Abstract
Many charophytes are rare and endangered algae species. All charophyte species significantly contribute to the stability and health of the ecosystems they inhabit. Charophytes survive in their habitats thanks to the longevity of the diaspores (oospores and gyrogonites) in the sediment. Many charophyte species have a specific phenology and can sometimes be overlooked in surveys of macrophyte vegetation. We monitored vegetation for three years and collected sediment from a small water body in Serbia to test the hypotheses that (a) Extant charophyte diaspores have promising, yet currently limited application as taxonomic markers, (b) Vegetation data on charophyte diversity may provide different information than data obtained by extracting diaspores from sediments and (c) parallel surveys of vegetation and sediments can provide a more comprehensive view of charophyte diversity compared to traditional annual vegetation monitoring. Diaspores proved to be promising taxonomic characters for charophyte identification. In our study, six taxa could be identified on a species level based on diaspores alone, while one species group (Chara spp.) requires further investigation as it could consist of up to four species. Compared to vegetation, the sediment survey provided different information on charophyte diversity and confirmed the presence of the species Sphaerochara intricata and Sphaerochara prolifera, which were never detected during the vegetation survey. Sediment studies conducted in parallel with vegetation studies provide important insight into the diversity of charophytes and the prospects for their habitat conservation.
Similar content being viewed by others
Data availability
The data that support the findings of this study are available from the corresponding author, Ivana Trbojević, upon reasonable request.
References
Abràmoff MD, Magalhães PJ, Ram SJ (2004) Image Processing with ImageJ. Biophoton Int 11(7):36–42
Alderton E, Sayer CD, Davies R, Lambert SJ, Axmacher JC (2017) Buried alive: aquatic plants survive in ‘ghost ponds’ under agricultural fields. Biol Conserv 212:105–110. https://doi.org/10.1016/j.biocon.2017.06.004
Alonso-Guillén JL (2011) Los carófitos en la restauración de ecosistemas acuáticos. Un caso práctico en el parc natural de l¿ Albufera de València. Dissertation, Universitat de València
Ayres KR, Sayer CD, Skeate ER et al (2008) Palaeolimnology as a tool to inform shallow lake management: an example from Upton Great Broad, Norfolk, UK. Biodivers Conserv 17:2153–2168. https://doi.org/10.1007/s10531-007-9223-1
Baastrup-Spohr L, Iversen L, Dahl-Nielsen J, Sand-Jensen K (2013) Seventy years of changes in the abundance of Danish charophytes. Freshw Biol 58(8):1682–1693. https://doi.org/10.1111/fwb.12159
Bhandari S, Momohara A, Paudayal KN (2009) Late Pleistocene plant macro-fossils from the Gokarna formation of the Kathmandu Valley Central Nepal. Bullet Dep Geol 12:75–88
Biggs J, Von Fumetti S, Kelly-Quinn M (2017) The importance of small waterbodies for biodiversity and ecosystem services: implications for policy makers. Hydrobiologia 793(1):3–39. https://doi.org/10.1007/s10750-016-3007-0
Blaženčić J (2014) Overview of the stoneworts (Charales) of Serbia with the estimation of the threat status. Bot Serb 38(1):121–130
Blaženčić J, Stevanović B, Blaženčić Ž, Stevanović V (2006) Red data list of charophytes in the Balkans. Biodivers Conserv 15(11):3445–3457. https://doi.org/10.1007/s10531-005-2008-5
Blindow I, Dahlke S, Dewart A, Flügge S, Hendreschke M, Kerkow A, Meyer J (2016) Long-term and interannual changes of submerged macrophytes and their associated diaspore reservoir in a shallow southern Baltic Sea bay: influence of eutrophication and climate. Hydrobiologia 778:121–136. https://doi.org/10.1007/s10750-016-2655-4
Blindow I, Carlsson M, van de Weyer K (2021) Re-Establishment techniques and transplantations of charophytes to support threatened species. Plants 10(9):1830. https://doi.org/10.3390/plants10091830
Blume M, Blindow I, Dahlke S, Vedder F (2009) Oospore variation in closely related Chara taxa. J Phycol 45(5):995–1002. https://doi.org/10.1111/j.1529-8817.2009.00725.x
Boissezon A, Auderset Joye D, Garcia T (2018) Temporal and spatial changes in population structure of the freshwater macroalga Nitellopsis obtusa (Desv.) J. Groves. Bot Lett 165(1):103–114. https://doi.org/10.1080/23818107.2017.1356239
Bonis A, Grillas P (2002) Deposition, germination and spatio-temporal patterns of charophyte propagule banks: a review. Aquat Bot 72(3–4):235–248. https://doi.org/10.1016/S0304-3770(01)00203-0
Casanova MT, Brock MA (1999) Charophyte occurrence, seed banks and establishment in farm dams in New South Wales. Aust J Bot 47(3):437–444. https://doi.org/10.1071/BT97099
Casanova MT (1997) Oospore variation in three species of Chara (Charales, Chlorophyta). Phycologia 36(4):274–280. https://doi.org/10.2216/i0031-8884-36-4-274.1
Charrad M, Ghazzali N, Boiteau V, Niknafs A (2014) NbClust: an R package for determining the relevant number of clusters in a data set. J Stat Softw 61:1–36. https://doi.org/10.18637/jss.v061.i06
Christodoulou MD, Clark JY, Culham A (2020) The Cinderella discipline: morphometrics and their use in botanical classification. Bot J Linn 194(4):385–396. https://doi.org/10.1093/botlinnean/boaa055
Corillion R (1957) Les Charophycées de France et de France et d’Europe Occidentale. Société Scientifique de Bretagne, Bretagne, p 499
Damnjanović B, Novković M, Vesić A, Živković M, Radulović S, Vukov D, Anđelković A, Cvijanović D (2019) Biodiversity-friendly designs for gravel pit lakes along the Drina River floodplain (the Middle Danube Basin, Serbia). Wetl Ecol Manag 27:1–22. https://doi.org/10.1007/s11273-018-9641-8
Digital Plant Atlas—RUG & DAI. Groningen Institute of Archaeology (GIA—RUG) and Deutsches Archäologisches Institut (DAI)—Berlin. Available at: https://www.plantatlas.eu/repository. Accessed 16 Feb 2023
Doege A, van de Weyer K, Becker R, Schubert H (2016) Bioindikation mit Characeen. In: Characeen Deutschlands AG (ed) Armleuchteralgen. Die Characeen Deutschlands. Springer, Berlin, pp 97–138
European Commission (1992) Council directive 92/43/EEC of 21 May 1992 on the conservation of natural habitats and of wild fauna and flora. Off J Eur Union L 206:7–50
European Commission (2000) Directive 2000/60/EC of the European Parliament and of the Council of 23 October 2000 establishing a framework for Community action in the field of water policy. Off J Eur Union L 327
Garcia A (1994) Pleistocene Charophyta from Arroyo Perucho Verna, Province of Entre Rios. Argent J Paleolimnol 10(1):53–58. https://doi.org/10.1007/BF00683146
Grillas P, Garcia-Murillo P, Geertz-Hansen O et al (1993) Submerged macrophyte seed bank in a Mediterranean temporary marsh: abundance and relationship with established vegetation. Oecologia 94(1):1–6. https://doi.org/10.1007/BF00317293
Groves J, Bullock-Webster GR (1924) The British Charophyta. Charae, vol 2. The Ray Society, London, p 129
Haas JN (1994) First identification key for charophyte oospores from central Europe. Eur J Phycol 29(4):227–235. https://doi.org/10.1080/09670269400650681
Holzhausen A, Porsche C, Schubert H (2017) Viability assessment and estimation of the germination potential of charophyte oospores: testing for site and species specificity. Bot Lett 165(1):147–158. https://doi.org/10.1080/23818107.2017.1393460
Holzhausen A, Nowak P, Ballot A, Becker R, Gebert J, Gregor T, Kenneth K, Lambert E, Pérez W, Raabe U, Schneider S, Stewart N, van de Weyer K, Wilde V, Schubert H (2023) Plastid DNA sequences and oospore characters of some European taxa of Tolypella section Tolypella (Characeae) identify five clusters, including one new cryptic Tolypella taxon from Sardinia, but they do not coincide with current morphological descriptions. Front Plant Sci 14:704. https://doi.org/10.3389/fpls.2023.1096181
Holzhausen A, Casanova M, Stewart N, Sayer C, Goldsmith B (2024) Extant oospores. In: Schubert H, Gregor T, Blindow I, Nat E, Stewart N, Romanov R, van de Weyer K, Denys L, Korsch H, Casanova M (eds) Characeae of Europe. Springer, Berlin (In Press)
Kassambara A, Mundt F (2020) factoextra: Extract and Visualize the Results of Multivariate Data Analyses R package version 1.0.7, https://CRAN.R-project.org/package=factoextra. Accessed 7 Apr 2023
Kirkbride JH, Gunn CR, Dallwitz MJ (2000) Family guide for fruits and seeds: descriptions, illustrations, identification, and information retrieval. Available at: https://www.delta-intkey.com/famfs/index.htm. Accessed 16 Feb 2023
Kolada A (2021) Charophyte variation in sensitivity to eutrophication affects their potential for the trophic and ecological status indication. Knowl Manag Aquat Ecosyst 422:30. https://doi.org/10.1051/kmae/2021030
Krause W (1986) Zur Bestimmungsmöglichkeit subfossiler Characeen-Oosporen an Beispielen aus Schweizer Seen. Vierteljahrsschrift Der Naturforschenden Gesellschaft in Zürich 141:295–313
Krause W (1997) Charales (Charophyceae). Süßwasserflora von Mitteleuropa. Gustav Fischer, Jena, p 202
Kröpelin S, Soulié-Märsche I (1991) Charophyte remains from Wadi Howar as evidence for deep Mid-Holocene freshwater lakes in the Eastern Sahara of Northwest Sudan. Quat Res 36(2):210–223. https://doi.org/10.1016/0033-5894(91)90026-2
Kuhn M (2022) caret: Classification and Regression Training. R package version 6.0-93. https://CRAN.R-project.org/package=caret Accessed 7 Apr 2023
Maechler M, Rousseeuw P, Struyf A, Hubert M, Hornik K (2022) cluster: Cluster Analysis Basics and Extensions. R package version 2.1.4, https://CRAN.R-project.org/package=cluster. Accessed 7 Apr 2023
Marković A, Blaženčić J, Tanasković A, Šinžar-Sekulić J (2023) Diversity and ecology of Charophytes from Vojvodina (Serbia) in relation to physico-chemical and bioclimatic habitat properties. Diversity 15(3):342. https://doi.org/10.3390/d15030342
Migula W (1897) Die Characeen Deutschlands, Oesterreichs und der Schweiz. In: Rabenhorst, L. (Hrsg.): Kryptogamenflora, Band V, 2. Auflage, Kummer, Leipzig
Milovanović V, Popović S, Predojević D, Simić GS, Ržaničanin A, Sekulić JŠ, Trbojević I (2022) Oospore features among morphologically similar and closely related charophyte species: consistency and variability. Cryptogam Algol 43(12):189–200. https://doi.org/10.5252/cryptogamie-algologie2022v43a12
Mouronval JB, Baudouin S, Borel N, Soulié-Märsche I, Klesczewski M, Grillas P (2015) Guide des Characées de France méditerranéenne. Office national de la chasse et de la faune sauvage, 211
Nat E (2024) Chara virgata. In: Schubert H, Gregor T, Blindow I, Nat E, Stewart N, Romanov R, van de Weyer K, Denys L, Korsch H, Casanova M (eds) Characeae of Europe. Springer, Berlin (In Press)
Nowak P, Steinhardt T, von Ammon U et al (2017) Diaspore bank analysis of Baltic coastal waters. Bot Lett 165(1):159–173. https://doi.org/10.1080/23818107.2017.1400464
Nowak P, Wiebe C, Karez R, Schubert H (2021) Applications of environmental DNA methods for charophyte biodiversity. ARPHA Conf Abstr 4:e64944
Peck RE, Morales GA (1966) The Devonian and Lower Mississippian charophytes of North America. Micropaleontology 12(3):303–324
Poikane S, Portielje R, Denys L, Elferts D, Kelly M, Kolada A, Mäemets H, Phillips G, Søndergaard M, Willby N, van den Berg M (2018) Macrophyte assessment in European lakes: diverse approaches but convergent views of ‘good’ecological status. Ecol Indic 94:185–197. https://doi.org/10.1016/j.ecolind.2018.06.056
Proctor VI (1967) Storage and germination of Chara oospores. J Phycol 3(2):90–92
R Core Team (2022) R: A language and environment for statistical computing. R Foundation for Statistical Computing
RAL Classic Colour Chart. https://www.e-paint.co.uk/pdfs/ral%20colour%20chart.pdf. Accessed 7 Apr 2023
Riley WD, Potter EC, Biggs J et al (2018) Small Water bodies in Great Britain and Ireland: ecosystem function, human-generated degradation, and options for restorative action. Sci Total Environ 645:1598–1616. https://doi.org/10.1016/j.scitotenv.2018.07.243
Rodrigo MA, Puche E, Segura M, Arnal A, Rojo C (2021) Sediment underneath charophyte meadows is enriched in viable ephippia and enhances the benthic periphytic biofilm. Hydrobiologia 848(21):5203–5221. https://doi.org/10.1007/s10750-021-04702-x
Romanov RE, Gontcharov AA, Barinova SS (2015) Chara globata Mig (Streptophyta: Charales): rare species revised. Fottea 15(1):39–50. https://doi.org/10.5507/fot.2015.004
Sanjuan J, Vicente A, Flor-Arnau N, Monleón T, Cambra J, Martín-Closas C (2016) Effects of light and temperature on Chara vulgaris (Charophyceae) gyrogonite productivity and polymorphism–palaeoenvironmental implications. Phycologia 56(2):204–212. https://doi.org/10.2216/15-140.1
Santoul F, Figuerola J, Green AJ (2004) Importance of gravel pits for the conservation of waterbirds in the Garonne river floodplain (southwest France). Biodivers Conserv 13:1231–1243. https://doi.org/10.1023/B:BIOC.0000018154.02096.4b
Schneider SC, García A, Martín-Closas C, Chivas AR (2015) The role of charophytes (Charales) in past and present environments: an overview. Aquat Bot 120:2–6. https://doi.org/10.1016/j.aquabot.2014.10.001
Schubert H, Blindow I, Bueno NC, Casanova MT, Pełechaty M, Pukacz A (2018) Ecology of charophytes–permanent pioneers and ecosystem engineers. Perspect Phycol. https://doi.org/10.1127/pip/2018/0080
Šinžar-Sekulić J, Tanasković A (2018) Preliminary research of macrophyte production in Danube reservoirs–case study of two invasive plant species–native Trapa natans and alien Paspalum paspalodes. In 8th Danube Academies Conference: Belgrade, 21–22 September, 2017 (pp. 33–43). Serbian Academy of Sciences and Arts, Belgrade
Søndergaard M, Johansson S, Lauridsen L, Jørgensen B, Liboriussen L, Jeppesen E (2010) Submerged macrophytes as indicators of the ecological quality of lakes. Freshw Biol 55(4):893–908. https://doi.org/10.1016/j.ecolind.2018.06.056
Soulié-Märsche I, García A (2015) Gyrogonites and oospores, complementary viewpoints to improve the study of the charophytes (Charales). Aquat Bot 120:7–17. https://doi.org/10.1016/j.aquabot.2014.06.003
Soulié-Märsche I, Vautier J (2004) Ecology and life cycle of Chara braunii (Charales) in a Mediterranean habitat. Vie et Milieu 54:37–45
Soulié-Märsche I, Benammi M, Gemayel P (2002) Biogeography of living and fossil Nitellopsis (Charophyta) in relationship to new finds from Morocco. J Biogeogr 29(12):1703–1711. https://doi.org/10.1046/j.1365-2699.2002.00749.x
Soulié-Märsche I (1989) Etude comparée de Gyrogonites de Charophytes actuelles et fossiles et phylogénie des genres actuels. Thesis, Universitet des Sciences et Techniques du Languedoc, Montpellier, 237
The Ministry of Environment and Spatial Planning and the Ministry of Agriculture, Forestry and Water Management (2016) Rules on the proclamation and protection of strictly protected and protected wild species of plants, animals and mushrooms. Official Gazette of the Republic of Serbia 5/2010, 47/2011, 32/2016, 98/2016: In Serbian
Trbojević I, Predojević D (2022) Algae in shallow and small water bodies of Serbia: a frame for species and habitat protection. Small Water Bodies of the Western Balkans. Springer, Cham, pp 147–188
Trbojević IS, Predojević DD, Šinžar-Sekulić JB, Nikolić NV, Jovanović IM, Subakov-Simić GV (2019) Charophytes of Gornje Podunavlje ponds: revitalization process aspect. Zbornik Matice Srpske Za Prirodne Nauke 136:123–131
Trbojević I, Marković A, Blaženčić J, Subakov Simić G, Nowak P, Ballot A, Schneider S (2020a) Genetic and morphological variation in Chara contraria and a taxon morphologically resembling Chara connivens. Bot Lett 167(2):187–200
Trbojević I, Milovanović V, Subakov Simić G (2020b) The discovery of the rare Chara baueri (Charales, Charophyceae) in Serbia. Plants 9(11):1606. https://doi.org/10.3390/plants9111606
Urbaniak JG, ˛abka M, (2014) Polish Charophytes. An Illustrated Guide to Identification. Universytet Przyrodniczy We Wroclawiu, Wroclaw
Urbaniak J, Langangen A, van Raam J (2012) Oospore wall ornamentation in the genus Tolypella (Charales, Charophyceae). J Phycol 48(6):1538–1545. https://doi.org/10.1111/jpy.12007
van de Weyer K (2016a) Tolypella intricata. In: Characeen Deutschlands AG (ed) Armleuchteralgen. Die Characeen Deutschlands. Springer, Berlin, pp 522–529
van de Weyer K (2016b) Tolypella prolifera. In: Characeen Deutschlands AG (ed) Armleuchteralgen. Die Characeen Deutschlands. Springer, Berlin, pp 539–546
van de Weyer K (2024a) Sphaerocharaa intricata. In: Schubert H, Gregor T, Blindow I, Nat E, Stewart N, Romanov R, van de Weyer K, Denys L, Korsch H, Casanova M (eds) Characeae of Europe. Springer, Berlin (In Press)
van de Weyer K (2024b) Sphaerocharaa prolifera. In: Schubert H, Gregor T, Blindow I, Nat E, Stewart N, Romanov R, van de Weyer K, Denys L, Korsch H, Casanova M (eds) Characeae of Europe. Springer, Berlin (In Press)
Vedder F (2004) Morphologie und Taxonomie rezenter und subfossiler Characeen-Oosporen aus der Ostsee [Morphology and Taxonomy of Recent and Subfossil Oospores of Charophytes out of the Baltic Sea]. Rostocker Meeresbiologische Beiträge 13:43–54
Venables WN, Ripley BD (2002) Modern applied statistics with S, 4th edn. Springer, New York
Vesić A (2016) Ekološka studija pršljenčica (Charophyceae) stajaćih i sporotekućih voda Vojvodine. Dissertation, Faculty of Biology University of Belgrade
Wood RD, Imahori K (1965) A revision of the characeae. First part: monograph of the characeae. J Cramer Verlag, Weinheim, p 904
Wood PJ, Greenwood MT, Agnew MD (2003) Pond biodiversity and habitat loss in the UK. Area 35(2):206–216. https://doi.org/10.1111/1475-4762.00249
Zhang L, Zheng Y, Zhong G, Wang Q (2019) Research on leaf species identification based on principal component and linear discriminant analysis. Cluster Comput 22:7795–7804. https://doi.org/10.1007/s10586-017-1439-6
Гoллepбax MM, Кpacaвинa ЛК (1983) Xapoвыe Boдopocли. Oпpeдeлитeль Πpecнoвoдныx Boдopocлeй CCCP. Nauka, Leningrad
Acknowledgements
The authors are sincerely grateful to Milica Petrović Ðurić for the technical assistance, expertise and commitment in material processing, and to Prof. Milica Ljaljević Grbić for her kind support of our study. We extend our gratitude to Ms Nadežda Buntić for English language editing. The authors owe special thanks to Dr. habil. Ingeborg Soulié-Märsche for constructive and supportive comments and suggestions, that directed and shaped our research outcomes. We thank the anonymous reviewers for their careful reading of our manuscript and their many insightful comments and suggestions, which have significantly improved our manuscript.
Funding
This work was supported by the Rufford foundation (Grant no. 25789-1 and Grant no. 34213-2), and Ministry of Education, Science and Technological Development of the Republic of Serbia (Grant no. 451-03-47/2023-01/ 200178).
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. In the field, the material was collected by Ivana Trbojević, Vanja Milovanović and Jasmina Šinžar Sekulić. Analyses of the material in the laboratory were performed by Ivana Trbojević and Vanja Milovanović. Data analysis and interpretation was done by Jasmina Šinžar Sekulić, Ivana Trbojević and Vanja Milovanović. The first draft of the manuscript was written by Vanja Milovanović and Ivana Trbojević, and all authors edited and commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Competing interest
The authors have no relevant financial or non-financial interests to disclose.
Additional information
Communicated by David Hawksworth.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Milovanović, V., Šinžar Sekulić, J., Cvijanović, D. et al. Charophyte diversity and their habitat conservation perspectives: insights from vegetation versus sediments survey of a small pond in Serbia. Biodivers Conserv 33, 1413–1437 (2024). https://doi.org/10.1007/s10531-024-02808-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10531-024-02808-x