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The influence of seasonality on benthic primary production in a Red Sea coral reef

Abstract

Northern Red Sea coral reefs experience pronounced seasonal variations in environmental factors such as water temperature, light intensity, and nutrient availability. This allows studying related effects on primary production by different functional groups. The present study therefore quantified primary production of all dominant benthic primary producers from a Jordanian fringing reef (29° 27′ 31″ N, 34° 58′ 26″ E) by measuring net photosynthesis (P n) and dark respiration (R) using stirred respirometry chamber incubations during all four seasons of 2013. Annual mean P n was highest for the macroalga Caulerpa (901 nmol O2 cm−2 h−1) and lowest for both the soft coral Sarcophyton and sedimentary microphytobenthos (212 and 223 nmol O2 cm−2 h−1, respectively). Sedimentary microphytobenthos exhibited the strongest response to seasonality with 5.7 times higher P n in spring than in winter. R was highest in hard corals among all groups in every season, likely due to nighttime calcification and heterotrophic activity. Gross photosynthesis-to-respiration ratios (P g:R) were highest for turf algae and macroalgae as well as cyanobacterial mats. While R was primarily positively related to PAR and temperature and P g:R to inorganic nutrients, few groups revealed significant relations between P n and environmental parameters. Seasonal budgets found daily gross primary production and respiration to be dominated by hard and soft corals. Total reef gross primary production was comparable between less oligotrophic spring and more oligotrophic summer. This indicates that processes such as heterotrophic feeding and microbial dinitrogen fixation may help the functional groups overcome potential nutrient limitation of primary production in summer.

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References

  • Adey W (1998) Coral reefs: algal structured and mediated ecosystems in shallow, turbulent, alkaline waters. J Phycol 34:393–406. doi:10.1046/j.1529-8817.1998.340393.x

    Article  Google Scholar 

  • Adey W, Steneck R (1985) Highly productive eastern Caribbean reefs: synergistic effects of biological, chemical, physical, and geological factors. NOAA Undersea Research Program, Rockville

    Google Scholar 

  • Al-Horani FA, Al-Moghrabi SM, de Beer D (2003) The mechanism of calcification and its relation to photosynthesis and respiration in the scleractinian coral Galaxea fascicularis. Mar Biol 142:419–426. doi:10.1007/s00227-002-0981-8

    CAS  Google Scholar 

  • Al-Zibdah M, Colgan L (2013) In-situ surveillance of coral-turf algae interactions in fringing reefs of the Jordan’s Gulf of Aqaba—Red Sea. Fresen Environ Bull 22:2379–2384

    CAS  Google Scholar 

  • Ateweberhan M, Bruggemann J, Breeman A (2006) Effects of extreme seasonality on community structure and functional group dynamics of coral reef algae in the southern Red Sea (Eritrea). Coral Reefs 25:391–406. doi:10.1007/s00338-006-0109-6

    Article  Google Scholar 

  • Atkinson M, Grigg R (1984) Model of a coral reef ecosystem. 2. Gross and net benthic primary production at French Frigate Shoals, Hawaii. Coral Reefs 3:13–22. doi:10.1007/BF00306136

    CAS  Article  Google Scholar 

  • Bahartan K, Zibdah M, Ahmed Y, Israel A, Brickner I, Abelson A (2010) Macroalgae in the coral reefs of Eilat (Gulf of Aqaba, Red Sea) as a possible indicator of reef degradation. Mar Pollut Bull 60:759–764. doi:10.1016/j.marpolbul.2009.11.017

    CAS  Article  Google Scholar 

  • Barnes D (1983) Profiling coral reef productivity and calcification using pH and oxygen electrodes. J Exp Mar Biol Ecol 66:149–161. doi:10.1016/0022-0981(83)90036-9

    CAS  Article  Google Scholar 

  • Bednarz V, Naumann M, Niggl W, Wild C (2012) Inorganic nutrient availability affects organic matter fluxes and metabolic activity in the soft coral genus Xenia. J Exp Biol 215:3672–3679. doi:10.1242/jeb.072884

    CAS  Article  Google Scholar 

  • Bednarz V, Cardini U, van Hoytema N, Al-Rshaidat M, Wild C (2015a) Seasonal variation in dinitrogen fixation and oxygen fluxes associated with two dominant zooxanthellate soft corals from the northern Red Sea. Mar Ecol Prog Ser 519:141–152. doi:10.3354/meps11091

    Article  Google Scholar 

  • Bednarz VN, van Hoytema N, Cardini U, Naumann MS, Al-Rshaidat MMD, Wild C (2015b) Dinitrogen fixation and primary productivity by carbonate and silicate reef sand communities of the Northern Red Sea. Mar Ecol Prog Ser 527:47–57. doi:10.3354/meps11224

    Article  Google Scholar 

  • Bennett S, Verges A, Bellwood D (2010) Branching coral as a macroalgal refuge in a marginal coral reef system. Coral Reefs 29:471–480. doi:10.1007/s00338-010-0594-5

    Article  Google Scholar 

  • Berumen M, Hoey A, Bass W, Bouwmeester J, Catania D, Cochran J, Khalil M, Miyake S, Mughal M, Spaet J, Saenz-Agudelo P (2013) The status of coral reef ecology research in the Red Sea. Coral Reefs 32:737–748. doi:10.1007/s00338-013-1055-8

    Article  Google Scholar 

  • Brocke H, Wenzhoefer F, de Beer D, Mueller B, van Duyl F, Nugues M (2015) High dissolved organic carbon release by benthic cyanobacterial mats in a Caribbean reef ecosystem. Sci Rep 5. Doi: 10.1038/srep08852

  • Cardini U, Bednarz VN, Foster RA, Wild C (2014) Benthic N2 fixation in coral reefs and the potential effects of human-induced environmental change. Ecol Evol 4:1706–1727. doi:10.1002/ece3.1050

    Article  Google Scholar 

  • Cardini U, van Hoytema N, Al-Rshaidat M, Schuhmacher H, Wild C, Naumann M (2015a) 37 Years later: revisiting a Red Sea long-term monitoring site. Coral Reefs. doi:10.1007/s00338-015-1321-z

    Google Scholar 

  • Cardini U, Bednarz VN, Naumann MS, van Hoytema N, Rix L, Foster RA, Al-Rshaidat MMD, Wild C (2015b) Functional significance of dinitrogen fixation in sustaining coral productivity under oligotrophic conditions. Proc R Soc B 282:20152257

    Article  Google Scholar 

  • Carlson D, Fredj E, Gildor H (2014) The annual cycle of vertical mixing and restratification in the Northern Gulf of Eilat/Aqaba (Red Sea) based on high temporal and vertical resolution observations. Deep Sea Res Pt I 84:1–17. doi:10.1016/j.dsr.2013.10.004

    Article  Google Scholar 

  • Carpenter R (1985) Relationships between primary production and irradiance in coral reef algal communities. Limnol Oceanogr 30:784–793

    Article  Google Scholar 

  • Charpy L, Casareto B, Langlade M, Suzuki Y (2012) Cyanobacteria in coral reef ecosystems: a review. J Mar Biol 259571

  • Cohen Y, Cohen J (2008) Statistics and Data with R: an applied approach through examples. John Wiley & Sons Ltd., Chippenham

    Book  Google Scholar 

  • D’Angelo C, Wiedenmann J (2014) Impacts of nutrient enrichment on coral reefs: new perspectives and implications for coastal management and reef survival. Curr Opin Environ Sustain 7:82–93. doi:10.1016/j.cosust.2013.11.029

    Article  Google Scholar 

  • Eidens C, Bayraktarov E, Hauffe T, Pizarro V, Wilke T, Wild C (2014) Benthic primary production in an upwelling-influenced coral reef. Colombian Caribbean. Peer J 2:22. doi:10.7717/peerj.554

    Article  Google Scholar 

  • Fabricius K, Klumpp D (1995) Widespread mixotrophy in reef-inhabiting soft corals—the influence of depth, and colony expansion and contraction on photosynthesis. Mar Ecol-Prog Ser 125:195–204. doi:10.3354/meps125195

    Article  Google Scholar 

  • Falkowski P, Raven J (1997) Photosynthesis and primary production in nature. In: Aquatic photosynthesis. Blackwell Science, Oxford, pp 263–299

  • Falter JL, Lowe RJ, Atkinson MJ, Monismith SG, Schar DW (2008) Continuous measurements of net production over a shallow reef community using a modified Eulerian approach. J Geophys Res-Oceans 113:14. doi:10.1029/2007jc004663

    Article  Google Scholar 

  • Fine M, Gildor H, Genin A (2013) A coral reef refuge in the Red Sea. Glob Change Biol 19:3640–3647. doi:10.1111/gcb.12356

    Article  Google Scholar 

  • Fong P, Paul V (2011) Coral reef algae. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition. Springer, Netherlands, pp 241–272

    Chapter  Google Scholar 

  • Franklin L, Seaton G, Lovelock C, Larkum A (1996) Photoinhibition of photosynthesis on a coral reef. Plant, Cell Environ 19:825–836. doi:10.1111/j.1365-3040.1996.tb00419.x

    Article  Google Scholar 

  • Fricke A, Teichberg M, Nugues M, Beilfuss S, Bischof K (2014) Effects of depth and ultraviolet radiation on coral reef turf algae. J Exp Mar Biol Ecol 461:73–84. doi:10.1016/j.jembe.2014.07.017

    Article  Google Scholar 

  • Gattuso J, Pichon M, Delesalle B, Canon C, Frankignoulle M (1996) Carbon fluxes in coral reefs. 1. Lagrangian measurement of community metabolism and resulting air-sea CO2 disequilibrium. Mar Ecol Prog Ser 145:109–121. doi:10.3354/meps145109

    Article  Google Scholar 

  • Gillooly J, Brown J, West G, Savage V, Charnov E (2001) Effects of size and temperature on metabolic rate. Science 293:2248–2251. doi:10.1126/science.1061967

    CAS  Article  Google Scholar 

  • Gomez I, Wiencke C (1996) Photosynthesis, dark respiration and pigment contents of gametophytes and sporophytes of the Antarctic brown alga Desmarestia menziesii. Bot Mar 39:149–157. doi:10.1515/botm.1996.39.1-6.149

  • Goreau T, Yonge C, Goreau N (1971) Reef corals—autotrophs or heterotrophs. Biol Bull 141:247. doi:10.2307/1540115

    Article  Google Scholar 

  • Grottoli A, Rodrigues L, Palardy J (2006) Heterotrophic plasticity and resilience in bleached corals. Nature 440:1186–1189. doi:10.1038/nature04565

    CAS  Article  Google Scholar 

  • Haas A, Naumann M, Struck U, Mayr C, el-Zibdah M, Wild C (2010) Organic matter release by coral reef associated benthic algae in the Northern Red Sea. J Exp Mar Biol Ecol 389:53–60. doi:10.1016/j.jembe.2010.03.018

    CAS  Article  Google Scholar 

  • Hatcher B (1988) Coral reef primary production—a beggar’s banquet. Trends Ecol Evol 3:106–111. doi:10.1016/0169-5347(88)90117-6

    CAS  Article  Google Scholar 

  • Hennige S, Suggett D, Warner M, McDougall K, Smith D (2009) Photobiology of symbiodinium revisited: bio-physical and bio-optical signatures. Coral Reefs 28:179–195. doi:10.1007/s00338-008-0444-x

    Article  Google Scholar 

  • Hoegh-Guldberg O (2014) Coral reef sustainability through adaptation: glimmer of hope or persistent mirage? Curr Opin Environ Sustain 7:127–133. doi:10.1016/j.cosust.2014.01.005

    Article  Google Scholar 

  • Holmes R, Aminot A, Kerouel R, Hooker B, Peterson B (1999) A simple and precise method for measuring ammonium in marine and freshwater ecosystems. Can J Fish Aquat Sci 56:1801–1808. doi:10.1139/cjfas-56-10-1801

    CAS  Article  Google Scholar 

  • Iglesias-Prieto R, Trench R (1994) Acclimation and adaption to irradiance in symbiotic dinoflagellates. 1. Responses of the photosynthetic unit to changes in photon flux-density. Mar Ecol Prog Ser 113:163–175. doi:10.3354/meps113163

    Article  Google Scholar 

  • Iglesias-Prieto R, Matta J, Robins W, Trench R (1992) Photosynthetic response to elevated temperature in the symbiotic dinoflagellate symbiodinium microadriaticum in culture. Proc Natl Acad Sci USA 89:10302–10305. doi:10.1073/pnas.89.21.10302

    CAS  Article  Google Scholar 

  • Jantzen C, Schmidt G, Wild C, Roder C, Khokiattiwong S, Richter C (2013) Benthic reef primary production in response to large amplitude internal waves at the Similan Islands (Andaman Sea, Thailand). PloS One 8. doi:10.1371/journal.pone.0081834

  • Khalaf MA, Kochzius M (2002) Changes in trophic community structure of shore fishes at an industrial site in the Gulf of Aqaba, Red Sea. Mar Ecol Prog Ser 239:287–299. doi:10.3354/meps239287

    Article  Google Scholar 

  • Kleypas J, McManus J, Menez L (1999) Environmental limits to coral reef development: where do we draw the line? Am Zool 39:146–159

    Article  Google Scholar 

  • Klumpp D, McKinnon A (1992) Community structure, biomass and productivity of epilithic algal communities on the Great Barrier Reef: dynamics at different spatial scales. Mar Ecol-Prog Ser 86:77–89. doi:10.3354/meps086077

    Article  Google Scholar 

  • Kremien M, Shavit U, Mass T, Genin A (2013) Benefit of pulsation in soft corals. Proc Natl Acad Sci USA 110:8978–8983. doi:10.1073/pnas.1301826110

    CAS  Article  Google Scholar 

  • Kubler J, Davison I (1993) High-temperature tolerance of photosynthesis in the red alga Chondrus crispus. Mar Biol 117:327–335. doi:10.1007/BF00345678

    Article  Google Scholar 

  • Larkum A, Koch E, Kuhl M (2003) Diffusive boundary layers and photosynthesis of the epilithic algal community of coral reefs. Mar Biol 142:1073–1082. doi:10.1007/s00227-003-1022-y

    CAS  Google Scholar 

  • Larned S (1998) Nitrogen- versus phosphorus-limited growth and sources of nutrients for coral reef macroalgae. Mar Biol 132:409–421. doi:10.1007/s002270050407

    Article  Google Scholar 

  • Lesser M, Mazel C, Gorbunov M, Falkowski P (2004) Discovery of symbiotic nitrogen-fixing cyanobacteria in corals. Science 305:997–1000. doi:10.1126/science.1099128

    CAS  Article  Google Scholar 

  • Levy O, Dubinsky Z, Schneider K, Achituv Y, Zakai D, Gorbunov MY (2004) Diurnal hysteresis in coral photosynthesis. Mar Ecol Prog Ser 268:105–117. doi:10.3354/meps268105

    Article  Google Scholar 

  • Littler MM, Littler DS, Brooks BL (2006) Harmful algae on tropical coral reefs: bottom-up eutrophication and top-down herbivory. Harmful Algae 5:565–585. doi:10.1016/j.hal.2005.11.003

    Article  Google Scholar 

  • Long S, Humphries S, Falkowski P (1994) Photoinhibition of photosynthesis in nature. Annu Rev Plant Phys 45:633–662. doi:10.1146/annurev.pp.45.060194.003221

    CAS  Article  Google Scholar 

  • Long M, Berg P, de Beer D, Zieman J (2013) In situ coral reef oxygen metabolism: an Eddy correlation study. PloS One 8. doi:10.1371/journal.pone.0058581

  • Loya Y, Genin A, el-Zibdeh M, Naumann M, Wild C (2014) Reviewing the status of coral reef ecology of the Red Sea: key topics and relevant research. Coral Reefs 33:1179–1180. doi:10.1007/s00338-014-1170-1

    Article  Google Scholar 

  • Montgomery D, Peck E, Vining G (2012) Diagnostics for leverage and influence. In: Introduction to linear regression analysis. Wiley, New York, pp 211–222

  • Murphy J, Riley J (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36

    CAS  Article  Google Scholar 

  • Nadon M, Stirling G (2006) Field and simulation analyses of visual methods for sampling coral cover. Coral Reefs 25:177–185. doi:10.1007/s00338-005-0074-5

    Article  Google Scholar 

  • Naumann M, Niggl W, Laforsch C, Glaser C, Wild C (2009) Coral surface area quantification-evaluation of established techniques by comparison with computer tomography. Coral Reefs 28:109–117. doi:10.1007/s00338-008-0459-3

    Article  Google Scholar 

  • Naumann M, Haas A, Struck U, Mayr C, El-Zibdah M, Wild C (2010) Organic matter release by dominant hermatypic corals of the Northern Red Sea. Coral Reefs 29:649–659. doi:10.1007/s00338-010-0612-7

    Article  Google Scholar 

  • Naumann M, Richter C, Mott C, el-Zibdah M, Manasrah R, Wild C (2012) Budget of coral-derived organic carbon in a fringing coral reef of the Gulf of Aqaba, Red Sea. J Mar Syst 105:20–29. doi:10.1016/j.jmarsys.2012.05.007

    Article  Google Scholar 

  • Naumann M, Jantzen C, Haas A, Iglesias-Prieto R, Wild C (2013) Benthic primary production budget of a Caribbean Reef Lagoon (Puerto Morelos, Mexico). PloS One 8. doi:10.1371/journal.pone.0082923

  • Naumann MS, Bednarz VN, Ferse SCA, Niggl W, Wild C (2015) Monitoring of coastal coral reefs near Dahab (Gulf of Aqaba, Red Sea) indicates local eutrophication as potential cause for change in benthic communities. Environ Monit Assess 187:14. doi:10.1007/s10661-014-4257-9

    Article  Google Scholar 

  • Odum H, Odum E (1955) Trophic structure and productivity of a windward coral reef community on Eniwetok Atoll. Ecol Monogr 25:291–320. doi:10.2307/1943285

    Article  Google Scholar 

  • Porter J, Muscatine L, Dubinsky Z, Falkowski P (1984) Primary production and photoadaptation in light-and shade-adapted colonies of the symbiotic coral, Stylophora pistillata. Proc R Soc Lond B Biol 222:161–180

    Article  Google Scholar 

  • Quinn GGP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Rasheed M, Badran MI, Richter C, Huettel M (2002) Effect of reef framework and bottom sediment on nutrient enrichment in a coral reef of the Gulf of Aqaba, Red Sea. Mar Ecol Prog Ser 239:277–285. doi:10.3354/meps239277

    Article  Google Scholar 

  • Rasheed M, Al-Trabeen K, Badran M (2012) Long-Term Water Quality Monitoring at an Industrial Site on the Northern Gulf of Aqaba, Red Sea. Mediterr Mar Sci 13:250–258

    Google Scholar 

  • R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/

  • Richter C, Wunsch M, Rasheed M, Kotter I, Badran M (2001) Endoscopic exploration of Red Sea coral reefs reveals dense populations of cavity-dwelling sponges. Nature 413:726–730. doi:10.1038/35099547

    CAS  Article  Google Scholar 

  • Rix L, Bednarz VN, Cardini U, van Hoytema N, Al-Horani FA, Wild C, Naumann MS (2015) Seasonality in dinitrogen fixation and primary productivity by coral reef framework substrates from the northern Red Sea. Coral Reefs 533:79–92

    CAS  Google Scholar 

  • Samiei J, Saleh A, Mehdinia A, Shirvani A, Kayal M (2015) Photosynthetic response of Persian Gulf acroporid corals to summer versus winter temperature deviations. Peer J 3. doi:10.7717/peerj.1062

  • Schlichter D, Svoboda A, Kremer B (1983) Functional autotrophy of Heteroxenia fuscescens (Anthozoa: Alcyonaria): carbon assimilation and translocation of photosynthates from symbionts to host. Mar Biol 78:29–38. doi:10.1007/BF00392968

    CAS  Article  Google Scholar 

  • Schneider K, Levy O, Dubinsky Z, Erez J (2009) In situ diel cycles of photosynthesis and calcification in hermatypic corals. Limnol Oceanogr 54:1995–2002. doi:10.4319/lo.2009.54.6.1995

    Article  Google Scholar 

  • Schneider C, Rasband W, Eliceiri K (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675. doi:10.1038/nmeth.2089

    CAS  Article  Google Scholar 

  • Schöttner S, Pfitzner B, Grunke S, Rasheed M, Wild C, Ramette A (2011) Drivers of bacterial diversity dynamics in permeable carbonate and silicate coral reef sands from the Red Sea. Environ Microbiol 13:1815–1826. doi:10.1111/j.1462-2920.2011.02494.x

    Article  Google Scholar 

  • Schrameyer V, Wangpraseurt D, Hill R, Kuhl M, Larkum A, Ralph P (2014) Light respiratory processes and gross photosynthesis in two scleractinian corals. PloS One 9. doi:10.1371/journal.pone.0110814

  • Silverman J, Lazar B, Erez J (2007) Community metabolism of a coral reef exposed to naturally varying dissolved inorganic nutrient loads. Biogeochemistry 84:67–82. doi:10.1007/s10533-007-9075-5

    CAS  Article  Google Scholar 

  • Smith J, Price N, Nelson C, Haas A (2013) Coupled changes in oxygen concentration and pH caused by metabolism of benthic coral reef organisms. Mar Biol 160:2437–2447. doi:10.1007/s00227-013-2239-z

    CAS  Article  Google Scholar 

  • Sorokin Y (1991) Biomass, metabolic rates and feeding of some common reef zoantharians an octocorals. Aust J Mar Fresh Res 42:729–741

    Article  Google Scholar 

  • Stambler N (2011) Zooxanthellae: the yellow symbionts inside animals. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition. Springer, Netherlands, pp 87–106

    Chapter  Google Scholar 

  • Strickland J, Parsons T (1968) A practical handbook of seawater analysis. Queens Printer, Ottawa

    Google Scholar 

  • Tilot V, Leujak W, Ormond RFG, Ashworth JA, Mabrouk A (2008) Monitoring of South Sinai coral reefs: influence of natural and anthropogenic factors. Aquat Conserv 18:1109–1126. doi:10.1002/aqc.942

    Article  Google Scholar 

  • Titlyanov E (1991) The stable level of coral primary production in a wide light range. Hydrobiologia 216:383–387. doi:10.1007/BF00026490

    Article  Google Scholar 

  • Titlyanov E, Titlyanova T (2012) Marine plants in a coral reef ecosystem. Russ J Mar Biol 38:201–210. doi:10.1134/S1063074012030133

    CAS  Article  Google Scholar 

  • Valiela I (1984) Marine ecological processes. Springer, New York

    Book  Google Scholar 

  • Veron JEN (2000) Corals of the world. Australian Institute of Marine science, Townsville

    Google Scholar 

  • Wijgerde T, Jurriaans S, Hoofd M, Verreth J, Osinga R (2012) Oxygen and heterotrophy affect calcification of the scleractinian coral galaxea fascicularis. PloS One 7. doi:10.1371/journal.pone.0052702

  • Wild C, Naumann M (2013) Effect of active water movement on energy and nutrient acquisition in coral reef-associated benthic organisms. Proc Natl Acad Sci USA 110:8767–8768. doi:10.1073/pnas.1306839110

    CAS  Article  Google Scholar 

  • Wild C, Laforsch C, Huettel M (2006) Detection and enumeration of microbial cells within highly porous calcareous reef sands. Mar Freshw Res 57:415–420. doi:10.1071/MF05205

    Article  Google Scholar 

  • Winters G, Beer S, Ben Zvi B, Brickner I, Loya Y (2009) Spatial and temporal photoacclimation of Stylophora pistillata: zooxanthella size, pigmentation, location and clade. Mar Ecol Prog Ser 384:107–119. doi:10.3354/meps08036

    Article  Google Scholar 

  • Wooldridge S (2010) Is the coral-algae symbiosis really ‘mutually beneficial’ for the partners? (vol 32, pg 615, 2010). BioEssays 32:1106. doi:10.1002/bies.201090060

    CAS  Article  Google Scholar 

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Acknowledgments

We would like to thank L. Rix, S. Helber, and S. Basyoni for fieldwork assistance and logistical support, as well as C. Staschok and M. Birkicht for fieldwork preparation and nutrient sample analyses, K. Boos for statistical assistance, and R. M. van der Ven for comments on the manuscript. This work was funded by German Research Foundation (DFG) grant Wi 2677/6-1 to C.W.

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Correspondence to Nanne van Hoytema.

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van Hoytema, N., Bednarz, V.N., Cardini, U. et al. The influence of seasonality on benthic primary production in a Red Sea coral reef. Mar Biol 163, 52 (2016). https://doi.org/10.1007/s00227-015-2787-5

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Keywords

  • Coral Reef
  • Macroalgae
  • Gross Primary Production
  • Hard Coral
  • Soft Coral