Skip to main content
Log in

Facilitation in Caribbean coral reefs: high densities of staghorn coral foster greater coral condition and reef fish composition

  • Community ecology – original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Recovery of the threatened staghorn coral (Acropora cervicornis) is posited to play a key role in Caribbean reef resilience. At four Caribbean locations (including one restored and three extant populations), we quantified characteristics of contemporary staghorn coral across increasing conspecific densities, and investigated a hypothesis of facilitation between staghorn coral and reef fishes. High staghorn densities in the Dry Tortugas exhibited significantly less partial mortality, higher branch growth, and supported greater fish abundances compared to lower densities within the same population. In contrast, partial mortality, branch growth, and fish community composition did not vary with staghorn density at the three other study locations where staghorn densities were lower overall. This suggests that density-dependent effects between the coral and fish community may only manifest at high staghorn densities. We then evaluated one facilitative mechanism for such density-dependence, whereby abundant fishes sheltering in dense staghorn aggregations deliver nutrients back to the coral, fueling faster coral growth, thereby creating more fish habitat. Indeed, dense staghorn aggregations within the Dry Tortugas exhibited significantly higher growth rates, tissue nitrogen, and zooxanthellae densities than sparse aggregations. Similarly, higher tissue nitrogen was induced in a macroalgae bioassay outplanted into the same dense and sparse aggregations, confirming greater bioavailability of nutrients at high staghorn densities. Our findings inform staghorn restoration efforts, suggesting that the most effective targets may be higher coral densities than previously thought. These coral-dense aggregations may reap the benefits of positive facilitation between the staghorn and fish community, favoring the growth and survivorship of this threatened species.

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

Access this article

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

Similar content being viewed by others

References

  • Agudo-Adriani EA, Cappelletto J, Cavada-Blanco F, Croquer A (2016) Colony geometry and structural complexity of the endangered species Acropora cervicornis partly explains the structure of their associated fish assemblage. PeerJ 4:e1861

    Article  PubMed  PubMed Central  Google Scholar 

  • Alvarez-Filip L, Dulvy NK, Gill JA, Côté IM, Watkinson AR (2009) Flattening of Caribbean coral reefs: region-wide declines in architectural complexity. P Roy Soc B-Biol Sci 276:3019–3025

    Article  Google Scholar 

  • Boyer KE, Zedler JB (1998) Effects of nitrogen additions on the vertical structure of a constructed cordgrass marsh. Ecol Appl 8:692–705

    Article  Google Scholar 

  • Bozec Y, Yakob L, Bejarano S, Mumby PJ (2013) Reciprocal facilitation and non-linearity maintain habitat engineering on coral reefs. Oikos 122:428–440

    Article  Google Scholar 

  • Bruno JF, Stachowicz JJ, Bertness MD (2003) Inclusion of facilitation into ecological theory. Trends Ecol Evol 18:119–125

    Article  Google Scholar 

  • Bruno JF, Selig ER, Casey KS, Page CA, Willis BL, Harvell CD, Sweatman H, Melendy AM (2007) Thermal stress and coral cover as drivers of coral disease outbreaks. PLoS Biol 5:e124

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  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  CAS  PubMed  PubMed Central  Google Scholar 

  • Gardner TA, Cote IM, Gill JA, Grant A, Watkinson AR (2003) Long-term region-wide declines in Caribbean corals. Science 301:958–960. doi:10.1126/science.1086050

    Article  CAS  PubMed  Google Scholar 

  • Gascoigne J, Lipcius RN (2004) Allee effects in marine systems. Mar Ecol Prog Ser 269:49–59

    Article  Google Scholar 

  • Gómez-Aparicio L, Zamora R, Gómez JM, Hódar JA, Castro J, Baraza E (2004) Applying plant facilitation to forest restoration: a meta-analysis of the use of shrubs as nurse plants. Ecol Appl 14:1128–1138

    Article  Google Scholar 

  • Graham MH (2004) Effects of local deforestation on the diversity and structure of southern California giant kelp forest food webs. Ecosystems 7:341–357

    Article  Google Scholar 

  • Griffin S, Spathias H, Moore T, Baums I, Griffin B (2012) Scaling up Acropora nurseries in the Caribbean and improving techniques, Cairns, Australia edn. James Cook University, Townsville, Queensland 4811, Australia

  • Griffin JN, Schrack EC, Lewis K, Baums IB, Soomdat N, Silliman BR (2015a) Density-dependent effects on initial growth of a branching coral under restoration. Restor Ecol 23:197–200

    Article  Google Scholar 

  • Griffin S, Nemeth M, Moore T, Gintert B (2015b) Restoration using Acropora cervicornis at the T/V MARGARA grounding site. Coral Reefs 34:885. doi:10.1007/s00338-015-1310-2

    Article  Google Scholar 

  • Halpern BS, Walbridge S, Selkoe KA, Kappel CV, Micheli F, D’Agrosa C, Bruno JF, Casey KS, Ebert C, Fox HE, Fujita R, Heinemann D, Lenihan HS, Madin EM, Perry MT, Selig ER, Spalding M, Steneck R, Watson R (2008) A global map of human impact on marine ecosystems. Science 319:948–952. doi:10.1126/science.1149345

    Article  CAS  PubMed  Google Scholar 

  • Heck K, Able K, Roman C, Fahay M (1995) Composition, abundance, biomass, and production of macrofauna in a New England estuary: comparisons among eelgrass meadows and other nursery habitats. Estuar Coast 18:379–389

    Article  Google Scholar 

  • Herzlieb S, Kadison E, Blondeau J, Nemeth RS (2006) Comparative assessment of coral reef systems located along the insular platform south of St. Thomas, US Virgin Islands and the relative effects of natural and human impacts. Proceedings of 10th International Coral Reef Conference 4:1144–1151

  • Huntington BE, Miller MW (2014) Location-specific metrics for rapidly estimating the abundance and condition of the threatened coral Acropora cervicornis. Restor Ecol 22:299–303

    Article  Google Scholar 

  • Idjadi J, Edmunds P (2006) Scleractinian corals as facilitators for other invertebrates on a Caribbean reef. Mar Ecol Prog Ser 319:117–127

    Article  Google Scholar 

  • Jaap W (1998) Boom-bust cycles in Acropora. Reef Encounter 23:12–13

    Google Scholar 

  • Jackson JBC (2001) What was natural in the coastal oceans? Proc Natl Acad Sci 98:5411–5418. doi:10.1073/pnas.091092898

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnston L, Miller M (2014) Negative indirect effects of neighbors on imperiled scleractinian corals. Coral Reefs 33:1047–1056

    Article  Google Scholar 

  • Knowlton N, Lang JC, Keller BD (1990) Case study of natural population collapse: post-hurricane predation on Jamaican staghorn corals. Smithson Contrib Mar Sci 31:1–36

    Article  Google Scholar 

  • Lenihan HS, Peterson CH (1998) How habitat degradation through fishery disturbance enhances impacts of hypoxia on oyster reefs. Ecol Appl 8:128–140

    Article  Google Scholar 

  • Lidz BH, Zawada DG (2013) Possible return of Acropora cervicornis at Pulaski Shoal, Dry Tortugas National Park, Florida. J Coast Res 29:256–271

    Article  Google Scholar 

  • Lirman D (1999) Reef fish communities associated with Acropora palmata: relationships to benthic attributes. Bull Mar Sci 65:235–252

    Google Scholar 

  • McClanahan T, Muthiga N, Kamukuru A, Machano H, Kiambo R (1999) The effects of marine parks and fishing on coral reefs of northern Tanzania. Biol Conserv 89:161–182

    Article  Google Scholar 

  • Meyer JL, Schultz ET (1985) Tissue condition and growth rate of corals associated with schooling fish. Limnol Oceanogr 30:157–166

    Article  Google Scholar 

  • Meyer JL, Schultz ET, Helfman GS (1983) Fish schools: an asset to corals. Science 220:1047–1049

    Article  CAS  PubMed  Google Scholar 

  • Miller M, Huntington B (2015) Coral, Fish and other data to inform staghorn coral recovery in the Caribbean Sea from 2012-04-05 to 2014-07-28 (NCEI accession 0127933). Version 1.1. NOAA National Centers for Environmental Information. Dataset

  • Miller RJ, Adams AJ, Ebersole JP, Ruiz E (2007) Evidence for positive density-dependent effects in recovering Diadema antillarum populations. J Exp Mar Biol Ecol 349:215–222

    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. doi:10.1016/j.tree.2008.06.011

    Article  PubMed  Google Scholar 

  • Mumby PJ, Harborne AR, Williams J, Kappel CV, Brumbaugh DR, Micheli F, Holmes KE, Dahlgren CP, Paris CB, Blackwell PG (2007) Trophic cascade facilitates coral recruitment in a marine reserve. Proc Natl Acad Sci USA 104:8362–8367. doi:10.1073/pnas.0702602104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Munday PL (2004) Habitat loss, resource specialization, and extinction on coral reefs. Global Change Biol 10:1642–1647

    Article  Google Scholar 

  • National Marine Fisheries Service (2015) Recovery plan for elkhorn (Acropora palmata) and staghorn (Acropora cervicornis) corals. Prepared by the Acropora Recovery Team for the National Marine Fisheries Service, Silver Spring, MD

  • Padilla FM, Pugnaire FI (2006) The role of nurse plants in the restoration of degraded environments. Front Ecol Environ 4:196–202

    Article  Google Scholar 

  • Perry CT, Steneck RS, Murphy GN, Kench PD, Edinger EN, Smithers SG, Mumby PJ (2015) Regional-scale dominance of non-framework building corals on Caribbean reefs affects carbonate production and future reef growth. Glob Change Biol 21:1153–1164

    Article  Google Scholar 

  • Riegl B, Purkis S, Keck J, Rowlands G (2009) Monitored and modeled coral population dynamics and the refuge concept. Mar Pollut Bull 58:24–38

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Rogers A, Blanchard JL, Mumby PJ (2014) Vulnerability of coral reef fisheries to a loss of structural complexity. Curr Biol 24:1000–1005

    Article  CAS  PubMed  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. doi:10.1371/journal.pone.0001548

    Google Scholar 

  • Schutte VGW, Selig ER, Bruno JF (2010) Regional spatio-temporal trends in Caribbean coral reef benthic communities. Mar Ecol Prog Ser 402:115–122

    Article  Google Scholar 

  • Shantz AA, Ladd MC, Schrack E, Burkepile DE (2015) Fish-derived nutrient hotspots shape coral reef benthic communities. Ecol Appl 25:2142–2152

    Article  PubMed  Google Scholar 

  • Shima JS, Osenberg CW, St. Mary CM (2008) Quantifying site quality in a heterogeneous landscape: recruitment of a reef fish. Ecology 89:86–94. doi:10.1890/07-0021.1

    Article  PubMed  Google Scholar 

  • Shinn EA (1966) Coral growth-rate, an environmental indicator. J Paleontol 40:233–240

    Google Scholar 

  • Silliman BR, Schrack E, He Q, Cope R, Santoni A, van der Heide T, Jacobi R, Jacobi M, van de Koppel J (2015) Facilitation shifts paradigms and can amplify coastal restoration efforts. Proc Natl Acad Sci USA 112:14295–14300. doi:10.1073/pnas.1515297112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stimson J (1997) The annual cycle of density of zooxanthellae in the tissues of field and laboratory-held Pocillopora damicornis (linnaeus). J Exp Mar Biol Ecol 214:35–48

    Article  Google Scholar 

  • Veal C, Carmi M, Fine M, Hoegh-Guldberg O (2010) Increasing the accuracy of surface area estimation using single wax dipping of coral fragments. Coral Reefs 29:893–897

    Article  Google Scholar 

  • Walker BK, Larson E, Moulding AL, Gilliam DS (2012) Small-scale mapping of indeterminate arborescent acroporid coral (Acropora cervicornis) patches. Coral Reefs 31:885–894

    Article  Google Scholar 

  • Young C, Schopmeyer S, Lirman D (2012) A review of reef restoration and coral propagation using the threatened genus Acropora in the Caribbean and western Atlantic. Bull Mar Sci 88:1075–1098

    Article  Google Scholar 

Download references

Acknowledgements

Funding for this project was provided by the National Oceanic and Atmospheric Administration (NOAA) Coral Reef Conservation Program and the National Marine Fisheries Service Southeast Regional Office. Logistical support was provided by the National Park Service (T. Ziegler, T. Gottshall, and K. Nimmo), The Nature Conservancy (K. Amon-Lewis and C. Clade), and the NOAA Restoration Center (T. Moore and S. Griffin). Sampling was conducted under permits DRTO-2014-SCI-0005 from the National Park Service, STX026-12 from the US Virgin Islands Division of Fish and Wildlife, and SAL-14-1546-SRP from the Florida Fish and Wildlife Conservation Commission. Field assistance from A. Bright, C. Cameron, M. Ladd, K. Ondrasik, and C. Vilmar is gratefully acknowledged. This manuscript was greatly improved by the constructive comments of two anonymous reviewers and Dr. Stuart Sandin, handling editor.

Author contribution statement

BH and MM conceived and designed the monitoring study and experiments. All authors contributed to completing field surveys and experiments. LR and RP processed experiments in the laboratory. BH analyzed the data and led authorship of the manuscript; other authors provided substantial editorial advice during multiple manuscript revisions.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Brittany E. Huntington.

Ethics declarations

Funding

Funding for this project was provided by the NOAA Coral Reef Conservation Program (CRCP Project ID 819), the National Marine Fisheries Service Southeast Regional Office, and a National Research Council Postdoctoral Research Fellowship (Huntington).

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Stuart Sandin.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 1206 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Huntington, B.E., Miller, M.W., Pausch, R. et al. Facilitation in Caribbean coral reefs: high densities of staghorn coral foster greater coral condition and reef fish composition. Oecologia 184, 247–257 (2017). https://doi.org/10.1007/s00442-017-3859-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-017-3859-7

Keywords

Navigation