Evaluating coral trophic strategies using fatty acid composition and indices

English version

Autoři: Veronica Z. Radice ^aff001; Michael T. Brett ^aff003; Brian Fry ^aff004; Michael D. Fox ^aff005; Ove Hoegh-Guldberg ^aff001; Sophie G. Dove ^aff001
Působiště autorů: Australian Research Council Centre of Excellence for Coral Reef Studies, The University of Queensland, St. Lucia, Queensland, Australia ^aff001; School of Biological Sciences, The University of Queensland, St. Lucia, Queensland, Australia ^aff002; Department of Civil and Environmental Engineering, University of Washington, Seattle, Washington, United States of America ^aff003; Australian Rivers Institute, Griffith University, Nathan, Queensland, Australia ^aff004; Department of Geology and Geophysics, Woods Hole Oceanographic Institution, Woods Hole, Massachusetts, United States of America ^aff005
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0222327

Souhrn

The ecological success of shallow water reef-building corals has been linked to the symbiosis between the coral host and its dinoflagellate symbionts (herein ‘symbionts’). As mixotrophs, symbiotic corals depend on nutrients 1) transferred from their photosynthetic symbionts (autotrophy) and 2) acquired by host feeding on particulate organic resources (heterotrophy). However, coral species differ in the extent to which they depend on heterotrophy for nutrition and these differences are typically poorly defined. Here, a multi-tracer fatty acid approach was used to evaluate the trophic strategies of three species of common reef-building coral (Galaxea fascicularis, Pachyseris speciosa, and Pocillopora verrucosa) whose trophic strategies had previously been identified using carbon stable isotopes. The composition and various indices of fatty acids were compared to examine the relative contribution of symbiont autotrophy and host heterotrophy in coral energy acquisition. A linear discriminant analysis (LDA) was used to estimate the contribution of polyunsaturated fatty acids (PUFA) derived from various potential sources to the coral hosts. The total fatty acid composition and fatty acid indices revealed differences between the more heterotrophic (P. verrucosa) and more autotrophic (P. speciosa) coral hosts, with the coral host G. fascicularis showing overlap with the other two species and greater variability overall. For the more heterotrophic P. verrucosa, the fatty acid indices and LDA results both indicated a greater proportion of copepod-derived fatty acids compared to the other coral species. Overall, the LDA estimated that PUFA derived from particulate resources (e.g., copepods and diatoms) comprised a greater proportion of coral host PUFA in contrast to the lower proportion of symbiont-derived PUFA. These estimates provide insight into the importance of heterotrophy in coral nutrition, especially in productive reef systems. The study supports carbon stable isotope results and demonstrates the utility of fatty acid analyses for exploring the trophic strategies of reef-building corals.

Klíčová slova:

Biology and life sciences – Biochemistry – Lipids – Fatty acids – Marine biology – Corals – Coral reefs – Microbiology – Medical microbiology – Microbial pathogens – Fungal pathogens – Phialophora verrucosa – Mycology – Species interactions – Symbiosis – Organisms – Eukaryota – Animals – Invertebrates – Arthropoda – Crustaceans – Copepods – Earth sciences – Marine and aquatic sciences – Reefs – Medicine and health sciences – Pathology and laboratory medicine – Pathogens – Research and analysis methods – Mathematical and statistical techniques – Statistical methods – Linear discriminant analysis – Physical sciences – Mathematics – Statistics – Materials science – Materials – Mixtures – Particulates

Zdroje

1. Frankowiak K, Wang XT, Sigman DM, Gothmann AM, Kitahara M V., Mazur M, et al. Photosymbiosis and the expansion of shallow-water corals. Sci Adv. American Association for the Advancement of Science; 2016;2: e1601122–e1601122. doi: 10.1126/sciadv.1601122 27847868

2. Goreau TF, Goreau NI, Yonge CM. Reef corals: autotrophs or heterotrophs? Biol Bull. 1971;141: 247–260. Available: http://www.biolbull.org/content/141/2/247.short

3. Muscatine L, Porter JW, Kaplan IR. Resource partitioning by reef corals as determined from stable isotope composition: I. d13C of zooxanthellae and animal tissue vs depth. Mar Biol. 1989;100: 185–193. doi: 10.1007/BF00391957

4. Anthony KR., Fabricius KE. Shifting roles of heterotrophy and autotrophy in coral energetics under varying turbidity. J Exp Mar Bio Ecol. 2000;252: 221–253. doi: 10.1016/S0022-0981(00)00237-9 10967335

5. Houlbrèque F, Ferrier-Pagès C. Heterotrophy in tropical scleractinian corals. Biol Rev Camb Philos Soc. 2009;84: 1–17. doi: 10.1111/j.1469-185X.2008.00058.x 19046402

6. Houlbrèque F, Tambutté E, Allemand D, Ferrier-Pagès C. Interactions between zooplankton feeding, photosynthesis and skeletal growth in the scleractinian coral Stylophora pistillata. J Exp Biol. The Company of Biologists Ltd; 2004;207: 1461–9. doi: 10.1242/JEB.00911 15037640

7. Hoegh-Guldberg O, Williamson J. Availability of two forms of dissolved nitrogen to the coral Pocillopora damicornis and its symbiotic zooxanthellae. Mar Biol. 1999; Available: http://link.springer.com/article/10.1007/s002270050496

8. Palardy JE, Rodrigues LJ, Grottoli AG. The importance of zooplankton to the daily metabolic carbon requirements of healthy and bleached corals at two depths. J Exp Mar Bio Ecol. 2008;367: 180–188. doi: 10.1016/j.jembe.2008.09.015

9. Rodrigues LJ, Grottoli AG, Pease TK. Lipid class composition of bleached and recovering Porites compressa Dana, 1846 and Montipora capitata Dana, 1846 corals from Hawaii. J Exp Mar Bio Ecol. 2008;358: 136–143. doi: 10.1016/j.jembe.2008.02.004

10. Harland AD, Navarro JC, Spencer Davies P, Fixter LM. Lipids of some Caribbean and Red Sea corals: total lipid, wax esters, triglycerides and fatty acids. Mar Biol. Springer-Verlag; 1993;117: 113–117. doi: 10.1007/BF00346432

11. Tolosa I, Treignier C, Grover R, Ferrier-Pagès C. Impact of feeding and short-term temperature stress on the content and isotopic signature of fatty acids, sterols, and alcohols in the scleractinian coral Turbinaria reniformis. Coral Reefs. Springer-Verlag; 2011;30: 763–774. doi: 10.1007/s00338-011-0753-3

12. Treignier C, Grover R, Ferrier-Pagès C, Tolosa I. Effect of light and feeding on the fatty acid and sterol composition of zooxanthellae and host tissue isolated from the scleractinian coral Turbinaria reniformis. Limnol Oceanogr. 2008;53: 2702–2710. doi: 10.4319/lo.2008.53.6.2702

13. Teece MA, Estes B, Gelsleichter E, Lirman D. Heterotrophic and autotrophic assimilation of fatty acids by two scleractinian corals, Montastraea faveolata and Porites astreoides. Limnol Oceanogr. 2011;56: 1285–1296. doi: 10.4319/lo.2011.56.4.1285

14. Gurr MI, Harwood JL, Frayn KN. Lipid biochemistry. 5th ed. Blackwell Science; 2002. doi: 10.1002/9780470774366

15. Furla P, Allemand D, Shick JM, Ferrier-Pagès C, Richier S, Plantivaux A, et al. The Symbiotic Anthozoan: A Physiological Chimera between Alga and Animal. Integr Comp Biol. Oxford University Press; 2005;45: 595–604. doi: 10.1093/icb/45.4.595 21676806

16. Patton JS, Abraham S, Benson AA. Lipogenesis in the intact coral Pocillopora capitata and its isolated zooxanthellae: Evidence for a light-driven carbon cycle between symbiont and host. Mar Biol. Springer-Verlag; 1977;44: 235–247. doi: 10.1007/BF00387705

17. Chen H-K, Song S-N, Wang L-H, Mayfield AB, Chen Y-J, Chen W-NU, et al. A Compartmental Comparison of Major Lipid Species in a Coral-Symbiodinium Endosymbiosis: Evidence that the Coral Host Regulates Lipogenesis of Its Cytosolic Lipid Bodies. Pond DW, editor. PLoS One. Public Library of Science; 2015;10: e0132519. doi: 10.1371/journal.pone.0132519 26218797

18. Wang L-H, Chen H-K, Jhu C-S, Cheng J-O, Fang L-S, Chen C-S. Different strategies of energy storage in cultured and freshly isolated Symbiodinium sp. Cock M, editor. J Phycol. Wiley/Blackwell (10.1111); 2015;51: 1127–1136. doi: 10.1111/jpy.12349 26987007

19. Jeong H, Yoo Y, Kang N, Lim A, Seong K, Lee S, et al. Heterotrophic feeding as a newly identified survival strategy of the dinoflagellate Symbiodinium. Proc Natl Acad Sci. 2012;109: 12604–12609. doi: 10.1073/pnas.1204302109 22814379

20. Lesser MP, Stat M, Gates RD. The endosymbiotic dinoflagellates (Symbiodinium sp.) of corals are parasites and mutualists. Coral Reefs. Springer Berlin Heidelberg; 2013;32: 603–611. doi: 10.1007/s00338-013-1051-z

21. Xiang T, Hambleton EA, DeNofrio JC, Pringle JR, Grossman AR. Isolation of clonal axenic strains of the symbiotic dinoflagellate Symbiodinium and their growth and host specificity. J Phycol. 2013;49: 447–458. doi: 10.1111/jpy.12055 27007034

22. Kabeya N, Fonseca MM, Ferrier DEK, Navarro JC, Bay LK, Francis DS, et al. Genes for de novo biosynthesis of omega-3 polyunsaturated fatty acids are widespread in animals. Sci Adv. American Association for the Advancement of Science; 2018;4: EAAR6849. doi: 10.1126/sciadv.aar6849 29732410

23. Monroig Ó, Tocher D, Navarro J. Biosynthesis of Polyunsaturated Fatty Acids in Marine Invertebrates: Recent Advances in Molecular Mechanisms. Mar Drugs. Multidisciplinary Digital Publishing Institute; 2013;11: 3998–4018. doi: 10.3390/md11103998 24152561

24. Monroig Ó, Kabeya N. Desaturases and elongases involved in polyunsaturated fatty acid biosynthesis in aquatic invertebrates: a comprehensive review. Fish Sci. Springer Japan; 2018;84: 911–928. doi: 10.1007/s12562-018-1254-x

25. Dunn SR, Thomas MC, Nette GW, Dove SG. A Lipidomic Approach to Understanding Free Fatty Acid Lipogenesis Derived from Dissolved Inorganic Carbon within Cnidarian-Dinoflagellate Symbiosis. Voolstra CR, editor. PLoS One. Public Library of Science; 2012;7: e46801. doi: 10.1371/journal.pone.0046801 23115631

26. Papina M, Meziane T, van Woesik R. Symbiotic zooxanthellae provide the host-coral Montipora digitata with polyunsaturated fatty acids. Comp Biochem Physiol Part B Biochem Mol Biol. 2003;135: 533–7. Available: http://dx.doi.org/10.1016/S1096-4959(03)00118-0

27. Imbs AB, Yakovleva IM, Dautova TN, Bui LH, Jones P. Diversity of fatty acid composition of symbiotic dinoflagellates in corals: Evidence for the transfer of host PUFAs to the symbionts. Phytochemistry. Pergamon; 2014;101: 76–82. doi: 10.1016/j.phytochem.2014.02.012 24612930

28. Meyers PA. Polyunsaturated fatty acids in corals: indicators of nutritional sources. Mar Biol Lett. 1979;1: 69–75.

29. Galloway AWE, Winder M. Partitioning the Relative Importance of Phylogeny and Environmental Conditions on Phytoplankton Fatty Acids. Quigg A, editor. PLoS One. Public Library of Science; 2015;10: e0130053. doi: 10.1371/journal.pone.0130053 26076015

30. Brett MT, Müller-Navarra DC, Persson J. Crustacean zooplankton fatty acid composition. Lipids in Aquatic Ecosystems. New York, NY: Springer New York; 2009. pp. 115–146. doi: 10.1007/978-0-387-89366-2_6

31. Imbs AB, Demidkova DA, Latypov YY, Pham LQ. Application of Fatty Acids for Chemotaxonomy of Reef-Building Corals. Lipids. 2007;42: 1035–1046. doi: 10.1007/s11745-007-3109-6 17710463

32. Imbs A, Latyshev N, Dautova T, Latypov Y. Distribution of lipids and fatty acids in corals by their taxonomic position and presence of zooxanthellae. Mar Ecol Prog Ser. 2010;409: 65–75. doi: 10.3354/meps08622

33. Budge SM, Iverson SJ, Koopman HN. Studying trophic ecology in marine ecosystems using fatty acids: a primer on analysis and interpretation. Mar Mammal Sci. Wiley/Blackwell (10.1111); 2006;22: 759–801. doi: 10.1111/j.1748-7692.2006.00079.x

34. Tagliafico A, Rudd D, Rangel M, Kelaher B, Christidis L, Cowden K, et al. Lipid-enriched diets reduce the impacts of thermal stress in corals. Mar Ecol Prog Ser. 2017;573: 129–141. doi: 10.3354/meps12177

35. Dalsgaard J, St John M, Kattner G, Müller-Navarra D, Hagen W. Fatty acid trophic markers in the pelagic marine environment. Adv Mar Biol. 2003;46: 225–340. Available: http://www.ncbi.nlm.nih.gov/pubmed/14601414 14601414

36. Schukat A, Auel H, Teuber L, Lahajnar N, Hagen W. Complex trophic interactions of calanoid copepods in the Benguela upwelling system. J Sea Res. Elsevier; 2014;85: 186–196. doi: 10.1016/J.SEARES.2013.04.018

37. Graeve M, Kattner G, Piepenburg D. Lipids in Arctic benthos: does the fatty acid and alcohol composition reflect feeding and trophic interactions? Polar Biol. Springer-Verlag; 1997;18: 53–61. doi: 10.1007/s003000050158

38. Mansour MP, Volkman JK, Jackson AE, Blackburn SI. THE FATTY ACID AND STEROL COMPOSITION OF FIVE MARINE DINOFLAGELLATES. J Phycol. John Wiley & Sons, Ltd (10.1111); 1999;35: 710–720. doi: 10.1046/j.1529-8817.1999.3540710.x

39. Matthews JL, Oakley CA, Lutz A, Hillyer KE, Roessner U, Grossman AR, et al. Partner switching and metabolic flux in a model cnidarian–dinoflagellate symbiosis. Proc R Soc B Biol Sci. The Royal Society; 2018;285: 20182336. doi: 10.1098/rspb.2018.2336 30487315

40. Sargent JR, Falk-Petersen S. Ecological investigations on the zooplankton community in balsfjorden, northern Norway: Lipids and fatty acids in Meganyctiphanes norvegica, Thysanoessa raschi and T. inermis during mid-winter. Mar Biol. Springer-Verlag; 1981;62: 131–137. doi: 10.1007/BF00388175

41. Kattner G, Hagen W. Lipids in marine copepods: latitudinal characteristics and perspective to global warming. Lipids in Aquatic Ecosystems. New York, NY: Springer New York; 2009. pp. 257–280. doi: 10.1007/978-0-387-89366-2_11

42. Latyshev NA, Naumenko N V., Svetashev VI, Latypov YY. Fatty acids of reef-building corals. Mar Ecol Prog Ser. 1991;76: 295–301. Available: http://www.int-res.com/articles/meps/76/m076p295.pdf

43. Al-Moghrabi S, Allemand D, Couret JM, Jaubert J. Fatty acids of the scleractinian coral Galaxea fascicularis: effect of light and feeding. J Comp Physiol B. 1995;165: 183–192. doi: 10.1007/BF00260809

44. Mortillaro JM, Pitt KA, Lee SY, Meziane T. Light intensity influences the production and translocation of fatty acids by zooxanthellae in the jellyfish Cassiopea sp. J Exp Mar Bio Ecol. Elsevier; 2009;378: 22–30. doi: 10.1016/J.JEMBE.2009.07.003

45. Dodds L, Black K, Orr H, Roberts J. Lipid biomarkers reveal geographical differences in food supply to the cold-water coral Lophelia pertusa (Scleractinia). Mar Ecol Prog Ser. 2009;397: 113–124. doi: 10.3354/meps08143

46. Sebens KP, Vandersall KS, Savina LA, Graham KR. Zooplankton capture by two scleractinian corals, Madracis mirabilis and Montastrea cavernosa, in a field enclosure. Mar Biol. 1996;127: 303–317. doi: 10.1007/BF00942116

47. Rocker MM, Francis DS, Fabricius KE, Willis BL, Bay LK. Temporal and spatial variation in fatty acid composition in Acropora tenuis corals along water quality gradients on the Great Barrier Reef, Australia. Coral Reefs. Springer Berlin Heidelberg; 2019; 1–14. doi: 10.1007/s00338-019-01768-x

48. Morales-Ramírez A, Murillo MM. Distribution, abundance and composition of coral reef zooplankton, Cahuita National Park, Limon, Costa Rica. Rev Biol Trop. 1996;44: 619–630. doi: 10.15517/rbt.v44i3.30924

49. Nakajima R, Yamazaki H, Lewis LS, Khen A, Smith JE, Nakatomi N, et al. Planktonic trophic structure in a coral reef ecosystem–Grazing versus microbial food webs and the production of mesozooplankton. Prog Oceanogr. 2017;156: 104–120. doi: 10.1016/j.pocean.2017.06.007

50. Radice VZ, Hoegh‐Guldberg O, Fry B, Fox MD, Dove SG. Upwelling as the major source of nitrogen for shallow and deep reef‐building corals across an oceanic atoll system. Dorrepaal E, editor. Funct Ecol. 2019; 1635–2435.13314. doi: 10.1111/1365-2435.13314

51. Meyers PA, Porter JW, Chad RL. Depth analysis of fatty acids in two caribbean reef corals. Mar Biol. Springer-Verlag; 1978;49: 197–202. doi: 10.1007/BF00391131

52. Ferrier-Pagès C, Rottier C, Beraud E, Levy O. Experimental assessment of the feeding effort of three scleractinian coral species during a thermal stress: Effect on the rates of photosynthesis. J Exp Mar Bio Ecol. 2010;390: 118–124. doi: 10.1016/j.jembe.2010.05.007

53. Folch J, Lees M, Sloane Stanley GH. A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem. 1957;226: 497–509. Available: http://www.ncbi.nlm.nih.gov/pubmed/13428781 13428781

54. Taipale S, Strandberg U, Peltomaa E, Galloway A, Ojala A, Brett M. Fatty acid composition as biomarkers of freshwater microalgae: analysis of 37 strains of microalgae in 22 genera and in seven classes. Aquat Microb Ecol. 2013;71: 165–178. doi: 10.3354/ame01671

55. Taipale SJ, Kainz MJ, Brett MT. Diet-switching experiments show rapid accumulation and preferential retention of highly unsaturated fatty acids in Daphnia. Oikos. Blackwell Publishing Ltd; 2011;120: 1674–1682. doi: 10.1111/j.1600-0706.2011.19415.x

56. Lowe A. Local ecological modulation of global environmental change and its influence on benthic foundation species. University of Washington. 2018.

57. Howell KL, Pond DW, Billett DSM, Tyler PA. Feeding ecology of deep-sea seastars (Echinodermata: Asteroidea): a fatty-acid biomarker approach. Mar Ecol Prog Ser. 2003;255: 193–206.

58. R-Core-Team. R: A Language and Environment for Statistical Computing [Internet]. Vienna, Austria: R Foundation for Statistical Computing; 2018. Available: https://www.r-project.org

59. Le S, Josse J, Husson F. FactoMineR: An R Package for Multivariate Analysis. J Stat Softw. 2008;25: 1–18. doi: 10.18637/jss.v025.i01

60. Kassambara A, Mundt F. factoextra: Extract and Visualize the Results of Multivariate Data Analyses [Internet]. 2017. Available: https://cran.r-project.org/package=factoextra

61. Stanca E, Roselli L, Durante G, Seveso D, Galli P, Basset A. A checklist of phytoplankton species in the Faafu atoll (Republic of Maldives). Transitional Waters Bull. 2013;7: 133–144. doi: 10.1285/I1825229XV7N2P133

62. Venables WN, Ripley BD. Modern Applied Statistics with S. Fourth. New York: Springer; 2002.

63. Fox MD, Smith EA, Smith JE, Newsome SD. Trophic plasticity in a common reef-building coral: Insights from d13C analysis of essential amino acids (Accepted). Funct Ecol. 2019;

64. Leal MC, Hoadley K, Pettay DT, Grajales A, Calado R, Warner ME. Symbiont type influences trophic plasticity of a model cnidarian-dinoflagellate symbiosis. J Exp Biol. 2015;218: 858–63. doi: 10.1242/jeb.115519 25617454

65. Matthews JL, Crowder CM, Oakley CA, Lutz A, Roessner U, Meyer E, et al. Optimal nutrient exchange and immune responses operate in partner specificity in the cnidarian-dinoflagellate symbiosis. Proc Natl Acad Sci U S A. National Academy of Sciences; 2017;114: 13194–13199. doi: 10.1073/pnas.1710733114 29158383

66. Schlichter D, Kremer BP, Svoboda A. Zooxanthellae providing assimilatory power for the incorporation of exogenous acetate in Heteroxenia fuscescens (Cnidaria: Alcyonaria). Mar Biol. Springer-Verlag; 1984;83: 277–286. doi: 10.1007/BF00397460

67. Séré MG, Massé LM, Perissinotto R, Schleyer MH. Influence of heterotrophic feeding on the sexual reproduction of Pocillopora verrucosa in aquaria. J Exp Mar Bio Ecol. Elsevier; 2010;395: 63–71. doi: 10.1016/J.JEMBE.2010.08.014

68. Hoogenboom M, Rottier C, Sikorski S, Ferrier-Pagès C. Among-species variation in the energy budgets of reef-building corals: scaling from coral polyps to communities. J Exp Biol. 2015;218: 3866–77. doi: 10.1242/jeb.124396 26486359

69. Lim C-S, Bachok Z, Hii Y-S. Effects of supplementary polyunsaturated fatty acids on the health of the scleractinian coral Galaxea fascicularis (Linnaeus, 1767). J Exp Mar Bio Ecol. 2017;491: 1–8. doi: 10.1016/j.jembe.2017.02.009

70. Figueiredo C, Baptista M, Rosa IC, Lopes AR, Dionísio G, Rocha RJM, et al. 3D chemoecology and chemotaxonomy of corals using fatty acid biomarkers: Latitude, longitude and depth. Biochem Syst Ecol. Pergamon; 2017;70: 35–42. doi: 10.1016/J.BSE.2016.10.016

71. Cooper TF, Ulstrup KE, Dandan SS, Heyward AJ, Kühl M, Muirhead A, et al. Niche specialization of reef-building corals in the mesophotic zone: metabolic trade-offs between divergent Symbiodinium types. Proc Biol Sci. The Royal Society; 2011;278: 1840–50. doi: 10.1098/rspb.2010.2321 21106586

72. Browne N, Precht E, Last K, Todd P. Photo-physiological costs associated with acute sediment stress events in three near-shore turbid water corals. Mar Ecol Prog Ser. 2014;502: 129–143. doi: 10.3354/meps10714

73. Tremblay P, Maguer JF, Grover R, Ferrier-Pagès C. Trophic dynamics of scleractinian corals: stable isotope evidence. J Exp Biol. 2015;218: 1223–34. doi: 10.1242/jeb.115303 25722004

74. Leray M, Alldredge AL, Yang JY, Meyer CP, Holbrook SJ, Schmitt RJ, et al. Dietary partitioning promotes the coexistence of planktivorous species on coral reefs. Mol Ecol. John Wiley & Sons, Ltd (10.1111); 2019; mec.15090. doi: 10.1111/mec.15090

75. Fox MD, Williams GJ, Johnson MD, Radice VZ, Zgliczynski BJ, Kelly ELA, et al. Gradients in Primary Production Predict Trophic Strategies of Mixotrophic Corals across Spatial Scales. Curr Biol. Cell Press; 2018;28: 3355–3363.e4. doi: 10.1016/J.CUB.2018.08.057

76. Anderson R, Adam M, Goes J. From monsoons to mantas: seasonal distribution of Manta alfredi in the Maldives. Fish Oceanogr. 2011;20: 104–113. doi: 10.1111/j.1365-2419.2011.00571.x

77. Vinogradov ME, Voronina N. The distribution of different groups of plankton in accordance with their trophic level in the Indian Equatorial Current Area (No. 33). Raport et Proces- Verbaux des Reunions (Vol 153). 1962. pp. 200–205.

78. Papina M, Meziane T, van Woesik R. Acclimation effect on fatty acids of the coral Montipora digitata and its symbiotic algae. Comp Biochem Physiol Part B Biochem Mol Biol. 2007;147: 583–589. doi: 10.1016/j.cbpb.2007.02.011

79. Grottoli AG, Rodrigues LJ, Palardy JE. Heterotrophic plasticity and resilience in bleached corals. Nature. 2006;440: 1186–9. doi: 10.1038/nature04565 16641995

80. Stafford-Smith M, Ormond R. Sediment-rejection mechanisms of 42 species of Australian scleractinian corals. Mar Freshw Res. 1992;43: 683. doi: 10.1071/MF9920683

81. Wijgerde T, Diantari R, Lewaru MW, Verreth JAJ, Osinga R. Extracoelenteric zooplankton feeding is a key mechanism of nutrient acquisition for the scleractinian coral Galaxea fascicularis. J Exp Biol. 2011;214: 3351–7. doi: 10.1242/jeb.058354 21957098

82. Leonilde R, Elena L, Elena S, Francesco C, Alberto B. Individual trait variation in phytoplankton communities across multiple spatial scales. J Plankton Res. Oxford University Press; 2017;39: 577–588. doi: 10.1093/plankt/fbx001

83. Ayukai T. Retention of phytoplankton and planktonic microbes on coral reefs within the Great Barrier Reef, Australia. Coral Reefs. Springer-Verlag; 1995;14: 141–147. doi: 10.1007/BF00367231

84. Genin A, Monismith SG, Reidenbach MA, Yahel G, Koseff JR. Intense benthic grazing of phytoplankton in a coral reef. Limnol Oceanogr. John Wiley & Sons, Ltd; 2009;54: 938–951. doi: 10.4319/lo.2009.54.3.0938

85. Glynn PW. Ecology of a Caribbean coral reef. The Porites reef-flat biotope: Part II. Plankton community with evidence for depletion. Mar Biol. Springer-Verlag; 1973;22: 1–21. doi: 10.1007/BF00388905

86. de Goeij JM, Moodley L, Houtekamer M, Carballeira NM, van Duyl FC. Tracing 13C-enriched dissolved and particulate organic carbon in the bacteria-containing coral reef sponge Halisarca caerulea: Evidence for DOM-feeding. Limnol Oceanogr. John Wiley & Sons, Ltd; 2008;53: 1376–1386. doi: 10.4319/lo.2008.53.4.1376

87. Seemann J, Carballo-Bolaños R, Berry KL, González CT, Richter C, Leinfelder RR. Importance of heterotrophic adaptations of corals to maintain energy reserves. Proceedings of the 12th International Coral Reef Symposium. 2012. pp. 1–6.

88. Leal MC, Ferrier-Pagès C, Calado R, Thompson ME, Frischer ME, Nejstgaard JC. Coral feeding on microalgae assessed with molecular trophic markers. Mol Ecol. 2014;23: 3870–3876. doi: 10.1111/mec.12486 24112432

89. Hughes AD, Grottoli AG. Heterotrophic compensation: a possible mechanism for resilience of coral reefs to global warming or a sign of prolonged stress? PLoS One. 2013;8: e81172. doi: 10.1371/journal.pone.0081172 24278392

90. Wilken S, Huisman J, Naus-Wiezer S, Van Donk E. Mixotrophic organisms become more heterotrophic with rising temperature. Fussmann G, editor. Ecol Lett. John Wiley & Sons, Ltd (10.1111); 2013;16: 225–233. doi: 10.1111/ele.12033 23173644

91. Tremblay P, Gori A, Maguer JF, Hoogenboom M, Ferrier-Pagès C. Heterotrophy promotes the re-establishment of photosynthate translocation in a symbiotic coral after heat stress. Sci Rep. Nature Publishing Group; 2016;6: 38112. doi: 10.1038/srep38112 27917888

92. Quesada A, Schoo K, Bingham B. Effect of symbiotic state on the fatty acid composition of Anthopleura elegantissima. Mar Ecol Prog Ser. 2016;545: 175–187. doi: 10.3354/meps11606

93. Grottoli AG, Rodrigues LJ, Juarez C. Lipids and stable carbon isotopes in two species of Hawaiian corals, Porites compressa and Montipora verrucosa, following a bleaching event. Mar Biol. Springer-Verlag; 2004;145: 621–631. doi: 10.1007/s00227-004-1337-3

94. Ibrahim N, Mohamed M, Basheer A, Ismail H, Nistharan F, Schmidt A, et al. Status of Coral Bleaching in the Maldives in 2016. Malé, Maldives; 2017.

95. Bachok Z, Mfilinge P, Tsuchiya M. Characterization of fatty acid composition in healthy and bleached corals from Okinawa, Japan. Coral Reefs. Springer-Verlag; 2006;25: 545–554. doi: 10.1007/s00338-006-0130-9

96. Gierz SL, Forêt S, Leggat W. Transcriptomic Analysis of Thermally Stressed Symbiodinium Reveals Differential Expression of Stress and Metabolism Genes. Front Plant Sci. Frontiers; 2017;8: 271. doi: 10.3389/fpls.2017.00271 28293249

97. Schoepf V, Grottoli AG, Levas SJ, Aschaffenburg MD, Baumann JH, Matsui Y, et al. Annual coral bleaching and the long-term recovery capacity of coral. Proc R Soc London B Biol Sci. 2015;282: 20151887.

Evaluating coral trophic strategies using fatty acid composition and indices

Souhrn

Klíčová slova:

Zdroje

PLOS One

INSIGHTS from European Respiratory Congress

Současné pohledy na riziko v parodontologii

Svět praktické medicíny 3/2024 (znalostní test z časopisu)

Kardiologické projevy hypereozinofilií

Střevní příprava před kolonoskopií