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Phytoplankton distribution and its ecological and hydrographic controls in two contrasting areas of a stratified oligotrophic system

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Abstract

In order to analyse the relationship between oceanographic factors and the distribution of marine phytoplankton in oligotrophic conditions, an oceanographic cruise was carried out in the waters surrounding Cozumel Island, Mexico. Due to the contrasting bathymetric characteristics around Cozumel, and the possible influence of such feature on the stratification and phytoplankton ecology, physico-chemical and biological variables were measured on both sides of the island in the surface, fluorescence maximum and the halocline. Our results show that there is a strong stratification in the water column at the east side of the island, unlike the Cozumel Channel on the west, where stratification is milder and there is an uplift of the picnocline associated with the powerful Yucatan current and the reduced bathymetry of the channel. The phytoplankton community, mainly composed of diatoms, dinoflagellates and the dominant cyanobacteria Trichodesmium, showed high dissimilarity between sides of Cozumel and presented low richness, diversity and cell density. The difference between the density and species composition of the surface phytoplankton (related with high temperature), compared to the halocline layer (related with high nutrient concentrations), suggests that the effect of dynamic uplifting on stratification is a key factor that controls the phytoplankton community structure in oligotrophic waters.

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Data availability

The datasets generated during the current study are available from the corresponding author on reasonable request.

References

  • Agard, J. B. R., R. H. Hubbard & J. K. Griffith, 1996. The relation between productivity, disturbance and the biodiversity of Caribbean phytoplankton: applicability of Huston’s dynamic equilibrium model. Journal of Experimental Marine Biology and Ecology 202: 1–17.

    Article  Google Scholar 

  • Agustí, S. & C. M. Duarte, 1999. Phytoplankton chlorophyll a distribution and water column stability in the central Atlantic Ocean. Oceanologica Acta 22: 193–203.

    Article  Google Scholar 

  • Alcérreca-Huerta, J. C., J. I. Encarnacion, S. Ordoñez-Sánchez, M. Callejas-Jiménez & G. Gallegos Diez Barroso, M. Allmark, I. Mariño-Tapia, R. Silva Casarín, T. O’Doherty, C. Johnstone & L. Carrillo, 2019. Energy yield assessment from ocean currents in the insular shelf of Cozumel Island. Journal of Marine Science and Engineering 7: 147.

    Article  Google Scholar 

  • Almazán-Becerril, A., S. Escobar-Morales, G. Rosiles-González & F. Valadez, 2015. Benthic-epiphytic dinoflagellates from the northern portion of the Mesoamerican Reef System. Botanica Marina 58: 115–128.

    Article  Google Scholar 

  • Aminot, A. & F. Rey, 2000. Standard procedure for the determination of chlorophyll a by spectroscopic methods. International Council for the Exploration of the Sea 17.

  • Anderson, M. J., R. N. Gorley & K. R. Clarke, 2008. PERMANOVA+ for PRIMER: Guide to software and statistical methods. PRIMER-E, Plymouth, UK.

  • APHA, 1998. Standard Methods for the Examination of Water and Wastewater, 20th ed. American Public Health Association, Washington, D.C.

    Google Scholar 

  • Arias-González, J. E., T. Fung, R. M. Seymour, J. R. Garza-Pérez, G. Acosta-González, Y.-M. Bozec & C. R. Johnson, 2017. A coral-algal phase shift in Mesoamerica not driven by changes in herbivorous fish abundance. PLoS ONE 12: e0174855.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Arrigo, K. R., 2005. Marine microorganisms and global nutrient cycles. Nature 437: 349–355.

    Article  CAS  PubMed  Google Scholar 

  • Athié, G., J. Candela, J. Sheinbaum, A. Badan & J. Ochoa, 2011. Yucatan current variability through the Cozumel and Yucatan channels. Ciencias Marinas 37: 471–492.

    Article  Google Scholar 

  • Bates, S. S., K. A. Hubbard, N. Lundholm, M. Montresor & C. P. Leaw, 2018. Pseudo-nitzschia, Nitzschia, and domoic acid: new research since 2011. Harmful Algae 79: 3–43.

    Article  PubMed  Google Scholar 

  • Berberian, G. A. & R. B. Starr, 1977. The circulation between the Cayman Sea and the Gulf of Mexico as deduced from nutrient distributions, CICAR-II Symp Progress in Marine Research in the Caribbean and Adjacent Regions. FAO Fisheries Report, Rome: 255–266.

    Google Scholar 

  • Bergman, B., G. Sandh, S. Lin, J. Larsson & E. J. Carpenter, 2013. Trichodesmium—a widespread marine cyanobacterium with unusual nitrogen fixation properties. FEMS Microbiology Reviews 37: 286–302.

    Article  CAS  PubMed  Google Scholar 

  • Capone, D. G., J. P. Zehr, H. W. Paerl, B. Bergman & E. J. Carpenter, 1997. Trichodesmium, a globally significant marine cyanobacterium. Science 276: 1221–1229.

    Article  CAS  Google Scholar 

  • Carrillo, L., E. M. Johns, R. H. Smith, J. T. Lamkin & J. L. Largier, 2015. Pathways and hydrography in the Mesoamerican Barrier Reef System Part 1: circulation. Continental Shelf Research 109: 164–176.

    Article  Google Scholar 

  • Carrillo, L., E. M. Johns, R. H. Smith, J. T. Lamkin & J. L. Largier, 2016. Pathways and hydrography in the Mesoamerican Barrier Reef System Part 2: water masses and thermohaline structure. Continental Shelf Research 120: 41–58.

    Article  Google Scholar 

  • Carriquiry, J. D., L. M. Barranco-Servin, J. A. Villaescusa, V. F. Camacho-Ibar, H. Reyes-Bonilla & A. L. Cupul-Magaña, 2013. Conservation and sustainability of Mexican Caribbean coral reefs and the threats of a human-induced phase-shift. In Silvern, S. & S. Young (eds), Environmental Change and Sustainability. IntechOpen: 29–51.

  • Chávez, G., J. Candela & J. Ochoa, 2003. Subinertial flows and transports in Cozumel Channel. Journal of Geophysical Research 108: 1901–1911.

    Article  Google Scholar 

  • Chollett, I., F. E. Müller-Karger, S. F. Heron, W. Skirving & P. J. Mumby, 2012. Seasonal and spatial heterogeneity of recent sea surface temperature trends in the Caribbean Sea and southeast Gulf of Mexico. Marine Pollution Bulletin 64: 956–965.

    Article  CAS  PubMed  Google Scholar 

  • Clarke, K. R., 1993. Non-parametric multivariate analyses of changes in community structure. Austral Journal of Ecology 18: 117–143.

    Article  Google Scholar 

  • Clarke, K. R. & R. M. Warwick, 2001. Changes in marine communities, an approach to statistical analysis and interpretation. Second ed. PRIMER-E, Plymouth.

  • De la Lanza-Espino, G., 2001. Características físico-químicas de los mares de México, Textos selectos de geografía de México. I. Textos Monográficos. Plaza y Valdés Editores, México, D. F.

  • Estrada, M., M. Delgado, D. Blasco, M. Latasa, A. M. Cabello, V. Benítez-Barrios, E. Fraile-Nuez, P. Mozetič & M. Vidal, 2016. Phytoplankton across tropical and subtropical regions of the Atlantic. Indian and Pacific Oceans. Plos One 11: e0151699.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Frings, P. J., W. Clymans, G. Fontorbe, C. L. De la Rocha & D. J. Conley, 2016. The continental Si cycle and its impact on the ocean Si isotope budget. Chemical Geology 425: 12–36.

    Article  CAS  Google Scholar 

  • Geider, R. & J. La Roche, 2002. Redfield revisited: variability of C:N:P in marine microalgae and its biochemical basis. European Journal of Phycology 37: 1–17.

    Article  Google Scholar 

  • Glibert, P. M., 2017. Eutrophication, harmful algae and biodiversity – challenging paradigms in a world of complex nutrient changes. Marine Pollution Bulletin 124: 591–606.

    Article  CAS  PubMed  Google Scholar 

  • Glibert, P. M. & J. M. Burkholder, 2011. Harmful algal blooms and eutrophication: “strategies” for nutrient uptake and growth outside the Redfield comfort zone. Chinese Journal of Oceanology and Limnology 29: 724–738.

    Article  Google Scholar 

  • Hasle, G. R., 1978. The inverted microscope method. In Sournia, A. (ed), Phytoplankton Manual, Monographs on Oceanographic Methodology UNESCO, París, France: 88–96.

    Google Scholar 

  • Hernández-Fontes, J. V., A. Felix, E. Mendoza, Y. R. Cueto & R. Silva, 2019. On the marine energy resources of Mexico. Journal of Marine Science and Engineering 7: 191.

    Article  Google Scholar 

  • Hernández-Terrones, L., M. Rebolledo-Vieyra, M. Merino-Ibarra, M. Soto, A. Le-Cossec & E. Monroy-Ríos, 2011. Groundwater pollution in a karstic region (NE Yucatan): baseline nutrient content and flux to coastal ecosystems. Water Air and Soil Pollution 218: 517–528.

    Article  CAS  Google Scholar 

  • Hernández-Terrones, L. M., K. A. Null, D. Ortega-Camacho & A. Paytan, 2015. Water quality assessment in the Mexican Caribbean: impacts on the coastal ecosystem. Continental Shelf Research 102: 62–72.

    Article  Google Scholar 

  • Herrera-Silveira, J. A. & S. M. Morales-Ojeda, 2009. Evaluation of the health status of a coastal ecosystem in southeast Mexico: assessment of water quality, phytoplankton and submerged aquatic vegetation. Marine Pollution Bulletin 59: 72–86.

    Article  CAS  PubMed  Google Scholar 

  • Irola-Sansores, E. D., B. Delgado-Pech, E. García-Mendoza, E. J. Núñez-Vázquez, A. Olivos-Ortiz & A. Almazán-Becerril, 2018. Population dynamics of benthic-epiphytic dinoflagellates on two macroalgae from coral reef systems of the northern mexican Caribbean. Frontiers in Marine Science 5: 487.

    Article  Google Scholar 

  • Jongman, R. H., C. J. F. Ter Braak & O. F. R. Van Tongeren, 1986. Data analysis in Community and Landscape Ecology, Cambridge University Press, Wageningen, Netherlands.

    Google Scholar 

  • Lapointe, B. E., R. A. Brewton, L. W. Herren, M. Wang, C. Hu, D. J. McGillicuddy Jr., S. Lindell, F. J. Hernandez & P. L. Morton, 2021. Nutrient content and stoichiometry of pelagic Sargassum reflects increasing nitrogen availability in the Atlantic Basin. Nature Communications 12: 30.

    Article  CAS  Google Scholar 

  • López-Fuerte, F. O., D. A. Siqueiros-Beltrones & L. Veleva, 2019. Diatoms (Bacillariophyta) from artificial substrates and sediments in the Caribbean Sea off Yucatan, Mexico. Phytotaxa 406: 1–54.

    Article  Google Scholar 

  • Lozier, M. S., A. C. Dave, J. B. Palter, L. M. Gerber & R. T. Barber, 2011. On the relationship between stratification and primary productivity in the North Atlantic. Geophysical Research Letters 38: L18609.

    Article  CAS  Google Scholar 

  • Lucas, C. H., C. Banham & P. M. Holligan, 2001. Benthic-pelagic exchange of microalgae at a tidal flat. 2. Taxonomic Analysis. Marine Ecology Progress Series 212: 39–52.

    Article  Google Scholar 

  • Marshall, H. G. & J. A. Solder, 1982. Pelagic phytoplankton in the Caribbean Sea. Bulletin of Marine Science 32: 354–365.

    Google Scholar 

  • Mateo-Cid, L. E. & A. C. Mendoza-González, 1991. Algas marinas bénticas de la Isla Cozumel, Quintana Roo, México. Acta Botanica Mexicana 16: 57–87.

    Google Scholar 

  • Melo-González, N., F. E. Müller-Karger, S. Cerdeira-Estrada, R. Pérez de los Reyes, I. Victoria del Río, P. Cárdenas-Pérez & I. Mitrani-Arenal, 2000. Near-surface phytoplankton distribution in the western Intra-Americas Sea: the influence of El Niño and weather events. Journal of Geophysical Research 105: 14029–14043.

    Article  Google Scholar 

  • Mena, C., P. Reglero, M. Hidalgo, E. Sintes, R. Santiago, M. Martín, G. Moyà & M. Balbín, 2019. Phytoplankton community structure is driven by stratification in the oligotrophic Mediterranean Sea. Frontiers in Microbiology 10: 1698.

    Article  PubMed  PubMed Central  Google Scholar 

  • Mojica, K. D. A., W. H. Van de Poll, M. Kehoe, J. Huisman, K. R. Timmermans, A. G. J. Buma, H. J. Van der Woerd, L. Hahn-Woernle, H. A. Dijkstra & C. P. D. Brussaard, 2015. Phytoplankton community structure in relation to vertical stratification along a north-south gradient in the Northeast Atlantic Ocean. Limnology and Oceanography 60: 1498–1521.

    Article  Google Scholar 

  • Mutchler, T., K. H. Dunton, A. Townsend-Small, S. Fredriksen & M. K. Rasser, 2007. Isotopic and elemental indicators of nutrient sources and status of coastal habitats in the Caribbean Sea, Yucatan Peninsula, Mexico. Estuarine Coastal and Shelf Science 74: 449–457.

    Article  Google Scholar 

  • Navarro Ramas, N., 1981. A survey of the marine diatoms of Puerto Rico. I. Suborders Coscinodiscineae and Rhizosoleniineae. Botanica Marina 24: 427–440.

    Google Scholar 

  • Navarro Ramas, N., 1982. A survey of the marine diatoms of Puerto Rico III. Suborder Biddulphineae: Familie Chaetocerotaceae. Botanica Marina 25: 305–319.

    Google Scholar 

  • Navarro Ramas, N., 1983. A survey of the marine diatoms of Puerto Rico VII. Suborder Raphidineae: Families Auriculaceae, Epithemiaceae. Nitzschiaceae and Surirellaceae. Botanica Marina 26: 393–408.

    Google Scholar 

  • Navarro Ramas, N. & D. U. Hernández-Becerril, 1997. Check-list of marine diatoms from the Caribbean Sea, Listados florísticos de México. Instituto de Biologia, UNAM, D.F., México.

  • Null, K. A., K. L. Knee, E. D. Crook, N. R. de Sieyes, M. Rebolledo-Vieyra, L. Hernández-Terrones & A. Paytan, 2014. Composition and fluxes of submarine groundwater along the Caribbean coast of the Yucatan Peninsula. Continental Shelf Research 77: 38–50.

    Article  Google Scholar 

  • Ochoa, J., J. Sheinbaum, A. Badan, J. Candela & D. Wilson, 2001. Geostrophy via potential vorticity inversion in the Yucatan Channel. Journal of Marine Research 59: 725–747.

    Article  Google Scholar 

  • Oksanen, J., F. Guillaume Blanchet, M. Friendly, R. Kindt, P. Legendre, D. McGlinn, P. R. Minchin, R. B. O´Hara, G. L. Simpson, P. Solymos, M. H. H. Stevens, E. Szoecs & H. Wagner, 2017. vegan: community ecology package.

  • Orellana, R., F. Nava & C. Espadas, 2007. El clima de Cozumel y la Riviera Maya. In Mejía-Ortíz, L. M. (ed), Biodiversidad acuática de la Isla de Cozumel Universidad de Quintana Roo, Plaza y Valdés, México, D.F.: 23–32.

    Google Scholar 

  • Oviatt, C. A., K. Huizenga, C. S. Rogers & W. J. Miller, 2019. What nutrient sources support anomalous growth and the recent Sargassum mass stranding on Caribbean beaches? A review. Marine Pollution Bulletin 145: 517–525.

    Article  CAS  PubMed  Google Scholar 

  • Palafox Muñoz, A. & L. Zizumbo Villarreal, 2009. Distribución territorial y turismo en Cozumel, Estado de Quintana Roo, México. Gestión Turística 11: 69–88.

    Article  Google Scholar 

  • Pérez-Gómez, J. A., E. García-Mendoza, A. Olivos-Ortiz, A. Paytan, M. Rebolledo-Vieyra, B. Delgado-Pech & A. Almazán-Becerril, 2020. Indicators of nutrient enrichment in coastal ecosystems of the northern Mexican Caribbean. Ecological Indicators 118: 106756.

    Article  CAS  Google Scholar 

  • R Core Team, 2017. R: a language and environment for statistical computing. Foundation for Statistical Computing, Vienna, Austria.

  • Reyes-Mendoza, O., J. Herrera-Silveira, I. Mariño-Tapia, C. Enriquez & J. L. Largier, 2019. Phytoplankton blooms associated with upwelling at Cabo Catoche. Continental Shelf Research 174: 118–131.

    Article  Google Scholar 

  • Ribeiro de Queiroz, A., M. Flores Montes, P. A. Mendes de Castro Melo, R. Araújo da Silva & M. L. Koening, 2015. Vertical and horizontal distribution of phytoplankton around an oceanic archipelago of the Equatorial Atlantic. Marine Biodiversity Records 8: e155.

    Article  Google Scholar 

  • Righetti, D., M. Vogt, N. Gruber, A. Psomas & N. Zimmermann, 2019. Global pattern of phytoplankton diversity driven by temperature and environmental variability. Science Advances 5: eaau6253.

  • Rioja-Nieto, R. & L. Álvarez-Filip, 2019. Coral reef systems of the Mexican Caribbean: status, recent trends and conservation. Marine Pollution Bulletin 140: 616–625.

    Article  CAS  PubMed  Google Scholar 

  • Rioja-Nieto, R., R. Garza-Pérez, L. Álvarez-Filip, I. Mariño-Tapia & C. Enriquez, 2019. The Mexican Caribbean: from Xcalak to Holbox. In Sheppard, C. (ed), World Seas: An Environmental Evaluation Academic Press, Second Edition: 637–653.

    Chapter  Google Scholar 

  • Sharples, J., M. C. Moore, T. P. Rippeth, P. M. Holligan, D. J. Hydes, N. R. Fisher & J. H. Simpson, 2001. Phytoplankton distribution and survival in the thermocline. Limnology and Oceanography 486: 486–496.

    Article  Google Scholar 

  • Sheinbaum, J., J. Candela, A. Badan & J. Ochoa, 2002. Flow structure and transport in the Yucatan Channel. Geophysical Research Letters 29: 1040.

    Article  Google Scholar 

  • Siegel, S. & N. J. Castellan, 1988. Nonparametric Statistics for the Behavioral Sciences, 2nd ed. McGraw-Hill, New York, NY.

    Google Scholar 

  • Strickland, J. D. & T. R. Parsons, 1972. A practical handbook of seawater analysis. Second edition. Fisheries research board of Canada. Ottawa, Canada.

  • Ter Braak, C. J. F., 1986. Canonical corrrespondence analysis: a new eigenvector technique for multivariate direct gradient analysis. Ecology 67: 1167–1179.

    Article  Google Scholar 

  • Tomas, C. R., 1997. Identifying Marine Phytoplankton, Academic Press, New York.

    Google Scholar 

  • Troccoli-Ghinaglia, L., J. A. Herrera-Silveira & F. A. Comín, 2004. Structural variations of phytoplankton in the coastal seas of Yucatan, Mexico. Hydrobiologia 519: 85–102.

    Article  Google Scholar 

  • Troccoli-Ghinaglia, L., J. A. Herrera-Silveira, F. A. Comín & J. R. Díaz-Ramos, 2010. Phytoplankton community variations in tropical coastal area affected where submarine groundwater occurs. Continental Shelf Research 30: 2082–2091.

    Article  Google Scholar 

  • Van Tussenbroek, B. I., H. A. Hernández Arana, R. E. Rodríguez-Martínez, J. Espinoza-Avalos, H. M. Canizales-Flores, C. E. González-Godoy, M. G. Barba-Santos, A. Vega-Zepeda & L. Collado-Vides, 2017. Severe impacts of brown tides caused by Sargassum spp. on near-shore Caribbean seagrass communities. Marine Pollution Bulletin 122: 272–281.

    Article  PubMed  CAS  Google Scholar 

  • Zar, J. H., 2010. Biostatistical Analysis, Prentice Hall, Upper Saddle River.

    Google Scholar 

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Acknowledgements

This study was financially supported by Centro Mexicano de Innovación en Energía del Océano (CEMIE-Océano, Project CONACYT-SENER S0019-2014-06 [0249795]) and Instituto de Ecología, A.C. (Project 902-11-280). Ariadna Martínez, Daniela Cela and Javier Tolome, from INECOL, A.C., helped with the nutrients and Chl-a analyses and provided logistic support. CFRG appreciates the postdoctoral scholarship granted by DGAPA-UNAM (Programa de Becas Posdoctorales en la UNAM). We thank the R/V Justo Sierra crew, and the multidisciplinary team that participated in oceanographic campaign CEMIE-I. María Elena Sánchez-Salazar translated the manuscript into English. We are grateful for the comments of two anonymous reviewers, whose comments helped to improve this paper.

Funding

This work was supported by CEMIE-Océano [project CONACYT-SENER S0019-2014-06 (0249795)] and Instituto de Ecología, A.C. [Project 902-11-280].

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  1. Escuela Nacional de Estudios Superiores, Unidad Mérida, Universidad Nacional Autónoma de México, Carretera Mérida-Tetiz, Km 4, 97357, Ucú, Yucatán, Mexico

    Carlos F. Rodríguez-Gómez, Vanesa Papiol, Ismael Mariño-Tapia & Cecilia Enriquez

  2. Instituto de Ecología A.C., Carretera Antigua a Coatepec #351, 91073, Xalapa, Veracruz, Mexico

    Gabriela Vázquez

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  1. Carlos F. Rodríguez-Gómez
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CFRG contributed to conceptualization, manuscript development, original draft and data analysis. GV contributed to conceptualization, manuscript development, original draft, data analysis and funding acquisition. VP contributed to manuscript development and data analysis. IMT and CE contributed to manuscript development, data analysis and funding acquisition.

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Correspondence to Carlos F. Rodríguez-Gómez.

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Rodríguez-Gómez, C.F., Vázquez, G., Papiol, V. et al. Phytoplankton distribution and its ecological and hydrographic controls in two contrasting areas of a stratified oligotrophic system. Hydrobiologia 849, 3175–3195 (2022). https://doi.org/10.1007/s10750-022-04924-7

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