Using Margalef’s vision to understand the current aquatic microbial ecology

Authors

DOI:

https://doi.org/10.3989/scimar.05199.026

Keywords:

aquatic ecology, integrated approach, succession, biogeochemical cycles, global change

Abstract


Ramon Margalef was a pioneering scientist who introduced an interdisciplinary approach to ecological studies. His studies were among the first to incorporate various concepts in the literature of aquatic ecology, covering topics such as organisms, ecosystem interactions and evolution. To bring Margalef’s approach into current scientific studies, in this review we explore his vision of aquatic ecology within four interrelated fields of study: ecological theory, microbial diversity, biogeochemical cycles and global environmental changes. Taking inspiration from his studies, we analyse current scientific challenges and propose an integrated approach, considering the unifying concept of Margalef’s Mandala with the aim of improving future studies on aquatic microbial ecology.

Downloads

Download data is not yet available.

References

Amaral-Zettler L.A., Zettler E.R., Mincer T.J. 2020. Ecology of the plastisphere. Nat. Rev. Microbiol.18: 139-151. https://doi.org/10.1038/s41579-019-0308-0PMid:31937947

Astudillo-García C., Hermans S.M., Stevenson B., Buckley H.L., Lear G. 2019. Microbial assemblages and bioindicators as proxies for ecosystem health status: potential and limitations. Appl. Microbiol. Biot. 103: 6407-6421. https://doi.org/10.1007/s00253-019-09963-0PMid:31243501

Bertagnolli A.D., Stewart F.J. 2018. Microbial niches in marine oxygen minimum zones. Nat. Rev. Microbiol. 16: 723-729.https://doi.org/10.1038/s41579-018-0087-zPMid:30250271

Biller S.J., Berube P.M., Dooley K., et al. 2018. Data descriptor: Marine microbial metagenomes sampled across space and time. Sci. Data 5: 180176. https://doi.org/10.1038/sdata.2018.176PMid:30179232 PMCid:PMC6122167

Boavida M.J. 2012. It all started with Margalef's paper of 1951. Limnetica 31: 187-192.https://doi.org/10.23818/limn.31.17

Borrero-Santiago A.R., DelValls T.A., Riba I. 2016. Carbon Capture and Storage (CCS): Risk assessment focused on marine bacteria. Ecotoxicol. Environ. Saf. 131: 157-163. https://doi.org/10.1016/j.ecoenv.2016.04.020PMid:27107627

Botta-Dukát Z. 2005. Rao's quadratic entropy as a measure of functional diversity based on multiple traits. J. Veg. Sci. 16: 533-540. https://doi.org/10.1111/j.1654-1103.2005.tb02393.x

Boyd P.W., Collins S., Dupont S., et al. 2018. Experimental strategies to assess the biological ramifications of multiple drivers of global ocean change-A review. Glob. Change Biol. 24: 2239-2261. https://doi.org/10.1111/gcb.14102PMid:29476630

Brown J.H., Gillooly J.F., Allen A.P., et al. 2004. Toward a metabolic theory of ecology. Ecology 85: 1771-1789. https://doi.org/10.1890/03-9000

Defining the scientific method. 2009. Nat. Methods 6: 237. https://doi.org/10.1038/nmeth0409-237PMid:19340960

Dlugokencky E., Tans P. 2020. Global Monitoring Laboratory-Carbon Cycle Greenhouse Gases. Retrieved July 6, 2020, from www.esrl.noaa.gov/gmd/ccgg/trends.

Dyhrman S.T., Ammerman J.W., Van Mooy B.A.S. 2007. Microbes and the marine phosphorus cycle. Oceanography 20: 110-116. https://doi.org/10.5670/oceanog.2007.54

Ehrlich P.R., Ehrlich A.H. 1981. Extinction: the causes and consequences of the disappearance of species. New York: Random House.

Emamalipour M., Seidi K., Vahed S. Z., et al. 2020. Horizontal gene transfer: from evolutionary flexibility to disease progression. Front. Cell Develop. Biol. 8. https://doi.org/10.3389/fcell.2020.00229PMid:32509768 PMCid:PMC7248198

Fastner J., Rucker J., Stuken A., et al. 2007.Occurrence of the cyanobacterial toxin cylindrospermopsin in northeast Germany. Environ. Toxicol. 22: 26-32. https://doi.org/10.1002/tox.20230PMid:17295278

Fontana S., Rasmann S., de Bello F., et al. 2021. Reconciling trait-based perspectives along a trait-integration continuum. Ecology 102(10): e03472. https://doi.org/10.1002/ecy.3472PMid:34260747

Fuente, M.d.L., Miranda, C.D., Jopia, P., et al. 2015. Growth inhibition of bacterial fish pathogens and quorum-sensing blocking by bacteria recovered from Chilean salmonid farms. J. Aquat. Anim. Health 27: 112-122. https://doi.org/10.1080/08997659.2014.1001534PMid:26000731

Fuhrman J.A., Hagstrom K. 2008. Bacterial and Archaeal Community Structure and its Patterns. In: Microbial Ecology of the Oceans (pp. 45-90). Hoboken, NJ, USA: John Wiley and Sons, Inc. https://doi.org/10.1002/9780470281840.ch3

Gattuso J.P., Hansson L. 2011. Ocean acidification: background and history. In: Ocean Acidification, Oxford Univ. Press, Inc. USA. https://doi.org/10.1093/oso/9780199591091.003.0006

Ghyoot C., Gypens N., Flynn K.J., Lancelot C. 2015. Modelling alkaline phosphatase activity in microalgae under orthophosphate limitation: the case of Phaeocystis globosa. J. Plankton Res. 37: 869-855. https://doi.org/10.1093/plankt/fbv062

González-Ortegón E.; Moreno-Andrés J. 2021. Anthropogenic Modifications to Estuaries Facilitate the Invasion of Non-Native Species. Processes 9: 740. https://doi.org/10.3390/pr9050740

Goodrich J.K., Waters J.L., Poole A.C., et al. 2014. Human genetics shape the gut microbiome. Cell 159: 789-799. https://doi.org/10.1016/j.cell.2014.09.053PMid:25417156 PMCid:PMC4255478

Goswami M., Bhattacharyya P., Mukherjee I., Tribedi P. 2017. Functional diversity: an important measure of ecosystem functioning. Adv. Microbiol. 7: 82-93. https://doi.org/10.4236/aim.2017.71007

Gruber N. 2011. Warming up, turning sour, losing breath: ocean biogeochemistry under global change. Philos. Trans. R. Soc. A 369: 1980-1996. https://doi.org/10.1098/rsta.2011.0003PMid:21502171

Guo X., Wang J. 2019. The chemical behaviors of microplastics in marine environment: A review. Mar. Poll. Bull. 142: 1-14. https://doi.org/10.1016/j.marpolbul.2019.03.019PMid:31232281

Heidelberg K.B., O'Neil K.L., Bythell J.C., Sebens K.P. 2010. Vertical distribution and diel patterns of zooplankton abundance and biomass at Conch Reef, Florida Keys (USA). J. Plankton Res. 32(1): 75-91. https://doi.org/10.1093/plankt/fbp101PMid:20046854 PMCid:PMC2787388

Hultman J., Waldrop M.P., Mackelprang R., et al. 2015. Multi-omics of permafrost, active layer, and thermokarst bog soil microbiomes. Nature. 521: 208-212. https://doi.org/10.1038/nature14238PMid:25739499

Jing H., Xia X., Suzuki K., Liu H. 2013.Vertical profiles of bacteria in the tropical and subarctic oceans revealed by pyrosequencing. PLoS ONE 8: e79423. https://doi.org/10.1371/journal.pone.0079423PMid:24236132 PMCid:PMC3827353

Jones S.J., Southward A.J., Wethey D.S. 2012. Climate change and historical biogeography of the barnacle. Global Ecol. Biogeogr. 21: 716-724. https://doi.org/10.1111/j.1466-8238.2011.00721.x

Lawton J. H. 1994. What do species do in ecosystems? Oikos 71: 367. https://doi.org/10.2307/3545824

Lawton J. H. 1999. Are there general laws in ecology? Oikos 84: 177-192. https://doi.org/10.2307/3546712

Lepš J. 2005. Diversity and ecosystem function. Veg. Ecol. 199-237.

Letscher R.T., Moore J.K. 2015. Preferential remineralization of dissolved organic phosphorus and non-Redfield DOM dynamics in the global ocean: Impacts on marine productivity, nitrogen fixation, and carbon export. Global Biogeochem. Cy. 29: 325-340.https://doi.org/10.1002/2014GB004904

Levine J.M., Adler P.B., Yelenik S.G. 2004. A meta-analysis of biotic resistance to exotic plant invasions. Ecol. Lett. 7: 975-989. https://doi.org/10.1111/j.1461-0248.2004.00657.x

Locey K.J. Lennon J.T. 2016. Scaling laws predict global microbial diversity. Proc. Nat. Acad. Sci. USA 113: 5970-5975. https://doi.org/10.1073/pnas.1521291113PMid:27140646 PMCid:PMC4889364

Logares R., Haverkamp T.H.A., Kumar S., et al. 2012. Environmental microbiology through the lens of high-throughput DNA sequencing: Synopsis of current platforms and bioinformatics approaches. J. Microbiol. Met. 91: 106-113. https://doi.org/10.1016/j.mimet.2012.07.017PMid:22849829

Margalef R. 1950. Rôle des entomostracés dans la régéneration des phosphates, internationale vereinigung für theoretische und angewandte. Limnologie: Verhandlungen. 11: 246-247. https://doi.org/10.1080/03680770.1950.11895232

Margalef R. 1951. Diversidad de especies en les communidades naturales. Publ. Inst. Biol. Apl. Barcelona 6: 59-72.

Margalef R. 1957. La teoría de la información en Ecología. Mem. Real Acad. Cien. Art. Barcelona 32: 373-436.

Margalef R. 1958. Information theory in ecology. General Systems: Yearbook of the Society for General Systems Research 3: 36-71.

Margalef R. 1963. On certain unifying principles in ecology. Amer. Nat. 97(897): 357-374. https://doi.org/10.1086/282286

Margalef R. 1968. Perspectives in ecological theory. University of Chicago Press. 111 pp.

Margalef R. 1975. Diversity, stability and maturity in natural ecosystems. In: Unifying Concepts in Ecology. Springer, Netherlands, pp. 151-160. https://doi.org/10.1007/978-94-010-1954-5_12

Margalef R. 1978. Life-forms of phytoplankton. Oceanol. Acta 1: 493-509.

Margalef R. 1985. Ecosystems: diversity and connectivity as measurable components of their complication. In: The Science & Praxis of Complexity. United Nations University (UNU), Tokyo, GLDB-2/UNUP-560.

Margalef R. 1991. Teoría de los sistemas ecológicos. Edicions Universitat Barcelona.

Margalef R. 1992. Oblik Biosfer (A View of the Biosphere). Moscow: Russian Academy of Sciences, Institute of Oceanology.

Margalef R. 1997. Our biosphere. In: O. Kinne (ed.), Excellence in Ecology, 10. Ecology Institute, Oldendrof/Luhe, 176 pp.

Margalef R. 1998. Elements limitants, explotabilitat i diversitat. Homenatge a Bolòs i al fòsfor. Acta Bot. Barcino. 45: 633-643. Retrieved from. https://raco.cat/index.php/ActaBotanica/article/view/59590

Margalef R. 2000a. El marco ecológico para iluminar la sociedad actual. In: Naredo J.M. and Parra F. (eds), Economía, Ecología y Sostenibilidad en la sociedad actual. Siglo XXI, Madrid, pp. 51-66.

Margalef R. 2000b. Organització de la biosfera i reflexions sobre el present i el futur de la nostra espècie i de la ciència ecològica. Treb. Soc. Cat. Biol. 50: 47-59. Retrieved from. https://raco.cat/index.php/TreballsSCBiologia/article/view/15701

Margalef R., Estrada M., Blasco D. 1979. Functional morphology of organisms involved in red tides, as adapted to decaying turbulence. In: Taylor, D., Seliger, H. (eds), Toxic Dinoflagellate Blooms. Elsevier, New York pp. 89-94.

Mestre M., Höfer J., Sala M.M., Gasol J.M. 2020. Seasonal variation of bacterial diversity along the marine particulate matter continuum. Front. Microbiol. 11: 1590. https://doi.org/10.3389/fmicb.2020.01590PMid:32793139 PMCid:PMC7385255

Morris E.K., Caruso T., Buscot F., et al. 2014. Choosing and using diversity indices: Insights for ecological applications from the German Biodiversity Exploratories. Ecol. Evol. 4: 3514-3524. https://doi.org/10.1002/ece3.1155PMid:25478144 PMCid:PMC4224527

Moseman S.M., Zhang R., Qian P.Y., Levin L.A. 2009. Diversity and functional responses of nitrogen-fixing microbes to three wetland invasions. Biol. Invasions 11: 225-239. https://doi.org/10.1007/s10530-008-9227-0

Ortiz-Álvarez R., Fierer N., De Los Ríos A., Casamayor E.O., Barberán A. 2018. Consistent changes in the taxonomic structure and functional attributes of bacterial communities during primary succession. ISME J. 12: 1658-1667. https://doi.org/10.1038/s41396-018-0076-2PMid:29463893 PMCid:PMC6018800

Pettorelli N., Schulte to Bühne H., Tulloch A., et al. 2018. Satellite remote sensing of ecosystem functions: opportunities, challenges and way forward. Remote Sens. Ecol. Cons. 4: 71-93. https://doi.org/10.1002/rse2.59

Pielou, E. C. 1966. The measurement of diversity in different types of biological collections. J. Theor. Biol. 13: 131-144. https://doi.org/10.1016/0022-5193(66)90013-0

Pinhassi J., Hagström Å. 2000. Seasonal succession in marine bacterioplankton. Aquat. Microb. Ecol. 21: 245-256.https://doi.org/10.3354/ame021245

Polaske N.W., Kelly B.D., Ashworth-Sharpe J., Bieniarz C. 2016. Quinone methide signal amplification: covalent reporter labeling of cancer epitopes using alkaline phosphatase substrates. Bioconjug. Chem. 27: 660-666. https://doi.org/10.1021/acs.bioconjchem.5b00652PMid:26731201

Prosser J.I. 2010.Replicate or lie. Env. Microbiol. 12: 1806-1810. https://doi.org/10.1111/j.1462-2920.2010.02201.xPMid:20438583

Pylro V.S., Roesch L.F.W., Morais D.K., et al. 2014. Data analysis for 16S microbial profiling from different benchtop sequencing platforms. J. Microbiol. Meth. 107: 30-37. https://doi.org/10.1016/j.mimet.2014.08.018PMid:25193439

Rao C.R. 1982. Diversity and dissimilarity coefficients: a unified approach. Theor. Pop. Biol. 21: 24-43. https://doi.org/10.1016/0040-5809(82)90004-1

Rosenzweig C., Parry M.L. 1994. Potential impact of climate change on world food supply. Nature 367: 133-138. https://doi.org/10.1038/367133a0

Sánchez-Quinto A., Falcón L.I. 2019. Metagenome of Acropora palmata coral rubble: Potential metabolic pathways and diversity in the reef ecosystem. PLoS ONE 14: e0220117. https://doi.org/10.1371/journal.pone.0220117PMid:31394568 PMCid:PMC6687439

Schroeder P.J., Jenkins D.G. 2018. How robust are popular beta diversity indices to sampling error? Ecosphere 9: e02100. https://doi.org/10.1002/ecs2.2100

Sebastian M., Ammerman J.W. 2009. The alkaline phosphatase PhoX is more widely distributed in marine bacteria than the classical PhoA. ISME J. 3: 563-572. https://doi.org/10.1038/ismej.2009.10PMid:19212430

Shade A. 2017. Diversity is the question, not the answer. ISME J. 11: 1-6. https://doi.org/10.1038/ismej.2016.118PMid:27636395 PMCid:PMC5421358

Shannon C.E., Weaver W. 1949. The mathematical theory of communication. The University of Illinois Press, Urbana.

Simpson E.H. 1949. Measurement of diversity. Nature 163: 688. https://doi.org/10.1038/163688a0

Sherwin W.B., Prat i Fornells N. 2019. The Introduction of Entropy and Information Methods to Ecology by Ramon Margalef. Entropy 21: 794. https://doi.org/10.3390/e21080794PMid:33267507 PMCid:PMC7515323

Terradas J. 2015. El pensamiento evolutivo de Margalef. Ecosistemas 24: 104-109.

Thomas M.K., Fontana S., Reyes M., Kehoe M., Pomati F. 2018. The predictability of a lake phytoplankton community, over time-scales of hours to years. Ecol. Lett. 21: 619-628. https://doi.org/10.1111/ele.12927PMid:29527797

Tuomisto H. 2010. A diversity of beta diversities: Straightening up a concept gone awry. Part 2. Quantifying beta diversity and related phenomena. Ecography 33: 23-45. https://doi.org/10.1111/j.1600-0587.2009.06148.x

Valdespino-Castillo P.M., Alcántara-Hernández R.J., Alcocer J., et al. 2014. Alkaline phosphatases in microbialites and bacterioplankton from Alchichica soda lake, Mexico. FEMS Microbiol. Ecol. 90: 504-519. https://doi.org/10.1111/1574-6941.12411PMid:25112496

Vellend M. 2016. The theory of ecological communities. In: Monographs in population biology. Princeton University Press. https://www.jstor.org/stable/j.ctt1kt82jg

Villamaña M., Marañón E., Cermeño P., Estrada M., Fernández-Castro B., Figueiras F. G., Latasa M., Otero-Ferrer J. L., Reguera B., Mouriño-Carballido B. 2019. The role of mixing in controlling resource availability and phytoplankton community composition. Prog. Oceanogr. 178: 102181. https://doi.org/10.1016/j.pocean.2019.102181

Vitorino L.C., Bessa L.A. 2018. Microbial diversity: the gap between the estimated and the known. Diversity 10: 46. https://doi.org/10.3390/d10020046

Wyatt T. 2014. Margalef's mandala and phytoplankton bloom strategies. Deep-Sea Res. Pt. II 101: 32-49.https://doi.org/10.1016/j.dsr2.2012.12.006

Wyatt T., Carlton J.T. 2002. Phytoplankton introductions in European coastal waters: why are so few invasions reported? In: Briand F. (ed), Alien Marine Organisms Introduced by Ships in the Mediterranean and Black Seas - Commission Internationale pour l'Exploration Scientifique de la Mer Mediterranee. 20: 41-46.

Young J.N., Rickaby R.E.M., Kapralov M., Filatov D.A. 2012. Adaptive signals in algal Rubisco reveal a history of ancient atmospheric carbon dioxide. Philos. Trans. R. Soc. B 367: 483-492.https://doi.org/10.1098/rstb.2011.0145PMid:22232761 PMCid:PMC3248704

Published

2022-04-07

How to Cite

1.
Borrero-Santiago AR, Dellisanti W, Sánchez-Quinto A, Moreno-Andrés J, Nemoy P, Richa K, Valdespino-Castillo PM, Diaz-de-Quijano D, Ontiveros VJ, Fontana S, Giner CR, Sanz-Sáez I, Mestre M. Using Margalef’s vision to understand the current aquatic microbial ecology. Sci. mar. [Internet]. 2022Apr.7 [cited 2024Mar.19];86(1):e026. Available from: https://scientiamarina.revistas.csic.es/index.php/scientiamarina/article/view/1915

Issue

Section

News & Comments