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RESEARCH ARTICLE (Open Access)
Contents Vol 75(9)

Global hotspots of endemicity, rarity and speciation of aquatic macrophytes

Tatiana Lobato-de Magalhães https://orcid.org/0000-0002-2356-6475 A B * , Kevin Murphy C , Julissa Tapia Grimaldo C , Thomas A. Davidson https://orcid.org/0000-0003-2326-1564 D , Eugenio Molina-Navarro https://orcid.org/0000-0001-5171-3180 E , José Arturo de-Nova https://orcid.org/0000-0002-1989-1355 F and Andrey Efremov https://orcid.org/0000-0001-8983-392X G
+ Author Affiliations
- Author Affiliations

A Faculty of Natural Sciences, Universidad Autónoma de Querétaro, Santiago de Querétaro 76230, Mexico.

B Biological Sciences Department, North Dakota State University, Fargo, ND 58102, USA.

C University of Glasgow, Glasgow, G12 8QQ, Scotland. Email: mearnskevin1@gmail.com; julstg@gmail.com

D Lake Group, Department of Ecoscience, Aarhus University, DK-C8000 Aarhus, Denmark. Email: thd@ecos.au.dk

E Department of Geology, Geography and Environment, University of Alcalá, E-28802 Madrid, Spain. Email: eugenio.molina@uah.es

F Instituto de Investigación de Zonas Desérticas, Universidad Autónoma de San Luis Potosí, San Luis Potosí 78377, Mexico. Email: arturo.denova@gmail.com

G Independent Researcher, Omsk Region, RU-644122 Omsk, Russian Federation. Email: stratiotes@yandex.ru

* Correspondence to: tatilobato@gmail.com, tatiana.lobato@uaq.mx

Handling Editor: Michelle Casanova

Marine and Freshwater Research 75, MF23121 https://doi.org/10.1071/MF23121
Submitted: 20 June 2023  Accepted: 7 May 2024  Published: 7 June 2024

© 2024 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)

Abstract

Context

Most aquatic macrophytes are ecozone-endemic species, and approximately two-thirds of them have rare occurrence at global scale. These small-range plants are seriously under-studied at macroecological scale, despite their marked vulnerability to extinction through habitat loss and climate change.

Aims

To identify global hotspots of endemism and rarity of aquatic macrophytes and examine the factors that resulted in speciation hotspots of macrophytes in some areas of the planet.

Methods

We analysed a database of 3499 macrophyte species to locate speciation hotspots and assess the biogeographic and environmental drivers that maintain ecozone-endemic, and globally rare species within their current limited global areas of occupancy.

Key results

Ecozone-endemic and globally rare macrophyte species hotspots across the planet showed similar occurrence patterns and drivers among ecozones. Ecozone environmental conditions, particularly harsh environments, influenced macrophyte phylogenetic diversity and structure. Most macrophyte species diversification is recent (<10 million years ago). A negative association with bird-mediated zoochory was seen for endemicity and rarity hotspots.

Conclusions

This study identified hotspots of endemicity and rarity, and potential cradle and museum speciation areas.

Implications

Our findings could inform global action to conserve the macrophyte diversity of wetlands, and other inland aquatic habitats, across the world.

Keywords: aquatic plants, diversification, ecozone-endemic, long-distance dispersal, phylogenetic diversity, range distribution, vicariance, globally rare species.

References

Alahuhta J, Johnson LB, Olker J, Heino J (2014) Species sorting determines variation in the community composition of common and rare macrophytes at various spatial extents. Ecological Complexity 20, 61-68.
| Crossref | Google Scholar |

Alahuhta J, Lindholm M, Baastrup-Spohr L, García-Girón J, Toivanen M, Heino J, Murphy K (2021) Macroecology of macrophytes in the freshwater realm: patterns, mechanisms and implications. Aquatic Botany 168, 103325.
| Crossref | Google Scholar |

Albrecht DE (2002) Elatine macrocalyx (Elatinaceae), a new species from central and western Australia. Nuytsia 14, 319-324.
| Crossref | Google Scholar |

Bishop IJ (2019) Understanding the habitat and decline of Najas flexilis (Willd.) Rostk. & Schmidt in the UK using ecology and paleoecology. PhD thesis, University College, London, UK.

Bishop IJ, Bennion H, Patmore IR, Sayer CD (2018) How effective are plant macrofossils as a proxy for macrophyte presence? The case of Najas flexilis in Scotland. Journal of Paleolimnology 60, 153-165.
| Crossref | Google Scholar |

Bishop IJ, Bennion H, Sayer CD, Patmore IR, Yang H (2019) Filling the ‘data gap’: using paleoecology to investigate the decline of Najas flexilis (a rare aquatic plant). Geo: Geography and Environment 6, e00081.
| Crossref | Google Scholar |

Borsch T, Wiersema JH, Hellquist CB, Löhne C, Govers K (2014) Speciation in North American water lilies: evidence for the hybrid origin of the newly discovered Canadian endemic Nymphaea loriana sp. nov. (Nymphaeaceae) in a past contact zone. Botany 92, 867-882.
| Crossref | Google Scholar |

Bove CP, Philbrick CT (2014) Rediscovery of a Neotropical rheophyte (Podostemaceae) after 160 years: implications for the location of conservation unit boundaries (Tocantins, Brazil). Check List 10, 1170-1173.
| Crossref | Google Scholar |

Burnham KP, Anderson DR (2002) ‘Model selection and multimodel inference: a practical information-theoretic approach.’ (Springer: New York, NY, USA)

Cheek M, Séné O, Ngansop E (2020) Three new critically endangered Inversodicraea (Podostemaceae) species from Tropical Africa: I. senei, I. tanzaniensis and I. botswana. Kew Bulletin 75, 31.
| Crossref | Google Scholar |

Chen L-Y, Chen J-M, Gituru RW, Wang Q-F (2012a) Generic phylogeny, historical biogeography and character evolution of the cosmopolitan aquatic plant family Hydrocharitaceae. BMC Evolutionary Biology 12, 30.
| Crossref | Google Scholar |

Chen L-Y, Chen J-M, Gituru RW, Temam TD, Wang Q-F (2012b) Generic phylogeny and historical biogeography of Alismataceae, inferred from multiple DNA sequences. Molecular Phylogenetics and Evolution 63, 407-416.
| Crossref | Google Scholar | PubMed |

Crawford DJ, Landolt E, Les DH, Kimball RT (2006) Speciation in duckweeds (Lemnaceae): phylogenetic and ecological inferences. Aliso: A Journal of Systematic and Floristic Botany 22, 231-242.
| Crossref | Google Scholar |

Dagallier L-PMJ, Janssens SB, Dauby G, Blach-Overgaard A, Mackinder BA, Droissart V, Svenning J-C, Sosef MSM, Stévart T, Harris DJ, Sonké B, Wieringa JJ, Hardy OJ, Couvreur TLP (2020) Cradles and museums of generic plant diversity across tropical Africa. New Phytologist 225, 2196-2213.
| Crossref | Google Scholar |

Dai X, Li X, Song X, Li X, Liu X (2021) The evolutionary history and phylogeographic pattern of Hippuris vulgaris: hybridization and long-distance dispersal from China. Plant Systematics and Evolution 307, 10.
| Crossref | Google Scholar |

Efimov D, Efimova L (2020) Флористические находки редких видов растений в Республике Хакасии. Floristic finds of rare plant species in the Republic of Khakassia. Turczaninowia 23(2), 91-98 [In Russian with title and abstract in Russian and English].
| Crossref | Google Scholar |

Efremov AN, Sviridenko BF (2016) О распространенииредких гидрофитов вОмской области. On distribution rare hydrophytes in Omsk Region. БОТАНИЧЕСКИЙ ЖУРНАЛ [Botanical Journal] 101, 923-927 [In Russian with title and abstract in Russian and English].
| Google Scholar |

Elith J, Leathwick JR, Hastie T (2008) A working guide to boosted regression trees. Journal of Animal Ecology 77, 802-813.
| Crossref | Google Scholar | PubMed |

Estrada-Ruiz E, Calvillo-Canadell L, Cevallos-Ferriz SRS (2009) Upper Cretaceous aquatic plants from Northern Mexico. Aquatic Botany 90, 282-288.
| Crossref | Google Scholar |

Faith DP (1992) Conservation evaluation and phylogenetic diversity. Biological Conservation 61, 1-10.
| Crossref | Google Scholar |

Fick SE, Hijmans RJ (2017) WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. International Journal of Climatology 37(12), 4302-4315.
| Crossref | Google Scholar |

Friis EM, Pedersen KR, Crane PR (2001) Fossil evidence of water lilies (Nymphaeales) in the Early Cretaceous. Nature 410, 357-360.
| Crossref | Google Scholar | PubMed |

García-Girón J, Heino J, Iversen LL, Helm A, Alahuhta J (2021) Rarity in freshwater vascular plants across Europe and North America: patterns, mechanisms and future scenarios. Science of The Total Environment 786, 147491.
| Crossref | Google Scholar | PubMed |

Grime JP (1979) ‘Plant strategies and vegetation processes.’ (Wiley: Chichester, UK)

Gunn IDM, Carvalho L (2021) Slender naiad (Najas flexilis) habitat quality assessment. (Centre for Expertise of Water, CREW: Aberdeen, UK) Available at https://nora.nerc.ac.uk/id/eprint/528396/1/N528396CR.pdf [Verified October 2022]

Ito Y, Tanaka N, Albach DC, Barfod AS, Oxelman B, Muasya AM (2017a) Molecular phylogeny of the cosmopolitan aquatic plant genus Limosella (Scrophulariaceae) with a particular focus on the origin of the Australasian L. curdieana. Journal of Plant Research 130, 107-116.
| Crossref | Google Scholar | PubMed |

Ito Y, Tanaka N, Barfod AS, Kaul RB, Muasya AM, Garcia-Murillo P, De Vere N, Duyfjes BEE, Albach DC (2017b) From terrestrial to aquatic habitats and back again: molecular insights into the evolution and phylogeny of Callitriche (Plantaginaceae). Botanical Journal of the Linnean Society 184, 46-58.
| Crossref | Google Scholar |

Jin Y, Qian H (2019) V.PhyloMaker: an R package that can generate very large phylogenies for vascular plants. Ecography 42(8), 1353-1359.
| Crossref | Google Scholar |

Kumar S, Stecher G, Suleski M, Hedges SB (2017) TimeTree: a resource for timelines, timetrees, and divergence times. Molecular Biology and Evolution 34, 1812-1819.
| Crossref | Google Scholar | PubMed |

Les DH, Crawford DJ, Kimball RT, Moody ML, Landolt KE (2003) Biogeography of discontinuously distributed hydrophytes: a molecular appraisal of intercontinental disjunctions. International Journal of Plant Sciences 164, 917-932.
| Crossref | Google Scholar |

Les DH, Peredo EL, King UM, Benoit LK, Tippery NP, Ball CJ, Shannon RK (2015) Through thick and thin: cryptic sympatric speciation in the submersed genus Najas (Hydrocharitaceae). Molecular Phylogenetics and Evolution 82(Part A), 15-30.
| Crossref | Google Scholar |

Li Z-Z, Lehtonen S, Martins K, Gichira AW, Wu S, Li W, Hu G-W, Liu Y, Zou C-Y, Wang Q-F, Chen J-M (2020) Phylogenomics of the aquatic plant genus Ottelia (Hydrocharitaceae): implications for historical biogeography. Molecular Phylogenetics and Evolution 152, 106939.
| Crossref | Google Scholar | PubMed |

Lobato-de Magalhães T, Murphy K, Efremov A, Chepinoga V, Davidson TA, Molina-Navarro E (2021) Ploidy state of aquatic macrophytes: global distribution and drivers. Aquatic Botany 173, 103417.
| Crossref | Google Scholar |

Lobato-de Magalhães T, Murphy K, Efremov A, Davidson TA, Molina-Navarro E, Wood KA, Tapia-Grimaldo J, Hofstra D, Fu H, Ortegón-Aznar I (2023) How on Earth did that get there? Natural and human vectors of aquatic macrophyte global distribution. Hydrobiologia 850, 1515-1542.
| Crossref | Google Scholar |

Martins SV, Milne J, Thomaz SM, McWaters S, Mormul RP, Kennedy M, Murphy K (2013) Human and natural drivers of changing macrophyte community dynamics over 12 years in a Neotropical riverine floodplain system. Aquatic Conservation: Marine and Freshwater Ecosystems 23, 678-697.
| Crossref | Google Scholar |

May RM (1995) Conceptual aspects of the quantification of the extent of biological diversity. Chapter 1. In ‘Biodiversity: measurement and estimation’. (Ed. DL Hawksworth) pp. 13–20. (Chapman & Hall: London, UK)

Mazel F, Davies TJ, Gallien L, Renaud J, Groussin M, Münkemüller T, Thuiller W (2016) Influence of tree shape and evolutionary time-scale on phylogenetic diversity metrics. Ecography 39, 913-920.
| Crossref | Google Scholar | PubMed |

Morlon H, Parsons TL, Plotkin JB (2011) Reconciling molecular phylogenies with the fossil record. Proceedings of the National Academy of Sciences 108, 16327-16332.
| Crossref | Google Scholar | PubMed |

Morlon H, Lewitus E, Condamine FL, Manceau M, Clavel J, Drury J (2016) RPANDA: an R package for macroevolutionary analyses on phylogenetic trees. Methods in Ecology and Evolution 7, 589-597.
| Crossref | Google Scholar |

Murphy KJ, Hall R (2005) Baseline monitoring of slender naiad (Najas flexilis) in five Lunan lochs, Perthshire 2004. Report to Scottish Natural Heritage. University of Glasgow, UK.

Murphy K, Efremov A, Davidson TA, Molina-Navarro E, Fidanza K, Crivelari Betiol TC, Chambers P, Tapia Grimaldo J, Varandas Martins S, Springuel I, Kennedy M, Mormul RP, Dibble E, Hofstra D, Lukács BA, Gebler D, Båastrup-Spohr L, Urrutia-Estrada J (2019) World distribution, diversity and endemism of aquatic macrophytes. Aquatic Botany 158, 103127.
| Crossref | Google Scholar |

Murphy K, Carvalho P, Efremov A, Tapia Grimaldo J, Molina-Navarro E, Davidson TA, Thomaz SM (2020) Latitudinal variation in global range-size of aquatic macrophyte species shows evidence for a Rapoport effect. Freshwater Biology 65, 1622-1640.
| Crossref | Google Scholar |

Nee S, Mooers AO, Harvey PH (1992) Tempo and mode of evolution revealed from molecular phylogenies. Proceedings of the National Academy of Sciences 89, 8322-8326.
| Crossref | Google Scholar |

O’Connor A (2013) Article 17 assessment form and audit trail for Najas flexilis, the slender naiad (species code 1833). Backing document. National Parks and Wildlife Service, Department of Arts, Heritage and the Gaeltacht, Ireland, UK.

Pereira JBS, Salino A, Arruda A, Stützel T (2016) Two new species of Isoetes (Isoetaceae) from northern Brazil. Phytotaxa 272, 141-148.
| Crossref | Google Scholar |

Qian H, Jin Y (2016) An updated megaphylogeny of plants, a tool for generating plant phylogenies and an analysis of phylogenetic community structure. Journal of Plant Ecology 9(2), 233-239.
| Crossref | Google Scholar |

Renner SS, Zhang L-B (2004) Biogeography of the Pistia clade (Araceae): based on chloroplast and mitochondrial DNA sequences and Bayesian Divergence Time Inference. Systematic Biology 53, 422-432.
| Crossref | Google Scholar | PubMed |

Sandel B, Arge L, Dalsgaard B, Davies RG, Gaston KJ, Sutherland WJ, Svenning J-C (2011) The influence of late Quaternary climate-change velocity on species endemism. Science 334(6056), 660-664.
| Crossref | Google Scholar | PubMed |

Shcherbakov AV, Lyubeznova NV (2017) Problems in creating lists of protected species for regional Red Data Books: aquatic vascular plants of European Russia and North Caucasus as case studies. Wulfenia 24, 171-192.
| Google Scholar |

Swenson NG (2011) Phylogenetic beta diversity metrics, trait evolution and inferring the functional beta diversity of communities. PLoS ONE 6, e21264.
| Crossref | Google Scholar | PubMed |

Takacs A, Molnár AV, Horváth O, Sramkó G, Popiela A, Mesterházy A, Lovas-Kiss A, Green AJ, Löki V, Nagy T, Lukács BA (2017) The rare aquatic angiosperm Elatine gussonei (Elatinaceae) is more widely distributed than previously thought. Aquatic Botany 141, 47-50.
| Crossref | Google Scholar |

Tippery NP, Sears NL, Zentner AB, Sivadas V (2018) Evidence for allopolyploid speciation in Nymphoides (Menyanthaceae). Systematic Botany 43, 117-129.
| Crossref | Google Scholar |

Trabucco A, Zomer R (2019) Global aridity index and potential evapotranspiration (ET0) climate database. FigShare v2. [Dataset, posted 18 January 2019] doi:10.6084/m9.figshare.7504448.v3

Trifonov VG, Artyushkov EV, Dodonov AE, Bachmanov DM, Mikolaichuk AV, Vishnyakov FA (2008) Pliocene–Quaternary orogeny in the Central Tien Shan. Russian Geology and Geophysics 49(2), 98-112.
| Crossref | Google Scholar |

van de Peer Y, Ashman T-L, Soltis PS, Soltis DE (2021) Polyploidy: an evolutionary and ecological force in stressful times. The Plant Cell 33(1), 11-26.
| Crossref | Google Scholar | PubMed |

Wang H, Dilcher DL (2006) Aquatic angiosperms from the Dakota Formation (Albian, Lower Cretaceous), Hoisington III locality, Kansan, USA. International Journal of Plant Sciences 167, 385-401.
| Crossref | Google Scholar |

Wang Y-F, Ferguson DK, Li C-S (2005) Ceratophyllum (Ceratophyllaceae) from the Miocene of eastern China and its paleoecological significance. Systematic Botany 30, 705-711.
| Crossref | Google Scholar |

Waters-Hart KE (2020) Assessing aquatic macrophyte recovery responses following lanthanum-modified bentonite applications. PhD thesis, University of Stirling, Scotland, UK.

Webb CO, Ackerly DD, McPeek MA, Donoghue MJ (2002) Phylogenies and community ecology. Annual Review of Ecology, Evolutiom, and Systematics 33, 475-505.
| Crossref | Google Scholar |

Wingfield RA (2002) The functional ecology of Najas flexilis. PhD thesis, University of Glasgow, Scotland, UK.

Wingfield R, Murphy K, Gaywood M (2005) Lake habitat suitability for the rare European macrophyte Najas flexilis (Willd.) Rostk. & Schmidt. Aquatic Conservation: Marine and Freshwater Ecosystems 15, 227-241.
| Crossref | Google Scholar |

Wingfield R, Murphy KJ, Gaywood M (2006) Assessing and predicting the success of Najas flexilis (Willd.) Rostk. & Schmidt, a rare European aquatic macrophyte, in relation to lake environmental conditions. Hydrobiologia 570, 79-86.
| Crossref | Google Scholar |

Zanne AE, Tank DC, Cornwell WK, Eastman JM, Smith SA, FitzJohn RG, McGlinn DJ, O’Meara BC, Moles AT, Reich PB, Royer DL, Soltis DE, Stevens PF, Westoby M, Wright IJ, Aarssen L, Bertin RI, Calaminus A, Govaerts R, Hemmings F, Leishman MR, Oleksyn J, Soltis PS, Swenson NG, Warman L, Beaulieu JM (2014) Three keys to the radiation of angiosperms into freezing environments. Nature 506, 89-92.
| Crossref | Google Scholar | PubMed |

Zhang Y, Jeppesen E, Liu X, Qin B, Shi K, Zhou Y, Thomaz SM, Deng J (2017) Global loss of aquatic vegetation in lakes. Earth-Science Review 173, 259-265.
| Crossref | Google Scholar |

Zhu J, Yu D, Xu X (2015) The phylogeographic structure of Hydrilla verticillata (Hydrocharitaceae) in China and its implications for the biogeographic history of this worldwide-distributed submerged macrophyte. BMC Evolutionary Biology 15, 95.
| Crossref | Google Scholar | PubMed |