Coral Reefs

, Volume 37, Issue 1, pp 105–120 | Cite as

Multiscale change in reef coral species diversity and composition in the Tropical Eastern Pacific

  • Catalina G. GomezEmail author
  • Andrew Gonzalez
  • Hector M. Guzman


Both natural and anthropogenic factors are changing coral-reef structure and function worldwide. Long-term monitoring has revealed declines in the local composition and species diversity of reefs. Here we report changes in coral-reef community structure over 12 yr (2000–2012) at 17 sites and three spatial scales (reef, gulf and country) in the Tropical Eastern Pacific (Panama). We found a significant 4% annual decline in species population sizes at the country and gulf scales, with significant declines ranging from 3 to 32% at all but one reef. No significant temporal change in expected richness was found at the country scale or in the Gulf of Chiriquí, but a 7% annual decline in expected species richness was found in the Gulf of Panama. There was a 2% increase in community evenness in the Gulf of Chiriquí, but no change in the Gulf of Panama. Significant temporal turnover was found at the country and gulf scales and at 29% of the reefs, a finding mostly explained by changes in species abundance, and losses and gains of rare species. Temporal trends in alpha and beta diversity metrics were explained by water temperature maxima, anomalies and variation that occurred even in the absence of a strong El Niño warming event.


Coral reef Panama Tropical Eastern Pacific Alpha diversity Turnover Biodiversity 



The authors thank Carlos Guevara, Marcela Herrera, Jorge Morales, Carlos Vega, Aldo Croquer and Carlos Sanhil for assistance in the field. The Nature Conservancy and the Environmental Science Program of the Smithsonian Tropical Research Institute sponsored the monitoring project to HMG. Thanks to the Government of Panama for financial support to CG during data analysis and manuscript preparation (IFARHU-SENACYT) and to the Panamanian Ministry of Environment for providing the permits to work in protected areas. AG acknowledges the support of the Canada Research Chair program, a Killam Fellowship and an NSERC Discovery grant. AG and CG acknowledge the support of the Québec Centre for Biodiversity Science.

Supplementary material

338_2017_1637_MOESM1_ESM.eps (1.8 mb)
Supplementary material 1 (EPS 1794 kb)
338_2017_1637_MOESM2_ESM.eps (1.3 mb)
Supplementary material 2 (EPS 1381 kb)
338_2017_1637_MOESM3_ESM.docx (13 kb)
Supplementary material 3 (DOCX 13 kb)
338_2017_1637_MOESM4_ESM.eps (1.3 mb)
Supplementary material 4 (EPS 1352 kb)


  1. Alvarado JJ, Aburto-Oropeza O, Abad R, Barraza E, Brandt M, Cantera J, Estrada P, Gaymer CF, Guzmán-Mora AG, Herlan JJ, Maté JL (2017) Coral reef conservation in the Eastern Tropical Pacific. In: Glynn PW, Manzello DP, Enoch AC (eds) Coral reefs of the Eastern Tropical Pacific. Springer, Dordrecht, pp 203–250Google Scholar
  2. Alvarez-Filip L, Carricart-Ganivet JP, Horta-Puga G, Iglesias-Prieto R (2013) Shifts in coral-assemblage composition do not ensure persistence of reef functionality. Sci Rep 3:3486CrossRefPubMedPubMedCentralGoogle Scholar
  3. Bellwood DR, Hughes TP, Folke C, Nyström M (2004) Confronting the coral reef crisis. Nature 429:827–833CrossRefPubMedGoogle Scholar
  4. Benzoni F, Stefani F, Pichon M, Galli P (2010) The name game: morpho-molecular species boundaries in the genus Psammocora (Cnidaria, Scleractinia). Zool J Linn Soc 160:421–456CrossRefGoogle Scholar
  5. Bruno JF, Selig ER (2007) Regional decline of coral cover in the Indo-Pacific: timing, extent, and subregional comparisons. PLoS ONE 8:e711CrossRefGoogle Scholar
  6. Cai W, Borlace S, Lengaigne M, Rensch Van, Collins M, Vecchi G, Timmermann A, Santoso A, McPhaden MJ, Wu L, England MH, Wang G, Guilyardi E, Jin FF (2014) Increasing frequency of extreme El Niño events due to greenhouse warming. Nat Clim Chang 4:111–116CrossRefGoogle Scholar
  7. Carpenter KE, Abrar M, Aeby G, Aronson RB, Banks S, Bruckner A, Chiriboga A, Cortes J, Delbeek JC, DeVantier L, Edgar GJ, Edwards AJ, Fenner D, Guzman HM, Hoeksema BW, Hodson G, Johan O, Licuanan WY, Livingston 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 321:560–563CrossRefPubMedGoogle Scholar
  8. Chao A (1987) Estimating the population size for capture-recapture data with unequal catchability. Biometrics 43:783–791CrossRefPubMedGoogle Scholar
  9. Combosch DJ, Vollmer SV (2015) Trans-Pacific RAD-Seq population genomics confirms introgressive hybridization in Eastern Pacific Pocillopora corals. Mol Phylogenet Evol 88:154–162CrossRefPubMedGoogle Scholar
  10. Cortés J, Reyes-Bonilla H (2017) Human influences on Eastern Tropical Pacific coral communities and coral reefs. In: Glynn PW, Manzello DP, Enoch AC (eds) Coral reefs of the Eastern Tropical Pacific. Springer, Dordrecht, pp 203–250CrossRefGoogle Scholar
  11. Cortés J, Enochs IC, Sibaja-Cordero J, Hernández L, Alvarado JJ, Breedy O, Cruz-Barraza JA, Esquivel-Garrote O, Fernández-García C, Hermosillo A, Kaiser KL, Medina-Rosas P, Morales-Ramírez A, Pacheco C, Pérez-Matus A, Reyes-Bonilla H, Riosmena-Rodríguez R, Sánchez-Noguera C, Wieters EA, Zapata FA (2017) Marine biodiversity of Eastern Tropical Pacific coral reefs. In: Glynn PW, Manzello DP, Enoch AC (eds) Coral reefs of the Eastern Tropical Pacific. Springer, Dordrecht, pp 203–250CrossRefGoogle Scholar
  12. D’Croz L, O’Dea A (2007) Variability in upwelling along the Pacific shelf of Panama and implications for the distribution of nutrients and chlorophyll. Estuar Coast Shelf Sci 73:325–340CrossRefGoogle Scholar
  13. 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 USA 109:17995–17999CrossRefPubMedPubMedCentralGoogle Scholar
  14. Dornelas M, Gotelli NJ, McGill B, Shimadzu H, Moyes F, Sievers C, Magurran AE (2014) Assemblage time series reveal biodiversity change but not systematic loss. Science 344:296–299CrossRefPubMedGoogle Scholar
  15. Elahi R, O’Connor MI, Byrnes JE, Dunic J, Eriksson BK, Hensel MJ, Kearns PJ (2015) Recent trends in local-scale marine biodiversity reflect community structure and human impacts. Curr Biol 25:1938–1943CrossRefPubMedGoogle Scholar
  16. Fiedler PC, Lavín MF (2017) Oceanographic conditions of the Eastern Tropical Pacific. In: Glynn PW, Manzello DP, Enoch AC (eds) Coral reefs of the Eastern Tropical Pacific. Springer, Dordrecht, pp 59–84CrossRefGoogle Scholar
  17. Francini-Filho RB, Moura RL, Thompson FL, Reis RM, Kaufman L, Kikuchi RK, Leão ZM (2008) Diseases leading to accelerated decline of reef corals in the largest South Atlantic reef complex (Abrolhos Bank, eastern Brazil). Mar Pollut Bull 56:1008–1014CrossRefPubMedGoogle Scholar
  18. Gardner TA, Côté IM, Gill JA, Grant A, Watkinson AR (2003) Long-term region-wide declines in Caribbean corals. Science 301:958–960CrossRefPubMedGoogle Scholar
  19. Glynn PW (1990) Coral mortality and disturbances to coral reefs in the Tropical Eastern Pacific. In: Glynn PW (ed) Global ecological consequences of the 1982–1983 El Niño-Southern Oscillation. Elsevier, Amsterdam, pp 141–182Google Scholar
  20. Glynn PW, Macintyre IG (1977) Growth rate and age of coral reefs on the Pacific coast of Panama. In: Proceedings 3rd international coral reef symposium, vol 2, pp 251–259Google Scholar
  21. Glynn PW, D’Croz L (1990) Experimental evidence for high temperature stress as the cause of El Niño-coincident coral mortality. Coral Reefs 8:181–191CrossRefGoogle Scholar
  22. Glynn PW, Maté JL, Stemann TA (2001a) Pavona chiriquiensis, a new species of zooxanthellate scleractinian coral (Cnidaria: Anthozoa: Agariciidae) from the Eastern Tropical Pacific. Bull Biol Soc Wash 10:210–225Google Scholar
  23. Glynn PW, Maté JL, Baker AC, Calderón MO (2001b) Coral bleaching and mortality in Panama and Ecuador during the 1997–1998 El Niño-Southern Oscillation event: spatial/temporal patterns and comparisons with the 1982–1983 event. Bull Mar Sci 69:79–109Google Scholar
  24. Glynn PW, Mones AB, Podesta GP, Colbert A, Colgan MW (2017a) El Niño-Southern Oscillation: effects on Eastern Pacific coral reefs and associated biota. In: Glynn PW, Manzello DP, Enochs IC (eds) Coral reefs of the Eastern Tropical Pacific. Springer, Netherlands, pp 251–290CrossRefGoogle Scholar
  25. Glynn PW, Alvarado JJ, Banks S, Cortés J, Feingold JS, Jiménez C, Maragos JE, Martínez P, Maté JL, Moanga DA, Navarrete S, Reyes-Bonilla H, Riegl B, Rivera F, Vargas-Angel B, Wieters EA, Zapata FA (2017b) Eastern Pacific coral reef provinces, coral community structure and composition: an overview. In: Glynn PW, Manzello DP, Enochs IC (eds) Coral reefs of the Eastern Tropical Pacific. Springer, Dordrecht, pp 107–176CrossRefGoogle Scholar
  26. Gonzalez A, Cardinale BJ, Allington GR, Byrnes J, Endsley KA, Brown DG, Hooper DU, Isbell F, O’Connor MI, Loreau M (2016) Estimating local biodiversity change: a critique of papers claiming no net loss of local diversity. Ecology 97:1949–1960CrossRefPubMedGoogle Scholar
  27. Graham NA, Cinner JE, Norström AV, Nyström M (2014) Coral reefs as novel ecosystems: embracing new futures. Curr Opin Environ Sustain 7:9–14CrossRefGoogle Scholar
  28. Graham NA, Bellwood DR, Cinner JE, Hughes TP, Norström AV, Nyström M (2013) Managing resilience to reverse phase shifts in coral reefs. Front Ecol Environ 11:541–548CrossRefGoogle Scholar
  29. Guzman HM, Holst I (1994) Inventario biológico y estado actual de los arrecifes coralinos a ambos lados del Canal de Panamá. Rev Biol Trop 42:493–514Google Scholar
  30. Guzman HM, Cortés J (2007) Reef recovery 20 years after the 1982–1983 El Niño massive mortality. Mar Biol 151:401–411CrossRefGoogle Scholar
  31. Guzman HM, Robertson DR, Díaz ML (1991) Distribución y abundancia de corales en el arrecife del Refugio de Isla Iguana, Pacífico de Panamá. Rev Biol Trop 39:225–231Google Scholar
  32. Guzman HM, Guevara CA, Breedy O (2004) Distribution, diversity, and conservation of coral reefs and coral communities in the largest marine protected area of Pacific Panama (Coiba Island). Environ Conserv J 31:111–121CrossRefGoogle Scholar
  33. Guzman HM, Benfield S, Breedy O, Mair JM (2008) Broadening reef conservation across the Tropical Eastern Pacific seascape: distribution and diversity of reefs in Las Perlas Archipelago, Panama. Environ Conserv J 35:1–9Google Scholar
  34. Harrell FE, Dupont C Jr, (2015) Hmisc: Harrell miscellaneous. R package version 3.17-0.
  35. Hill MO (1973) Diversity and evenness: a unifying notation and its consequences. Ecology 54:427–432CrossRefGoogle Scholar
  36. Hobbs RJ, Arico S, Aronson J, Baron JS, Bridgewater P, Cramer VA, Epstein PR, Ewel JJ, Klink CA, Lugo AE, Norton D, Ojima D, Richardson DM, Sanderson EW, Valladares F, Vilá M, Zomora R, Zobel M (2006) Novel ecosystems: theoretical and management aspects of the new ecological world order. Glob Ecol Biogeogr 15:1–7CrossRefGoogle Scholar
  37. Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–866CrossRefGoogle Scholar
  38. Hueerkamp C, Glynn PW, D’Croz L, Maté JL, Colley SB (2001) Bleaching and recovery of five eastern Pacific corals in an El Niño-related temperature experiment. Bull Mar Sci 69:215–236Google Scholar
  39. Hughes TP (1994) Catastrophes, phase shifts, and large-scale degradation of a Caribbean coral reef. Science 265:1547–1551CrossRefPubMedGoogle Scholar
  40. Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, Folke C, Grosberg R, Hoegh-Guldberg O, Jackson JBC, Kleypas J, Lough JM, Marshall P, Nystöm M, Palumbi SR, Pandolfi M, Rosen B, Roughgarden J (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301:929–933CrossRefPubMedGoogle Scholar
  41. Jacox MG, Hazen EL, Zaba KD, Rudnick DL, Edwards CA, Moore AM, Bograd SJ (2016) Impacts of the 2015–2016 El Niño on the California current system: early assessment and comparison to past events. Geophys Res Lett 43:7072–7080CrossRefGoogle Scholar
  42. Jost L (2006) Entropy and diversity. Oikos 113:363–375CrossRefGoogle Scholar
  43. Kindt R, Van Damme P, Simons AJ (2006) Tree diversity in western Kenya: using profiles to characterise richness and evenness. In: Hawksworth DL, Bull AT (eds) Forest diversity and management. Topics in biodiversity and conservation, vol 2. Springer, Dordrecht, pp 193–210CrossRefGoogle Scholar
  44. Kleypas JA, Yates KK (2009) Coral reefs and ocean acidification. Oceanography 284:118–120Google Scholar
  45. Lamy T, Legendre P, Chancerelle Y, Siu G, Claudet J (2015) Understanding the spatio-temporal response of coral reef fish communities to natural disturbances: insights from beta-diversity decomposition. PLoS ONE 10:e0138696CrossRefPubMedPubMedCentralGoogle Scholar
  46. Legendre P (2014) Interpreting the replacement and richness difference components of beta diversity. Glob Ecol Biogeogr 23:1324–1334CrossRefGoogle Scholar
  47. Legendre P, Cáceres M (2013) Beta diversity as the variance of community data: dissimilarity coefficients and partitioning. Ecol Lett 16:951–963CrossRefPubMedGoogle Scholar
  48. Legendre P, Salvat B (2015) Thirty-year recovery of mollusc communities after nuclear experimentations on Fangataufa atoll (Tuamotu, French Polynesia). Proc R Soc Lond B Biol Sci 282:20150750CrossRefGoogle Scholar
  49. Loh J, Green RE, Ricketts T, Lamoreux J, Jenkins M, Kapos V, Randers J (2005) The Living Planet Index: using species population time series to track trends in biodiversity. Philos Trans R Soc Lond B Biol Sci 360:289–295CrossRefPubMedPubMedCentralGoogle Scholar
  50. Magurran AE, Henderson PA (2010) Temporal turnover and the maintenance of diversity in ecological assemblages. Philos Trans R Soc Lond B Biol Sci 365:3611–3620CrossRefPubMedPubMedCentralGoogle Scholar
  51. Maté JL (2003) Corals and coral reefs of the Pacific coast of Panama. In: Cortés J (ed) Latin American coral reefs. Elsevier Science, Amsterdam, pp 387–418CrossRefGoogle Scholar
  52. Normile D (2016) El Niño’s warmth devastating reefs worldwide. Science 352:15–16CrossRefPubMedGoogle Scholar
  53. Oksanen JF, Blanchet G, Friendly M, Kindt R, Legendre P (2016) Vegan: community ecology package. R package version 2.4-0.
  54. Pandolfi JM, Bradbury RH, Sala E, Hughes TP, Bjorndal KA, Cooke RG, Warner R (2003) Global trajectories of the long-term decline of coral reef ecosystems. Science 301:955–958CrossRefPubMedGoogle Scholar
  55. Pauly D (1995) Anecdotes and the shifting baseline syndrome of fisheries. Trends Ecol Evol 10:430CrossRefPubMedGoogle Scholar
  56. Peres-Neto PR, Legendre P, Dray S, Borcard D (2006) Variation partitioning of species data matrices: estimation and comparison of fractions. Ecology 87:2614–2625CrossRefPubMedGoogle Scholar
  57. Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2016) nlme: linear and nonlinear mixed effects models. R package version 3.1-128.
  58. R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  59. Rényi A (1961) On measurements of entropy and information. In: Neyman J (ed) Proceedings of the 4th Berkeley symposium on mathematical statistics and probability. University of California Press, Berkeley, USAGoogle Scholar
  60. Reyes-Bonilla H (2002) Checklist of valid names and synonyms of stony corals (Anthozoa: Scleractinia) from the eastern Pacific. J Nat Hist 36:1–13CrossRefGoogle Scholar
  61. Riegl B, Purkis SJ, Keck J, Rowlands GP (2009) Monitored and modeled coral population dynamics and the refuge concept. Mar Pollut Bull 58:24–38CrossRefPubMedGoogle Scholar
  62. Skirving WJ, Strong AE, Liu G, Liu C, Arzayus F, Sapper J, Bayler E (2006) Extreme events and perturbations of coastal ecosystems. In: Richardson LL, LeDrew EF (eds) Remote sensing of aquatic coastal ecosystem processes. Springer, Netherlands, pp 11–25CrossRefGoogle Scholar
  63. Sweatman H, Delean S, Syms C (2011) Assessing loss of coral cover on Australia’s Great Barrier Reef over two decades, with implications for longer-term trends. Coral Reefs 30:521–531CrossRefGoogle Scholar
  64. Toth LT, Macintyre IG, Aronson RB (2017) Holocene reef development in the Eastern Tropical Pacific. In: Glynn PW, Manzello DP, Enochs IC (eds) Coral reefs of the Eastern Tropical Pacific. Springer, Dordrecht, pp 177–202CrossRefGoogle Scholar
  65. Xie SP, Xu H, Kessler WS, Nonaka M (2005) Air–sea interaction over the Eastern Pacific warm pool: gap winds, thermocline dome, and atmospheric convection. J Climate 18:5–20CrossRefGoogle Scholar
  66. Zuur A, Ieno EN, Smith GM (2007) Analyzing ecological data. Springer Science & Business Media, BerlinCrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.Department of BiologyMcGill UniversityMontréalCanada
  2. 2.Smithsonian Tropical Research InstituteBalboa, AnconPanama

Personalised recommendations