Abstract
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.
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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 203–250
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 3:3486
Bellwood DR, Hughes TP, Folke C, Nyström M (2004) Confronting the coral reef crisis. Nature 429:827–833
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 160:421–456
Bruno JF, Selig ER (2007) Regional decline of coral cover in the Indo-Pacific: timing, extent, and subregional comparisons. PLoS ONE 8:e711
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 4:111–116
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 321:560–563
Chao A (1987) Estimating the population size for capture-recapture data with unequal catchability. Biometrics 43:783–791
Combosch DJ, Vollmer SV (2015) Trans-Pacific RAD-Seq population genomics confirms introgressive hybridization in Eastern Pacific Pocillopora corals. Mol Phylogenet Evol 88:154–162
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 203–250
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 203–250
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 73:325–340
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 109:17995–17999
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 344:296–299
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 25:1938–1943
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 59–84
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 56:1008–1014
Gardner TA, Côté IM, Gill JA, Grant A, Watkinson AR (2003) Long-term region-wide declines in Caribbean corals. Science 301:958–960
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 141–182
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 251–259
Glynn PW, D’Croz L (1990) Experimental evidence for high temperature stress as the cause of El Niño-coincident coral mortality. Coral Reefs 8:181–191
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 10:210–225
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 69:79–109
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 251–290
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 107–176
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 97:1949–1960
Graham NA, Cinner JE, Norström AV, Nyström M (2014) Coral reefs as novel ecosystems: embracing new futures. Curr Opin Environ Sustain 7:9–14
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 11:541–548
Guzman HM, Holst I (1994) Inventario biológico y estado actual de los arrecifes coralinos a ambos lados del Canal de Panamá. Rev Biol Trop 42:493–514
Guzman HM, Cortés J (2007) Reef recovery 20 years after the 1982–1983 El Niño massive mortality. Mar Biol 151:401–411
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 39:225–231
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 31:111–121
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 35:1–9
Harrell FE, Dupont C Jr, (2015) Hmisc: Harrell miscellaneous. R package version 3.17-0. http://CRAN.R-project.org/package=Hmisc
Hill MO (1973) Diversity and evenness: a unifying notation and its consequences. Ecology 54:427–432
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 15:1–7
Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–866
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 69:215–236
Hughes TP (1994) Catastrophes, phase shifts, and large-scale degradation of a Caribbean coral reef. Science 265:1547–1551
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 301:929–933
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 43:7072–7080
Jost L (2006) Entropy and diversity. Oikos 113:363–375
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 193–210
Kleypas JA, Yates KK (2009) Coral reefs and ocean acidification. Oceanography 284:118–120
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:e0138696
Legendre P (2014) Interpreting the replacement and richness difference components of beta diversity. Glob Ecol Biogeogr 23:1324–1334
Legendre P, Cáceres M (2013) Beta diversity as the variance of community data: dissimilarity coefficients and partitioning. Ecol Lett 16:951–963
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 282:20150750
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 360:289–295
Magurran AE, Henderson PA (2010) Temporal turnover and the maintenance of diversity in ecological assemblages. Philos Trans R Soc Lond B Biol Sci 365:3611–3620
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 387–418
Normile D (2016) El Niño’s warmth devastating reefs worldwide. Science 352:15–16
Oksanen JF, Blanchet G, Friendly M, Kindt R, Legendre P (2016) Vegan: community ecology package. R package version 2.4-0. http://CRAN.R-project.org/package=vegan
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 301:955–958
Pauly D (1995) Anecdotes and the shifting baseline syndrome of fisheries. Trends Ecol Evol 10:430
Peres-Neto PR, Legendre P, Dray S, Borcard D (2006) Variation partitioning of species data matrices: estimation and comparison of fractions. Ecology 87:2614–2625
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. http://CRAN.R-project.org/package=nlme
R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
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, USA
Reyes-Bonilla H (2002) Checklist of valid names and synonyms of stony corals (Anthozoa: Scleractinia) from the eastern Pacific. J Nat Hist 36:1–13
Riegl B, Purkis SJ, Keck J, Rowlands GP (2009) Monitored and modeled coral population dynamics and the refuge concept. Mar Pollut Bull 58:24–38
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 11–25
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 30:521–531
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 177–202
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 18:5–20
Zuur A, Ieno EN, Smith GM (2007) Analyzing ecological data. Springer Science & Business Media, Berlin
Acknowledgements
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.
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Gomez, C.G., Gonzalez, A. & Guzman, H.M. Multiscale change in reef coral species diversity and composition in the Tropical Eastern Pacific. Coral Reefs 37, 105–120 (2018). https://doi.org/10.1007/s00338-017-1637-y
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DOI: https://doi.org/10.1007/s00338-017-1637-y