The effects of temperature on plasticity, shape symmetry and seasonal variation in the freshwater benthic green microalga Micrasterias thomasiana

Hydrobiological Bulletin
Jiří Neustupa1, Kateřina Woodard1
1Department of Botany, Faculty of Science, Charles University, Benatska 2, 12801, Prague, Czech Republic

Tóm tắt

AbstractDesmids are usually abundant in shallow peatland pools. In these localities, water temperature is closely linked to seasonal fluctuations in air temperature, so with increasing temperature extremes in temperate ecosystems, these microalgae are exposed to conditions of high-temperature stress. We investigated whether the shape, size, and growth rates of Micrasterias thomasiana, a frequently occurring species, are associated with varying temperatures in cultures and natural populations. The research was based on parallel analysis of clonal populations in temperature levels from 13 to 33 °C as well as cells from natural populations collected during the season. The effects of high temperature on morphological plasticity and fluctuating asymmetry in the shape of cellular parts were investigated by the landmark-based geometric morphometrics. The results showed that variation among individuals and fluctuating asymmetry between the lateral lobes of Micrasterias cells increased at 29 °C and in natural samples taken in July and October. In parallel, the size of semicells growing at temperatures above 25 °C decreased compared to those grown at lower temperatures. However, the temperature effects on shape and size were not directly related to the growth rates. The overall bilateral asymmetry between semicell halves did not change in relation to varying temperatures. In general, the results showed that morphological variation in natural populations of M. thomasiana reflected seasonal cycles and corresponded to plasticity associated with temperature changes in clonal cultures. It might therefore be possible to use these phenotypic markers as indicators of thermal stress in natural populations inhabiting shallow pools in peatlands.

Từ khóa


Tài liệu tham khảo

Adams DC, Otárola-Castillo E (2013) Geomorph: an R package for the collection and analysis of geometric morphometric shape data. Meth Ecol Evol 4:393–399. https://doi.org/10.1111/2041-210X.12035

Adams GL, Pichler DE, Cox EJ, O’Gorman EJ, Seeney A, Woodward G, Reuman DC (2013) Diatoms can be an important exception to temperature–size rules at species and community levels of organization. Glob Change Biol 19:3540–3552. https://doi.org/10.1111/gcb.12285

Andersen RA (2005) Algal culturing techniques. Elsevier Acad Press, London

Anderson MJ (2017) Permutational multivariate analysis of variance (PERMANOVA). In: Balakrishnan N, Colton T, Everitt B, Piegorsch W, Ruggeri F, Teugels JL (eds) Wiley StatsRef: statistics reference online. Wiley, Oxford, pp 1–15. https://doi.org/10.1002/9781118445112.stat07841

Atkinson D, Ciotti BJ, Montagnes DJS (2003) Protists decrease in size linearly with temperature: ca. 2.5% °C–1. Proc R Soc Lond B Biol Sci 270:2605–2611. https://doi.org/10.1098/rspb.2003.2538

Benítez HA, Lemic D, Villalobos-Leiva A, Bažok R, Órdenes-Claveria R, Pajač Živkovič I, Mikac KM (2020) Breaking symmetry: Fluctuating asymmetry and geometric morphometrics as tools for evaluating developmental instability under diverse agroecosystems. Symmetry 12:1789. https://doi.org/10.3390/sym12111789

Bookstein FL (2018) A course in morphometrics for biologists. Cambridge Univ Press, Cambridge. https://doi.org/10.1017/9781108120418

Brook AJ (1981) The biology of desmids. Blackwell, Oxford

Cardini A, Seetah K, Barker G (2015) How many specimens do I need? Sampling error in geometric morphometrics: testing the sensitivity of means and variances in simple randomized selection experiments. Zoomorphology 134:149–163. https://doi.org/10.1007/s00435-015-0253-z

CHMI (2023) Daily meteorological data. Czech Hydrometeorological Institute. https://www.chmi.cz/historicka-data/pocasi/denni-data/Denni-data-dle-z.-123-1998-Sb. Accessed 24 July 2023

Coesel PFM, Meesters J (2007) Desmids of the lowlands. KNNV Publ, Zeist

Dryden IL (2021) Shapes package. R Foundation for Statistical Computing. https://www.R-project.org. Accessed 24 July 2023

Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeont Electr 4:1–9

Jacobs AFG, Jetten TH, Lucassen DC, Heusinkveld BG, Nieveen JP (1997) Diurnal temperature fluctuations in a natural shallow water body. Agric for Meteorol 88:269–277. https://doi.org/10.1016/S0168-1923(97)00039-7

Jaroš F, Klouda J (2021) Introduction. In: Jaroš F, Klouda J (eds) Adolf Portmann—a thinker of self-expressive life. Springer, Cham, pp 1–9

Klingenberg CP (2015) Analyzing fluctuating asymmetry with geometric morphometrics: concepts, methods, and applications. Symmetry 7:843–934. https://doi.org/10.3390/sym7020843

Klingenberg CP (2019) Phenotypic plasticity, developmental instability, and robustness: the concepts and how they are connected. Front Ecol Evol 7:56. https://doi.org/10.3389/fevo.2019.00056

Klingenberg CP, Barluenga M, Meyer A (2002) Shape analysis of symmetric structures: quantifying variation among individuals and asymmetry. Evolution 56:1909–1920. https://doi.org/10.1111/j.0014-3820.2002.tb00117.x

Lürling M, Van Donk E (1999) Grazer-induced colony formation in Scenedesmus acutus (Chlorophyceae): ecomorph expression at different temperatures. J Phycol 35:1120–1126. https://doi.org/10.1046/j.1529-8817.1999.3561120.x

Lütz-Meindl U (2016) Micrasterias as a model system in plant cell biology. Front Pl Sci 7:999. https://doi.org/10.3389/fpls.2016.00999

Meindl U (1990) Effects of temperature on cytomorphogenesis and ultrastructure ofMicrasterias denticulata Bréb. Protoplasma 157:3–18. https://doi.org/10.1007/BF01322635

Meindl U (1993) Micrasterias cells as a model system for research on morphogenesis. Microbiol Rev 57:415–433. https://doi.org/10.1128/mr.57.2.415-433.1993

Morabito G, Oggioni A, Caravati E, Panzani P (2007) Seasonal morphological plasticity of phytoplankton in Lago Maggiore (N. Italy). Hydrobiologia 578:47–57. https://doi.org/10.1007/s10750-006-0432-5

Mpho M, Callaghan A, Holloway GJ (2002) Temperature and genotypic effects on life history and fluctuating asymmetry in a field strain of Culex pipiens. Heredity 88:307–312. https://doi.org/10.1038/sj.hdy.6800045

Naselli-Flores L, Padisák J (2023) Analysis of morphological traits as a tool to identify the realized niche of phytoplankton populations: what do the shape of planktic microalgae, Anna Karenina and Vincent van Gogh have in common? Hydrobiologia. https://doi.org/10.1007/s10750-023-05195-6

Neustupa J (2016) Static allometry of unicellular green algae: scaling of cellular surface area and volume in the genus Micrasterias (Desmidiales). J Evol Biol 29:292–305. https://doi.org/10.1111/jeb.12781

Neustupa J (2017) Asymmetry and integration of cellular morphology in Micrasterias compereana. BMC Evol Biol 17:1. https://doi.org/10.1186/s12862-016-0855-1

Neustupa J, Stastny J (2018) Symmetry breaking of the cellular lobes closely relates to phylogenetic structure within green microalgae of the Micrasterias lineage (Zygnematophyceae). PeerJ 6:e6098. https://doi.org/10.7717/peerj.6098

Neustupa J, Stastny J, Hodac L (2008) Temperature-related phenotypic plasticity in the green microalga Micrasterias rotata. Aquat Microb Ecol 51:77–86. https://doi.org/10.3354/ame01184

Neustupa J, Stastny J, Woodard K (2023) Ecological monitoring of disturbed mountain peatlands: an analysis based on desmids. Biodiv Conserv 32:2671–2691. https://doi.org/10.1007/s10531-023-02624-9

Neustupa J, Woodard K (2023) Supplementary data to "The effects of temperature on plasticity, shape symmetry and seasonal variation in freshwater benthic green microalga Micrasterias thomasiana" Zenodo. https://doi.org/10.5281/zenodo.8189080

Nishizaki MT, Barron S, Carew E (2015) Thermal stress increases fluctuating asymmetry in marine mussels: environmental variation and developmental instability. Ecosphere 6:85. https://doi.org/10.1890/ES14-00399.1

Portmann A (1960) Neue Wege der Biologie. R. Piper & Co Verl, München

Portmann A (2021) New fronts of biological work. In: Jaroš F, Klouda J (eds) Adolf Portmann—a thinker of self-expressive life. Springer, Cham, pp 13–21

Ralfs J (1848) British desmidieae. Reeve, Benham, and Reeve, Wheldon & Wesleyss London

R Core Team (2021) A language and environment for statistical computing. R Foundation for Statistical Computing. https://www.r-project.org. Accessed 24 July 2023

Rohlf FJ (2015) The tps series of software. Hystrix Ital J Mammal 26:9–12. https://doi.org/10.4404/hystrix-26.1-11264

Santos MAD, Ferragut C, Simoes NR, Da Silva DML, Moura CWN (2022) What are the main environmental predictors of diferences in the community structure of periphytic desmids in a semi-arid foodplain lake? Aquat Ecol 56:1037–1053. https://doi.org/10.1007/s10452-022-09957-7

Savriama Y, Neustupa J, Klingenberg CP (2010) Geometric morphometrics of symmetry and allometry in Micrasterias rotata (Zygnematophyceae, Viridiplantae). Nova Hedw Beih 136:43–54. https://doi.org/10.1127/1438-9134/2010/0136-0043

Stamenković M, Hanelt D (2011) Growth and photosynthetic characteristics of several Cosmarium strains (Zygnematophyceae, Streptophyta) isolated from various geographic regions under a constant light-temperature regime. Aquat Ecol 45:455–472. https://doi.org/10.1007/s10452-011-9367-7

Stamenković M, Hanelt D (2017) Geographic distribution and ecophysiological adaptations of desmids (Zygnematophyceae, Streptophyta) in relation to PAR, UV radiation and temperature: a review. Hydrobiologia 787:1–26. https://doi.org/10.1007/s10750-016-2958-5

Škaloud P, Nemjová K, Veselá J, Černá K, Neustupa J (2011) A multilocus phylogeny of the desmid genus Micrasterias (Streptophyta): evidence for the accelerated rate of morphological evolution in protists. Mol Phylog Evol 61:933–943. https://doi.org/10.1016/j.ympev.2011.08.018

Tabi A, Garnier A, Pennekamp F (2020) Testing multiple drivers of the temperature–size rule with nonlinear temperature increase. Funct Ecol 34:2503–2512. https://doi.org/10.1111/1365-2435.13676

Tanneberger F, Tegetmeyer C, Busse S et al (2017) The peatland map of Europe. Mires Peat 19(22):1–17. https://doi.org/10.19189/MaP.2016.OMB.264

Weiss D, Lütz C, Lütz-Meindl U (1999) Photosynthesis and heat response of the green alga Micrasterias denticulata (Desmidiaceae). Z Naturforsch 54:508–516. https://doi.org/10.1515/znc-1999-7-809

Weiss D, Lütz-Meindl U (1999) Heat response in the green alga Micrasterias denticulata (Desmidiaceae): immunodetection and localization of BiP and heat shock protein 70. Nova Hedw 69:217–228. https://doi.org/10.1127/nova.hedwigia/69/1999/217

West-Eberhard MJ (1989) Phenotypic plasticity and the origins of diversity. Ann Rev Ecol Syst 20:249–278. https://doi.org/10.1146/annurev.es.20.110189.001341

Zelditch ML, Swiderski DL, Sheets DH (2012) Geometric morphometrics for biologists: a primer. Elsevier Acad Press, London

Zohary T, Fishbein T, Shlichter M, Naselli-Flores L (2017) Larger cell or colony size in winter, smaller in summer—a pattern shared by many species of Lake Kinneret phytoplankton. Inland Wat 7:200–209. https://doi.org/10.1080/20442041.2017.1320505

Zohary T, Flaim G, Sommer U (2021) Temperature and the size of freshwater phytoplankton. Hydrobiologia 848:143–155. https://doi.org/10.1007/s10750-020-04246-6

Thông tin
Thông tin xuất bản

Hydrobiological Bulletin

Thông tin tác giả