The 2011 edition of “The Freshwater Algal Flora of the British Isles”: additions, corrections, nomenclatural and taxonomic changes

ABSTRACT Taxonomic, nomenclatural and distributional changes since the publication of the 2011 edition (reprinted 2021) of The Freshwater Algal Flora of the British Isles (“Flora”) are reviewed together with some changes overlooked earlier. Many of the more recent changes are a result of studies combining an analysis of morphological and DNA sequence data. Of the 473 changes reported most concern the Chlorophyta (131) and the Charophyta (156) followed by the Cyanobacteria (101), with most of the alterations to the Charophyta involving the desmids (136). Also included are 83 new additions to the British and Irish freshwater algal floras, including 20 overlooked in the Flora. Most of these additions are new records: four are newly described desmids and Synura hibernica (Ochrophyta, Chrysophyceae, Synurales) and Chlorococcum turfosum (Chlorophyta, Chlorophyceae, Chlamydomonadales) are also new. The new additions to Flora include information on locality, collector and publication source. Reference is made to discussions in the Flora giving reasons why some genera and species combinations were not accepted, particularly concerning the Cyanobacteria for which a relatively conservative approach had been adopted in the previous edition of the Flora.


Introduction
The second edition of the "Freshwater Algal Flora of the British Isles" (John, Whitton, & Brook, 2011; hereafter the "Flora") is a much expanded and updated version of the original edition first published in 2002. The second edition of the Flora (reprinted in 2021) remains the only comprehensive account and identification guide to the freshwater and terrestrial algae (excluding diatoms) of Britain and Ireland. It includes information on their ecology, worldwide distribution, identification keys and many line drawings of species. The second edition is accompanied by a DVD containing a photographic catalogue of 680 images, some highly illustrated articles and video clips. The 2021 reprint is not accompanied by the DVD, however its contents are available for download from the Cambridge University Press (CUP) website. Since publication of the last edition, there have been major advances in our understanding of algal diversity and phylogenetic relationships, often due to molecular investigations involving the analysis of DNA sequence data and reassessment of the characters used to define genera and species.
Reviewed here are all taxonomic and/or nomenclatural changes (up to June 2021) since publication of the second edition of the Flora, including all new additions. The conservative approach adopted for the Cyanobacteria has meant that some of the changes predate publication of this edition. Over the past decade, taxonomic studies have focussed on some groups more than others and this is reflected in the number of changes. For example, there is a disproportionately large number of changes in the desmids (Charophyta, Desmidiales) due in large part to a revision of the genera Staurastrum & Staurodesmus based on morphology by Coesel & Meesters (2013). Many of the new desmid records are thanks to David Williamson who has also described a number of new taxa from these islands. Since of the second edition of the Flora the number of images has increased to over 2,300 due largely to new photographs contributed by Chris Carter. The original and new images are searchable on the AlgaeVision website (Carter, John, & Wilbraham, 2016; http://algae vision.myspecies.info) hosted by the Natural History Museum, London, developed by Joanna Wilbraham. The original photo catalogue is now available on the CUP website (under "Resources") and many of the images are also available on the AlgaeBase website . The text accompanying each image entry on AlgaeVision gives the page number of the description/illustration(s) in the Flora and provides a weblink to the entry in AlgaeBase. Worldwide sales of the Flora volumes (almost 2,700 copies) reflect the requirement for a user-friendly guide to enable the identification of frequently very widely distributed freshwater algae. The need for accurate species level identification using morphological characters and, in future, species-specific DNA sequences ("barcodes"), is increasingly important as the health of our freshwater environment continues to decline due to anthropogenic impact and climate change. Undesirable changes to freshwater environments worldwide will inevitably cause the disruption of food webs in which often algae play a key role as primary producers. It is predicted that "lake heatwaves" will in the future threaten biodiversity by changing the composition of aquatic communities, with algae, together with entire lake ecosystems, being driven to the very limits of their resilience (e.g., Woolway et al., 2021). Interest in freshwater algae continues unabated as these algae are increasingly used as indicators of the ecological and conservation status of aquatic habitats (see John & Williamson, 2007;Stewart, 2004), as sources of useful chemicals, producers of toxins and as nuisance organisms, and potential sequestrators or capturers of carbon and therefore used to combat or mitigate against some of the worst impacts of climate change.

Methodology
The current status of the taxonomic entries in the Flora was determined using AlgaeBase , employed worldwide as a reliable source of such information. The website, however, cautions that some of the species names it as current are " . . . a compromise of taxonomic opinions that may or may not reflect your conclusions". AlgaeBase was also used as a source of information the literature for most of the taxonomic and nomenclatural changes listed here.
Many of the important references, new records, errors and taxonomic and/or nomenclatural changes mentioned here are in the web-based version of the Coded List of British and Irish Freshwater Algae (Whitton & John, 2014) and published as corrections or updates in a series of articles (John & Whitton, 2012, 2015, 2017, John, Williamson, & van Weston, 2018, 2019.
Some of the changes and new additions include taxa overlooked previously, ones newly described, and many discovered in Britain and Ireland over the past decade. Also noted are a few taxa erroneously recorded from Britain and Ireland.
If the names of the taxa listed have changed more than once since publication of the Flora then the synonym(s) is in parentheses under the currently accepted name. The consensus classification published by Ruggiero et al. (2014) is generally adopted here (as in AlgaeBase), with some phyla in the Flora now classes under the Phylum Ochrophyta.
A double asterisk (**) before a binomial indicates the correction of an error in the Flora. Nomenclatural authorities with more than four authors have been reduced to the first author and "et". As far as possible names of authorities comply with The International Plant Names Index (https://ipni.org). In accordance with best practice, a double bar " = " indicates a heterotypic synonym whilst a triple bar "≡" indicates a homotypic synonym. "ICN Art". Refers to an Article of the International Code of Nomenclature (Wiersema et al., 2018). Invalid designations ("names") are in double quotes.

Cyanobacteria Stanier ex Cavalier-Smith
In a series of monographs and papers Anagnostidis, Komárek and colleagues have proposed extensive rearrangements and splitting of cyanobacterial genera. Many of the changes were not adopted in the second edition of the Flora and some of the reasons given for not these new taxa were because ". . . culture and molecular studies are still insufficient in most cases to establish sound generic limits, which can be applied to both field identifications and laboratory research" (John et al., 2011: p. 36). The following genera were not recognized: Blennothrix, Leibleinia, Planktolyngbya, Limnococcus, Leptolyngbya, Dolichospermum, Phormidesmis, Pseudophormidium, Jaaginema, Tapinothrix, Trichormus and Jaaginema. The following new genera were in the Flora for "practical reasons" (see discussion in John et al., 2011: p. 34-38), or considered to be supported by particularly convincing evidence: Planktothrix, Tychonema, Sphaerospermum, Cuspidothrix and Heteroleibleinia. Since publication of the second edition there have been some combined morphological and molecular phylogenetic studies that have resulted in the creation of the following new genera: Anagnostidinema, Chrysosporum, Kamptonema, Potamolinea, Anathece, Desmonostoc, Johanseninema and Drouetiella. Names accepted in AlgaeBase and mentioned here are recommended in the Handbook of Cyanobacterial Monitoring and Cyanotoxin Analysis (Santos et al., 2017) for use by water managers dealing with cyanobacterial blooms and toxigenic species.
Note: Species are listed in orders in accordance with their present ordinal attribution.

Class Cyanophyceae Schaffner Order Chroococcales Schaffner
Gloeocapsa magma (Brébisson) Kützing is now Gloeocapsopsis magma (Brébisson) Komárek & Anagnostidis ex Komárek. In the Flora the author of the cyanobacteria considered Gloeocapsopsis magma to be a homotypic synonym of Gloeocapsa magma, commenting (p. 60) that "it seems unlikely that most users will be confident in separating the two" when referring to the difficulty of separating the genera on the characters mentioned by Komárek and Anagnostidis (1999). ** "Microcystis wesenbergii" (Komárek) Komárek, nom. inval. now Microcystis wesenbergii (Komárek) Komárek ex Komárek. The name was first validated in Joosten (2006, p. 209) when he cited the basionym and gave the name as "Microcystis wesenbergii (Komárek) Komárek ex Komárek" which meets the requirements of the ICN for validation of a name.

Order Oscillatoriales Schaffner
For practical difficulties associated with distinguishing genera of the Oscillatoriales, including the distinction between Pseudanabaena and Limnothrix, see discussion in the Flora (John et al., 2011: pp. 78-80). Also discussed (John et al., 2011: p. 83) is the reason for not recognizing some of the new genera (including Leptolyngbya, Leibleinia, Planktolyngbya) created by the splitting and rearrangement of species of Lyngbya sensu lato, with these changes by Komárek and Anagnostidis (2005 Komárek. The supposed basionym, "Calothrix caespitosa" Rabenhorst, is invalid (pre-starting-point name). Homoeothrix caespitosa Kirchner could be treated as a new name but is illegitimate as included in the synonymy of Dichothrix nordstedtii Bornet & Flahault [erroneously given as "Diplothrix nordstedtii"], a valid and legitimate name and transferred to Phormidiochaete by Komárek in Anagnostidis (2001).

DINOZOA Cavalier-Smith [as DINOPHYTA Dillon]
Notes: The phylum Dinozoa includes a number of classes that are generally treated under the ICZN (see Ruggiero et al., 2014). Over the past two decades many studies on phylogenetic relationships have resulted in a revision of generic boundaries, the recognition of several new genera and a number of species reassignments (Craveiro, Calado, Daugbjerg, Hansen, & Moestrup, 2011;Moestrup & Calado, 2018), and the description of several new orders.

CHAROPHYTA Migula
The Flora included the Charophyta in the Chlorophyta.

Order Desmidiales C.E.Bessey
Note: Changes proposed by Coesel & Meesters (2013) are indicated by a single asterisk (*). The majority are the result of new combinations, with a few forms and varieties not considered to be worthy of recognition by them.

Order Nostocales Borzi
"Anabaena azollae" Strasburger, nom. inval. now "Trichormus azollae" Komárek & Anagnostidis, nom. inval. Only included as the fern Azolla has been reported but not this, its obligate cyanobacterial symbiont. Anabaena azollae Strasburger is a pre-startingpoint invalid designation; Trichormus azollae is also invalid as it was not validated by Komárek & Anagnostidis (1989: 303).  . According to Chris Carter (pers. comm.), Johanna Knappe believes the River Wye material to correspond closely to Lemanea nodosa Kützing which she considers a form of Paralemanea catenata although Vis & Sheath (1992) had earlier reduced it to a synonym of this species. "Paralemanea catenata f. nodosa" Knappe & Huth is an invalid designation. It is unclear in the original publication what the authors' intentions were: if it were to make a new combination for Lemanea nodosa Kützing, then there was no "full and direct" citation (ICN Art. 41.5) of the putative basionym (the authors cite as "syn" [synonyms] "Lemanea nodosa Kütz. 1849" and "Lemanea nodosa Sirodot 1872"); if it were to be described as a new form, no description in Latin or English is provided as required by ICN Art. 39.2 and no type was designated.

Euglenozoa Cavalier-Smith [Euglenophyta]
Note: the Euglenozoa includes the Class Euglenophyceae and a number of phyla now regarded as animal taxa (Ruggiero et al., 2014).

Ochrophyta Cavalier-Smith
Note: the classes Chrysophyceae, Xanthophyceae and Eustigmatophyceae are currently included in the Phylum Ochrophyta, the Class Chrysophyceae now includes the Class Synurophyceae.

Order Hibberdiales R.A.Andersen
Bitrichia ollula (Fott) Fott. Collected in a plankton sample from East Loch Ollay (Loch Olaidh an Ear) located on the machair plain along the west coast of South Uist in the Outer Hebrides, Scotland (Lang et al., 2016b).

Order Heterogloeales Fott ex P.C.Silva
Gloeochloris smithiana Pascher. Collected by Chris Carter between 2013 and 2015 on the submerged branches of a bramble (Rubus sp.) in a ditch at Yardley Chase, Northamptonshire, England .  Stockner and Lund (1970) as in the plankton of Lake Windermere in the Cumbrian Lake District, England.  (Beadle, 2015;Beadle, Brown, Carter, & Holden, 2014;.

Order Prasiolales Schaffner
Koliella tatrae (Kol) Hindák. Recorded by Pentecost (2011) who collected it on 20 August 2010 "from a snow patch on Cairngorm known as Cuidhe Crom on the head wall of Coire Cas [NJ002042] about 250 m NW of Cairngorm summit at an altitude of 1010 m" and mentions that "a few cells were subsequently observed on a winter snow patch on the slopes of High Street in Cumbria in February 2011". Accompanying this snow alga was a species of Chromulina which apparently resembled C. sphaeridia J.Schiller although having smaller dimensions. Further studies are required.
England (John et al., 2018). According to Marien van Westen (pers. comm.), a very distinctive species that is similar to Staurastrum brachiatum Ralfs but is smaller and has less pronounced ends. Staurastrum chavesii var. latiusculum (West & G.S. West) Coesel & Meesters. The basionym Staurastrum latiusculum West & West (1902: p. 53) was collected from "near Glenties", Co. Donegal, Ireland (see John, Williamson, & Guiry, 2012). *Staurastrum controversum var. semivestitum (West) Coesel. Staurastrum vestitum var. semivestitum West, the basionym, was described Loughrigg Fell in the Cumbrian Lake District, England (West, 1892b: p. 732). Staurastrum forficulatum var. verrucosum Grönblad. Collected in September 2017 by Marien van Westen from "Lily Tarn" on Loughrigg Fell in the Cumbrian Lake District, England (see John et al., 2018).  Table 1. The number of nomenclatural/taxonomic changes and new additions since publication of the 2nd edition of The Freshwater Algal Flora of the British Isles. The numbers of changes and new records are shown under each of the phyla, with the numbers given under the classes in the Phylum Ochrophyta since each class is recognised as a phylum in the 2 nd ed of the Flora. The total numbers for the Chlorophyta and Charophyta are also broken down to changes and records under classes and orders. The total numbers are based upon the numbers in the shaded blocks.

Discussion
Of the 473 taxonomic and nomenclatural changes (Table 1), the vast majority have occurred since publication of the Flora in 2011. The majority involve the green algae (287), comprising the Chlorophyta and Charophyta, followed by the Cyanobacteria (101), the Dinozoa, Dinophyceae (23), Euglenozoa (28) and Ochrophyta, Chrysophyceae (13). Each of the remaining major groups having less than 10 changes. Most of the changes to the Charophyta concern the desmids (136; Desmidiales), with many resulting from the revision by Coesel & Meesters (2013) of the genus Staurastrum and monospinous forms belonging to Staurodesmus. In this revision, a considerable number of intraspecific taxa have been consigned to synonymy under the type variety based on what is often termed "best professional judgement". All the changes proposed by Coesel and Meesters (2013) are listed here, and most are accepted in AlgaeBase ). There will undoubtedly be further changes, since DNA sequence studies (e.g., Gontcharov & Melkonian, 2011;Štastný & Kouwets, 2012;Štastný et al., 2013) indicate that many desmid genera are polyphyletic. Future molecular studies will undoubtedly lead to wide-ranging revisions of the group, with many subspecies probably reproductively and phylogenetically distinct so probably representing separate species and, possibly, genera. Many of the changes listed here are based on investigations that increasingly involve the analysis of gene sequences in tandem with morphological data   sets. Such polyphasic investigations have resulted in the recognition of at least eight cyanobacterial genera and account for many of the large number of taxonomic and morphological changes in this phylum. A conservative approach was adopted for the Cyanobacteria which resulted in the rejection of a number of genera and new combinations have been 83 new additions to the freshwater algal complement of Britain and Ireland since publication of the second edition of the Flora, including 20 previously overlooked and six species new to science ( Table 2). Of the overlooked species, eight are desmids mentioned by William and George West (see West, 1892aWest, , 1892bWest & West, 1896, 1912. Some of the desmids recorded by the Wests have not been rediscovered despite David Williamson (DBW) having examined thousands of British and Irish samples since the 1970s. There are at least a further 40 desmids recorded by DBW and these and others will be reported upon following an analysis of the information transferred to a searchable database from his card index of site-specific records (Wilbraham et al., in preparation). Of the six new species, four are desmid taxa from Britain and Ireland and have been described by DBW (see Table 2) who has contributed very significantly to the new desmid records. Molecular techniques continue to alter radically our understanding of the taxonomy, phylogeny, diversity and species relationships of non-marine algae. Over the past decade the analysis of DNA sequence data has resulted in some of the changes reported here, but molecular studies on freshwater algae remain patchy. In the long term the intention is to make it possible for non-specialists to identify quickly and accurately algal species based upon sequence similarities against a priori-defined species rather than relying on morphological characters, such as used in the Flora and other traditional identification tools. This still remains aspirational rather than an actuality, particularly as barcode sequences are not available for types, even when the types can be found and are amenable to DNA extraction.