Seasonal variation in size structure and production of autotrophic plankton community in eutrophied, low-light environment: A focus on Mesodinium rubrum

Labucis, Atis; Labuce, Astra; Jurgensone, Iveta; Barda, Ieva; Andersone, Ingrida; Ikauniece, Anda

doi:10.1016/j.oceano.2022.11.003

Artykuł - szczegóły

Tytuł artykułu

Seasonal variation in size structure and production of autotrophic plankton community in eutrophied, low-light environment: A focus on Mesodinium rubrum

Autorzy

Labucis Atis , Labuce Astra , Jurgensone Iveta , Barda Ieva , Andersone Ingrida , Ikauniece Anda

Wybrane pełne teksty z tego czasopisma

Identyfikatory

DOI

10.1016/j.oceano.2022.11.003

Warianty tytułu

Języki publikacji

Abstrakty

Temporal variations in the primary production of the size-fractionated autotrophic plankton community were studied in coastal-estuarine waters of the eutrophic Gulf of Riga, Baltic Sea. The community was net-autotrophic during spring and summer and net-heterotrophic during autumn. The results of the present study clearly demonstrate strong covariation between net primary production (NPP) and <56 µm fractionated community biomass, particularly small-sized (16–33 µm) Mesodinium rubrum, implying that the majority of NPP stems from the lower end of the size spectrum. A pronounced size distribution shift was observed within the M. rubrum population. Large-sized (length ≥34 µm) M. rubrum was the most abundant in the first half of the productive season (until week 24), whereas small-sized M. rubrum dominated during the stratified period.

Słowa kluczowe

primary production coastal brackish Gulf of Riga Baltic Sea ciliate

Wydawca

Polish Academy of Sciences, Institute of Oceanology
Elsevier

Czasopismo

Oceanologia

Rocznik

2023

Tom

Vol. 65 (2)

Strony

398--409

Opis fizyczny

Bibliogr. 72 poz., map., rys., tab., wykr.

Twórcy

autor

Labucis Atis

atis.labucis@lhei.lv

Latvian Institute of Aquatic Ecology, Riga, Latvia

https://orcid.org/0000-0002-2528-2142

autor

Labuce Astra

Latvian Institute of Aquatic Ecology, Riga, Latvia

https://orcid.org/0000-0002-2764-678X

autor

Jurgensone Iveta

Latvian Institute of Aquatic Ecology, Riga, Latvia

autor

Barda Ieva

Latvian Institute of Aquatic Ecology, Riga, Latvia

autor

Andersone Ingrida

Latvian Institute of Aquatic Ecology, Riga, Latvia

https://orcid.org/0000-0002-1642-9560

autor

Ikauniece Anda

Latvian Institute of Aquatic Ecology, Riga, Latvia

https://orcid.org/0000-0002-1720-8049

Bibliografia

1. BACC II, 2015. Second Assessment of Climate Change for the Baltic Sea Basin. Springer Int. Publ. https://doi.org/10.1007/978-3-319-16006-1
2. Bender, M., Grande, K., Johnson, K., Marra, J., Williams, P.J.L., Sieburth, J., Pilson, M., Langdon, C., Hitchcock, G., Orchardo, J., Hunt, C., Donaghay, P., Heinemann, K., 1987. A comparison of four methods for determining planktonic community production. Limnol. Oceanogr. 32, 1085-1098.
3. Berzinsh, V., 1995. Hydrology. Ecosystem of the Gulf of Riga between 1920 and 1990. Academia 5, 7-8.
4. Calbet, A., Landry, M.R., 2004. Phytoplankton growth, microzooplankton grazing, and carbon cycling in marine systems. Limnol. Oceanogr. 49, 51-57. https://doi.org/10.4319/lo.2004.49.1.0051
5. Cloern, J.E., Cole, B.E., Hager, S.W., 1994. Notes on a Mesodinium rubrum red tide in San Francisco Bay (California, USA). J. Plankton Res. 16, 1269-1276.
6. Cotti-Rausch, B.E., Lomas, M.W., Lachenmyer, E.M., Baumann, E.G., Richardson, T.L., 2020. Size-fractionated biomass and primary productivity of Sargasso Sea phytoplankton. Deep Sea Res. Pt. I 156, 103141. https://doi.org/10.1016/j.dsr.2019.103141
7. Crawford, D.W., 1989. Mesodinium rubrum: the phytoplankter that wasn’t. Mar. Ecol. Prog. Ser. 58, 161-174.
8. Crawford, D.W., Lindholm, T., 1997. Some observations on vertical distribution and migration of the phototrophic ciliate Mesodinium rubrum (= Myrionecta rubra) in a stratified brackish inlet. Aquat. Microb. Ecol. 13, 267-274. https://doi.org/10.3354/ame013267
9. Daneri, G., Crawford, D.W., Purdie, D.A., 1992. Algal blooms in coastal waters: a comparison between two adaptable members of the phytoplankton, Phaeocystis sp. and Meso dinium rubrum. In: Vollenweider, R.A., Marchetti, R., Viviani, R. (Eds.), Marine Coastal Eutrophication. Elsevier, Amsterdam, 879-890. https://doi.org/10.1016/B978-0-444-89990-3.50076-6
10. De Jong, S., 1993. SIMPLS: an alternative approach to partial least squares regression. Chemometr. Intell. Lab. 251-263. https://doi.org/10.1016/0169-7439(93)85002-X
11. Falkowski, P.G., Oliver, M.J., 2007. Mix and match: how climate selects phytoplankton. Nat. Rev. Microbiol. 5, 813-819. https:// doi.org/10.1038/nrmicro1751
12. Fenchel, T., 1988. Marine plankton food chains. Annu. Rev. Ecol. Syst. 19, 19-38.
13. Gaillard, S., Charrier, A., Malo, F., Carpentier, L., Bougaran, G., Hégaret, H., Réveillon, D., Hess, P., Séchet, V., 2020. Combined Effects of Temperature, Irradiance, and pH on Teleaulax amphioxeia (Cryptophyceae) Physiology and Feeding Ratio For Its Predator Mesodinium rubrum (Ciliophora). J. Phycol. 56, 775- 783. https://doi.org/10.1111/jpy.12977
14. Garcia-Cuetos, L., Moestrup, Ø., Hansen, P.J., 2012. Studies on the genus Mesodinium II. Ultrastructural and molecular investigations of five marine species help clarifying the taxonomy
A. Labucis, A. Labuce, I. Jurgensone et al. J. Eukaryot. Microbiol. 59, 374-400. https://doi.org/10.1111/j.1550-7408.2012.00630.x
15. Grasshoff, P., Ehrhardt, M., Kremling, K., 1983. Methods of seawa ter analysis. Verlag Chemie, Weinheim, 419 pp.
16. Griffiths, J.R., Hajdu, S., Downing, A.S., Hjerne, O., Lars son, U., Winder, M., 2016. Phytoplankton community interactions and environmental sensitivity in coastal and offshore habitats. Oikos 125, 1134-1143. https://doi.org/10.1111/oik. 02405
17. Gustafson Jr, D.E., Stoecker, D.K., Johnson, M.D., Van Heukelem, W.F., Sneider, K., 2000. Cryptophyte algae are robbed of their organelles by the marine ciliate Mesodinium rubrum. Nature 405, 1049-1052. https://doi.org/10.1038/35016570
18. Hajdu, S., Höglander, H., Larsson, U., 2007. Phytoplankton vertical distributions and composition in Baltic Sea cyanobacterial blooms. Harmful Algae 6, 189-205. https://doi.org/10.1016/j.hal.2006.07.006
19. Hansen, P.J., Fenchel, T., 2006. The bloom-forming ciliate Mesodinium rubrum harbours a single permanent endosymbiont. Mar. Biol. Res. 2, 169-177. https://doi.org/10.1080/17451000600719577
20. Haraguchi, L., Jakobsen, H.H., Lundholm, N., Carstensen, J., 2018. Phytoplankton Community Dynamic: A Driver for Ciliate Trophic Strategies. Front. Mar. Sci. 5. https://doi.org/10.3389/fmars. 2018.00272
21. Havenhand, J.N., 2012. How will ocean acidification affect Baltic sea ecosystems? an assessment of plausible impacts on key functional groups. Ambio 41, 637-644. https://doi.org/10.1007/s13280-012-0326-x
22. HELCOM, 2017. Manual for Marine Monitoring in the COMBINE Programme of HELCOM. http://www.helcom.fi/actionareas/monitoring-and-assessment/manuals-and-guidelines/combine-manual
23. Herfort, L., Peterson, T.D., Prahl, F.G., McCue, L.A., Needoba, J.A., Crump, B.C., Roegner, G.C., Campbell, V., Zuber, P., 2012. Red Waters of Myrionecta rubra are Biogeochemical Hotspots for the Columbia River Estuary with Impacts on Primary/Secondary Productions and Nutrient Cycles. Estuaries Coasts 35, 878-891. https://doi.org/10.1007/s12237-012-9485-z
24. Höglander, H., Larsson, U., Hajdu, S., 2004. Vertical distribution and settling of spring phytoplankton in the offshore NW Baltic Sea proper. Mar. Ecol. Prog. Ser. 283, 15-27. https://doi.org/10.3354/meps283015
25. Johansson, M., 2004. Annual variability in ciliate community structure, potential prey and predators in the open northern Baltic Sea proper. J. Plankton Res. 26, 67-80. https://doi.org/10.1093/plankt/fbg115
26. Johnson, M.D., Beaudoin, D.J., Laza-Martinez, A., Dyhrman, S.T., Fensin, E., Lin, S., Merculief, A., Nagai, S., Pompeu, M., Setälä, O., Stoecker, D.K., 2016. The Genetic Diversity of Mesodinium and Associated Cryptophytes. Front. Microbiol. 7, 2017. https://doi.org/10.3389/fmicb.2016.02017
27. Johnson, M.D., Stoecker, D.K., 2005. Role of feeding in growth and photophysiology of Myrionecta rubra. Aquat. Microb. Ecol. 39, 303-312. https://doi.org/10.3354/ame039303
28. Johnson, M.D., Stoecker, D.K., Marshall, H.G., 2013. Seasonal dynamics of Mesodinium rubrum in Chesapeake Bay. J. Plankton Res. 35, 877-893. https://doi.org/10.1093/plankt/fbt028
29. Kotta, J., Lauringson, V., Martin, G., Simm, M., Kotta, I., Herkül, K., Ojaveer, H., 2008. Gulf of Riga and Pärnu Bay. In: Schiewer, U. (Ed.), Ecology of Baltic Coastal Waters. Springer, Heidelberg, Berlin, 217-243.
30. Kuhn, M., 2021. caret: Classification and Regression Training. R package version 6.0-90. https://CRAN.R-project.org/package=caret
31. Labucis, A., Purina, I., Labuce, A., Barda, I., Strake, S., 2017. Spring seasonal pattern of primary production in the Gulf of Riga (Baltic Sea) after a mild winter. Environ. Exp. Biol. 15, 247-255. https://doi.org/10.22364/eeb.15.26
32. Lancelot, C., Muylaert, K., 2011. 7.02 - Trends in Estuarine Phytoplankton Ecology. In: Wolanski, E., McLusky, D. (Eds.), Treatise on Estuarine and Coastal Science. Acad. Press, Waltham, 5-15. https://doi.org/10.1016/B978-0-12-374711-2.00703-8
33. Leles, S.G., Mitra, A., Flynn, K.J., Stoecker, D.K., Hansen, P.J., Cal bet, A., McManus, G.B., Sanders, R.W., Caron, D.A., Not, F., Hallegraeff, G.M., Pitta, P., Raven, J.A., Johnson, M.D., Glibert, P.M., Våge, S., 2017. Oceanic protists with different forms of acquired phototrophy display contrasting biogeographies and abundance. Proc. Biol. Sci. B 284 (1860). https://doi.org/10.1098/rspb.2017.0664
34. Liland, K.H., Mevik, B.H., Wehrens, R., 2022. pls: Partial Least Squares and Principal Component Regression. R package version 2.8-1. https://CRAN.R-project.org/package=pls
35. Lindholm, T., Mörk, A.-C., 1990. Depth maxima of Mesodinium rubrum (Lohmann) Hamburger & Buddenbrock - examples from a stratified Baltic Sea inlet. Sarsia 75, 53-64. https://doi.org/10.1080/00364827.1990.10413441
36. Lips, I., Lips, U., 2017. The Importance of Mesodinium rubrum at Post-Spring Bloom Nutrient and Phytoplankton Dynamics in the Vertically Stratified Baltic Sea. Front. Mar. Sci. 4, 407. https://doi.org/10.3389/fmars.2017.00407
37. Lischka, S., Bach, L.T., Schulz, K.-G., Riebesell, U., 2017. Ciliate and mesozooplankton community response to increasing CO2 levels in the Baltic Sea: insights from a large-scale mesocosm experiment. Biogeosciences 14, 447-466. https://doi.org/10.5194/bg-14-447-2017
38. Malone, T.C., Chervin, M.B., 1979. The production and fate of phytoplankton size fractions in the plume of the Hudson River, New York Bight. Limnol. Oceanogr. 24, 683-696.
39. Menden-Deuer, S., Lessard, E.J., 2000. Carbon to volume relationships for dinoflagellates, diatoms, and other protist plankton. Limnol. Oceanogr. 45, 569-579. https://doi.org/10.4319/lo.2000.45.3.0569
40. Mevik, B.H., Wehrens, R., 2015. Introduction to the pls Package. Help Section of The “Pls” Package of R Studio Software, 1-23.
41. Mitra, A., Flynn, K.J., Burkholder, J.M., Berge, T., Calbet, A., Raven, J.A., Granéli, E., Glibert, P.M., Hansen, P.J., Stoecker, D.K., Thingstad, F., Tillmann, U., Våge, S., Wilken, S., Zubkov, M.V., 2014. The role of mixotrophic protists in the biological carbon pump. Biogeosciences 11, 995-1005. https://doi.org/10.5194/bg-11-995-2014
42. Mitra, A., Flynn, K.J., Tillmann, U., Raven, J.A., Caron, D., Stoecker, D.K., Not, F., Hansen, P.J., Hallegraeff, G., Sanders, R., Wilken, S., McManus, G., Johnson, M., Pitta, P., Våge, S., Berge, T., Calbet, A., Thingstad, F., Jeong, H.J., Burkholder, J., Glibert, P.M., Granéli, E., Lundgren, V., 2016. Defining Planktonic Protist Functional Groups on Mechanisms for Energy and Nutrient Acquisition: Incorporation of Diverse Mixotrophic Strategies. Protist 167, 106-120. https://doi.org/10.1016/j.protis.2016.01.003
43. Moeller, H.V., Johnson, M.D., Falkowski, P.G., 2011. Photoacclimation in the phototrophic marine ciliate Mesodinium rubrum (Cil iophora). J. Phycol. 47, 324-332. https://doi.org/10.1111/j. 1529-8817.2010.00954.x
44. Montagnes, D.J.S., Allen, J., Brown, L., Bulit, C., Davidson, R., Díaz-Avalos, C., Fielding, S., Heath, M., Holliday, N.P., Rasmussen, J., Sanders, R., Waniek, J.J., Wilson, D., 2008. Fac tors controlling the abundance and size distribution of the phototrophic ciliate Myrionecta rubra in open waters of the North Atlantic. J. Eukaryot. Microbiol. 55, 457-465. https://doi.org/10.1111/j.1550-7408.2008.00344.x
45. Mousseau, L., Fortier, L., Legendre, L., 1998. Annual production of fish larvae and their prey in relation to size-fractionated primary production (Scotian Shelf, NW Atlantic). ICES J. Mar. Sci. 55, 44- 57. https://doi.org/10.1006/jmsc.1997.0224
46. Nielsen, T.G., Kiørboe, T., 1994. Regulation of zooplankton biomass and production in a temperate, coastal ecosystem. 2. Ciliates. Limnol. Oceanogr. 39, 508-519.
47. Nishitani, G., Yamaguchi, M., 2018. Seasonal succession of ciliate Mesodinium spp. with red, green, or mixed plastids and their association with cryptophyte prey. Sci. Rep. 8, 17189. https://doi.org/10.1038/s41598-018-35629-4
48. Olenina, I., Hajdu, S., Edler, L., Andersson, A., Wasmund, N., Busch, S., Gobel, J., Gromisz, S., Huseby, S., Huttunen, M., Jaanus, A., Kokkonen, P., Ledaine, I., Niemkiewicz, E., 2006. Biovolumes and size-classes of phytoplankton in the Baltic Sea. Baltic Sea Environ. Proc. No 106. https://epic.awi.de/30141/1/bsep106.pdf
49. Olesen, M., Lundsgaard, C., Andrushaitis, A., 1999. Influence of nutrients and mixing on the primary production and community respiration in the Gulf of Riga. J. Marine Syst. 23, 127-143. https://doi.org/10.1016/S0924-7963(99)00054-8
50. Olli, K., Heiskanen, A.-S., Seppälä, J., 1996. Development and fate of Eutreptiella gymnastica bloom in nutrient-enriched enclosures in the coastal Baltic Sea. J. Plankton Res. 18, 1587-1604. https://doi.org/10.1093/plankt/18.9.1587
51. Omstedt, A., Edman, M., Claremar, B., Frodin, P., Gustafsson, E., Humborg, C., Hägg, H., Mörth, M., Rutgersson, A., Schurgers, G., Smith, B., Wällstedt, T., Yurova, A., 2012. Future changes in the Baltic Sea acid—base (pH) and oxygen balances. Tellus B Chem. Phys. Meteorol. 64, 19586. https://doi.org/10.3402/tellusb.v64i0.19586
52. Probyn, T.A., 1990. Size-fractionated measurements of nitrogen uptake in aged upwelled waters: Implications for pelagic food webs. Limnol. Oceanogr. 35, 202-210. https://doi.org/10.1093/plankt/fbh110
53. Purina, I., Labucis, A., Barda, I., Jurgensone, I., Aigars, J., 2018. Primary productivity in the Gulf of Riga (Baltic Sea) in relation to phytoplankton species and nutrient variability. Oceanologia 60 (4), 544-552. https://doi.org/10.1016/j.oceano.2018.04.005
54. R Core Team, 2019. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Rychert, K., 2004. The size structure of the Mesodinium rubrum population in the Gdańsk Basin. Oceanologia 46 (3), 439-444. https://old.iopan.pl/oceanologia/463ryche.pdf
55. Sanders, R.W., 1995. Seasonal distributions of the photosynthesizing ciliates Laboea strobila and Myrionecta rubra (= Mesodinium rubrum) in an estuary of the Gulf of Maine. Aquat. Microb. Ecol. 9, 237-242.
56. Sin, Y., 2000. Seasonal variations of size-fractionated phytoplankton along the salinity gradient in the York River estuary, Virginia (USA). J. Plankton Res. 22, 1945-1960. https://doi.org/10.1093/plankt/22.10.1945
57. Skudra, M., Lips, U., 2017. Characteristics and inter-annual changes in temperature, salinity and density distribution in the Gulf of Riga. Oceanologia 59 (1), 37-48. https://doi.org/10.1016/j.oceano.2016.07.001
58. Sommer, U., Adrian, R., De Senerpont Domis, L., Elser, J.J., Gaedke, U., Ibelings, B., Jeppesen, E., Lürling, M., Molinero, J.C., Mooij, W.M., van Donk, E., Winder, M., 2012. Beyond the Plankton Ecology Group (PEG) Model: Mechanisms Driving Plankton Succession. Annu. Rev. Ecol. Evol. Syst. 43, 429- 448. https://doi.org/10.1146/annurev-ecolsys-110411-160251
59. Sommer, U., Charalampous, E., Genitsaris, S., Moustaka-Gouni, M., 2016. Benefits, costs and taxonomic distribution of marine phytoplankton body size. J. Plankton Res. 39, 494-508. https://doi.org/10.1093/plankt/fbw071
60. Soria-Píriz, S., García-Robledo, E., Papaspyrou, S., Aguilar, V., Seguro, I., Acuña, J., Morales, Á., Corzo, A., 2017. Size fractionated phytoplankton biomass and net metabolism along a tropical estuarine gradient. Limnol. Oceanogr. 62, S309-S326. https://doi.org/10.1002/lno.10562
61. Spilling, K., Markager, S., 2008. Ecophysiological growth characteristics and modeling of the onset of the spring bloom in the Baltic Sea. J. Marine Syst. 73, 323-337. https://doi.org/10.1016/j.jmarsys.2006.10.012
62. Stoecker, D.K., Putt, M., Davis, L.H., Michaels, A.E., 1991. Photo synthesis in Mesodinium rubrum: species-specific measurements and comparison to community rates. Mar. Ecol. Prog. Ser. 73, 245-252.
63. Taylor, F.J.R., Blackbourn, D.J., Blackbourn, J., 1971. The Red-Water Ciliate Mesodinium rubrum and its “Incomplete Symbionts”: A Review Including New Ultrastructural Observations. J. Fish. Res. Board Can. 28, 391-407.
64. Tong, M., Smith, J.L., Kulis, D.M., Anderson, D.M., 2015. Role of dissolved nitrate and phosphate in isolates of Mesodinium rubrum and toxin-producing Dinophysis acuminata. Aquat. Microb. Ecol. 75, 169-185. https://doi.org/10.3354/ame01757
65. Tremblay, J.-E., Legendre, L., 1994. A model for the size fractionated biomass and production of marine phytoplankton. Limnol. Oceanogr. 39, 2004—2014. https://doi.org/10.4319/lo.1994.39.8.2004
66. Utermöhl, H., 1958. Zur Vervollkommnung Der Quantitativen Phytoplankton-Methodik. Mitt. Internat. Verein. Limnol. 9, 1-38. Van Niel, C.B., 1949. The comparative biochemistry of photosynthesis. Am. Sci. 37, 371-383.
67. Wasmund, N., Andrushaitis, A., Łysiak-Pastuszak, E., Müller-Karulis, B., Nausch, G., Neumann, T., Ojaveer, H., Olenina, I., Postel, L., Witek, Z., 2001. Trophic status of the south-eastern Baltic sea: a comparison of coastal and open areas. Estuar. Coast. Shelf Sci. 53 (6), 1-16. https://doi.org/10.1006/ecss.2001.0828
68. Wasmund, N., Uhlig, S., 2003. Phytoplankton trends in the Baltic Sea. ICES J. Mar. Sci. 60, 177-186. https://doi.org/10.1016/S1054-3139(02)00280-1
69. Wassman, P., Tamminen, T., 1999. Pelagic eutrophication and sed imentation in the Gulf of Riga: a synthesis. J. Marine Syst. 23, 269-283. https://doi.org/10.1016/S0924-7963(99)00062-7
70. Wickham, H., 2009. ggplot2: Elegant Graphics for Data Analysis. Springer Science & Business Media.
71. Wilkerson, F.P., Grunseich, G., 1990. Formation of blooms by the symbiotic ciliate Mesodinium rubrum: the significance of nitrogen uptake. J. Plankton Res. 12, 973-989. https://doi.org/10.1093/plankt/12.5.973
72. Winder, M., Schindler, D.E., 2004. Climate change uncouples trophic interactions in an aquatic ecosystem. Ecology 85, 2100-2106. https://doi.org/10.1890/04-0151 Witek, M., 1998. Annual changes of abundance and biomass of planktonic ciliates in the Gdańsk basin, southern Baltic. Int. Rev. Hydrobiol. 83, 163-182. https://doi.org/10.1002/iroh.19980830207

Uwagi

Opracowanie rekordu ze środków MEiN, umowa nr SONP/SP/546092/2022 w ramach programu "Społeczna odpowiedzialność nauki" - moduł: Popularyzacja nauki i promocja sportu (2022-2023). (PL)

Typ dokumentu

Bibliografia

Identyfikator YADDA

bwmeta1.element.baztech-8d510a0c-f92c-440e-a868-d0d0d5b239bf