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.
Similar content being viewed by others
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
Adey W, Steneck R (1985) Highly productive eastern Caribbean reefs: synergistic effects of biological, chemical, physical, and geological factors. NOAA Undersea Research Program, Rockville
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Carpenter R (1985) Relationships between primary production and irradiance in coral reef algal communities. Limnol Oceanogr 30:784–793
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
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
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
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
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
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
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
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
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
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
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
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
Grottoli A, Rodrigues L, Palardy J (2006) Heterotrophic plasticity and resilience in bleached corals. Nature 440:1186–1189. doi:10.1038/nature04565
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
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
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
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
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
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
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
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
Kleypas J, McManus J, Menez L (1999) Environmental limits to coral reef development: where do we draw the line? Am Zool 39:146–159
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Quinn GGP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge
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
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
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
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
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
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
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
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
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
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
Sorokin Y (1991) Biomass, metabolic rates and feeding of some common reef zoantharians an octocorals. Aust J Mar Fresh Res 42:729–741
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
Strickland J, Parsons T (1968) A practical handbook of seawater analysis. Queens Printer, Ottawa
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
Titlyanov E (1991) The stable level of coral primary production in a wide light range. Hydrobiologia 216:383–387. doi:10.1007/BF00026490
Titlyanov E, Titlyanova T (2012) Marine plants in a coral reef ecosystem. Russ J Mar Biol 38:201–210. doi:10.1134/S1063074012030133
Valiela I (1984) Marine ecological processes. Springer, New York
Veron JEN (2000) Corals of the world. Australian Institute of Marine science, Townsville
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
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
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
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
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.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: F. Weinberger.
Reviewed by M. Al-Zibdeh, M. Ziegler.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00227-015-2787-5