Protistan plankton communities in the Galápagos Archipelago respond to changes in deep water masses resulting from the 2015/16 El Niño
Erika F. Neave
Department of Earth, Marine and Environmental Sciences, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA
Department of Life Sciences, Natural History Museum, London, UK
School of Biological and Environmental Sciences, Liverpool John Moores University, Liverpool, UK
Search for more papers by this authorHarvey Seim
Department of Earth, Marine and Environmental Sciences, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA
Search for more papers by this authorScott M. Gifford
Department of Earth, Marine and Environmental Sciences, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA
Search for more papers by this authorOlivia Torano
Department of Earth, Marine and Environmental Sciences, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA
Search for more papers by this authorZackary I. Johnson
Marine Laboratory and Biology Department, Duke University, Beaufort, NC, USA
Search for more papers by this authorDiego Páez-Rosas
Galápagos Science Center, Universidad San Francisco de Quito, Isla San Cristóbal, Islas Galápagos, Ecuador
Search for more papers by this authorCorresponding Author
Adrian Marchetti
Department of Earth, Marine and Environmental Sciences, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA
For correspondence.E-mail [email protected]; Tel. (+1) 919 843 3473; Fax (+1) 919 962 1254.
Search for more papers by this authorErika F. Neave
Department of Earth, Marine and Environmental Sciences, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA
Department of Life Sciences, Natural History Museum, London, UK
School of Biological and Environmental Sciences, Liverpool John Moores University, Liverpool, UK
Search for more papers by this authorHarvey Seim
Department of Earth, Marine and Environmental Sciences, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA
Search for more papers by this authorScott M. Gifford
Department of Earth, Marine and Environmental Sciences, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA
Search for more papers by this authorOlivia Torano
Department of Earth, Marine and Environmental Sciences, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA
Search for more papers by this authorZackary I. Johnson
Marine Laboratory and Biology Department, Duke University, Beaufort, NC, USA
Search for more papers by this authorDiego Páez-Rosas
Galápagos Science Center, Universidad San Francisco de Quito, Isla San Cristóbal, Islas Galápagos, Ecuador
Search for more papers by this authorCorresponding Author
Adrian Marchetti
Department of Earth, Marine and Environmental Sciences, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA
For correspondence.E-mail [email protected]; Tel. (+1) 919 843 3473; Fax (+1) 919 962 1254.
Search for more papers by this authorSummary
The Galápagos Archipelago lies within the Eastern Equatorial Pacific Ocean at the convergence of major ocean currents that are subject to changes in circulation. The nutrient-rich Equatorial Undercurrent upwells from the west onto the Galápagos platform, stimulating primary production, but this source of deep water weakens during El Niño events. Based on measurements from repeat cruises, the 2015/16 El Niño was associated with declines in phytoplankton biomass at most sites throughout the archipelago and reduced utilization of nitrate, particularly in large-sized phytoplankton in the western region. Protistan assemblages were identified by sequencing the V4 region of the 18S rRNA gene. Dinoflagellates, chlorophytes and diatoms dominated most sites. Shifts in dinoflagellate communities were most apparent between the years; parasitic dinoflagellates, Syndiniales, were highly detected during the El Niño (2015) while the dinoflagellate genus, Gyrodinium, increased at many sites during the neutral period (2016). Variations in protistan communities were most strongly correlated with changes in subthermocline water density. These findings indicate that marine protistan communities in this region are regimented by deep water mass sources and thus could be profoundly affected by altered ocean circulation.
Supporting Information
Filename | Description |
---|---|
emi15863-sup-0001-supinfo1.docxWord 2007 document , 576.6 KB | Appendix S1: Supporting Information. |
emi15863-sup-0002-supinfo2.pdfPDF document, 6.9 MB | Appendix S2: Supporting Information. |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
References
- Anderson, D.M., Coats, D.W., and Tyler, M.A. (1985) Encystment of the dinoflagellate Gyrodinium uncatenum: temperature and nutrient effects. J Phycol 21: 200–206.
- Barber, R.T., and Chavez, F.P. (1991) Regulation of primary productivity rate in the equatorial Pacific. Limnol Oceanogr 36: 1803–1808.
- Barber, R.T., Sanderson, M.P., Lindley, S.T., Chai, F., Newton, J., Trees, C.C., et al. (1996) Primary productivity and its regulation in the equatorial Pacific during and following the 1991–1992 El Niño. Deep-Sea Res II Top Stud Oceanogr 43: 933–969.
- Behrenfeld, M.J., Bale, A.J., Kolber, Z.S., Aiken, J., and Falkowski, P.G. (1996) Confirmation of iron limitation of phytoplankton photosynthesis in the equatorial Pacific Ocean. Nature 383: 508–511.
- Bensted-Smith, R. (1998) The special law for Galápagos. Noticias de Galápagos 59. 6.
- Bravo, I., and Figueroa, R. (2014) Towards an ecological understanding of dinoflagellate cyst functions. Microorganisms 2: 11–32.
- Carnicer, O., De La Fuente, P., Canepa, A., Keith, I., Rebolledo-Monsalve, E., Diogène, J., and Fernández-Tejedor, M. (2019) Marine dinoflagellate assemblage in the Galápagos marine reserve. Front Mar Sci 6: 235.
- Chavez, F.P., and Brusca, R.C. (1991) The Galápagos Islands and their relation to oceanographic processes in the tropical Pacific. In Galapagos Marine Invertebrates. Boston, MA: Springer, pp. 9–33.
10.1007/978-1-4899-0646-5_2 Google Scholar
- Chavez, F.P., Buck, K.R., Service, S.K., Newton, J., and Barber, R.T. (1996) Phytoplankton variability in the central and eastern tropical pacific. Deep-Sea Res Part II: Top Stud Oceanogr 43: 835–870.
- Clarke, K.R., and Ainsworth, M. (1993) A method of linking multivariate community structure to environmental variables. Mar Ecol Prog Ser 92: 205–219.
- Clarke, L.J., Bestley, S., Bissett, A., and Deagle, B.E. (2019) A globally distributed Syndiniales parasite dominates the Southern Ocean micro-eukaryote community near the sea-ice edge. ISME J 13: 734–737.
- Collado-Fabbri, S., Vaulot, D., and Ulloa, O. (2011) Structure and seasonal dynamics of the eukaryotic picophytoplankton community in a wind-driven coastal upwelling ecosystem. Limnol Oceanogr 56: 2334–2346.
- De Vargas, C., Audic, S., Henry, N., Decelle, J., Mahé, F., Logares, R., et al. (2015) Eukaryotic plankton diversity in the sunlit ocean. Science 348: 7–8.
- Dugdale, R.C., and Goering, J.J. (1967) Uptake of new and regenerated forms of nitrogen in primary productivity. Limnol Oceanogr 12: 196–206.
- Edgar, G.J., Bustamante, R.H., Farina, J.M., Calvopina, M., Martinez, C., and Toral-Granda, M.V. (2004) Bias in evaluating the effects of marine protected areas: the importance of baseline data for the Galapagos Marine Reserve. Environ Conserv 31: 212–218.
- Feldman, G.C. (1986) Patterns of phytoplankton production around the Galapagos Islands. In Tidal Mixing and Plankton Dynamics. New York, NY: Springer, pp. 77–106.
10.1007/978-1-4612-4966-5_3 Google Scholar
- Fiedler, P.C., and Talley, L.D. (2006) Hydrography of the eastern tropical Pacific: a review. Prog Oceanogr 69: 143–180.
- Gifford, S.M., Zhao, L., Stemple, B., DeLong, K., Medeiros, P.M., Seim, H., and Marchetti, A. (2020) Microbial niche diversification in the Galápagos Archipelago and its response to El Niño. Front Microbiol 11: 2636.
- Guillou, L., Viprey, M., Chambouvet, A., Welsh, R.M., Kirkham, A.R., Massana, R., et al. (2008) Widespread occurrence and genetic diversity of marine parasitoids belonging to Syndiniales (Alveolata). Environ Microbiol 10: 3349–3365.
- Hama, T., Miyazaki, T., Ogawa, Y., Iwakuma, T., Takahashi, M., Otsuki, A., and Ichimura, S. (1983) Measurement of photosynthetic production of a marine phytoplankton population using a stable 13 C isotope. Mar Biol 73: 31–36.
- Hoppenrath, M., Murray, S.A., Chomérat, N., and Horiguchi, T. (2014) Marine Benthic Dinoflagellates: Unveiling Their Worldwide Biodiversity: Stuttgart, Germany: Schweizerbart science publishers.
- Jakoboski, J., Todd, R.E., Owens, W.B., Karnauskas, K.B., and Rudnick, D.L. (2020) Bifurcation and upwelling of the equatorial undercurrent west of the Galápagos archipelago. J Phys Oceanogr 50: 887–905.
- Jephcott, T.G., Alves-De-Souza, C., Gleason, F.H., Van Ogtrop, F.F., Sime-Ngando, T., Karpov, S.A., and Guillou, L. (2016) Ecological impacts of parasitic chytrids, syndiniales and perkinsids on populations of marine photosynthetic dinoflagellates. Elsevier 19: 47–58.
- Johnson, Z., Shyam, R., Romano, A., Mioni, C.E., Lance, V., Murray, J.W., and Zinser, E. (2010) The effect of iron-and light-limitation on phytoplankton communities of deep chlorophyll maxima of the western Pacific Ocean. J Mar Res 68: 283–308.
- Kessler, W.S. (2006) The circulation of the eastern tropical Pacific: a review. Prog Oceanogr 69: 181–217.
- Kislik, E., Mantilla, G., Torres, G., and Borbor-Córdova, M. (2017) Biological hotspots in the Galápagos Islands: exploring seasonal trends of ocean climate drivers to monitor algal blooms. Int Scholarly Sci Res Innov 11: 824–834.
- Lavrinienko, A., Jernfors, T., Koskimäki, J.J., Pirttilä, A.M., and Watts, P.C. (2021) Does intraspecific variation in rDNA copy number affect analysis of microbial communities? Trends Microbiol 29: 19–27.
- Lindley, S.T., and Barber, R.T. (1998) Phytoplankton response to natural and experimental iron addition. Deep-Sea Res Part II: Top Stud Oceanogr 45: 1135–1150.
- Liu, Y., Xie, L., Morrison, J.M., Kamykowski, D., and Sweet, W.V. (2014) Ocean circulation and water mass characteristics around the Galápagos Archipelago simulated by a multiscale nested ocean circulation model. Int J Oceanogr 2014: 1–16.
- Lopes Dos Santos, A., Pollina, T., Gourvil, P., Corre, E., Marie, D., Garrido, J.L., et al. (2017) Chloropicophyceae, a new class of picophytoplanktonic prasinophytes. Sci Rep 7: 1–20.
- Marchetti, A., Varela, D.E., Lance, V.P., Lance, V.P., Palmucci, M., Giordano, M., and Virginia Armbrust, E. (2010) Iron and silicic acid effects on phytoplankton productivity, diversity, and chemical composition in the central equatorial Pacific Ocean. Limnol Oceanogr 55: 11–29.
- Masotti, I., Moulin, C., Alvain, S., Bopp, L., Tagliabue, A., and Antoine, D. (2011) Large-scale shifts in phytoplankton groups in the equatorial Pacific during ENSO cycles. Biogeosciences 8: 539–550.
- Maxwell, D.C. (1975) Marine primary productivity of the Galapagos Archipelago. PhD Dissertation. The Ohio State University.
- McCulloch, A. (2011) A spatio-temporal context for the phytoplankton community patterns of the Galapagos Archipelago and the Northwest Florida Shelf. PhD Dissertation. North Carolina State University.
- Moore, L.R., Post, A.F., Rocap, G., and Chisholm, S.W. (2002) Utilization of different nitrogen sources by the marine cyanobacteria Prochlorococcus and Synechococcus. Limnol Oceanogr 47: 989–996.
- Naranjo, C., and Tapia, M.E. (2015) Plancton en el canal bolívar de la isla isabela (caleta tagus), islas galápagos durante marzo de 2009. Acta Oceanográfica del Pacífico 20: 71–90.
- Palacios, D.M. (2002) Factors influencing the Island-mass effect of the Galápagos Archipelago. Geophys Res Lett 29: 49–41.
- Palacios, D.M. (2004) Seasonal patterns of sea-surface temperature and ocean color around the Galápagos: regional and local influences. Deep-Sea Res Part II: Top Stud Oceanogr 51: 43–57.
- Park, J., Dunne, J.P., and Stock, C.A. (2018) Ocean chlorophyll as a precursor of ENSO: an earth system modeling study. Geophys Res Lett 45: 1939–1947.
- Pauly, D., and Christensen, V. (1995) Primary production required to sustain global fisheries. Nature 374: 255–257.
- Pennington, J.T., Mahoney, K.L., Kuwahara, V.S., Kolber, D.D., Calienes, R., and Chavez, F.P. (2006) Primary production in the eastern tropical Pacific: a review. Prog Oceanogr 69: 285–317.
- Pitcher, G.C., Walker, D.R., Mitchell-Innes, B.A., and Moloney, C.L. (1991) Short-term variability during an anchor station study in the southern Benguela upwelling system: phytoplankton dynamics. Prog Oceanogr 28: 39–64.
- Pospelova, V., and Head, M.J. (2002) Islandinium brevispinosum sp. nov. (Dinoflagellata), a new organic-walled dinoflagellate cyst from modern estuarine sediments of New England (USA). J Phycol 38: 593–601.
- Rafter, P.A., Sigman, D.M., and Mackey, K.R.M. (2017) Recycled iron fuels new production in the eastern equatorial Pacific Ocean. Nat Commun 8: 1100.
- Rii, Y.M., Duhamel, S., Bidigare, R.R., Karl, D.M., Repeta, D.J., and Church, M.J. (2016) Diversity and productivity of photosynthetic picoeukaryotes in biogeochemically distinct regions of the south East Pacific Ocean. Limnol Oceanogr 61: 806–824.
- Sakamoto, C.M., Millero, F.J., Yao, W., Friederich, G.E., and Chavez, F.P. (1998) Surface seawater distributions of inorganic carbon and nutrients around the Galapagos Islands: results from the PlumEx experiment using automated chemical mapping. Deep-Sea Res Part II: Top Stud Oceanogr 45: 1055–1071.
- Salomon, P., and Stolte, W. (2010) Predicting the population dynamics in Amoebophrya parasitoids and their dinoflagellate hosts using a mathematical model. Mar Ecol Prog Ser 419: 1–10.
- Santoso, A., Mcphaden, M.J., and Cai, W. (2017) The defining characteristics of ENSO extremes and the strong 2015/2016 El Niño. Rev Geophys 55: 1079–1129.
- Sartory, D.P., and Grobbelaar, J.U. (1984) Extraction of chlorophyll a from freshwater phytoplankton for spectrophotometric analysis. Hydrobiologia 114: 177–187.
- Schaeffer, B.A., Morrison, J.M., Kamykowski, D., Feldman, G.C., Xie, L., Liu, Y., et al. (2008) Phytoplankton biomass distribution and identification of productive habitats within the Galapagos Marine Reserve by MODIS, a surface acquisition system, and in-situ measurements. Remote Sens Environ 112: 3044–3054.
- Shang, L., Hu, Z., Deng, Y., Liu, Y., Zhai, X., Chai, Z., et al. (2019) Metagenomic sequencing identifies highly diverse assemblages of dinoflagellate cysts in sediments from ships' ballast tanks. Microorganisms 7: 250.
- Smayda, T.J. (2000) Ecological features of harmful algal blooms in coastal upwelling ecosystems. Afr J Mar Sci 22: 219–253.
- Smayda, T.J., and Trainer, V.L. (2010) Dinoflagellate blooms in upwelling systems: seeding, variability, and contrasts with diatom bloom behaviour. Prog Oceanogr 85: 92–107.
- Sweet, W.V., Morrison, J.M., Kamykowski, D., Schaeffer, B.A., Banks, S., and McCulloch, A. (2007) Water mass seasonal variability in the Galápagos Archipelago. Deep Sea Res Part 1 Oceanogr Res Pap 54: 2023–2035.
- Tapia, M., and Naranjo, C. (2012) Aspectos oceanográficos del plancton y su relación con el frente ecuatorial, durante septiembre del 2011. Acta Oceanográfica del Pacífico 17: 67–91.
- Tilstone, G.H., Taylor, B.H., Blondeau-Patissier, D., Powell, T., Groom, S.B., Rees, A.P., and Lucas, M.I. (2015) Comparison of new and primary production models using SeaWiFS data in contrasting hydrographic zones of the northern North Atlantic. Remote Sens Environ 156: 473–489.
- Torres, G. (1998) Variabilidad anual del fitoplancton marino en áreas costeras de La Libertad y Manta (Ecuador), su inter-relación con eventos El Niño. Acta Oceanográfica del Pacífico 9: 115–128.
- Torres, G., and Tapia, M. (2000) Distribución del fitoplancton y su comportamiento en el afloramiento en las Islas Galápagos. Acta Oceanográfica del Pacífico 10: 137–150.
- Torres, G., and Tapia, M. (2002) Distribución del fitoplancton en la región costera del mar ecuatoriano, durante diciembre 2000. Acta Oceanográfica del Pacífico 11: 63–72.
- Torres, G., and Tapia, M.E. (1998) Distribución del primer nivel trófico (fitoplancton) en el Pacífico ecuatoriano, período 1996-1997 (pre-El Niño). Acta Oceanográfica del Pacífico 9: 79–94.
- Yokouchi, K., Onuma, R., and Horiguchi, T. (2018) Ultrastructure and phylogeny of a new species of mixotrophic dinoflagellate, Paragymnodinium stigmaticum sp. nov. (Gymnodiniales, Dinophyceae). Phycologia 57: 539–554. https://doi.org/10.2216/17-140.1.