grazing, competition and biological disturbance. J Exp Mar Biol Ecol 45:245–272

    Article  Google Scholar 

  • Sammarco PW (1982) Echinoid grazing as a structuring force in coral communities: Whole reef manipulations. J Exp Mar Biol Ecol 61:31–55

    Article  Google Scholar 

  • Sammarco PW (1987) A comparison of some ecological processes on coral reefs of the Caribbean and the Great Barrier Reef. UNESCO Rep Mar Sci 46:127–166

    Google Scholar 

  • Sandin SA, Smith JE, DeMartini EE, Dinsdale EA, Donner SD, Friedlander AM, Konotchick T, Malay M, Maragos JE, Obura D, Pantos O, Paulay G, Richie M, Rohwer F, Schroeder RE, Walsh S, Jackson JBC, Knowlton N, Sala E (2008) Baselines and degradation of coral reefs in the Northern Line Islands. PLoS One 3:e1548

    Article  PubMed  Google Scholar 

  • Steneck RS (1983) Quantifying herbivory on coral reefs: just scratching the surface and still biting off more than we can chew. In: Reaka ML (ed) The ecology of deep and shallow coral reefs. Symposia series for undersea research NOAA, pp103-112

  • Steneck RS (1994) Is herbivore loss more damaging to reefs than hurricanes? Case studies from two Caribbean reef systems (1978-1988). In: Ginsburg RN (ed) Global aspects of coral reefs: Health, hazards, and history. RSMAS, Univ. of Miami, Miami, pp C32-C37

  • Steneck RS (1988) Herbivory on coral reefs: a synthesis. Proc 6th Int Coral Reef Symp 37–49

  • Steneck RS (1997) Crustose corallines, other algal functional groups, herbivores and sediments: complex interactions along reef productivity gradients. Proc 8th Int Coral Reef Symp 1:695–700

    Google Scholar 

  • Steneck RS, Dethier M (1994) A functional group approach to the structure of algal-dominated communities. Oikos 69:476–498

    Article  Google Scholar 

  • 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 389:1–15

    Article  Google Scholar 

  • Tanner JE (1995) Competition between scleractinian corals and macroalgae: an experimental investigation of coral growth, survival and reproduction. J Exp Mar Biol Ecol 190:151–168

    Article  Google Scholar 

  • van Beukering P, Haider W, Longland M, Cesar HSJ, Sablan J, Shjegstad S, Beardmore B, Liu Y, Garces GO (2007) The economic value of Guam’s coral reefs. Report prepared by Cesar Environmental Consulting, funded by the National Oceanic and Atmospheric Administration, Silver Springs, MD

  • van Beukering P, Haider W, Wolfs E, Liu Y, van der Leeuw K, Longland M, Sablan J, Beardmore B, Di Prima S, Massey E, Cesar HSJ, Hausfather Z, Gourley J (2006) The economic value of the coral reefs of Saipan, Commonwealth of the Northern Mariana Islands. Report prepared by Cesar Environmental Consulting. Funded by the National Oceanic and Atmospheric Administration, Silver Springs, MD

    Google Scholar 

  • Williams ID, Polunin NVC (2000) Large-scale associations between macroalgal cover and grazer biomass on mid-depth reefs in the Caribbean. Coral Reefs 19:358–366

    Google Scholar 

  • Williams ID, Polunin NVC, Hendrick VJ (2001) Limits to grazing by herbivorous fishes and the impact of low coral cover on macroalgal abundance on a coral reef in Belize. Mar Ecol Prog Ser 222:187–196

    Article  Google Scholar 

  • Wismer S, Hoey AS, Bellwood DR (2009) Cross-shelf benthic community structure on the Great Barrier Reef: relationships between macroalgal cover and herbivore biomass. Mar Ecol Prog Ser 376:45–54

    Article  Google Scholar 

  • Young MAL, Bellwood DR (2011) Diel patterns in sea urchin activity and predation on sea urchins on the Great Barrier Reef. Coral Reefs 30:729–736

    Article  Google Scholar 

  • Zeller DC, Booth S, Pauly D (2006) Fisheries contributions to the gross domestic product: underestimating small-scale fisheries in the Pacific. Mar Resour Econ 21:355–374

    Google Scholar 

Download references

Acknowledgments

The study was funded by the National Fish and Wildlife Foundation and a small grant from the World Bank/GEF Coral Reef Targeted Research.

Author information

Authors and Affiliations

  1. Marine Spatial Ecology Lab, School of Biological Sciences, University of Queensland, St. Lucia, QLD, 4072, Australia

    P. J. Mumby & S. Bejarano

  2. Palau International Coral Reef Center, Koror, Republic of Palau

    Y. Golbuu

  3. Darling Marine Center, University of Maine, Walpole, ME, 04573, USA

    R. S. Steneck & S. N. Arnold

  4. Florida Institute of Technology, 150 West University Boulevard, Melbourne, FL, 32901, USA

    R. van Woesik

  5. US Geological Survey, Hawaii Cooperative Fishery Research Unit, University of Hawaii, Honolulu, HI, 96822, USA

    A. M. Friedlander

Authors
  1. P. J. Mumby
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. Bejarano
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Y. Golbuu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. R. S. Steneck
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. S. N. Arnold
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. R. van Woesik
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. A. M. Friedlander
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to P. J. Mumby.

Additional information

Communicated by Ecology Editor Prof. Mark Hay

Appendix

Appendix

See Table 8.

Table 8 Species of reef fish surveyed in the band transects in the different passes
Full size table

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mumby, P.J., Bejarano, S., Golbuu, Y. et al. Empirical relationships among resilience indicators on Micronesian reefs. Coral Reefs 32, 213–226 (2013). https://doi.org/10.1007/s00338-012-0966-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00338-012-0966-0

Keywords

Search

Navigation