SpringerLink
Log in

Indicator Framework for Monitoring Ecosystem Integrity of Coral Reefs in the Western Caribbean

  • Review
  • Published:
Ocean Science Journal Aims and scope Submit manuscript

Abstract

Ecosystem monitoring is a key priority for evaluating ecosystem conditions, but high costs, especially with regard to marine ecosystems, hamper its large-scale implementation. Despite a wide range of monitoring programs for tropical coral reefs, it has not been possible to establish a minimum set of the most relevant metrics. This leads to heterogeneous methods, the collection of different metrics that are difficult to compare and lengthy, time- and money-consuming surveys. In the present study, we use ecosystem integrity as an underlying conceptual framework to establish a minimum set of metrics for evaluating the ecosystem condition of Caribbean coral reefs. We reviewed ten existing monitoring protocols for their conceptual framework, metrics used, their reference ranges and sampling methods and documented the ecological relevance of indicators, as reported in the literature. Of the 64 in situ metrics, 15 with high ecological relevance were selected as a minimum set, covering aspects of composition (Hill numbers for corals and fish), structure (coral, red algae, macroalgae and filamentous algae cover, topographic complexity, and habitat extent) and function (recruit density, disease and bleaching incidence, fish biomass, and filamentous and macroalgae height) of coral reefs across a range of ecological scales. Besides the lack of underlying conceptual frameworks and reference levels for specific regions in existing monitoring protocols, landscape scale and connectivity metrics are also missing, producing negative impacts on indicator interpretation. The presented indicator framework constitutes a valuable guideline, as it documents the most relevant metrics for ecosystem condition, considering composition, structure, and function.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Canada)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Álvarez-Filip L, Dulvy KN, Coté M, Gill AJ, Watkinson AR (2009) Flattening of caribbean coral reefs: region-wide declines in architectural complexity. Proc R Soc B 276:3019–3025. https://doi.org/10.1098/rspb.2009.0339

    Article  Google Scholar 

  • Álvarez-Filip L, Dulvy KN, Coté M, Watkinson AR, Gill AJ (2011) Coral identity underpins architectural complexity on Caribbean reefs. Ecol Appl 21(6):2223–2231. https://doi.org/10.1890/10-1563.1

    Article  Google Scholar 

  • Bak RP, Meesters EH (1998) Coral population structure: the hidden information of colony size-frequency distributions. Mar Ecol Prog Ser 162:301–306. https://doi.org/10.3354/meps162301

    Article  Google Scholar 

  • Barranco LM, Carriquiry JD, Rodríguez-Zaragoza FA, Cupul-Magaña L, Villaescusa JA, Calderón-Aguilera LE (2016) Spatiotemporal variations of live coral cover in the northern Mesoamerican Reef System Yucatan Peninsula, Mexico. Sci Mar 80(2):143–150. https://doi.org/10.3989/scimar.04294.23A

    Article  Google Scholar 

  • Bodmer M, Rogers A, Speight M, Lubbock N, Exton D (2015) Using an isolated population boom to explore barriers to recovery in the keystone Caribbean coral reef herbivore Diadema antillarum. Coral Reefs 34(4):1011–1021. https://doi.org/10.1007/s00338-015-1329-4

    Article  Google Scholar 

  • Brokovich E, Baranes A, Goren M (2006) Habitat structure determines coral reef fish assemblages at the northern tip of the Red Sea. Ecol Indic 6:494–507. https://doi.org/10.1016/j.ecolind.2005.07.002

    Article  Google Scholar 

  • Brown E, Williams B (2016) Ecological integrity assessment as a metric of biodiversity: are we measuring what we are? Biodivers Conserv 25:1011–1035. https://doi.org/10.1007/s10531-016-1111-0

    Article  Google Scholar 

  • Bubb P, Almond R, Kapos V, Stanwell-Smith D, Jenkins M (2010) Guidance for national biodiversity indicator development and use. UNEP-WCMC, Cambridge, p 120

    Google Scholar 

  • Castro NG (2001) Monitoring ecological and socioeconomic indicators for coral reef management in Colombia. Bull Mar Sci 69(2):847–859

    Google Scholar 

  • Cooper TF, Gilmour JP, Fabricius KE (2009) Bioindicators of changes in water quality on coral reefs: review and recommendations for monitoring programmes. Coral Reefs 28:589–606. https://doi.org/10.1007/s00338-009-0512-x

    Article  Google Scholar 

  • Cortés J, Oxenford HA, Tussenbroek BI, Jordán-Dahlgren E, Cróquer A, Bastidas C, Ogden JC (2019) The CARICOMP network of caribbean marine laboratories (1985–2007): history, key findings, and lessons learned. Front Mar Sci 5:519. https://doi.org/10.3389/fmars.2018.00519

    Article  Google Scholar 

  • Dale VH, Beyeler SC (2001) Challenges in the development and use of ecological indicators. Ecol Indic 1(1):3–10. https://doi.org/10.1016/S1470-160X(01)00003-6

    Article  Google Scholar 

  • Dale VH, Polasky S (2007) Measures of the effects of agricultural practices on ecosystem services. Ecol Econ 64(2):286–296. https://doi.org/10.1016/j.ecolecon.2007.05.009

    Article  Google Scholar 

  • De Leo GA, Levin S (1997) The multifaceted aspects of ecosystem integrity. Conserv Ecol 1(1):3

    Google Scholar 

  • Díaz-Pérez L, Rodríguez-Zaragoza FA, Ortiz M, Cupul-Magaña AL, Carriquiry JD, Ríos-Jara E, Del Carmen G-R (2016) Coral reef health indices versus the biological, ecological and functional diversity of fish and coral assemblages in the Caribbean sea. PLoS One 11(8):1–20. https://doi.org/10.1371/journal.pone.0161812

    Article  Google Scholar 

  • Done TJ (1997) Decadal changes in reef-building communities: implications for reef growth and monitoring programs. In: Lessios HA, Macintyre IG (eds) Proceedings of the 8th International Coral Reef Symposium. Smithsonian Tropical Research Institute, Panama, pp 411–416

  • Downs C, Woodley C, Richmond L, Lanning L, Owen R (2005) Shifting the paradigm of coral-reef health assessment. Mar Poll Bull 51(5–7):486–494. https://doi.org/10.1371/journal.pone.0161812

    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. https://doi.org/10.1073/pnas.071524598

    Article  Google Scholar 

  • Enríquez S, Pantoja-Reyes NI (2005) Form-function analysis of the effect of canopy morphology on leaf self-shading in the seagrass Thalassia testudinum. Oecologia 145:235–243. https://doi.org/10.1007/s00442-005-0111-7

    Article  Google Scholar 

  • Equihua M, Aldama ME, Gershenson C, López-Corona O, Munguía M, Pérez-Maqueo O, Ramírez-Carrillo E (2020) Ecosystem antifragility: beyond integrity and resilience. PeerJ 8:e8533. https://doi.org/10.7717/peerj.8533

    Article  Google Scholar 

  • Equihua M, García N, Pérez O, Benítez G, Kolb M, Shcmidt M, Equihua J, Álvarez-Palacios J (2014) Integridad ecológica como indicador de la calidad ambiental. In: González CA, Vallarino A, Pérez JC, Low AM (eds) Bioindicadores: guardianes de nuestro futuro ambiental. Capítulo 33 El Colegio de la Frontera Sur, Instituto Nacional de Ecología y Cambio Climático, pp 687–710

  • Equihua M, Benítez G, Pérez M, Hernández H, García A, Equihua J, Maeda P, Kolb M, Schmidt M (2015) Integridad ecológica para la gestión de la sustentabilidad ambiental frente al cambio climático. In: Yañez A (ed) Cambio, Climático: Adaptación y Mitigación hacia Agenda Siglo XXI AGT Editorial S.A., México DF, pp 75–88

  • Faber-Langendoen D, Hedge C, Kost M, Thomas S, Smart L, Smyth R, Drake J, Menard S (2012) Assessment of wetland ecosystem condition across landscape regions: a multi-metric approach. Part A. Ecological integrity assessment overview and field study in Michigan and Indiana. U.S. Environmental Protection Agency report EPA/600/R-12/021a, Washington DC, p 30

  • Faber-Langendoen D, Nichols W, Rocchio J, Walz K, Lemly J (2016) An Introduction to NatureServe’s Ecological Integrity Assessment Method. NatureServe, Arlington, p 33

  • Fabricius KE (2005) Effects of terrestrial runoff on the ecology of corals and coral reefs: review and synthesis. Mar Poll Bull 50(2):125–146. https://doi.org/10.1016/j.marpolbul.2004.11.028

    Article  Google Scholar 

  • Fabricius KE, Cooper TF, Humphrey C, Uthicke S, De’ath G, Davidson J, LeGrand H, Thompson A, Schaffelke B (2012) A bioindicator system for water quality on inshore coral reefs of the Great Barrier Reef. Mar Poll Bull 65:320–332. https://doi.org/10.1016/j.marpolbul.2011.09.004

    Article  Google Scholar 

  • Ferrari R, Bryson M, Bridge T, Hustache J, Williams SB, Byrne M, Figueroa W (2016) Quantifying the response of structural complexity and community composition to environmental change in marine communities. Glob Change Biol 22:1965–1975. https://doi.org/10.1111/gcb.13197

    Article  Google Scholar 

  • Fisher WS, Fore LS, Hutchins A, Quarles RL, Campbell JG, LoBue C, Davis WS (2008) Evaluation of stony coral indicators for coral reef management. Mar Poll Bull 56(10):1737–1745. https://doi.org/10.1016/j.marpolbul.2008.07.002

    Article  Google Scholar 

  • Flower J, Ortiz J, Chollet I, Abdullah S, Castro-Sanguiano C, Hock K, Lam V, Mumby P (2017) Interpreting coral reef monitoring data: a guide for improved management decisions. Ecol Indic 72:848–869. https://doi.org/10.1016/j.ecolind.2016.09.003

    Article  Google Scholar 

  • Ford AK, McAndrews AERS, Mangubhai S, Nugues MM, Bejarano S, Moore BR, Rico C, Wild C, Ferse SCA (2018) Evaluation of coral reef management effectiveness using conventional versus resilience-based metrics. Ecol Indic 85:308–317. https://doi.org/10.1016/j.ecolind.2017.10.002

    Article  Google Scholar 

  • Garza-Pérez JR (2012) Evaluación de Comunidades Bentónicas Arrecifales: Guía de Campo y Laboratorio, 1a Edición, DGAPA-PAPIME, UNAM, p 22

  • Gonzáles-Vallejo NE (2011) Moluscos. In: Pozo C, Armijo Canto N, Calmé S (eds) Riqueza Biológica de Quintana Roo: Un análisis para su conservación, Tomo I. Chapter IV. Ecosur, pp 108–112

  • Graham N, Nash K (2013) The importance of structural complexity in coral reef ecosystems. Coral Reefs 32(2):315–326. https://doi.org/10.1007/s00338-012-0984-y

    Article  Google Scholar 

  • Hill J, Wilkinson C (2004) Methods for ecological monitoring of coral reefs. Australian Institute of Marine Science, Townsville, p 117. https://doi.org/10.1017/CBO9781107415324.004

  • Jameson S, Erdman M, Karr J, Potts K (2001) Charting a course toward diagnosis monitoring: a continuing review of coral reef attributes and a research strategy for creating coral reef indexes of biotic integrity. Bull Mar Sci 69(2):701–704

    Google Scholar 

  • Johnson D, Benn A, Ferreira A (2013) Review of ecosystem-based indicators and indices on the state of the Regional Seas. UNEP, p 118

  • Jordán-Dahlgren E, Rodríguez-Martínez R (2003) The Atlantic coral reefs of Mexico. In: Cortes J (ed) Latin American coral reefs. Elsevier Science, pp 131–157

    Chapter  Google Scholar 

  • Jost L (2006) Entropy and diversity. Oikos 113(2):363–375. https://doi.org/10.1111/j.2006.0030-1299.14714.x

    Article  Google Scholar 

  • Kandziora M, Burkhard B, Müller F (2013) Interactions of ecosystem properties, ecosystem integrity and ecosystem service indicators: a theoretical matrix exercise. Ecol Indic 28:54–78. https://doi.org/10.1016/j.ecolind.2012.09.006

    Article  Google Scholar 

  • Karr JR (1993) Defining and assessing ecological integrity: beyond water quality. Environ Toxicol Chem 12(9):1521–1531. https://doi.org/10.1002/etc.5620120902

    Article  Google Scholar 

  • Kay JJ (1991) A nonequilibrium thermodynamic framework for discussing ecosystem integrity. Environ Manage 15:483–495

    Article  Google Scholar 

  • Koff H, Zamora ME, Maganda C, Pérez-Maqueo O (2016) Ecosystem integrity and policy coherence for development: tools aimed at achieving balance as the basis for transformative development. Reg Cohes 6(3):77–92. https://doi.org/10.3167/reco.2016.060304

    Article  Google Scholar 

  • Kramer P, McField M, Álvarez-Filip L, Drysdale I, Rueda Flores M, Giró A, Pott R (2015) Reporte de la Salud Ecológica del Arrecife Mesoamericano 2015. Iniciativa Arrecifes Saludables

  • Lam VYY, Doropoulos C, Mumby PJ (2017) The influence of resilience-based management on coral reef monitoring: a systematic review. PLoS One 12:e0172064. https://doi.org/10.1371/journal.pone.0172064

    Article  Google Scholar 

  • Lang JC, Marks KW, Kramer PA, Richards P, Ginsburg RN (2010) AGRRA Protocols Version V4. Atlantic and Gulf Rapid Reef Assessment, p 31

  • Leveque C (2003) Ecology from ecosystem to biosphere. Science, Enfield, p 472

  • Lirman D, Formel N, Schopmeyer S, Ault JS, Smith SG, Gilliam D, Riegl B (2014) Percent recent mortality (PRM) of stony corals as an ecological indicator of coral reef condition. Ecol Indic 44:120–127. https://doi.org/10.1016/j.ecolind.2013.10.021

    Article  Google Scholar 

  • McClanahan TR, Donner SD, Maynard JA, MacNeil MA, Graham NJ, Maina J, van Woesik R (2012) Prioritizing key resilience indicators to support coral reef management in a changing climate. PLoS One 7(8):e42884. https://doi.org/10.1371/journal.pone.004288

    Article  Google Scholar 

  • McCook LJ, Almany GR, Berumen ML, Day JC, Green AL, Jones GP, Leis JM, Planes S, Russ GR, Sale PF, Thorrold SR (2009) Management under uncertainty: guide-lines for incorporating connectivity into the protection of coral reefs. Coral Reefs 28:353–366. https://doi.org/10.1007/s00338-008-0463-7

    Article  Google Scholar 

  • McField M, Kramer P (2007) Healthy Reefs for Healthy People: A Guide to Indicators of Reef Health and Social Well-being in the Mesoamerican Reef Region. Healthy Reefs Initiative, p 208

  • McField M, Kramer P, Petersen AG, Soto M, Drysdale I, Craig N, Flores MR (2020) 2020 Mesoamerican reef report card. Healthy Reefs Initiative, p 36

  • Moreno CE, Barragán F, Pineda E, Pavón P (2011) Reanálisis de la diversidad alfa: alternativas para interpretar y comparar información sobre comunidades ecológicas. Rev Mex Biodivers 82(4):1249–1261

    Google Scholar 

  • Morris JA (2012) Invasive Lionfish: A Guide to Control and Management. Gulf and Caribbean Fisheries. Institute Special Publication Series Number 1, Gulf and Caribbean Fisheries Institute, Marathon, p 113

  • Mumby PJ, Hastings A, Edwards HJ (2007) Thresholds and the resilience of Caribbean coral reefs. Nature 450:98–101. https://doi.org/10.1038/nature06252

    Article  Google Scholar 

  • Mumby P, Flower J, Chollett I, Box S, Bozec Y, Fitzsimmons C, Forster J, Gill D, Griffh-Mumby R, Oxenford H, Peterson A, Stead S, Turner R, Townsley P, van Beukering P, Booker F, Brocke H, Cabañillas-Terán N, Canty S, Carricart-Ganivet J, Charlery J, Dryden C, van Duyl F, Enríquez S, Haan J, Iglesias-Prieto R, Kennedy E, Mahon R, Mueller B, Newman S, Nugues M, Núñez J, Nurse L, Osinga R, Paris C, Petersen D, Polunin N, Sánchez C, Schep S, Stevens J, Vallès H, Vermeij M, Visser P, Whittingham E, Williams S (2014) Hacia la resiliencia del arrecife y medios de vida sustentables: un manual para los administradores de arrecifes de coral del Caribe. University of Exeter, Exeter, p 172

    Google Scholar 

  • Nughes MM, Roberts CM (2003) Partial mortality in massive reef corals as an indicator of sediment stress on coral reefs. Mar Poll Bull 46:314–323. https://doi.org/10.1016/S0025-326X(02)00402-2

    Article  Google Scholar 

  • Obura DO, Grimsdith G (2009) Resielience Assessment of coral reefs. Assessment protocol for coral reefs, focusing on coral bleaching and thermal stress. IUCN, Gland, p 70

  • Parrish JD, Braun DP, Unnasch RS (2003) Are we conserving what we say we are? Measuring ecological integrity within protected areas. Bioscience 53(9):851–860. https://doi.org/10.1641/0006-3568(2003)053[0851:AWCWWS]2.0.CO;2

    Article  Google Scholar 

  • Pereira HM, Ferrier S, Walters M, Geller GN, Jongman RHG, Scholes RJ, Bruford MW, Brummitt N, Butchart SHM, Cardoso AC, Coops NC, Dulloo E, Faith DP, Freyhof J, Gregory RD, Heip C, Höft R, Hurtt G, Jetz W, Karp DS, McGeoch MA, Obura D, Onoda Y, Pettorelli N, Reyers B, Sayre R, Scharlemann JPW, Stuart SN, Turak E, Walpole M, Wegmann M (2013) Essential biodiversity variables. Science 339(6117):277–278. https://doi.org/10.1126/science.1229931

    Article  Google Scholar 

  • Perera-Valderrama S, Cerdeira-Estrada S, Martell-Dubois R, Rosique-de la Cruz LO, Caballero-Aragón H, Ressl R (2020) Protocolos de monitoreo de la biodiversidad marina en áreas naturales protegidas del Caribe mexicano. Conabio, México, p 162

  • Perry C, Edinger E, Kench P, Murphy G, Smithers S, Steneck R, Mumby P (2012) Estimating rates of biologically driven coral reef framework production and erosion: a new census-based carbonate budget methodology and applications to the reefs of Bonaire. Coral Reefs 31(3):853–868. https://doi.org/10.1007/s00338-012-0901-4

    Article  Google Scholar 

  • Raymundo LJ, Couch SC, Harwell (2008) A coral disease handbook: guidelines for assessment, monitoring and management. Currie Communications, Melbourne, p 124

  • Ritson-Williams R, Arnold S, Fogarty N, Steneck RS, Vermeij M, Paul VJ (2009) New perspectives on ecological mechanisms affecting coral recruitment on reefs. Smithson Contrib Mar Sci 38:437–457. https://doi.org/10.5479/si.01960768.38.437

    Article  Google Scholar 

  • Rodríguez-Martínez RE, Jordán-Garza AG, Baker DM, Jordán-Dahlgren E (2012) Competitive interactions between corals and Trididemnum solidum on Mexican Caribbean reefs. Coral Reefs 31:571–577. https://doi.org/10.1007/s00338-011-0871-y

    Article  Google Scholar 

  • Santavy DL, Summers JK, Engle VD, Harwell LC (2005) The condition of coral reefs in South Florida (2000) using coral disease and bleaching as indicators. Environ Monit Asses 100(1–3):129–152. https://doi.org/10.1007/s10661-005-4767-6

    Article  Google Scholar 

  • Sosa-Cordero E, Ramírez-González A (2011) Pesca marina. In: Pozo C, Canto NA, Calmé S (eds) Riqueza Biológica de Quintana Roo. Un análisis para su conservación, Capítulo 3. El Colegio de la Frontera Sur (ECOSUR), Comisión Nacional para el Conocimiento y Uso de la Biodiversidad (CONABIO), Gobierno del Estado de Quintana Roo y Programa de Pequeñas Donaciones (PPD). México, pp 183–189

  • Spalding MD, Fox HE, Allen GR, Davidson N, Ferdaña ZA, Finlayson M, Halpern S, Jorge MA, Lombana A, Lourie SA, Martin KD, McManus E, Molnar J, Recchia CA, Robertson J (2007) Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. Bioscience 57(7):573–583. https://doi.org/10.1641/B570707

    Article  Google Scholar 

  • Steneck RS, Dethier MN (1994) A Functional group approach to the structure of algal-dominated communities. Oikos 69(3):476–498. https://doi.org/10.2307/3545860

    Article  Google Scholar 

  • Suter G (1993) A critique to ecosystem health concepts and indexes. Environ Toxicol Chem 12:1533–1539. https://doi.org/10.1002/etc.5620120903

    Article  Google Scholar 

  • Tierney GL, Faber-Langendoen D, Mitchell BR, Shriver WG, Gibbs JP (2009) Monitoring and evaluating the ecological integrity of forest ecosystems. Front Ecol Environ 7(6):308–316. https://doi.org/10.1890/070176

    Article  Google Scholar 

  • Vega-Thurber RL, Burkepile DE, Fuchs C, Shantz AA, Mcminds R, Zaneveld JR (2014) Chronic nutrient enrichment increases prevalence and severity of coral disease and bleaching. Glob Change Biol 20:544–554. https://doi.org/10.1111/gcb.12450

    Article  Google Scholar 

  • Weil E, Jordán-Dahlgren E, Bruckner A, Raymundo L (2008) Assessment and Monitoring Protocols. In: Raymundo LJ, Couch CS, Harwell CD (eds) A Coral Disease Handbook: Guidelines for Assessment, Monitoring and Management. CRTR Program, pp 47–64

  • Work T, Woodley C, Raymundo L (2008) Confirming Field Assessments and Measuring Disease Impacts. In: Raymundo LJ, Couch CS, Harwell CD (eds) A Coral Disease Handbook: Guidelines for Assessment, Monitoring and Management. CRTR Program, pp 34–46

Download references

Acknowledgements

We would like to thank Ricardo Cruz-Cano for his support in proof reading the article.

Funding

This research was supported by Instituto de Ecología, Universidad Nacional Autónoma de México.

Author information

Authors and Affiliations

  1. Institute of Geography, National Autonomous University of Mexico, Mexico City, 04510, Mexico

    Diana Margarita Carrillo-García & Melanie Kolb

Authors
  1. Diana Margarita Carrillo-García
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Melanie Kolb
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Melanie Kolb.

Additional information

Publisher's Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Carrillo-García, D.M., Kolb, M. Indicator Framework for Monitoring Ecosystem Integrity of Coral Reefs in the Western Caribbean. Ocean Sci. J. 57, 1–24 (2022). https://doi.org/10.1007/s12601-022-00055-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12601-022-00055-1

Keywords

Search

Navigation