Skip to main content

Advertisement

SpringerLink
Log in

Localized hypoxia may have caused coral reef mortality at the Flower Garden Banks

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

Abstract

On July 25, 2016, turbid water and dead corals, sponges and other invertebrates were discovered at the East Bank (EB) of the Flower Garden Banks (FGB) National Marine Sanctuary. Mortality was spread over 0.06 km2, with up to 80% coral mortality reported in some areas. Within days, response efforts were underway to investigate the potential mechanisms leading to the mortality event. Hydrographic surveys, moored buoy data, and a regional hydrodynamic model were used to characterize water chemistry, hydrography, and microbial communities within the FGB. Low salinity (~ 31–33), total alkalinity (~ 2284–2330 µmol kg−1), and dissolved inorganic carbon (DIC, ~ 1968–2011 µmol kg−1) were detected in surface waters over the EB and eastern stations, revealing the presence of river-derived water. The Mississippi/Atchafalaya rivers were the primary sources of freshwater during the event, although Texas rivers, all of which had unusually high discharge during 2016, contributed approximately one-fifth to the total freshwater mass. At 75 m depth, high density, salinity, DIC, ammonium, and abundance of microbial taxa associated with deep waters were coincident with low temperature and aragonite saturation state at the northern and eastern stations, indicating a deeper source water at these stations. Cross-slope density gradients were also consistent with an upwelling circulation pattern. Using these observations and data, we hypothesize that the mortality event was most likely caused by the combination of two processes. The turbid freshwater layer inhibited photosynthesis, leading to net respiration of coral reef organic matter. Additionally, deep, dense waters upwelled onto the bank and formed a stratified bottom layer, which prevented re-oxygenation from the overlying water column and led to localized areas of hypoxia within pockets on the reef. Hypoxia likely formed rapidly, within two days. Moving forward, high-frequency temporal measurements of oxygen and carbonate chemistry are critical for monitoring risks (e.g., hypoxia and acidification) associated with freshwater discharge and upwelling, since these processes may adversely affect coral reef health.

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

Similar content being viewed by others

References

  • Altieri AH, Harrison SB, Seemann J, Collin R, Diaz RJ, Knowlton N (2017) Tropical dead zones and mass mortalities on coral reefs. Proc Natl Acad Sci 114:3660–3665

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baird AH, Keith SA, Woolsey E, Yoshida R, Naruse T (2017) Rapid coral mortality following doldrums-like conditions on Iriomote, Japan. F1000Research 6:1728

    Article  PubMed  Google Scholar 

  • Baohua ZG, Bo W, Huang Tseng C (2004) Effects of temperature, hypoxia, ammonia and nitrate on the bleaching among three coral species. Chin Sci Bull 49:1923–1928

    Article  Google Scholar 

  • Bianchi TS, DiMarco SF, Cowan JH, Hetland RD, Chapman P, Day JW, Allison MA (2010) The science of hypoxia in the northern Gulf of Mexico: a review. Sci Total Environ 408:1471–1484

    Article  CAS  PubMed  Google Scholar 

  • Bray JR, Curtis JT (1957) An ordination of the upland forest communities of southern Wisconsin. Ecol Monogr 27:325–349

    Article  Google Scholar 

  • Cai W-J (2003) Riverine inorganic carbon flux and rate of biological uptake in the Mississippi River plume. Geophys Res Lett 30:1032

    Google Scholar 

  • Cai WJ, Hu X, Huang WJ, Murrell MC, Lehrter JC, Lohrenz SE, Chou WC, Zhai W, Hollibaugh JT, Wang Y, Zhao P, Guo X, Gundersen K, Dai M, Gong GC (2011) Acidification of subsurface coastal waters enhanced by eutrophication. Nat Geosci 4:766–770

    Article  CAS  Google Scholar 

  • Cho K, Reid RO, Nowlin WD (1998) Objectively mapped stream function fields on the Texas–Louisiana shelf based on 32 months of moored current meter data. J Geophys Res Ocean 103:10377–10390

    Article  Google Scholar 

  • Cochrane JD, Kelly FJ (1986) Low-frequency circulation on the Texas–Louisiana continental shelf. J Geophys Res 91:10645

    Article  Google Scholar 

  • Dale VH, Kling CL, Meyer JL, Sanders J, Stallworth H, Armitage T, Wangsness D, Bianchi T, Blumberg A, Boynton W, Conley DJ, Crumpton W, David M, Gilbert D, Howarth RW, Lowrance R, Mankin K, Opaluch J, Paerl H, Reckhow K, Sharpley AN, Simpson TW, Snyder CS, Wright D (2010) Hypoxia in the Northern Gulf of Mexico introduction. Springer, New York

    Book  Google Scholar 

  • DeCarlo TM, Cohen AL, Wong GTF, Shiah F-K, Lentz SJ, Davis KA, Shamberger KEF, Lohmann P (2017) Community production modulates coral reef pH and the sensitivity of ecosystem calcification to ocean acidification. J Geophys Res Ocean 122:745–761

    Article  CAS  Google Scholar 

  • Deslarzes KJ, Lugo-Fernández A (2007) Influence of terrigenous runoff on offshore coral reefs: an example from the Flower Garden Banks, Gulf of Mexico. In: Aronson RB (ed) Geological approaches to coral reef ecology. Springer, Berlin, pp 126–160

    Chapter  Google Scholar 

  • Diaz RJ, Rosenberg R (2008) Spreading dead zones and consequences for marine ecosystems. Science (80-) 321:926–929

    Article  CAS  Google Scholar 

  • Dickson AG, Millero FJ (1987) A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep Sea Res Part A Oceanogr Res Pap 34:1733–1743

    Article  CAS  Google Scholar 

  • Dickson AG, Sabine CL, Christian JR (2007) Guide to best practices for ocean CO2 measurements: PICES Special Publication 3. PICES, Sidney, Canada

  • DiMarco S, Zimmerle HM (2017) MCH atlas: oceanographic observations of the mechanism controlling hypoxia project. Texas Sea Grant TAMU-SG-17-601

  • DiMarco S, Strauss J, May N, Mullins-Perry RL, Grossman EL, Shormann D (2012) Texas coastal hypoxia linked to Brazos river discharge as revealed by oxygen isotopes. Aquat Geochem 18:159–181

    Article  CAS  Google Scholar 

  • Dodge RE, Lang JC (1983) Environmental correlates of hermatypic coral (Montastrea annularis) growth on the East Flower Gardens Bank, northwest Gulf of Mexico. Limnol Oceanogr 28:228–240

    Article  Google Scholar 

  • Doyle SM, Whitaker EA, De Pascuale V, Wade TL, Knap AH, Santschi PH, Quigg A, Sylvan JB (2018) Rapid formation of microbe-oil aggregates and changes in community composition in coastal surface water following exposure to oil and the dispersant corexit. Front Microbiol 9:1–16

    Article  CAS  Google Scholar 

  • Falter JL, Lowe RJ, Atkinson MJ, Cuet P (2012) Seasonal coupling and de-coupling of net calcification rates from coral reef metabolism and carbonate chemistry at Ningaloo Reef, Western Australia. J Geophys Res Ocean 117:C05003

    Article  CAS  Google Scholar 

  • Gajdzik L, DeCarlo T (2017) The perfect calm: Reoccurring mass die-offs on a remote coral atoll. Matters. https://doi.org/10.19185/matters.201707000003

    Article  Google Scholar 

  • Gardner TA, Côté IM, Gill JA, Grant A, Watkinson AR (2003) Long-term region-wide declines in caribbean corals. Science (80-) 301:958–960

    Article  CAS  Google Scholar 

  • Gattuso J-P, Pichon M, Delesalle B, Canon C, Frankignoulle M (1996) Carbon fluxes in coral reefs. I. Lagrangian measurement of community metabolism and resulting air-sea CO2 disequilibrium. Mar Ecol Prog Ser 145:109–121

    Article  Google Scholar 

  • Georgian SE, Deleo D, Durkin A, Gomez CE, Kurman M, Lunden JJ, Cordes EE (2016) Oceanographic patterns and carbonate chemistry in the vicinity of cold-water coral reefs in the Gulf of Mexico: implications for resilience in a changing ocean. Limnol Oceanogr 61:648–665

    Article  CAS  Google Scholar 

  • Gillies LE, Thrash JC, deRada S, Rabalais NN, Mason OU (2015) Archaeal enrichment in the hypoxic zone in the northern Gulf of Mexico: Archaea in the hypoxic northern GOM water column. Environ Microbiol 17:3847–3856

    Article  CAS  PubMed  Google Scholar 

  • Gordon LI, Jennings JC, Ross AA, Krest JM (1994) World ocean circulation experiment. WOCE operations manual. Volume 3. The observational programme. Section 3.1. WOCE hydrographic programme. Part 3.1.3. WHP operations and methods. (Revision 1). United States

  • Hagman DK, Gittings SR (1992) Coral bleaching on high latitude reefs at the Flower Garden Banks, NW Gulf of Mexico. In: Proceeding of the seventh international coral reef symposium, vol 1, pp 38–43

  • Hetland RD, Zhang X (2017) Interannual variation in stratification over the Texas–Louisiana continental shelf and effects on seasonal hypoxia. In: Justic D, Rose K, Hetland R, Fennel K (eds) Modeling coastal hypoxia: numerical simulations of patterns, Controls and Effects of Dissolved Oxygen Dynamics. Springer, Berlin, pp 49–60

    Chapter  Google Scholar 

  • Hobbs J-PA, Macrae H (2012) Unusual weather and trapped coral spawn lead to fish kill at a remote coral atoll. Coral Reefs 31:961–961

    Article  Google Scholar 

  • Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742

    Article  CAS  PubMed  Google Scholar 

  • Holmes I, Harris K, Quince C (2012) Dirichlet multinomial mixtures: Generative models for microbial metagenomics. PLoS One 7:e30126

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu X, Nuttall MF, Wang H, Yao H, Staryk CJ, McCutcheon MR, Eckert RJ, Embesi JA, Johnston MA, Hickerson EL, Schmahl GP, Manzello D, Enochs IC, DiMarco S, Barbero L (2018) Seasonal variability of carbonate chemistry and decadal changes in waters of a marine sanctuary in the Northwestern Gulf of Mexico. Mar Chem 205:16–28

    Article  CAS  Google Scholar 

  • Huang W-J, Cai W-J, Wang Y, Lohrenz SE, Murrell MC (2015) The carbon dioxide system on the Mississippi River-dominated continental shelf in the northern Gulf of Mexico: 1. Distribution and air-sea CO2 flux. J Geophys Res Ocean 120:1–17

    Google Scholar 

  • Johnston MA, Eckert RJ, Hickerson EL, Nuttall MF, Embesi JA, Sterne TK, Blakeway RD, Lee MT, Schmahl GP, MacMillan J (2019a) Localized coral reef mortality event at East Flower Garden Bank, Gulf of Mexico. Bull Mar Sci 95:1–12

    Article  Google Scholar 

  • Johnston MA, Nuttall MF, Eckert RJ, Embesi JA, Slowey NC, Hickerson EL, Schmahl GP (2013) Long-term monitoring at the east and west Flower Garden Banks National Marine Sanctuary, 2009–2010, vol 1. Technical report.

  • Johnston MA, Hickerson EL, Nuttall MF, Blakeway RD, Sterne TK, Eckert RJ, Schmahl GP (2019b) Coral bleaching and recovery from 2016 to 2017 at east and west Flower Garden Banks, Gulf of Mexico. Coral Reefs 38:787–799

    Article  Google Scholar 

  • Kleypas JA, Mcmanus JW, Menez LAB (1999) Environmental limits to coral reef development: where do we draw the line ? Am Zool 39:146–159

    Article  Google Scholar 

  • Lohrenz SE, Fahnenstiel GL, Redalje DG, Lang GA, Chen X, Dagg MJ (1997) Variations in primary production of northern Gulf of Mexico continental shelf waters linked to nutrient inputs from the Mississippi River. Mar Ecol Prog Ser 155:45–54

    Article  CAS  Google Scholar 

  • Lugo-Fernández A (2006) Travel times of passive drifters from the western Caribbean to the Gulf of Mexico and Florida–Bahamas. Gulf Mex Sci 24:61–67

    Google Scholar 

  • Mehrbach C, Culberson CH, Hawley JE, Pytkowicx RM (1973) Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnol Oceanogr 18:897–907

    Article  CAS  Google Scholar 

  • Morrison JM, Merrell WJ, Key RM, Key TC (1983) Property distributions and deep chemical measurements within the western Gulf of Mexico. J Geophys Res Ocean 88:2601–2608

    Article  CAS  Google Scholar 

  • Nowlin W Jr, Jochens A, Reid RO, Dimarco SF (1998) Texas–Louisiana shelf circulation and transport processes study: synthesis report. US Department of the Interior, Minerals Management Service, Gulf of Mexico OCS Region, New Orleans

    Google Scholar 

  • Nowlin WD, Jochens AE, Dimarco SF, Reid RO, Howard MK (2005) Low-frequency circulation over the Texas–Louisiana continental shelf. In: Sturges W, Lugo-Fernandez A (eds) CIrculation of the Gulf of Mexico: observations and models. Geophysical Monograph Series, AGU, Washington D.C., pp 219–240

    Google Scholar 

  • Pacanowski RC, Philander SGH (1981) Parameterization of vertical mixing in numerical models of tropical oceans. J Phys Oceanogr 11:1443–1451

    Article  Google Scholar 

  • Pandolfi JM, Bradbury RH, Sala E, Hughes TP, Bjorndal KA, Cooke RG, McArdle D, McClenachan L, Newman MJH, Paredes G, Warner RR, Jackson JBC (2003) Global trajectories of the long-term decline of coral reef ecosystems. Science (80-) 301:955–958

    Article  CAS  Google Scholar 

  • Parada AE, Fuhrman JA (2017) Marine archaeal dynamics and interactions with the microbial community over 5 years from surface to seafloor. ISME J 11:2510–2525

    Article  PubMed  PubMed Central  Google Scholar 

  • Partensky F, Blanchot J, Vaulot D (1999) Differential distribution and ecology of Prochlorococcus and Synechococcus in oceanic waters: a review. Bull Oceanogr Monaco-Numero Spec 19:457–476

    Google Scholar 

  • Pierrot D, Lewis E, Wallace D (2006) MS Excel program developed for CO2 system calculations. ORNL/CDIAC-105a. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, US Department of Energy, Oak Ridge, Tennessee

  • Rabalais NN, Turner RE, Sen Gupta BK, Boesch DF, Chapman P, Murrell MC (2007) Hypoxia in the northern Gulf of Mexico: does the science support the plan to reduce, mitigate, and control hypoxia? Estuaries Coasts 30:753–772

    Article  CAS  Google Scholar 

  • Rezak R, Gittings SR, Bright TJ (1990) Biotic assemblages and ecological controls on reefs and banks of the Northwest Gulf of Mexico. Integr Comp Biol 30:23–35

    Google Scholar 

  • Sargent M, Austin T (1949) Organic productivity of an Atoll. EOS Trans Am Geophys Union 30:245–249

    Article  Google Scholar 

  • Shamberger K, Feely R, Sabine C, Atkinson M, DeCarlo E, Mackenzie F, Drupp P, Butterfield D (2011) Calcification and organic production on a Hawaiian coral reef. Mar Chem 127:64–75

    Article  CAS  Google Scholar 

  • Smith SV, Marsh JA (1973) Organic production on the windward reef flat of Eniwetok Atoll. Limnol Oceanogr 18:953–961

    Article  CAS  Google Scholar 

  • Stewart FJ, Ulloa O, DeLong EF (2012) Microbial metatranscriptomics in a permanent marine oxygen minimum zone: OMZ community gene expression. Environ Microbiol 14:23–40

    Article  CAS  PubMed  Google Scholar 

  • Teague WJ, Wijesekera HW, Jarosz E, Fribance DB, Lugo-Fernández A, Hallock ZR (2013) Current and hydrographic conditions at the East Flower Garden Bank in 2011. Cont Shelf Res 63:43–58

    Article  Google Scholar 

  • Tolar BB, King GM, Hollibaugh JT (2013) An analysis of thaumarchaeota populations from the Northern Gulf of Mexico. Front Microbiol 4:72

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang ZA, Wanninkhof R, Cai WJ, Byrne RH, Hu X, Peng TH, Huang WJ (2013) The marine inorganic carbon system along the Gulf of Mexico and Atlantic coasts of the United States: insights from a transregional coastal carbon study. Limnol Oceanogr 58:325–342

    Article  CAS  Google Scholar 

  • Wanninkhof R, Barbero L, Byrne R, Cai WJ, Huang WJ, Zhang JZ, Baringer M, Langdon C (2015) Ocean acidification along the Gulf Coast and East Coast of the USA. Cont Shelf Res 98:54–71

    Article  Google Scholar 

  • Zhang Z, Hetland R (2012) A numerical study on convergence of alongshore flows over the Texas–Louisiana shelf. J Geophys Res Ocean 117:1–18

    Google Scholar 

  • Zhang X, Hetland RD, Marta-Almeida M, Dimarco SF (2012a) A numerical investigation of the Mississippi and Atchafalaya freshwater transport, filling and flushing times on the Texas–Louisiana Shelf. J Geophys Res Ocean 117:1–21

    Google Scholar 

  • Zhang X, Marta-Almeida M, Hetland RD (2012b) A high-resolution pre-operational forecast model of circulation on the Texas–Louisiana continental shelf and slope. J Oper Oceanogr 5:19–34

    CAS  Google Scholar 

  • Zhang Z, Hetland R, Zhang X (2014) Wind-modulated buoyancy circulation over the Texas–Louisiana shelf. J Geophys Res Ocean 119:5705–5723

    Article  Google Scholar 

  • Zhang W, Hetland R, DiMarco S, Fennel K (2015) Processes controlling mid-water column oxygen minima over the Texas–Louisiana shelf. J Geophys Res Ocean 120:28002812

    Google Scholar 

  • Zwirglmaier K, Jardillier L, Ostrowski M, Mazard S, Garczarek L, Vaulot D, Not F, Massana R, Ulloa O, Scanlan DJ (2008) Global phylogeography of marine synechococcus and prochlorococcus reveals a distinct partitioning of lineages among oceanic biomes. Environ Microbiol 10:147–161

    PubMed  Google Scholar 

Download references

Acknowledgements

Thanks go to the Captain and crew of the RV Manta, operated by the FGB Foundation, for sea going operations during the rapid response cruise; staff of FGBNMS/ONMS (E. Hickerson, M, Johnston, G.P. Schmahl and S. Gittings) for access to early reports of the event and for multiple discussions pertaining to this manuscript; J. Schiff, E.A Whitaker and B. Buckingham for collecting carbonate chemistry, microbiology, and oxygen samples. This work is dedicated to Matthew K. Howard (TAMU), who served as Chief Scientist for the 2016 rapid response cruise and passed away suddenly in February 2018; he was a valued friend and dedicated scientist. Special thanks to the TAMU Geochemical and Environmental Research Group (GERG) for access to the Texas Automated Buoy System (https://tabs.gerg.tamu.edu) historical and real-time data. Funds for this work were provided by the GoM Coastal Ocean Observing System (GCOOS), the College of Geosciences (TAMU), the Department of Oceanography (TAMU), FGBNMS (NOAA), the Geochemical and Environmental Research Group (TAMU), the Harte Research Institute, the Texas General Land Office, the Texas OneGulf Center of Excellence, the GoM Research Initiative to support the Aggregation and Degradation of Dispersants and Oil by Microbial Exopolymers (ADDOMEx) consortium, and a NOAA Nancy Foster Scholarship to A. Kealoha. Partial funding of this research was provided by the Texas Governor Fund through the Texas Restore Program as well as the G. Unger Vetlesen Foundation to A. H. Knap (TAMU). The author’s thank A.H. Knap for his assistance in facilitating the response cruise aboard the R/V Manta in July/August 2016. We also thank two anonymous reviewers for their constructive and thoughtful comments that substantially improved this manuscript. The funders had no role in study design, data collection, and interpretation, or the decision to submit the work for publication.

Author information

Authors and Affiliations

  1. Department of Oceanography, Texas A&M University, College Station, TX, 77843, USA

    Andrea K. Kealoha, Shawn M. Doyle, Kathryn E. F. Shamberger, Jason B. Sylvan, Robert D. Hetland & Steven F. DiMarco

Authors
  1. Andrea K. Kealoha
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shawn M. Doyle
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kathryn E. F. Shamberger
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jason B. Sylvan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Robert D. Hetland
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Steven F. DiMarco
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Andrea K. Kealoha.

Ethics declarations

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

Additional information

Topic editor: Mark R Patterson

Publisher's Note

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

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kealoha, A.K., Doyle, S.M., Shamberger, K.E.F. et al. Localized hypoxia may have caused coral reef mortality at the Flower Garden Banks. Coral Reefs 39, 119–132 (2020). https://doi.org/10.1007/s00338-019-01883-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00338-019-01883-9

Keywords

Search

Navigation